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TUGAS MATA KULIAH

ILMU BEDAH KHUSUS VETERINER

Teknik Operasi Amputasi Dewclaw

Disusun Oleh :

No NIM Nama Mahasiswa


1. 1509005101 Leoni Arifah Agustina
2. 1509005112 Putri Nur Hasanah
3. 1509005114 I Gede Pratama Candra Wibawa
4. 1509005115 Dzikri Nurma’rifah Takariyanti
5. 1509005116 Kadek Satria Adi Marhendra
6. 1509005119 Dinda Nur Hidayah

LABORATORIUM BEDAH VETERINER

FAKULTAS KEDOKTERAN HEWAN

UNIVERSITAS UDAYANA

TAHUN 2018

i
RINGKASAN

Cakar adalah anggota tambahan badan yang terlindung dari ujung kaki. Cakar
sebenarnya adalah pembesaran dan pengerasan dari kuku. Pencabutan cakar atau
dewclaw adalah operasi yang bertujuan untuk mengangkat dan menghilangkan cakar
hewan (misalnya kucing dan anjing) dengan cara mengamputasikan seluruh atau
sebagian dari falang distal, atau memutuskan tulang, jari kaki hewan. Operasi amputasi
dewclaw disebut juga dengan onychectomy. Operasi ini dibagi tiga jenis berdasarkan
instrument bedahnya yaitu dengan menggunakan laser, dengan pisau bedah (scalpel)
serta metode gullotine. Daerah operasi dibalut selama 2-3 hari dan jahitan dibuka
setelah 7-14 hari. Anjing atau kucing dapat dipasangkan Elizabethan collar selama 7-10
hari untuk mencegah anjing/kucing menjilati balutan. Pengobatan dengan antibiotik dan
analgesik dapat diberikan di pagi hari keesokan hari setelah tindakan operasi.

Kata Kunci : Cakar, dewclaw, onychectomy

SUMMARY

Claws are additional members of the body that are protected from the toes. Actual claws
are enlargement and hardening of the nails. Claw or dewclaw extraction is an operation
that aims to remove and remove animal claws (such as cats and dogs) by amputating all
or part of the distal phalanx, or breaking the bones, toes of the animal. Dewclaw
amputation surgery is also called onychectomy. This operation is divided into three
types based on the surgical instrument using a laser, with a scalpel and gullotine
method. The operating area is bandaged for 2-3 days and the sutures are opened after 7-
14 days. Dogs or cats can be paired with Elizabethan collar for 7-10 days to prevent
dogs / cats from licking bandages. Treatment with antibiotics and analgesics can be
given in the morning the following day after surgery.

Keywords: Claws, dewclaw, onychectomy

ii
KATA PENGANTAR

Puji syukur penulis panjatkan kehadirat Tuhan Yang Maha Esa yang telah memberikan
rahmat serta hidayah-Nya sehingga penyusunan paper ini dapat diselesaikan.

Paper ini disusun penulis sebagai tugas dari mata kuliah Ilmu Bedah Khusus Veteriner,
yang berjudul “Teknik Operasi Amputasi Dewclaw”. Melalui penulisan paper ini, diharapkan
mahasiswa mampu memahami lebih dalam tentang Teknik Operasi Amputasi Dewclaw.

Terima kasih penulis sampaikan kepada dosen mata kuliah Ilmu Bedah Khusus Veteriner
yang telah membimbing dan memberikan kuliah demi lancarnya penulisan tugas paper ini. Kritik
dan saran yang membangun sangat penulis harapkan untuk penulisan paper yang lebih baik lagi
kedepannya.

Demikianlah paper ini penulis susun, semoga bermanfaat dan dapat memenuhi tugas mata
kuliah Ilmu Bedah Khusus Veteriner.

Denpasar, 3 September 2018

Hormat Saya,

Penulis

iii
DAFTAR ISI

COVER ....................................................................................................................i

RINGKASAN ..........................................................................................................ii

KATA PENGANTAR..............................................................................................iii

DAFTAR ISI ............................................................................................................iv

DAFTAR GAMBAR ...............................................................................................v

DAFTAR LAMPRAN .............................................................................................vi

BAB I. PENDAHULUAN .......................................................................................1

1.1 Latar Belakang ..........................................................................................1

1.2 Rmumusan Masalah ..................................................................................1

1.3 Tujuan Penulisan .......................................................................................1

1.4 Manfaat Penulisan .....................................................................................2

BAB II. TINJAUAN PUSTAKA .............................................................................3


2.1 Teknik Operasi ..........................................................................................3
2.1.1 Preoperasi ....................................................................................3
2.1.2 Operasi .........................................................................................4
2.1.3 Tindakan Pasca Operasi Pengangkatan Dewclaw .......................5

BAB III. PEMBAHASAN .......................................................................................7

BAB IV. SIMPULAN DAN SARAN ......................................................................8

4.1 Simpulan....................................................................................................8

4.2 Saran ..........................................................................................................8

DAFTAR PUSTAKA ..............................................................................................9

LAMPIRAN JURNAL.............................................................................................10

iv
DAFTAR GAMBAR

Gambar 1. Metode Operasi Amputasi Dewclaw. ..................................................... 4

Gambar 2. Anjing Pasca Operasi Pengangkatan Dewclaw Di Kedua Kaki Belakang.


Daerah Operasi Dibalut Dan Lehernya Dipasangkan E-Collar ............. 6

v
DAFTAR LAMPIRAN

Jurnal 1. A review of medically unnecessary surgeries in dogs and cats…………....10

Jurnal 2. Perioperative Pain Management in Veterinary Patients............................... 10

Jurnal 3. Postoperative Bleeding in Retired Racing Greyhounds ............................... 10

Jurnal 4. Dewclaws in wolves as evidence of admixed ancestry with dogs ............... 10

vi
BAB I

PENDAHULUAN

1.1 Latar Belakang Masalah


Prosedur bedah kosmetika dalam dunia veteriner dilakukan dengan dua tujuan yaitu
estetika untuk menampilkan hewan kesayangan sesuai standar ras hewan dan memberikan
kebanggaan bagi pemilik hewan atas penampilan hewan kesayangannya berbeda dari yang
lain, serta tujuan terapeutik bagi hewan pasca kecelakaan atau cedera permanen. Salah satu
contoh operasi bedah kosmetika adalah pencabutan cakar atau dewclaw.

Cakar adalah anggota tambahan badan yang terlindung dari ujung kaki. Cakar
sebenarnya adalah pembesaran dan pengerasan dari kuku. Hewan berkuku disebut ungulata.
Ungulata terbagi dalam 2 kelompok besar: hewan berkuku genap (misalnya antelop, sapi,
rusa, babi, domba, kambing) dan hewan berkuku gasal (kuda, badak dan tapir). Hewan
berkuku genap yang berjari kaki lebih dari 3 dan 4 lebih kuat, sehingga hewan itu lebih bisa
membawa beban yang lebih berat, sementara hewan berkuku ganjil adalah dengan jari kaki 1
dan 2 kurang bisa.

Pencabutan cakar atau dewclaw adalah operasi yang bertujuan untuk mengangkat dan
menghilangkan cakar hewan (misalnya kucing dan anjing) dengan cara mengamputasikan
seluruh atau sebagian dari falang distal, atau memutuskan tulang, jari kaki hewan. Karena
cakar berkembang dari jaringan germinal dalam falang ketiga, maka amputasi tulang
diperlukan untuk sepenuhnya menghapus cakar. Meskipun hal ini umum di Amerika Utara,
pencabutan kuku dianggap sebagai tindakan kekejaman terhadap hewan dibanyak Negara
seperti Australia, Brazil, Eropa, Austria, Britania Raya, Israel, dan Amerika Serikat.

1.2 Rumusan Masalah


1.2.1 Bagaimana teknik pre-operasi dan anestesi operasi amputasi dewclaw?
1.3.1 Bagaimana teknik operasi amputasi dewclaw?
1.4.1 Bagaimana hasil dan pasca operasi amputasi dewclaw?
1.3 Tujuan
1.3.1 Untuk mengetahui teknik pre-operasi dan anestesi operasi amputasi dewclaw.
1.3.2 Untuk mengetahui teknik operasi amputasi dewclaw.
1.3.3 Untuk mengetahui hasil dan pasca operasi amputasi dewclaw.

1
1.4 Manfaat Tulisan
Manfaat dari penulisan paper ini yaitu agar mahasiswa dapat mengetahui bagaimana
definisi operasi amputasi dewclaw, teknik pre-operasi dan anestesi operasi amputasi
dewclaw, teknik operasi dewclaw, hingga hasil dan pasca operasi amputasi dewclaw, dan
juga pembuatan paper ini untuk melengkapi tugas Ilmu Bedah Khusus Veteriner tentang
teknik operasi amputasi dewclaw.

2
BAB II.

TINJAUAN PUSTAKA

2.1 Teknik Operasi

2.1.1 Preoperasi

- Waktu
Operasi amputasi dew claw pada hewan yang baru lahir bisa dilakukan
bersamaan dengan tail docking pada umur 1-2 hari. Jika prosedur tidak dilakukan
saat itu, maka dianjutkan untuk menunggu hingga hewan berusia setidaknya
berusia 12 minggu.
- Persiapan Obat dan Alat
Sebelum melakukan operasi, obat yang harus disiapkan adalah obat
premedikasi seperti atropin sulfat, obat anestesi yang meliputi xylasin dan
ketamin, serta antibiotik cair. Alat yang digunakan adalah alat steril individu
seperti : hands glove, masker dan baju operasi, serta seperangkat alat bedah
(Curcio, 2006)
- Persiapan Tempat Operasi
Tempat operasi harus dalam keadaan bersih dan steril, letakkan alas plastik di
atas meja operasi dan suhu ruangan operasi harus stabil.
- Persiapan Operator
Sebelum melakukan operasi, operator maupun co-operator terlebih dahulu
melepas asesoris yang dapat mengganggu jalannya operasi. Tangan operator dan
co-operator hharus steril dalam melakukan operasi untuk menghindari timbulnya
infeksi bawaan dari luar tubuh hewan. Tangan dicuci menggunakan air bersih dan
sabun. Selanjutnya di steriliasi menggunakan alkohol 70%. Penghitungan dosis
obat yang diberikan untuk tujuan premedikasi dan anastesi harus tepat dan
pengunaan alat-alat sterilisasi individu dengan benar serta memperhatikan SOP
dalam melakukan operasi. (Quartarone et al, 2012)
- Anastesi
Sebelum melakukan anastesi, perlu dilakukan pendataan riwayat pasien
(Posner, 2010) meliputi :
o Hewan
o Berat
3
o Umur
Sebelum operasi dilaksanakan, pasien diperiksa keadaan fisiknya dan
dipuasakan selama 8-12 jam dengan tujuan menghindari terjadinya hipersalivasi
dan vomit pada pemberian anestesi. Selanjutnya melakukan hitungan untuk
mengetahui dosis obat premedikasi dan anestesi yang diberikan terhadap pasien.
Sedasi dan anestesi lokal dianjurkan ketika melakukan prosedur ini pada anak
anjing dan anestesi umum dianjurkan untuk hewan yang lebih tua. (Niel et al,
2016)
Rumus : Berat Badan x Dosis Anjuran
Sediaan

Dosis Anjuran
a. Atropin sulfat : 0,02 – 0,04 mg/kg
b. Xylasin : 1-3 mg/kg
c. Ketamin : anjing 10-15 mg/kg & kucing 10-30 mg /kg

2.1.2 Operasi

Gambar 1. Metode operasi amputasi dewclaw.

4
Operasi amputasi dewclaw disebut juga dengan onychectomy. Operasi ini dibagi tiga
jenis berdasarkan instrument bedahnya yaitu dengan menggunakan laser, dengan
pisau bedah (scalpel) serta metode gullotine. Semua onychectomy dilakukan oleh
dokter hewan berpengalaman yang telah melakukan operasi ini setidaknya 1 tahun
dengan jumlah tindakan sebanyak 7 kali operasi.

a. Onychectomy yang menggunakan laser dilakukan dengan laser karbon dioksida


menggunakan metode disartikulasi (21) (Gambar 1B).
b. Onychectomy yang menggunakan scalpel dilakukan dengan menggunakan pisau
bedah (scalpel) dengan metode yang sama seperti onychectomy laser.
c. Onychectomy guillotine dilakukan dengan gunting kuku tipe guillotine yang steril
menggunakan metode disartikulasi atau amputasi tulang. Metode guillotine
disartikulasi didefinisikan sebagai penghilangan seluruh phalanx ketiga dengan
disartikulasi ruang sendi interphalangeal distal dengan gunting kuku atau
amputasi phalanx ketiga pada fleksor dengan pisau bedah. Metode guillotine
amputasi tulang adalah amputasi di bawah proses ungual meninggalkan prosesus
fleksor dari phalanx ketiga bagian dalam (Gambar 1A) (Clark et al., 2014)

2.1.3 Tindakan Pasca Operasi Pengangkatan Dewclaw

Daerah operasi dibalut selama 2-3 hari dan jahitan dibuka setelah 7-14 hari.
Anjing atau kucing dapat dipasangkan Elizabethan collar selama 7-10 hari untuk
mencegah anjing/kucing menjilati balutan. Jika balutan kotor atau basah maka harus
segera diganti untuk mencegah infeksi. Jika daerah operasi terlihat bengkak
menandakan balutan terpasang terlalu ketat sehingga harus segera dilepas.

5
Gambar 2. Anjing pasca operasi pengangkatan dewclaw di kedua kaki belakang. Daerah
operasi dibalut dan lehernya dipasangkan E-collar. Sumber:
https://www.dogforums.com/dog-health-questions/262546-dew-claw-surgery-surgery.html

Pengobatan dengan antibiotik dan analgesik dapat diberikan di pagi hari keesokan
hari setelah tindakan operasi. Jenis antibiotik yang dapat diberikan secara topikal seperti
neosporin dua kali sehari, dan obat analgesik seperti carprofen dengan dosis 2 mg/kgBB
(Dyson, 2008). Dianjurkan agar anjin/kucing dibatasi pergerakannya selama beberapa hari.

6
BAB III

PEMBAHASAN

Operasi amputasi dewclaw merupakan operasi yang masih dipertanyakan


kelegalannya dan masih menjadi pro kontra di kalangan masyarakat. Hal ini dihubungkan
dengan perlindungan animal welfare sehingga tidak semua negara mengizinkan tindakan ini
seperti Australia, New Zealand dan beberapa negara di Eropa.

Operasi pengangkatan dewclaw dikatakan diperlukan khususnya pada kaki belakang


karena secara umum hanya terhubung dengan kulit, berbeda dengan dewclaw di kaki depan
yang tersambung dengan tulang. Jika hanya terhubung kulit maka ada resiko robek saat
tersangkut. Namun hingga saat ini belum ada penelitian mengenai tingkat kejadian cidera
akibat dewclaw.

Pada anjing Toy breeds dewclaw dihilangkan untuk memudahkan menggunting dan
menyisir bulunya. Pada anjing yang dipakai untuk berburu, dewclaw pada kaki belakang
biasanya dipotong karena mudah tersangkut bila berada di lapangan. Beberapa bangsa anjing
ynag biasanya diamputasi dewclawnya adalah Alsatian, boxer, dalmatian, papillon dan silku
terrie.

Adanya claw juga dikhawatirkan akan merusak perabotan rumah terutama pada
hewan peliharaan seperti kucing dan anjing membuat pemilik hewan melakukan operasi ini
pada peliharaannya.

Tak jarang pula operasi ini dilakukan karena alasan medis seperti infeksi, adanya
tumor, atau adanya gangrene pada phalanx ketiga. Kejadian claw tumbuh kembali biasanya
akibat dari metode operasi yang tidak menghilangkan sel germinal pada prosesus ungual,
seperti pada jenis operasi dengan pisau bedah dan dengan gunting kuku guillotine.

Menghilangkan dew claws berpotensi menimbulkan stres, rasa sakit atau infeksi
setelah prosedur dilakukan dan/atau selama penyembuhan. Beberapa breeder di Amerika
memilih untuk menghilangkan dewclaw saat anak anjing masih berusia 3-5 hari pertama
untuk tujuan estetika/penampilan.

7
BAB IV

SIMPULAN DAN SARAN

4.1 Simpulan

Pencabutan cakar atau dewclaw adalah operasi yang bertujuan untuk


mengangkat dan menghilangkan cakar hewan (misalnya kucing dan anjing) dengan
cara mengamputasikan seluruh atau sebagian dari falang distal, atau memutuskan
tulang, jari kaki hewan. Operasi amputasi dewclaw disebut juga dengan
onychectomy. Operasi ini dibagi tiga jenis berdasarkan instrument bedahnya yaitu
dengan menggunakan laser, dengan pisau bedah (scalpel) serta metode gullotine.
Daerah operasi dibalut selama 2-3 hari dan jahitan dibuka setelah 7-14 hari. Anjing
atau kucing dapat dipasangkan Elizabethan collar selama 7-10 hari untuk mencegah
anjing/kucing menjilati balutan. Pengobatan dengan antibiotik dan analgesik dapat
diberikan di pagi hari keesokan hari setelah tindakan operasi.

4.2 Saran

Saran yang dapat penulis berikan adalah operasi amputasi de claw ini
harus ditangani dengan cepat dan tepat dengan cara pembedahan. Pembedahan
merupakan tindakan yang paling efektif dalam penanganan amputasi de claw

8
DAFTAR PUSTAKA

Niel L, Keyserlingk MAG, Mills KE. 2016. A review of medically unnecessary surgeries in

dogs and cats. Canada : JAVMA vol 248 (2)

Sudisma, IGN. 2016. Ilmu Bedah dan Teknik Operasi. Denpasar : Plawa Sari.

Clark et al. 2014. Comparison Of 3 Methods Of Onychectomy. Can Vet J 2014;55:255–262

Dogs Forum: Dew Claw Surgery.....From Surgery Thru Recovery. From


https://www.dogforums.com/dog-health-questions/262546-dew-claw-surgery-
surgery.html

Dyson, D.H., 2008. Perioperative Pain Management in Veterinary Patients. Vet Clin Small
Anim 38 (2008) 1309–1327

Katz&Dogs Wellness Clinic: Post-Operative Care Instructions. From


http://katzdogswellness.com/wp-content/uploads/2010/10/Post-Operative-Care-
Instructions.pdf

9
LAMPIRAN JURNAL

10
Reference Point

A review of medically unnecessary surgeries


in dogs and cats
Katelyn E. Mills BSC From the Animal Welfare Program, Faculty of Land and Food Systems, University of
British Columbia, Vancouver, BC V6T 1Z6, Canada (Mills, von Keyserlingk); and the
Marina A. G. von Keyserlingk PhD Department of Population Medicine, Ontario Veterinary College, University of Guelph,
Lee Niel PhD Guelph, ON N1G 2W1, Canada (Niel).
Address correspondence to Dr. Niel (lee.niel@uoguelph.ca).

I n ancient Rome, during the First Century CE, Lucius


Columella wrote that it was proper to remove the
tails of puppies to prevent their growth to an “abomi-
present review, we did not classify elective neuter-
ing of dogs and cats as an MUS, even though there is
evidence that elective neutering, while decreasing the
nable length” and to prevent madness, which is pre- risk of certain health issues in dogs, may increase the
sumed to refer to rabies.1 Although the idea that this risk of others.4
procedure could protect dogs against rabies has long
since been abandoned, tail docking is still commonly
performed, both because of a belief that it reduces MUSs Commonly Performed
the incidence of injuries and because of the result-
ing perceived improvements in aesthetics. However,
on Dogs and Cats
the effectiveness of this procedure in preventing inju- Tail docking
ries has been questioned, and the idea of performing Tail docking (caudectomy) is the surgical removal
this and other surgical procedures on animals solely of the distal portion of the tail. In the Middle Ages, tail
for cosmetic reasons has been heavily criticized in docking was performed on hunting and fighting dogs
many parts of the world.2 In fact, some countries have to lessen the risk of injury to the tail5 and is still com-
passed legislation restricting these types of surgeries. monly performed on dogs of various hunting, work-
While anecdotal reports suggest that certain cosmet- ing, and terrier breeds.Tail docking is most often done
ic procedures such as ear cropping are in decline in within the first week after birth. Typically, a scissors
North America, to our knowledge there are no reliable or scalpel is used to remove the distal portion of the
estimates on the numbers of these procedures per- tail, with 1 or more sutures used to close the result-
formed annually. ing wound. Alternatively, an elasticized band is placed
Most surgical procedures performed on dogs and around the tail, causing loss of tissue circulation and
cats in North America are performed for therapeutic, eventual death and sloughing of the tail.6 According to
diagnostic, or preventive purposes; that is, they are 1 study,6 tail docking is often carried out by dog breed-
medically necessary. In contrast, procedures that are ers without the use of anesthetics or analgesics. Even
not necessary for maintaining health or that are not when tail docking is performed by veterinarians, an-
beneficial to the animal can be classified as MUSs.This esthetics or analgesics may not be used, with 1 study6
would include procedures performed mainly to alter finding that only 10% of veterinarians used anesthetics
the appearance of animals (eg, ear cropping and tail or analgesics in conjunction with tail docking. Given
docking in dogs), procedures performed solely to pre- that the use of anesthetics and analgesics in veterinary
vent behaviors that are destructive or annoying (eg, practice has increased in general since that study was
devocalization and defanging in dogs and onychec- published,7 it is possible that the percentage of vet-
tomy in cats), and procedures of dubious or minimal erinarians using pain management techniques in con-
benefit (eg, dewclaw removal in dogs). Note that elec- junction with tail docking has also increased. Howev-
tive neutering of healthy dogs and cats has historically er, good estimates are not available.
been performed to prevent or reduce the risk of fu- Tail docking is sometimes performed in adult dogs
ture health problems (eg, pyometra, mammary gland because of tail injury, neoplasia, or self-trauma and in
neoplasia, and reproductive tract–related neoplasia) these instances would be considered a medically nec-
and to prevent unplanned breeding, which benefits essary surgery. Note that treatments other than tail
the population as a whole by reducing the number docking have been described for dogs with self-trau-
of unwanted animals.3 Thus, for the purposes of the ma of the tail, including behavioral modification and
pharmacologic treatment.8 However, the efficacy of
ABBREVIATIONS these alternative treatments has not been examined.
CVMA Canadian Veterinary Medical Association One argument in favor of tail docking is that these
MUS Medically unnecessary surgery breeds require docking to avoid future tail injury.2 To

162 JAVMA • Vol 248 • No. 2 • January 15, 2016


test this theory, Diesel et al9 completed a case-con- be “significant” or “severe.” In a study14 of 50 puppies
trol study of tail injuries in working and nonworking (Doberman Pinschers, Rottweilers, and Bouviers des
dogs with and without docked tails. Tail injuries that Flandres) that underwent tail docking at 3 to 5 days of
were reported included fractures, dislocations, lac- age, all puppies vocalized intensely at the time of tail
erations, contusions, self-trauma, and neoplasia. The amputation, indicating that the procedure was indeed
weighted risk of tail injuries in working dogs (0.29%) painful. The authors also reported that the puppies
was significantly higher than the risk in nonworking settled down relatively quickly after the procedure,
dogs (0.19%), and the risk for dogs with docked tails suggesting that the pain did not last long; however,
(0.03%) was significantly lower than the risk for dogs puppies were only monitored until they settled, which
without docked tails (0.23%). However, the overall tail took approximately 3 minutes, and further pain behav-
injury rate was quite low, and the authors estimated iors may have occurred at later time points. Despite
that 500 dogs would need to have their tails docked the seemingly short duration of pain, some opponents
to prevent 1 tail injury.9 A separate study10 reported of tail docking have argued that any pain is unjust if it
similar results, with a tail injury risk of 0.90% for work- is unnecessary.15
ing breeds and 0.53% for nonworking breeds, and an Whether tail docking can result in chronic pain
estimate that 232 dogs would need to have their tails in dogs has not been extensively studied. Gross and
docked to prevent 1 tail injury severe enough to re- Carr16 described 5 Cocker Spaniels and a Miniature
quire treatment by a veterinarian. Recently, Lederer et Poodle that had extensive self-trauma at the surgical
al11 examined owner reports of tail injuries in docked site for several months up to 1 year after tail amputa-
and undocked hunting dogs during the shooting sea- tion and reported that application of mild pressure to
son in Scotland and found that rates of injuries were the affected tail areas elicited a severe pain response.
higher in undocked spaniels and undocked dogs of The pain in these dogs was attributed to neuroma de-
the hunt, point, and retrieve breeds. The authors also velopment. Young female cattle that have undergone
found that the number of injuries reported for both tail docking show increased agitation following appli-
docked and undocked hunting dogs was higher than cation of hot or cold packs to the tail stub, suggesting
previously reported for working and nonworking that hypersensitive nerve bundles may be present,17
dogs. For example, 54.7% of undocked spaniels and and up to 80% of human amputees report experienc-
20.8% of docked spaniels reportedly had at least 1 in- ing phantom pain following limb amputation.18 Thus,
jury during the shooting season. However, only 4.4% of there is a potential for neuropathic pain in dogs fol-
dogs with a tail injury required veterinary treatment, lowing tail docking, although whether or how fre-
suggesting that the risk of serious injury was much quently this occurs is unknown.
lower than the overall injury estimate. These results Tail docking may also have detrimental effects on
indicate that there may be some minor benefits to tail social communication in dogs,19 as research suggests
docking but likely only in particular breeds of dogs that social communication in dogs is largely reliant on
that are participating in hunting activities. body language, with the tail playing an important role.
Notably, a number of dog breeds, including the For example, Leaver and Reimchen19 examined behav-
Pembroke Welsh Corgi and Australian Shepherd, have ioral responses to dogs with different tail lengths by
a naturally occurring mutation in the T-box transcrip- placing a remotely controlled life-sized dog replica in
tion factor T gene (C189G) that results in a short-tail a park.They assessed responses to tails that were short
phenotype.12 In addition, a few breeds with naturally or long and to tails that were wagging or still. Large
occurring short tails do not have this mutation, sug- dogs showed more caution approaching the replica
gesting that there are other yet-to-be-discovered genet- dog when it had a short tail than when it had a long
ic factors affecting tail phenotype. Recently, selective tail, and the authors speculated that this was a con-
breeding by outcrossing to a Pembroke Welsh Corgi sequence of failure by the replica dog to signal. Also,
with the natural bobtail gene resulted in the birth of large dogs approached the replica dog with a long, still
Boxers with naturally short tails.13 Thus, it may be pos- tail less frequently than they approached the replica
sible for breeds that traditionally have undergone tail dog with a long, wagging tail but approached repli-
docking to develop family lines with naturally short ca dogs with short, wagging tails and short, still tails
tails. Note, however, that there have been anecdotal with about equal frequency. In contrast, small dogs
reports that breeding for a bobtail appearance has re- showed greater caution than large dogs, regardless of
sulted in health concerns related to deformed tails and tail length or motion, likely because of the height dif-
spinal cord defects. Unfortunately, no scientific litera- ference and the small dogs’ inability to view the tail.
ture is available on this topic, and the extent of this Results of this study indicated that social communica-
problem is currently unknown. tion in dogs relies on proper observation of tail sig-
Individuals disagree as to whether there is pain naling, suggesting that tail docking may impair social
associated with tail docking. When asked about the communication in dogs.
degree of pain associated with tail docking in pup- Collectively, the available evidence suggests that
pies, 82% of dog breeders sampled in Australia indi- tail docking is unnecessary as a routine procedure to
cated “none” or “mild.”6 In contrast, the majority of prevent injury, particularly in nonworking companion
veterinarians (76%) reported the associated pain to dogs; that it causes short-term pain and has the po-

JAVMA • Vol 248 • No. 2 • January 15, 2016 163


tential to cause long-term neuropathic pain in some cations and animal welfare issues will arise if the pro-
animals; and that it impairs social communication, cedure is done by unqualified individuals who are not
which could lead to increased negative interactions veterinarians and do not have access to appropriate
with other dogs. facilities, anesthetics, and analgesics.26

Ear cropping Dewclaw removal


In dogs, ear cropping involves reshaping the ap- In dogs, the dewclaws represent the vestigial first
pearance of the external ear, usually by removing up digits of the forelimbs and, occasionally, hind limbs.27
to half of the caudal portion of the pinna (auricula). Some breeds, such as the Great Pyrenees, Bauceron,
Following removal of the pinna, the ears are taped and and Norwegian Lundehund, have double dewclaws on
splinted to facilitate healing in the desired shape. This each of the hind limbs.28 Dewclaw removal is typically
procedure is typically performed when puppies are performed within the first few days after birth, usually
between 9 and 12 weeks old, after they have received without anesthesia or analgesia,29 but it may also be
their initial vaccinations.20 Most often, dogs are anes- performed later in life (eg, when the dog is spayed or
thetized during the procedure and may or may not be neutered).30 Sedation and local anesthesia are recom-
given analgesics afterward. mended when performing this procedure on young
Historically, ear cropping was performed to pre- puppies, and general anesthesia is recommended for
vent ear damage during hunting or fighting, and some older animals.31
proponents of ear cropping continue to suggest that The main argument in support of dewclaw re-
cropping is necessary to prevent accidental tearing moval is that it prevents injuries associated with ac-
of pendulous ears, particularly in hunting dogs. How- cidental tearing of the dewclaws.29 While the forelimb
ever, there is no evidence to support these claims, and dewclaws are typically attached by bone, the hind
many working breeds, such as spaniels and retrievers, limb dewclaws are often attached only by skin, which,
have naturally pendulous ears. It has also been sug- some have suggested, makes them prone to catching
gested that ear cropping reduces the risk of ear infec- and tearing. Furthermore, because there is no wear of
tion, as a result of less trapping of moisture and debris the associated nail, regular trimming is required to re-
in the ear canal.21 While there is some evidence to sug- duce the chances of the nail being caught. However, to
gest that dogs with pendulous ears have a higher risk date, no research is available to determine the actual
of otitis externa, compared with dogs with erect ears, incidence of dewclaw tearing, so the true scope of this
it appears that specific breeds tend to have a higher problem is unknown.
predisposition than others regardless of ear conforma- To our knowledge, the impact of dewclaw remov-
tion.22,23 For example, 1 study found that otitis externa al on the welfare of dogs has not been researched. As
is more common in Cocker Spaniels, Poodles, and Ger- with any surgery, there is the potential for acute and
man Shepherd Dogs,24 and another found a higher chronic pain, but the severity of the pain is unknown.
prevalence in Golden Retrievers and West Highland
White Terriers.23 None of these breeds traditionally Declawing
have their ears cropped, and their natural ear position Declawing (onychectomy) is an elective surgi-
varies between hanging and erect. At least 1 textbook cal procedure that involves removal of the claws
on veterinary surgery25 no longer includes detailed in- through amputation of all or part of the distal pha-
formation on ear cropping in dogs because of ethical lanx. Several variations of the procedure have been
concerns associated with the procedure, with the au- described, including removal of the entire distal pha-
thors indicating their support for the AVMA position lanx with a scalpel or surgical laser and removal of
statement against this procedure. all or most of the distal phalanx with a nail clipper.32
To the best of our knowledge, there are no pub- Removal of the distal phalanx with a surgical laser
lished studies on whether ear cropping results in appears to be the quickest procedure and is associat-
acute or chronic pain in dogs, although given the ed with lower levels of postoperative stress and pain
length of the resulting wound, it is clear that the pro- than removal with a scalpel.33 However, it has also
cedure results in some level of acute pain. However, been associated with a higher number of postopera-
information is lacking on common anesthetic and an- tive complications in the days following the proce-
algesic practices for dogs undergoing ear cropping. In dure.33 Transection of the tendons of the deep flexor
addition, we are not aware of any studies on whether muscle (ie, tendonectomy) is sometimes performed
alterations in ear conformation influence communica- as an alternative to onychectomy, as it prevents ex-
tion with humans or other dogs. tension of the claws and results in fewer signs of
Importantly, ear cropping is no longer taught at pain.34 Both onychectomy and tendonectomy should
colleges of veterinary medicine in the United States. be performed only by veterinarians with appropriate
Thus, veterinarians performing this procedure in the anesthesia and postoperative analgesia.
future will largely be self-taught,26 particularly as vet- Declawing is usually performed to prevent
erinarians experienced with this procedure retire. scratching-related injuries to people and damage to
Some veterinarians have justified performing this property. Recent surveys35,36 of veterinarians indi-
procedure because of concerns that serious compli- cate that aggression and property destruction due to

164 JAVMA • Vol 248 • No. 2 • January 15, 2016


scratching are frequent behavior problems reported cats, butorphanol-treated cats had higher analgesia
by cat owners. Scratching of people and other animals scores during the first 24 hours after surgery. Further-
is undesirable because of the potential for injury and more, according to owner reports, butorphanol-treat-
infection, particularly in people who are immuno- ed cats were more likely to eat and act normally and to
compromised. In some cases, this scratching may be have lower lameness scores during the first day after
intentional and related to aggression, but in others it discharge. Cloutier et al45 found that even when cats
is unintentional during play and handling. There ap- were treated with butorphanol before surgery, they
pears to be a relatively high prevalence of aggression had evidence of postoperative pain, as determined by
in owned cats, with recent research suggesting 36% comparison with control cats that underwent a sham
of cats display aggression toward their owners37 and procedure. Both of these studies involved removal of
almost 50% of cats display aggression toward either the distal phalanx with a scalpel or clipper, but recent
familiar or unfamiliar people.38 However, although de- studies assessing the effect of laser removal suggest
clawing will prevent scratching-related injuries, it is that this procedure also results in postoperative pain,
unlikely to resolve the problem of aggression in gener- although to a lesser degree than that associated with
al owing to the potential for cats to bite as an alterna- other methods. Clark et al46 found that cats that under-
tive to scratching. More research is needed to identify went laser onychectomy were less reluctant to jump
means to prevent aggression-related behaviors by cats after surgery than were cats in which onychectomy
toward their owners. was performed with a scalpel or clipper. Similarly,
Scratching items in the environment is a normal Holmberg and Brisson47 compared pain scores dur-
behavior that serves a number of functions for cats, ing the 10 days following onychectomy with either
including territorial marking and nail conditioning.39 a scalpel or a laser and found that both groups had
Farm cats have been reported to scratch between 1 elevated pain scores during the first 9 days but that
and 6 times a day. Scratching behavior is driven almost the mean score over the first 7 days was higher for the
entirely by the presence of conspecifics39 but is still scalpel group, compared with the laser group. Finally,
present in cats housed singly in homes.Although it is a Robinson et al33 assessed limb function by measur-
normal behavior, environmental scratching is general- ing ground reaction forces following laser or scalpel
ly deemed to be undesirable by owners because it can onychectomy and found that forces were reduced in
lead to property damage.While recent estimates of the both groups following surgery, but the reduction was
prevalence of environmental scratching are unavail- greater in the scalpel group.
able, 2 older studies40,41 suggest that 15% to 25% of Researchers have also studied the pain associat-
cats show inappropriate scratching of property, with ed with tendonectomy versus onychectomy, but dif-
one of these studies40 indicating that scratching might ferences between the procedures are unclear. While
increase the risk of cat relinquishment. Although de- 1 study48 found that tendonectomy resulted in lower
clawing is 1 method of preventing scratching dam- pain scores, compared with onychectomy, during the
age, there are alternative methods that do not involve first 24 hours after surgery, another study45 found no
surgery. For example, owners can provide appropriate differences in pain scores when comparing the 2 pro-
outlets for scratching and trim their cats’ nails regular- cedures. Jankowski et al48 reported differences in post-
ly. Therefore, when this procedure is requested, every operative complications associated with the 2 proce-
effort should be made to educate and assist owners of dures. Of 18 cats that underwent onychectomy, 1 had
cats to pursue possible alternatives that could allevi- severe postoperative pain and another had long-term
ate the need for surgery. lameness. Of 20 cats that underwent tendonectomy,
The National Council for Pet Population has esti- 1 had long-term lameness, but owners of 6 cats ex-
mated that approximately 14.4 million of the 59 mil- pressed dissatisfaction with the procedure because of
lion cats in the United States are declawed.42 Similarly, continued scratching and issues with claw growth and
a recent study43 reported that 20% of cats admitted trimming.
in the Raleigh, NC, area had undergone declawing Although both onychectomy and tendonectomy
or, more specifically, onychectomy. Interestingly, the have the potential to cause acute postoperative pain,
percentage of cats that are declawed has apparently it is likely that a multimodal analgesic approach will
not changed in the past decade despite the growing provide adequate pain control. Although a review of
controversy surrounding the procedure.43 In a survey all studies assessing efficacy of analgesic regimens for
conducted by Yeon et al,34 cats reportedly continued control of postoperative pain following onychectomy
to make scratching movements following declawing, and tendonectomy is beyond the scope of the cur-
but 91% of owners surveyed had an overall positive rent discussion, we encourage future research to de-
attitude about the procedure, whether onychectomy termine which analgesic regimes are commonly used
or tendonectomy. in current veterinary practice and whether they are
Various studies44–47 have demonstrated that ony- sufficient.
chectomy causes postoperative pain in cats. For exam- A number of studies have assessed short-term
ple, Carroll et al44 examined postoperative pain in cats and long-term postoperative complication rates fol-
receiving either butorphanol or no analgesia following lowing onychectomy. Short-term postoperative com-
onychectomy and found that in comparison to control plications following onychectomy include pain and

JAVMA • Vol 248 • No. 2 • January 15, 2016 165


associated lameness, hemorrhage, swelling, infection, degree.54 As a result, some owners administer tranquil-
and changes in behavior.48,49 Pollari and Bonnett50 izers after surgery.54
examined the risk of postoperative complications Excessive barking is seen as an undesirable behav-
when onychectomy was performed alone or in com- ior by owners and others affected by the barking and
bination with other surgeries and reported that cats reportedly increases the risk of relinquishment.55,56
that underwent onychectomy in combination with One study56 found that excessive barking accounts
ovariohysterectomy or castration were more likely for 11.3% of reported undesirable behaviors in dogs.
to have postoperative complications than were cats Alternatives to devocalization are typically aimed at
that underwent either procedure alone.This was par- addressing the underlying cause of the undesirable
ticularly concerning because 53% of cats underwent barking. Common causes of undersirable barking in-
both procedures. clude general anxiety, separation anxiety, and compul-
One common long-term complication of ony- sive disorders,57 and treatment by means of behavior
chectomy is claw regrowth, with rates reportedly modification with or without adjunctive medication
ranging from 3.4% to 15.4%, depending on the study should be attempted first. One study58 found that
and the method of claw removal.46,48,49 One study46 positive reinforcement training was effective at reduc-
found that claw regrowth was more common with use ing barking in response to someone knocking at the
of a nail clipper than with use of a scalpel or laser door, and dogs that are exercised more frequently are
(15.4% vs 6.5% and 3.4%). Other long-term complica- found to bark less than dogs that are not exercised.59
tions include persistent lameness and signs of chronic While there appears to be general agreement within
pain.46,48,49 Clark et al46 reported the highest rates of the veterinary behavior community that positive re-
pain-related complications, with up to 23% of cats inforcement is the most appropriate training method
having ongoing lameness and 42.3% of cats showing for dogs, barking is often treated through the use of
signs of pain on paw palpation. Owners have also re- methods that incorporate positive punishment. Both
ported long-term behavioral changes in cats following electric shock and citronella spray collars have been
onychectomy such as house soiling and an increased found to reduce the incidence of certain types of bark-
resistance to allowing the paws to be handled or an in- ing.60,61 However, the effectiveness of citronella spray
creased incidence or severity of biting, compared with collars is decreased when the collar is worn continu-
behavior before the procedure.51 ously, and a rebound effect (increased barking) is
Alternatives to declawing include regular nail frequently observed after the collar is removed.60 In
trimming and use of artificial nail caps to minimize addition, there are concerns that electric shock and
property damage and provision of appropriate citronella spray collars may cause fear and pain in
scratching surfaces such as scratching posts and sub- dogs. One study61 found no difference in serum cor-
strates.52 A study53 of 128 Italian cat owners found that tisol concentrations between dogs wearing electric
sexually intact male cats were more likely to scratch shock or citronella spray collars and control dogs.
other surfaces when a scratching post was absent However, another study62 found behavioral signs of
from the environment, and Cozzi et al39 reported that fear and stress in dogs in response to use of an electric
a feline interdigital semiochemical, a cat pheromone shock collar, including lowered posture, vocalizations,
replacement made of fatty acids, can be used to con- oral behaviors, and aggression toward the handler.62
trol excess behavioral scratching through placement In addition, when used improperly, electric shock col-
of this substance on a desired scratching location. lars can lead to burns and infections. Finally, in dogs
Behavior modification methods may also decrease en- with excessive barking, devocalization only removes
vironmental scratching. Given clear evidence of pain the manifestation of the problem (ie, the dog is no
and postoperative complications with declawing, this longer being able to bark) and does not address the
procedure should be considered as a last resort after underlying behavioral problem, which may be nega-
all other behavior modifying measures have been at- tively affecting the dog’s quality of life. Thus, in dogs
tempted and when the only other alternative is relin- with excessive barking, the underlying cause should
quishment or euthanasia. be identified and addressed before devocalization is
considered.
Devocalization A potential long-term complication of devocaliza-
In dogs, devocalization (ventriculocordectomy) tion in dogs is formation of a laryngeal web that ob-
involves complete or partial removal of the vocal folds structs airflow63 and may require corrective surgery.31
to prevent vocalization or reduce the intensity of vo- Laryngeal web formation occurs more commonly af-
calizations that are produced. The procedure can be ter devocalization through an oral approach, with clin-
done through an oral approach or by means of a lar- ical signs developing between 3 months and 3 years
yngotomy. Anecdotally, the oral approach appears to after surgery in 1 report.63
be more commonly used in clinical practice, although
laryngotomy is the recommended approach.54 Devo- Defanging
calization procedures vary in effectiveness, with great Defanging involves removal or reduction of the
variation among breeds.54 In particularly excitable canine teeth and can be performed in either puppies
dogs, increased airflow through the larynx following or adult dogs. Although this procedure should only be
devocalization can result in the ability to bark to some performed with appropriate dental techniques, it is,

166 JAVMA • Vol 248 • No. 2 • January 15, 2016


in some cases, performed by cutting or breaking the AVMA position statement on tail docking and ear
teeth near the gingival margin and may or may not cropping states that it “opposes ear cropping and tail
involve adequate anesthesia and analgesia.64 docking of dogs when done solely for cosmetic pur-
Defanging was originally developed to decrease poses.”68 The AVMA has also produced comprehensive
the danger captive wild animals posed to humans, literature reviews and fact sheets to support these
and similar justifications have been presented by ad- position statements. The CVMA has taken a stronger
vocates of this procedure in companion animals.65 stance by indicating that the organization “opposes
Although aggression can be a serious concern in cer- the alteration of any animal by surgical or other inva-
tain dogs, this procedure is not fully effective at reduc- sive methods for cosmetic or competitive purposes,”
ing the risks of biting injuries. Appropriate treatment which includes tail docking and ear cropping in dogs
of aggression should involve risk management and as well as cosmetic dentistry, tattooing, and piercing.69
treatment to reduce the behavior problem. Although Although these position statements are decidedly
research has not been conducted on pain and behav- against MUSs, they are ultimately only suggestions be-
ioral effects of defanging in companion animals, this cause these organizations have no enforcement ca-
procedure is considered unnecessary when trying pabilities. Indeed, veterinarians practicing in Canada
to prevent human-animal conflicts with exotic carni- and the United States are still able to perform these
vores and similar results can be predicted for compan- procedures at their own discretion, with a few excep-
ion animals.65 tions. In addition, anecdotal reports suggest that some
procedures, most notably tail docking, are performed
Legislation Related to MUSs by breeders without the assistance of a veterinarian.
It has been suggested that some veterinarians elect to
Some of the earliest legislation restricting MUSs
continue tail docking puppies in fear that failure to do
in dogs and cats was passed in the European Union
so will result in less qualified people, such as breeders,
in 1987, when the European Convention for the Pro-
undertaking the procedure without access to proper
tection of Pet Animals was implemented. This treaty
medical facilities and appropriate analgesics.2 This
prohibits any “surgical operation for the purpose of
modifying [the] appearance of a pet animal or for concern is supported by a study6 that found 51% of
other non-curative purposes,”66 which would include the breeders that were surveyed were performing the
procedure on their own.
tail docking, ear cropping, devocalization, declawing,
The CVMA position statement on cosmetic al-
and defanging. Veterinarians can make exceptions
terations also states that the association “strongly
to these prohibitions if the procedure is considered
encourage breed associations to change the breed
necessary for curative reasons or the benefit of a par-
standards” in the hopes that the number of dogs
ticular animal, or to prevent reproduction.66 However,
that are ear cropped and tail docked will decrease.69
regardless of the reason, all surgical operations must
Breed standards in Canada and the United States
be carried out by a veterinarian and under anesthesia
have changed to allow showing of dogs that have not
if the animal is believed to be in, or have the possibil-
undergone ear cropping or tail docking. This is like-
ity of being in, severe pain.66 Although this convention
ly to have reduced the number of dogs undergoing
was initially ratified by 4 member states in 1992, it is
these procedures, but relevant figures are not avail-
noteworthy that as of 2014 some members of the EU
able. Although the Canadian Kennel Club and Ameri-
had yet to ratify it. In some of the countries that have
can Kennel Club do not encourage these procedures,
not yet ratified the convention, alternative legislation
they also do not specifically discourage them. The
restricts at least some of these procedures. For exam-
American Kennel Club, for instance, states that it
ple, in the United Kingdom and the Netherlands, ear
endorses “acceptable practices integral to defining
cropping, tail docking, and declawing are restricted. In
and preserving breed character and enhancing good
addition, some countries, such as France, have ratified
health.”70
the convention but excluded tail docking from the list
The CVMA and AVMA also have position state-
of prohibited procedures.67
ments against MUSs used primarily for behavioral
Many additional countries have incorporated
modification, including declawing, devocalization, and
MUSs into their animal welfare legislation, but rec-
removal or reduction of the teeth.52,69,71,72 For exam-
ommendations vary by country. For example, de-
ple, the CVMA position statement on onychectomy
clawing, ear cropping, and tail docking are restrict-
of domestic cats states that the association “strongly
ed in Australia and Israel; declawing, devocalization,
discourages onychectomy of domestic cats for routine
and ear cropping are restricted in New Zealand; and
purposes” as it “prevents cats from expressing nor-
tail docking and ear cropping are restricted in Bra-
mal behaviors and causes pain.”52 The AVMA position
zil. We are not aware of legislation in any countries
statement echoes this message and encourages client
that restricts surgical removal of the dewclaws in
education and other preventive measures be taken be-
dogs.
fore declawing is considered. Similar suggestions for
attempts at behavioral modification to prevent the
Current Status in North America problem behavior are included in the devocalization
Both the CVMA and AVMA have a number of po- position statements of both the CVMA and AVMA.
sition statements regarding MUSs. For instance, the However, for each of these position statements there is

JAVMA • Vol 248 • No. 2 • January 15, 2016 167


little guidance as to what attempts at alternative strat- also prohibited in 4 other US states, unless medically
egies are sufficient to justify the need for these pro- necessary. In addition to state-level restrictions, mu-
cedures. Thus, owners with a lower tolerance for be- nicipalities have in some cases implemented bylaws
havioral problems may elect to pursue them without restricting MUSs in animals. For example, declawing
first attempting alternative strategies.42 Notably, pur- is banned in a number of municipalities throughout
suing alternative strategies to correct behavior prob- California.
lems related to scratching, aggression, and barking can While veterinary organizations in North America
involve substantial time, expertise, and expense, and have been clear about discouraging various MUSs
owners may not be willing to invest their resources in through the publication of position statements, their
alternative strategies when a surgical option is avail- role to date has been relatively passive. In contrast, the
able. Some have argued that if these procedures were Australian Veterinary Association actively called for a
unavailable, such owners might opt for relinquish- ban on tail docking in dogs starting in 2008,77 which
ment or euthanasia. However, many veterinary clinics was in part responsible for passage of national legisla-
offer declawing of kittens in conjunction with spaying tion banning this procedure. This legislation ensures
or neutering as a preventive measure when scratching that no persons in Australia, including nonveterinar-
behavior is not yet a concern.Thus, further discussion ians, can perform this procedure. We would suggest
among stakeholders to determine how best to balance that there may be value in veterinarians in Canada and
these ethical tradeoffs with an aim toward reducing the United States taking a similar stance in suggesting
the number of these procedures being performed is formal legislation as a method of reducing the number
needed. of MUSs in dogs and cats.
The role of national veterinary organizations such
as the CVMA and AVMA in reducing the number of
MUSs that are performed should not be underestimat- Public Attitudes Toward
ed. In some cases, their position statements have been MUSs in Dogs and Cats
incorporated into regulations initiated by provincial
or state regulatory bodies to restrict veterinarians Community consensus regarding right and wrong
from performing these surgeries. For instance, restric- governs the actions of society, which then forms
tions on veterinarians performing ear cropping and, policies and laws.78 Challenges arise when there is
in some cases, tail docking have been incorporated disagreement among stakeholders, preventing a con-
into the bylaws of veterinary organizations in 6 Cana- sensus from being reached. This is the case for many
dian provinces (British Columbia, Manitoba, Saskatch- MUSs, in that stakeholders differ in what they consid-
ewan, Newfoundland and Labrador, New Brunswick, er to be acceptable. Given the distributed authority
and Prince Edward Island).73 However, these restric- governing companion animal welfare regulations and
tions do not apply to nonveterinarians who may be legislation in Canada and the United States, it is not
performing tail docking and dewclaw removal outside surprising that leadership comes in large part from
of a clinic environment. Newfoundland and Labrador the CVMA and AVMA, in combination with the Cana-
is the only Canadian province that has incorporated dian and American kennel clubs and specific breed
MUSs into formal legislation. In this province, the An- associations. Equally disconcerting is that despite the
imal Health and Protection Act was passed in 2010, American Kennel Club stating that unaltered dogs will
banning ear cropping in dogs for the purposes of con- not be disqualified when entered into competitions,79
forming to breed standards.74 Additionally, this prov- many owners believe that failure to comply with tradi-
ince has bylaws that prohibit docking of tails in all tional breed standards will reduce their dogs’ chances
animals except when medically necessary. of winning. Some organizations have argued that ban-
A number of similar bylaws have been created in ning these procedures is a violation of an individual’s
some states within the United States, many of which rights. For example, the United Kingdom–based Coun-
are based in principle on the AVMA guidelines. Four- cil of Docked Breeds campaigns to protect the own-
teen states restrict tail docking in some species; how- er’s right to choose tail docking as an option, argu-
ever, only Maryland and Pennsylvania restrict tail ing that legislating these practices removes a person’s
docking of dogs.75 In Pennsylvania, this restriction is freedom of choice.80
for unqualified persons performing the procedure af- Social distance is defined as the emotional, psycho-
ter 5 days of age, but veterinarians can perform the logical, and physical distance between one individual
surgery regardless of age.75 Legislation restricting ear and another, typically 2 humans.81 In the past few de-
cropping of dogs is the most common in the United cades, the social distance between humans and com-
States, with 9 states having restrictions. In the case of panion animals has decreased drastically. This likely
Washington State, ear cropping is permitted when in accounts for the change in attitudes regarding what is
line with good husbandry practices.75 After the CVMA acceptable versus unacceptable in relation to animal
released a position statement in 2009 that “discour- treatment, with the effect that practices that were once
ages devocalization of dogs unless it is the only alter- seen as being acceptable are now questioned.81 In
native to euthanasia,” and the AVMA released a similar some cases, language choice can be used to influence
statement 4 years later, a law was passed in Massachu- stakeholders and evoke emotion, a strategy commonly
setts that banned this procedure.76 Devocalization is used by animal rights advocates, who employ words

168 JAVMA • Vol 248 • No. 2 • January 15, 2016


such as oppression, suffering, and cruelty to appeal 2. Bennett P, Perini E.Tail docking in dogs: can attitude change be
to human emotion.82 In other cases, euphemisms can achieved? Vet J 2003;81:277–282.
3. Root Kustritz MV. Effects of surgical sterilization on canine and fe-
be used to increase social distance and decrease em- line health and on society. Reprod Domest Anim 2012;47:214–222.
pathy. Both the CVMA and AVMA have acknowledged 4. Hart B, Hart L,Thigpen A, et al. Long-term health effects of neu-
these potential concerns in their position statements tering dogs: comparison of Labrador Retrievers with Golden
regarding declawing and devocalization by stating that Retrievers. PLoS ONE 2014;9:e102241.
5. Broughton A. Cropping and docking: a discussion of the con-
owners must be educated with regards to the poten- troversy and role of law in preventing unnecessary cosmetic
tial alternatives, the details of the procedure to be per- surgery in dogs. Available at: www.animallaw.info/article/
formed, and the potential risks. However, there are no cropping-and-docking-discussion-controversy-and-role-law-
data available to determine how often these conversa- preventing-unnecessary-cosmetic. Accessed Nov 28, 2014.
tions between veterinarians and owners occur or what 6. Noonan GJ, Rand JS, Blackshaw JK, et al. Tail docking in dogs:
a sample of attitudes of veterinarians and dog breeders in
effect they have on the owner’s willingness to proceed Queensland. Aust Vet J 1996;73:86–88.
with the procedure. Further research in this area is 7. Weber GH, Morton JM, Keates H. Postoperative pain and periop-
critical to accurately gauge current societal views on erative analgesic administration in dogs: practices, attitudes and
MUSs in dogs and cats. beliefs of Queensland veterinarians. Vet J 2012;90:186–193.
8. Landsberg G, Hunthausen W, Ackerman L. Behavior problems
Conclusions 9.
of the dog & cat. 3rd ed. St Louis: Saunders Elsevier, 2012.
Diesel G, Pfeiffer D, Crispin S, et al. Risk factors for tail injuries
in dogs in Great Britain. Vet Rec 2010;166:812–817.
We strongly believe that in a clinical setting, surgi- 10. Cameron N, Lederer R, Bennett D, et al. The prevalence of tail
cal procedures should be performed on animals only injuries in working and non-working breed dogs visiting vet-
if they have or can be expected to have clear benefits erinary practices in Scotland. Vet Rec 2014;174:450.
for the animal or the population as a whole. At a mini- 11. Lederer R, Bennett D, Parkin T. Survey of tail injuries sustained by
mum, the procedures discussed in the present review working gun dogs and terriers in Scotland. Vet Rec 2014;174:451.
12. Hytonen MK, Grall A, Hedan B, et al. Ancestral t-box mutation
all cause some degree of acute pain and are associated is present in many, but not all, short-tailed dog breeds. J Hered
with some risk of infection or other adverse effects. 2009;100:236–240.
Society’s attitudes toward dogs and cats have changed 13. Cattanach B. Bobtail Boxers. Available at: bobtailboxers.com/
over time, likely because of decreased social distance, the-cross-corgi-ex-boxer. Accessed Mar 15, 2015.
with the result that attitudes toward certain proce- 14. Noonan GJ, Rand JS, Blackshaw JK, et al. Behavioural observa-
tions of puppies undergoing tail docking. Appl Anim Behav
dures that were once considered acceptable are now Sci 1996;49:335–342.
being reconsidered. In many countries, discussions 15. Wansbrough R. Cosmetic tail docking of dogs. Aust Vet J
among broad ranges of stakeholders have resulted in 1996;74:59–63.
legislation banning surgical procedures that are con- 16. Gross T, Carr S. Amputation neuroma of docked tails in dogs.
sidered elective or unnecessary. Vet Pathol 1990;27:61–62.
17. Eicher SD, Cheng HW, Sorrells AD, et al. Short communication:
People are willing to acknowledge that animals behavioral and physiological indicators of sensitivity of chron-
experience pain but do not always appear to be will- ic pain following tail docking. J Dairy Sci 2006;89:3047–3051.
ing to take appropriate action to treat or prevent 18. Jensen T, Nikolajsen L. Phantom pain and other phenomena
that pain.83 This appears to be true in the case of the after amputation. In: Wall P, Melzack R, eds. Textbook of pain.
4th ed. Edinburgh: Churchill Livingstone, 1999;799–814.
procedures discussed in the present review, which
19. Leaver S, Reimchen T. Behavioural responses of Canis famil-
are known to be painful but are still commonly per- iaris to different tail lengths of a remotely-controlled life-size
formed.84 We recommend the following strategies dog replica. Behaviour 2008;145:377–390.
for enacting change in Canada and the United States 20. Henderson R, Horne R. The pinna. In: Slatter D, ed. Small ani-
with regards to MUSs in dogs and cats. First, further mal surgery. 2nd ed. Philadelphia: Saunders Elsevier Science,
1993;1545–1559.
research and education are needed on effective meth- 21. Rosser E. Causes of otitis externa. Vet Clin North Am Small
ods for preventing or treating the underlying behavior Anim Pract 2004;34:459–468.
problems that traditionally have resulted in declaw- 22. Hayes HM Jr, Pickle LW, Wilson GP. Effects of ear type and
ing, devocalization, and defanging. Second, further weather on the hospital prevalence of canine otitis externa.
research on public attitudes toward MUSs is needed; Res Vet Sci 1987;42:294–298.
23. Lehner G, Sauter Louis C, Mueller R. Reproducibility of ear cy-
specifically, understanding the beliefs and values held tology in dogs with otitis externa. Vet Rec 2010;167:23–26.
by the public must be a priority, as only then will it be 24. Fernandez G, Barboza G, Villabos A. Isolation and identification
possible to encourage policy and legislation that ac- of microorganisms present in 53 dogs suffering from otitis ex-
curately reflect the views of current society.Third, vet- terna. Rev Cient 2006;16:23–30.
erinarians should take a leadership role in educating 25. Henderson R, Horne R. The pinna. In: Slatter D, ed. Textbook
of small animal surgery. Vol 1. 3rd ed. Philadelphia: Saunders
both owners and the broader public on the important Elsevier Science, 2003;1737–1746.
topic of MUSs in dogs and cats. 26. Crook A. Cosmetic surgery in North America and Latin Amer-
ica, in Proceedings. World Small Animal Veterinary Association
References 27.
World Congress 2001; 54–55.
Ciucci P, Lucchini V, Boitani L, et al. Dewclaws in wolves
1. Columella LJML. L Junius Moderatus Columella of husband- as evidence of admixed ancestry with dogs. Can J Zool
ry. In twelve books: and his book concerning trees. Translat- 2003;81:2077–2081.
ed into English, with several illustrations from Pliny, Cato, 28. Park K, Kang J, Park S, et al. Linkage of the locus for canine
Varro, Palladius, and other ancient and modern authors. dewclaw to chromosome 16. Genomics 2004;83:216–224.
London: A. Miller, 1745;335. 29. Savant-Harris M. Removal of dew claws. In: Canine reproduc-

JAVMA • Vol 248 • No. 2 • January 15, 2016 169


tion and whelping: a dog breeder’s guide. Wenatchee, Wash: and their owners in US pet-owning households. J Appl Anim
Dogwise Publishing, 2005. Welf Sci 2000;3:179–201.
30. Becker M. Does our puppy need his dewclaws? Available at: 56. Wells DL, Hepper PG. Prevalence of behaviour problems re-
www.vetstreet.com/dr-marty-becker/does-our-puppy-need- ported by owners of dogs purchased from an animal rescue
his-dewclaws. Accessed Nov 28, 2014. shelter. Appl Anim Behav Sci 2000;69:55–65.
31. Hedlund CS. Surgery of the integumentary system. In: Fossum T, 57. Stafford K. Training methods. In: Stafford K, ed. The welfare of
ed. Small animal surgery. 3rd ed. St Louis: Mosby, 2007;254–255. dogs. Dordecht, the Netherlands: Springer, 2007.
32. Hedlund CS. Surgery of the integumentary system. In: Fossum T, 58. Yin S, Fernandez E, Pagan S, et al. Efficacy of a remote-con-
ed. Small animal surgery. 4th ed. St Louis: Mosby, 2011;251–259. trolled, positive-reinforcement, dog-training system for modify-
33. Robinson DA, Romans CW, Gordon-Evans WJ, et al. Evaluation ing problem behaviors exhibited when people arrive at the
of short-term limb function following unilateral carbon diox- door. Appl Anim Behav Sci 2008;113:123–138.
ide laser or scalpel onychectomy in cats. J Am Vet Med Assoc 59. Flint E, Minot E, Stevenson M, et al. Barking in home alone suburban
2007;230:353–358. dogs (Canis familiaris) in New Zealand. J Vet Behav 2013;8:302–305.
34. Yeon SC, Flanders JA, Scarlett JM, et al. Attitudes of owners re- 60. Wells D. The effectiveness of a citronella spray collar in reduc-
garding tendonectomy and onychectomy in cats. J Am Vet Med ing certain forms of barking in dogs. Appl Anim Behav Sci
Assoc 2001;218:43–47. 2001;73:299–309.
35. Fatjo J, Ruiz-de-la-Torre J, Manteca X. The epidemiology of be- 61. Steiss J, Schaffer C,Ahmad H, et al. Evaluation of plasma cortisol
havioural problems in dogs and cats: a survey of veterinary levels and behavior in dogs wearing bark control collars. Appl
practitioners. Anim Welf 2006;15:179–185. Anim Behav Sci 2007;106:96–106.
36. de Souza-Dantas L, Soares G, D’Almeida J, et al. Epidemiology of do- 62. Schilder M, van der Borg J.Training dogs with help of the shock
mestic cat behavioural and welfare issues: a survey of Brazilian refer- collar: short and long term behavioural effects. Appl Anim Be-
ral animal hospitals in 2009. Int J Appl Res Vet Med 2009;7:130–137. hav Sci 2004;85:319–334.
37. Strickler B, Shull E.An owner survey of toys, activities, and be- 63. Mehl ML, Kyles AE, Pypendop BH, et al. Outcome of laryngeal
havior problems in indoor cats. J Vet Behav 2014;9:207–214. web resection with mucosal apposition for treatment of air-
38. Ramos D, Mills DS. Human directed aggression in Brazilian do- way obstruction in dogs: 15 cases (1992–2006). J Am Vet Med
mestic cats: owner reported prevalence, contexts and risk fac- Assoc 2008;233:738–742.
tors. J Feline Med Surg 2009;11:835–841. 64. CVMA. Cutting canine teeth in adult dogs, and deciduous teeth in
39. Cozzi A, Leucelle CL, Monneret P, et al. Induction of scratch- puppies. Available at: www.canadianveterinarians.net/documents/
ing behaviour in cats: efficacy of synthetic feline interdigital cutting-canine-teeth-in-dogs-and%20deciduous%20teeth-in-puppies.
semiochemical. J Feline Med Surg 2013;15:872–878. Accessed Mar 3, 2014.
40. Patronek GJ, Glickman LT, Beck AM. Risk factors for relin- 65. United States Department of Agriculture. Animal welfare: pol-
quishment of cats to an animal shelter. J Am Vet Med Assoc icy#3: veterinary care. Available at: www.aphis.usda.gov/ani-
1996;209:582–588. mal_welfare/policy.php?policy=3. Accessed Mar 6, 2014.
41. Heidenberger E. Housing conditions and behavioural prob- 66. Council of Europe. European convention for the protection
lems of indoor cats as assessed by their owners. Appl Anim of pet animals. Available at: conventions.coe.int/Treaty/en/
Behav Sci 1997;52:345–364. Treaties/Html/125.htm. Accessed Nov 28, 2014.
42. Patronek GJ.Assessment of claims of short and long term com- 67. Lefebvre D, Lips D, Giffroy JM. The European convention for
plications associated with onychectomy in cats. J Am Vet Med the protection of pet animals and tail docking in dogs. Rev Sci
Assoc 2001;219:932–937. Tech 2007;26:619–628.
43. Lockhart LE, Motsinger-Reif AA, Simpson WM, et al. Prevalence 68. AVMA. Ear cropping and tail docking of dogs. Available at:
of onychectomy in cats presented for veterinary care near Ra- www.avma.org/KB/Policies/Pages/Ear-Cropping-and-Tail-
leigh, NC and educational attitudes toward the procedure. Vet Docking-of-Dogs.aspx. Accessed Dec 15, 2014.
Anaesth Analg 2014;41:48–53. 69. CVMA. Cosmetic alterations.Available at: www.canadianveterinarians.
44. Carroll GL, Howe LB, Slater MR, et al. Evaluation of analgesia pro- net/documents/cosmetic-alteration.Accessed Nov 28, 2014.
vided by postoperative administration of butorphanol to cats un- 70. American Kennel Club. Canine legislation position statement.Avail-
dergoing onychectomy. J Am Vet Med Assoc 1998;213:246–250. able at: images.akc.org/pdf/canine_legislation/position_statements/
45. Cloutier S, Newberry R, Cambridge A, et al. Behavioural signs Ear_Cropping_Tail_Docking_and_Dewclaw_Removal.pdf.Accessed
of postoperative pain in cats following onychectomy of tenec- Nov 28, 2014.
tomy surgery. Appl Anim Behav Sci 2005;92:325–335. 71. AVMA. Welfare implications of canine devocalization. Available
46. Clark K, Bailey T, Rist P, et al. Comparison of 3 methods of ony- at: https://www.avma.org/KB/Resources/LiteratureReviews/
chectomy. Can Vet J 2014;55:255–262. Documents/Backgrounder-Canine%20Devocalization-Final.
47. Holmberg D, Brisson B. A prospective comparison of postop- pdf. Accessed Dec 1, 2015.
erative morbidity associated with the use of scalpel blades and 72. CVMA. Devocalization of dogs. Available at: www.canadianvet-
lasers for onychectomy in cats. Can Vet J 2006;27:162–163. erinarians.net/documents/devocalization-of-dogs#.UxT7yvm-
48. Jankowski AJ, Brown DC, Duval J, et al. Comparison of effects wKyI. Accessed Mar 3, 2014.
of elective tenectomy or onychectomy in cats. J Am Vet Med 73. The College of Veterinarians of Ontario. Medically unnecessary
Assoc 1998;213:370–373. veterinary surgery (“Cosmetic surgery”).Available at: www.cvo.
49. Tobias KS. Feline onychectomy at a teaching institution: a ret- org/CVO/media/College-of-Veterinarians-of-Ontario/Resources
rospective study of 163 cases. Vet Surg 1994;23:274–280. %20and%20Publications/Position%20Statements%20and%20
50. Pollari FL, Bonnett BN. Evaluation of postoperative complica- Guidelines/MUVSCosmeticSurgery.pdf.Accessed Nov 27, 2014.
tions following elective surgeries of dogs and cats in private 74. Newfoundland and Labrador.Animal health and protection act.
practices using computer records. Can Vet J 1996;37:672–678. Available at: www.assembly.nl.ca/legislation/sr/statutes/a09-1.
51. Landsberg G. Cat owners’ attitudes towards declawing. Anthro- htm#76_. Accessed May 15, 2015.
zoos 1991;4:192–197. 75. AVMA. State law governing elective surgical procedures. Avail-
52. CVMA website. Onychectomy (declaw) of the domestic felid.Avail- able at: www.avma.org/Advocacy/StateAndLocal/Pages/sr-
able at: www.canadianveterinarians.net/documents/onychectomy- elective-procedures.aspx. Accessed Nov 27, 2014.
of-the-domestic-felid.Accessed Nov 28, 2014. 76. The Commonwealth of Massachusetts. An act prohibiting devo-
53. Mengoli M, Mariti C, Cozzi A, et al. Scratching behaviour and calization of dogs and cats. Available at: malegislature.gov/Laws/
its features: a questionnaire-based study in an Italian sample of SessionLaws/Acts/2010/Chapter82.Accessed May 15, 2015.
domestic cats. J Feline Med Surg 2013;15:886–892. 77. Australian Veterinary Association. Surgical alteration to the natu-
54. Monnet E. Small animal soft tissue surgery. John Wiley & ral state of animals. Available at: www.ava.com.au/policy/31-
Sons, Inc, 2013. surgical-alteration-natural-state-animals.Accessed May 15, 2015.
55. New J Jr, Salman M, King M, et al. Characteristics of shelter- 78. Rollin B.Animal production and the new social ethic for animals,
relinquished animals and their owners compared with animals in Proceedings. Food Anim Well-Being Conf Workshop 1993;3–13.

170 JAVMA • Vol 248 • No. 2 • January 15, 2016


79. American Kennel Club. Frequently asked conformation ques- 82. Croney C.Words matter: implications of semantics and imagery in
tions. Available at: www.akc.org/events/conformation/faqs.cfm. framing animal-welfare issues. J Vet Med Educ 2010;37:101–106.
Accessed Feb 25, 2014. 83. Weary D, Niel L, Flower F, et al. Identifying and preventing pain
80. Council of Docked Breeds. Available at: www.cdb.org/. Ac- in animals. Appl Anim Behav Sci 2006;100:64–76.
cessed Mar 6, 2014. 84. Robertson SA, Lascelles BD. Long-term pain in cats: how much
81. Atwood-Harvey D. Death or declaw: dealing with moral ambi- do we know about this important welfare issue? J Feline Med
guity in a veterinary hospital. Soc Anim 2005;13:315–342. Surg 2010;12:188–199.

Correction: Compendium of Veterinary Standard Precautions for Zoonotic Disease Prevention


in Veterinary Personnel

In the report “Compendium of Veterinary Standard Precautions for Zoonotic Disease Prevention in Veterinary Personnel”
(J Am Vet Med Assoc 2015;247:1252–1277), several paragraphs at the end of Appendix 4 (Model infection control plan for
veterinary practices, 2015) were mistakenly omitted.The final sections of the appendix should read as follows:
OCCUPATIONAL HEALTH
Infection control and employee health management:The following personnel are responsible for
development and maintenance of the practice’s infection control policies, record keeping, and
management of workplace exposure and injury incidents.
Staff responsible: ______________________________________
Record keeping: Current emergency contact information will be maintained for each employee. Records
will be maintained on vaccinations, rabies virus antibody titers, and exposure and injury incidents. Changes
in health status (eg, pregnancy) that may affect work duties should be reported to and recorded by the
office manager so that accommodations may be made.
Pre-exposure rabies vaccination: All staff with animal contact must be vaccinated against rabies, followed
by periodic titer checks and rabies vaccine boosters, in accordance with the recommendations of the
Advisory Committee on Immunization Practices.
Tetanus vaccination:Tetanus immunizations must be up-to-date. Report and record puncture wounds, animal
bites, and other animal-related trauma. Consult a health-care provider regarding the need for a tetanus booster.
Influenza vaccination:Veterinary personnel are encouraged to receive the current seasonal influenza vaccine.
The CDC website and healthcare consultation will be used for guidance (www.cdc.gov).
Documenting and reporting exposure incidents: Report incidents that result in injury or potential exposure
to an infectious agent to: __________________________ Information will be collected for each exposure
incident using OSHA forms 301, 300, and 300A. Incident reporting includes documenting the date, time,
location, person(s) injured or exposed, vaccination status of injured person(s), other persons present,
description of the incident, whether health-care providers and public health authorities were consulted, the
status of any animals involved (eg, vaccination history, clinical condition, and diagnostic information), first aid
provided, and plans for follow-up.
Staff training and education: Infection control and hazard awareness training and education will be
documented in the employee health record.
Pregnant and immunocompromised personnel: Pregnant and immunocompromised employees are at
increased risk from zoonotic diseases. If you are concerned that your work responsibilities may put you
at increased risk, inform: _____________________ so that preventive measures may be taken (such as
increased use of PPE) and other accommodations may be made. Consultation between the supervising
veterinarian and a health-care provider may be needed.
ADDITIONAL INFORMATION
The following information is attached to the infection control plan:
• Emergency services telephone numbers—fire, police, sheriff, animal control, poison control, etc
• Reportable or notifiable veterinary diseases and where to report
• State department of agriculture or board of animal health contact information and regulations
• State and local public health contacts for consultation on zoonotic diseases
• Public health laboratory services and contact information
• Environmental Protection Agency–registered disinfectants
• Occupational Safety and Health Administration regulations
• Animal waste disposal and biohazard regulations
• Rabies regulations
• Animal control and exotic animal regulations and contacts
• Other useful resources
Note that a modifiable electronic version of the model infection control plan is available on the National Association of
State Public Heath Veterinarians website (www.nasphv.org).

JAVMA • Vol 248 • No. 2 • January 15, 2016 171


Perioperative Pain
Ma nagement in
Veterinar y Patients
Doris H. Dyson, DVM, DVSc

KEYWORDS
 Analgesia  Surgical pain  Dog  Cat

As veterinarians in the twenty-first century, we have an ethical responsibility to our


patients and clients to avoid, or at least to reduce significantly, pain in animals under
our care. The American Animal Hospital Association and the American Association of
Feline Practitioners have joined to promote an emphasis in veterinary medicine on
pain management.1 Although this mandate can be stretched to cover a range from
‘‘less than appropriate’’ management to ‘‘unnecessary extremes’’ in analgesia admin-
istration, this article attempts to define a safe, practical, and yet suitable approach to
management of pain in the perioperative period. Treatment for pain that approaches
either extreme should be addressed by observation and refinement, because exact
recipes do not suit all individuals, even animals that have undergone a similar proce-
dure. Veterinarians must use their best judgment related to a starting point (often
beginning with guidelines), monitor the patient’s response to such treatment, and
adjust accordingly. Clearly, the veterinarian’s role in pain management is not
complete after establishment of an analgesic plan.

ADJUNCTS TO PAIN MANAGEMENT

Usually, we think of analgesic drugs when the topic of pain management is mentioned,
but it is important to keep in mind the other aspects that contribute to successful pain
control. Anxiety, stress, and uncomfortable surroundings have an impact on the indi-
vidual ’s ability to handle pain. We recognize the comfort of our own bed in a quiet
home with loving people, familiar objects nearby, and appetizing food as significant
determinants in our overall feeling of well-being. Research has also shown that psy-
chologic and physical aspects have an impact on the achievement of pain control.2
Veterinarians may be able to reduce anxiety and uncomfortable surroundings with
simple actions. Noise, temperature, and light can be maintained at a more optimal
level for our patients. Quiet rooms can be defined to isolate the patient to keep it
from disturbing others or to provide a calmer environment for the more sensitive

Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph,


Ontario, Canada N1G 2W1
E-mail address: ddyson@ovc.uoguelph.ca

Vet Clin Small Anim 38 (2008) 1309–1327


doi:10.1016/j.cvsm.2008.06.006 vetsmall.theclinics.com
0195-5616/08/$ – see front matter ª 2008 Published by Elsevier Inc.
1310 Dyson

animal. Nursing care that includes provision of clean bedding, comforting words, pet-
ting, cuddling, and playing with the pet should contribute significantly to the manage-
ment of mild pain and supplement the pharmacologic treatment of more severe pain,
as has been reported in human infants.3 Many practices encourage family visits during
hospital stays to help reduce patient stress and gain insight on other interventions to-
ward analgesia for the individual involved. Further information on good nursing care for
surgical patients can be found in the article by Shaffron, Fagella, and Taylor elsewhere
in this issue.
Nonanalgesic pharmacologic approaches can also provide calming effects that in-
tensify the pain relief from specific analgesic drugs. This is the principle behind neuro-
leptanalgesia, which is able to provide better results than analgesia alone when minor
surgical procedures are required. Therefore, the use of sedatives and tranquilizers is
considered along with the administration of analgesic drugs, when appropriate.

ADVANCE APPLICATION OF ANALGESIA

Fentanyl patches require advance application to be effective for perioperative pain


management. Animals that are admitted the night before can have a patch placed if
this is an option for postoperative management. The advantage of this method is
achievement of a steady-state level of analgesia in 12 hours (cats) to 24 hours (dogs)
and lasting 72 hours. Fentanyl plasma concentrations vary significantly among individ-
uals, however, and it may not be possible to guarantee achievement of good analgesic
levels at the time of surgery. The impact of a fentanyl patch on inhalant requirements
during surgery has been estimated by minimum alveolar concentration (MAC) mea-
surement. A MAC reduction of 18% in cats4 and 37% in normothermic dogs is ex-
pected, with no significant MAC reduction in hypothermic (34.5 C) dogs.5 The
reduction in MAC in cats is not much different than after administration of butorphanol,6
and because hypothermia, which is commonly expected during longer and more pain-
ful surgical procedures, reduces the impact on MAC as well, further intramuscular opi-
oid administration in premedication should not cause concerns. If clinical signs of
opioid administration are apparent in advance of premedication (eg, panting, mild se-
dation), one may elect to give only half of the opioid dose planned. Further opioid can
be administered if needed during the operation. Many anesthetists believe that these
results and the safety associated with opioid use during surgery provide little reason
to reduce opioid doses significantly in the premedication period, however (Table 1).
Thus, the entire dose is usually used for premedication when fentanyl patches are used.
Some nonsteroidal anti-inflammatory analgesics (NSAIAs) may also be adminis-
tered in advance of premedication if there are no present or expected contraindica-
tions for use (see the article by Papich and the article by Mathews elsewhere in this
issue). This preoperative use may be a reasonable option to ensure analgesia at the
time of recovery if the operation is unlikely to be associated with excessive blood
loss or hypotension. A complete history from the owner and careful assessment of
the patient are critical to ensure that NSAIA use is actually safe, however, irrespective
of time of administration. For example, owners may administer aspirin to their pet and
yet not consider this when asked indirectly if the animal is on any medication. Related
to considering use before surgery, not all NSAIAs can be recommended. Carprofen,
meloxicam, and tepoxalin have been assessed and found to be safe in healthy dogs
when given in advance of anesthesia.7–10 Recommendations on timing of NSAIA
administration varies according to the route selected. If oral drugs are selected,
they are usually not given with premedication but at the last meal, although oral admin-
istration can result in a rapid effect similar to that achieved with intravenous dosing
Perioperative Pain Management 1311

(30–60 minutes). Research indicates that the achievement of maximum plasma con-
centrations is longer, and that onset of analgesia for acute synovitis is slower, after
meloxicam administration when compared with other NSAIAs,11 although clinical
experience associated with treatment of surgical pain shows an onset that is typical
of other NSAIAs. Subcutaneous administration of any NSAIA may result in a longer
onset, however.
The analgesic efficacy of NSAIAs has been documented for several surgical proce-
dures in dogs12–15 and cats,16–19 but this should not eliminate consideration of
additional analgesic drugs. Because no significant MAC reduction results from the
preoperative administration of NSAIAs,20,21 the addition of opioid analgesics can
provide this and other benefits, such as prevention of wind-up.

PREMEDICATION

Most surgical procedures performed in general practice are elective; thus, the patient
is presented without pain. The ideal approach to managing pain in these patients is to
prevent it, and this usually starts with the premedication analgesics. Other patients
presented for surgery may have accompanying pain and have analgesia on board
as discussed previously or may be receiving continuous rate infusions (CRIs; as dis-
cussed elsewhere in this article) according to the level of pain on admission to the hos-
pital. The anesthetist or practitioner must consider any present opioid effects at time of
presentation for surgery in addition to the impact of other drugs on board when decid-
ing on premedication requirements. If the analgesic administered during the preoper-
ative period is effective, it should never be assumed that the intraoperative and
postoperative pain is going to be managed equally as well. For some surgical proce-
dures, the pain may be less after surgery (eg, cervical disk surgery), whereas for
others, the pain may be greater during and after surgery (eg, most fracture repairs,
peritonitis).
Opioid analgesics are the most commonly selected drugs for perioperative pain pre-
vention or treatment. The specific drug selection and dose should be based on the level
of expected pain. Butorphanol or buprenorphine is appropriate for mild (to moderate)
pain (likely that involved in an ovariohysterectomy or castration performed by an expe-
rienced veterinarian). Buprenorphine has the advantage of a 6-hour duration of effect
compared with as little as 2 hours with butorphanol. Morphine or hydromorphone could
be selected for a longer effect as well, but low doses (eg, 0.2–0.3 mg/kg, 0.02–0.03 mg/
kg, respectively) may be more appropriate for milder pain. Occasionally the ‘‘harder to
handle’’ patient requires use of these more profound opioids at higher doses for the ad-
ditional sedating effect that they achieve; however, dysphoria and panting may be a dis-
advantage. It is important to keep in mind that elective surgery is not always associated
with mild pain. Surgical skill (ie, inexperienced) and patient condition (eg, severe obe-
sity) can change the expected pain level of a procedure. Onychectomy in a cat is an
elective procedure associated with a greater level of pain. Good analgesia has been
shown after administration of buprenorphine (0.01 mg/kg),22 although hydromorphone
(0.05 mg/kg) could also be chosen for premedication for such procedures. When other
surgical procedures are required that involve more extensive tissue trauma or take lon-
ger to perform (thus increasing inflammation from tissue handling), the m-agonists are
usually selected, and typical doses in dogs are 0.3 to 0.5 mg/kg and 0.03 to 0.05
mg/kg for morphine and hydromorphone, respectively, or fentanyl at a dose of 3 to 5
mg/kg. Extremely painful operations or those in which significant wind-up may be
present may require up to 1.0 mg/kg and 0.1 mg/kg, respectively, especially when
performed in smaller patients (surface area impact on drug dosing). Cats are safely
1312
Dyson
Table 1
Common analgesic drugs are listed with suggested doses and expected duration of effect based on various indications

Drug Indication Dose Duration


Buprenorphine Minor procedures (eg, castration, joint tap, laceration) 0.003–0.005 mg/kg 4–8 hours
Mild to moderate pain (eg, ovariohysterectomy) 0.005–0.1 mg/kg 4–8 hours
Butorphanol Minor procedures (eg, castration, joint tap, laceration) 0.1–0.2 mg/kg 3–6 hours
Mild to moderate pain (eg, ovariohysterectomy) 0.2–0.4 mg/kg 2–4 hours
Fentanyl Premedication or loading dose 2–10 mg/kg 15–20 minutes
Moderate pain associated with most orthopedic 2–5 mg/kg/h Infusion duration
procedures (eg, fracture repair, back surgery) 1 20 minutes
Moderate to severe pain associated with major surgery 3–10 mg/kg/h Infusion duration
(eg, thoracotomy, amputation) 1 20 minutes
Fentanyl patch Painful procedures that may benefit from extended Cats, dogs <10 kg: 25 mg/h 3–5 days
duration of effect (eg, declawing) or from steady 10–20 kg: 50 mg/h 3 days
level of underlying analgesia (eg, trauma surgery,
20–30 kg: 75 mg/h 3 days
orthopedic surgery) in association with other
analgesic techniques >30 kg: 100 mg/h 3 days
Hydromorphone Mild to moderate pain associated with straightforward 0.02–0.03 mg/kg 3–6 hours
abdominal surgery (eg, ovariohysterectomy) or
elective orthopedic surgeries (eg, dew claw removal)
Moderate pain associated with most orthopedic 0.03–0.05 mg/kg 3–4 hours
procedures (eg, cruciate surgery, declawing)
Moderate to severe pain associated with major surgery 0.05–0.1 mg/kg. (monitor for 3–4 hours
(eg, thoracotomy, amputation) hyperthermia in cats if high doses are given)
Ketamine Used as premedication (usually in combination) for Cat: 5–7 mg/kg 20–30 minutes
good restraint and somatic analgesia Dog: 3–5 mg/kg
Short-term analgesia 0.2–4 mg/kg 10–30 minutes
Analgesic infusion (usually with other drugs) 0.1–2 mg/kg/h Infusion duration
Ketamine with Used to supplement premedication effect 0.03–0.04 mL/kg 4–6 minutes
diazepam
(1:1 or 2:1)
Lidocaine Used in association with any induction for analgesia 2 mg/kg 5> 50–200 mg/kg/min Infusion duration
and MAC reduction; often given before induction (reduce dose in 1 hour or stop 20 minutes
and then infusion used before recovery)
Used in association with any induction for antiarrhythmic 2 mg/kg (twice in 10 minutes) 1 Infusion duration
effect, analgesia and MAC reduction; bolus often given 120 mg/kg/min (reduce dose in 1 hour)
before and after induction and then infusion used
Medetomidine Used as premedication in healthy animals for more Dog: 10–20 mg/kg 1–2 hours
profound restraint and associated analgesia Cat: 20 mg/kg
Supplementation of analgesia (and sedation) 1–2 mg/kg/h Infusion duration
Used immediately after surgery (in close association 1–2 mg/kg 0.2–0.5 hour
with extubation)
Meperidine Short-term mild to moderate analgesia for 5–10 mg/kg 0.5–2 hours
intramuscular use only
Morphine Mild to moderate pain associated with straightforward Dog: 0.2–0.3 mg/kg 3–4 hours
abdominal surgery (eg, ovariohysterectomy) or Cat: 0.2 mg/kg
elective orthopedic operations (eg, dew claw removal)
Moderate pain associated with most orthopedic Dog: 0.3–0.5 mg/kg 3–4 hours
procedures (eg, cruciate surgery, declawing) (not in cats)
Moderate to severe pain associated with major surgery Dog: 0.5–1 mg/kg 3–4 hours
(eg, thoracotomy, amputation) (not in cats)

Perioperative Pain Management


Nonsteroidal Possibly alone in mild to moderately painful
anti-inflammatory procedures and as supplementation of other
analgesics analgesia in moderate to severe pain
Loading dose is rarely needed in elective procedures
(without wind-up and less painful)
Injectable formulations are noted as follows:
Carprofen Cat: 4 mg/kg once >24 hours
Dog: 4 mg/kg/d 5> 2 mg/kg/d 12–24 hours
Ketoprofen (postoperative use only) 2 mg/kg/d 5> 1 mg/kg/d 24 hours
Meloxicam 0.2 mg/kg/d 5> 0.1 mg/kg/d 24 hours

Range noted relates to surface area adjustment or degree of effect required. A separate cat dose is noted when needed. An extended list of drugs and more detail
are found in this article and in the other article by Dyson elsewhere in this issue.

1313
1314 Dyson

premedicated with hydromorphone for procedures associated with moderate to severe


pain, using a starting dose of 0.05 mg/kg and considering that the duration of effect may
be longer in cats than in dogs. Caution related to use of high doses or early repeat dos-
ing is warranted to avoid hyperthermia (see section on preparation for recovery for more
detail). Fentanyl can also be used in the cat at similar doses as used in the dog. Mor-
phine, however, is rarely used at a dose higher than 0.2 mg/kg in the cat.
Ketamine is a somatic analgesic that may be added to the premedication. Telazol
contains tiletamine, another N-methyl-D-aspartate (NMDA) antagonist with similar
analgesic properties. Hyperalgesia associated with surgery in people seems to be
less with ketamine, and the requirement for postoperative analgesia is reduced.23,24
Ketamine is a useful premedication in cats (5–7 mg/kg), although it is more often
selected in those that are hard to handle. Although ketamine is rarely used in dogs
for premedication, evidence for incorporation as an intraoperative infusion is pre-
sented elsewhere in this article.
At the time of premedication, this author often administers sedatives to reduce anx-
iety from the handling involved (Table 2). Acepromazine is quite effective in most cats
and dogs. Even low doses can be helpful (0.01–0.02 mg/kg) when selected in the quiet
or older dog. Cats typically require a minimum of 0.05 mg/kg if an effect is to be
achieved by its addition to the premedication, whereas more may be required after
surgery to produce an improvement in analgesia (discussed in the section on prepa-
ration for recovery). The older cat or dog may be managed without acepromazine as
part of the premedication in most situations, however, with the option of adding this for
recovery if necessary. Compromised patients are best managed without using ace-
promazine. Preliminary evidence indicates that treatment of hypotension may be
more difficult when acepromazine is on board.25 Benzodiazepines (diazepam or mid-
azolam at a dose of 0.2 mg/kg) can produce an anxiolytic effect and are occasionally

Table 2
Drugs (dosages listed reflect combination use) that are useful in combination with some
of the analgesics inTable 1

Acepromazine Preoperative use in Cat: 0.05–0.15 mg/kg 3–4 hours


young healthy Dog: 0.02–0.05 mg/kg
animals
Preoperative use in Cat: 0.02–0.05 mg/kg 3–4 hours
geriatric patients Dog: 0.01–0.02 mg/kg
Immediate Cat: 0.02–0.05 0.5–2 hours
postoperative use (in Dog: 0.01–0.02
close association with
extubation)
Diazepam or Used with 0.2–0.5 mg/kg 10–20 minutes
midazolam premedication
Used intravenously in 0.2 mg/kg 5 minutes
association with
induction, during
surgery, or with
recovery
Propofol Used to supplement 0.5–1 mg/kg 2–3 minutes
premedication effect

These are typically used with opioids and have no analgesic properties but enable the analgesic to
be more effective because of the calming effect achieved.
Perioperative Pain Management 1315

selected in place of acepromazine in more critical patients when an additional sedative


effect beyond that of the opioid alone is desired. In most critical cases, however, it is
not necessary to include a benzodiazepine, because opioid use in these patients usu-
ally is associated with a good level of sedation.
a2-Agonists can also be used for analgesia and sedation in healthy dogs and cats.
Those animals showing any potential for cardiovascular compromise or organ dys-
function should not be given this class of drug because of its peripheral vasocon-
striction effects and depression of cardiac output. Medetomidine is the most
commonly used a2-agonist in small animals (5–20 mg/kg for dogs, 10–20 mg/kg for
cats). At these doses, one can expect significant MAC reduction and analgesia for
approximately 1 hour, although some animals show a more prolonged sedative ef-
fect. Low doses reduce the duration of cardiovascular depression rather than the
degree.26 During the postoperative period, microdoses (as discussed elsewhere in
this article) may be used, and such low doses (<2 mg/kg) have less effect on the car-
diovascular system.
NSAIAs can be administered at this time (if not given earlier) if no contraindications
exist, but it must be recognized that the full effect may not be present at the comple-
tion of short procedures. Patients need to be covered with other means of analgesia
for 30 to 60 minutes before an NSAIA is effective.

INDUCTION

Such drugs as opioids, ketamine, a2-agonists, or lidocaine may be components of the


induction protocol; as such, they result in analgesia at this time.
Only in critical cases do opioids facilitate induction (usually combined with diazepam
at a dose of 0.2 mg/kg). The opioid dose required is at the high end (hydromorphone at
0.05–0.1 mg/kg administered intravenously, fentanyl at a dose of 10–20 mg/kg
administered intravenously) and provides good analgesia, although respiratory de-
pression and bradycardia are to be expected. Fortunately, the associated negative
effects from opioids are managed easily with positive-pressure ventilation or anticho-
linergic administration. The higher doses suggested previously are more likely required
when minimal premedication or analgesia is on board in advance. Such patients are
often continued on opioid infusions (as described elsewhere in this article) to maximize
MAC reduction.
For the more common situations, ketamine is frequently used for induction, com-
bined with opioids, acepromazine, a2-agonists, or benzodiazepines. The dose used
for intravenous administration may have a short duration of analgesia, whereas typical
doses that are used intramuscularly, as often performed in cats, should provide some
analgesia for the duration of surgery. Nevertheless, it must be recognized that the an-
algesia associated with ketamine is more somatic than visceral, so further analgesia
may be required. Teletamine (in Telazol) would have similar effects.
a2-Agonists may be administered intramuscularly with ketamine to achieve induc-
tion. Postoperative analgesia was apparent after ovariohysterectomy in cats that
received ketamine and medetomidine intramuscularly for anesthesia.27 Comments
and concerns related to this combination are similar to those given for premedication.
It is important to recognize that although good analgesia is associated with these
drugs, the duration is limited to, and often less than, the sedative effect.28
Lidocaine is discussed in greater detail related to use in CRIs. A single dose (2 mg/kg)
should result in a short period of analgesia and MAC reduction. For this reason, it may
be used as part of the induction.
1316 Dyson

MAINTENANCE

Inhalants, propofol, and thiopental do not produce analgesia, although excessive


depth of anesthesia may allow painful procedures to be performed. These depths
are associated with significant respiratory and cardiovascular depression, however,
and wind-up is unlikely to be avoided. Thus, a more balanced method of anesthesia
is preferred.
Local anesthesia should be included in procedures in which a significant benefit is
possible. Digital (onychectomy), dental (extractions), intercostal (thoracotomy), epidu-
ral (hind limb fractures), and brachial plexus (forelimb fractures) blockade has been
used to improve intraoperative and postoperative analgesia in small animals. Readers
are referred to the articles by Lemke and Valverde elsewhere in this issue for details on
techniques.
Single-dose administration of any of the analgesics previously mentioned can be
performed as needed during maintenance of anesthesia. If the premedication dose
is waning or was poorly judged, another dose can be given to bring the level up to
what may be effective. For example, one may see that the hydromorphone effect is
not as good 2 hours into a procedure. At least half of the dose has been eliminated
by this time, and another half-dose could be given. Repeat dosing of long-duration
drugs (eg, hydromorphone) may be helpful during surgery but can create adverse
effects in recovery if the dose on board is greater than required when the animal is
recovering (ie, a full dose given at 2 hours may be beneficial for the surgery but results
in too high a dose at recovery). For this reason and others, CRI administration has
gained popularity. A CRI may be calculated as described under this topic elsewhere
in this article.
Epidural administration of morphine or hydromorphone may reduce further analge-
sia requirements for 12 to 24 hours. The analgesia effect has been measured as far
forward as the forelimbs and can be an excellent supplementation of analgesia for tho-
racotomy and peritonitis. More detail on this technique is found in the article by Valve-
rde elsewhere in this issue.
Morphine has also been placed intra-articularly to affect receptors directly in joints.
The evidence on its benefit is controversial,29,30 but the addition of local anesthetic is
effective and the technique is simple. Morphine (0.1 mg/kg) is added to bupivacaine
(approximately 0.1 mL/kg [0.5% solution]) and placed intra-articularly at time of joint
closure. With this technique and epidural administration, the dose of morphine is so
low that systemic side effects are not significant.
Patient monitoring is invaluable in assessing patient analgesia during surgery.
Increases in respiratory rate, heart rate, or blood pressure are typically noted when fur-
ther analgesia is necessary. It is necessary to ensure that ventilation is adequate, how-
ever, because an increase in pCO2 attributable to hypoventilation is a common
confounder associated with similar physiologic changes.

CONTINUOUS RATE INFUSIONS

The following discussion covers the use of CRI analgesia administration in the preop-
erative, intraoperative, and postoperative situations. There are several advantages to
this technique of administration in the management of pain. A steady level of analgesia
is more likely to be achieved, because the mountains and peaks associated with
intermittent analgesic use are avoided. A steady level is more likely to avoid significant
adverse effects and is more easily titrated to achieve continuous comfort. When cer-
tain procedures or periods of time require a greater level of analgesia, it can be
‘‘dialed’’ to effect. Although the benefit of steady-state pain relief is difficult to
Perioperative Pain Management 1317

measure, preemptive analgesia achieved in various ways has been shown to reduce
postoperative analgesia demand in a multitude of studies (339 papers displayed in
a recent search) ranging from local anesthetic31 to nonsteroidal32 and even inhaled
opioid use.33 Therefore, it is likely that our patients also reap such benefits with con-
tinuous analgesia control. Considering that infusions can be used during surgery, the
anesthetist and the patient can gain from the impact on inhalant requirements (MAC
reduction). Based on drug selection for these infusions, there may be other benefits
that arise (discussed under the section on specific infusions).
Anyone can administer a CRI if he or she is capable of giving fluid therapy to
a patient. A syringe pump is not required, although it is the simple way to manage
infusions, especially when frequent adjustment of the dose is required. An ordinary
fluid pump is usually capable of delivering drugs from a syringe, however. Test the
consistency of fluid administration of the pump at hand with a saline infusion (watching
the drips falling from an extension set) in advance of using this technique. If the con-
sistency is limited to higher rates, the analgesic can be diluted in a part of, or the entire,
hourly surgical or maintenance fluid to enable accurate administration. Only diazepam
cannot be diluted because of concerns about precipitation. Midazolam can be used
interchangeably with diazepam (same dosing recommendations would apply), and it
can be diluted in fluids or mixed with other analgesics without such concerns. If neither
a fluid pump nor a syringe pump is available, the use of a burrette inserted within the
fluid line enables drug administration in a smaller volume of surgical or maintenance
fluid (add analgesic to the volume to be given in 15–60 minutes). Another alternative
is to reduce the volume in a bag of fluids to that appropriate for the duration of admin-
istration (eg, 250 or 500 mL rather than 1000 mL) and to spike this remaining volume
with the expected drug requirement at the fluid rate to be administered. This last rec-
ommendation is more suitable for surgical patients than for awake patients, which
would be less tolerant of fluid volume adjustment. The volume during surgery would
be given at 10 mL/kg/h. A surgical fluid rate adjustment from 5 to 20 mL/kg/h could
be safe in most animals, however, and would allow analgesia dose modification
from half to double the starting point if deemed necessary. A second bag of fluids
would have to be connected should fluid requirements dictate an increase in rate,
as needed for blood loss correction.
Almost any analgesic can be adjusted to be given as an hourly rate by using the fol-
lowing calculation:[Effective Dose (mg)/Typical Duration of Effect (h)]
The calculation can be performed using pharmacologic data. For example, a dose
of morphine at 0.5 mg/kg is likely to provide 4 hours of pain relief in a dog. This pro-
vides an estimate of the dose per hour (0.125 mg/kg/h), which can usually be adjusted
as the effect is observed in the individual. In some situations, one might observe that
a dose of 0.5 mg/kg given to a particular dog provides only 3 hours of analgesia. The
calculation can use this clinical information to define the individual patient ’s infusion
guideline (0.17 mg/kg/h). Because there is a possibility of a reduced drug requirement
with the CRI method of administration, either calculation may result in an overestima-
tion of the dosage and require adjustment according to the patient ’s response. Similar
analgesic effects were observed in dogs administered half the dose as a CRI com-
pared with intermittent intramuscular injection of morphine.34 CRIs are usually limited
to drugs with a duration of effect of 6 hours or less.
It must also be recognized that an hourly rate maintains analgesia that was achieved
by an initial loading dose. As long as the expected duration of the loading dose is sim-
ilar to that of the infusion drug, it does not have to be the same drug. Also, a short-
duration drug like fentanyl can be easily used after a longer duration drug like
morphine. Analgesia needs may increase over the first 4 hours (morphine ’s expected
1318 Dyson

duration) if the pain involved remains constant. Careful observation of the patient
should indicate if this is the case. Because surgical pain may actually lessen over
the first 4 to 24 hours after surgery, changes in fentanyl infusion may not be required,
may be increased for only a few hours, or may actually decrease over time.
Veterinarians have several analgesic drug options for CRIs. Typically, an opioid is
chosen first (eg, morphine, hydromorphone, fentanyl) in awake patients or during
surgery. When a long-lasting opioid is on board during surgery (usually part of the pre-
medication), however, lidocaine may be the first drug selected as a CRI to improve
analgesia during surgery. The reasons for this are discussed elsewhere in this article.
Other infusions (eg, ketamine, medetomidine) are usually added when these options
alone are ineffective. These drugs are rarely selected alone for analgesia by CRI.
One analgesic cocktail (morphine, lidocaine, and ketamine [MLK]) has gained popular-
ity for surgery and is also discussed elsewhere in this article.

Opioid Continuous Rate Infusion


There are several reports on morphine CRI in dogs.34–36 Although a rapid intravenous
bolus of morphine is contraindicated because of histamine release,37 a slow intrave-
nous infusion can be used without concern. The doses that have been assessed range
from 0.12 mg/kg/h34 to 0.34 mg/kg/h.36 The analgesia produced varied from mild to
moderate. The higher dose resulted in plasma concentrations that were greater
than the previously suggested analgesia range but were not associated with signifi-
cant cardiovascular or respiratory side effects in healthy awake dogs. Because seda-
tion is apparent at the higher CRI, it should be safe to assume that in the awake animal,
undesirable central nervous system (CNS) depression would accompany any respira-
tory depression and provide a clue to overdosage. Sedation and mild hypothermia are
expected consequences of using opioids for analgesia in the awake animal. In the
anesthetized dog, bradycardia and respiratory depression are obvious, but both are
easily treated in this setting, as mentioned previously. A conservative dose range
for a morphine CRI may fall within the range of 0.12 to 0.25 mg/kg/h (corresponding
roughly to the effect from 0.5–1.0 mg/kg as an intermittent dose) for dogs. Fentanyl
is preferred in cats.
There are no published studies using hydromorphone as a CRI in dogs or cats. Con-
sidering the fact that the duration of effect tends to be similar to morphine and that
hydromorphone is 10 times as potent as morphine, however, one should be able to
extrapolate safely from the studies using a CRI with morphine. Thus, a dose range
of 0.01 to 0.03 mg/kg/h should be effective. In either case, a loading dose of morphine
from 0.3 to 1.0 mg/kg or a loading dose of hydromorphone from 0.03 to 0.1 mg/kg
would be given to achieve appropriate analgesia in advance of starting the CRI. Hy-
dromorphone, in contrast to morphine, is safe given rapidly intravenously at these
doses.38 The selected dose would vary with the procedure performed and the
expected pain associated with it, in addition to the individual patient. Smaller patients
would need a higher dose per kilogram than large dogs.
Fentanyl is presently the most popular opioid for CRI. The effectiveness and cardio-
vascular safety of this infusion in dogs have been reported.39,40 Its short duration of ef-
fect makes it suitable for administration by this method. The dose-related MAC
reduction and ceiling effect (42 mg/kg/h) from fentanyl CRI were first reported in
1982.41 Doses of 3, 12, and 42 mg/kg/h showed a MAC reduction of 20%, 44%, and
65%, respectively. Practical intraoperative administration involves a loading dose of
3 to 5 mg/kg followed by a CRI of 10 mg/kg/h. This infusion can be halved or doubled
based on the desired effect on the inhalant requirements. In rare critical cases in which
isoflurane must be extremely low, fentanyl (50 mg/mL] and midazolam (5mg/mL)
Perioperative Pain Management 1319

(10:1 as vol/vol) have been administered at 1 mL/kg/h (45 mg/kg/h 1 0.45 mg/kg/h,
respectively). High intraoperative infusions of fentanyl (>5 mg/kg/h) need to be lowered
in advance of recovery (approximately 20 minutes before the end of surgery). This
should reduce the chance of postoperative dysphoria. Infusions used in the awake
or recovering patient are usually 2 to 5 mg/kg/h, with doses as high as 10 mg/kg/h in
extremely painful conditions.
Butorphanol has also been used as a CRI at 0.1 to 0.4 mg/kg/h. This infusion would
be most appropriate for mild to moderate pain. A loading dose of 0.1 to 0.4 mg/kg
would be appropriate.
Practical evidence for use of opioid CRIs in cats is nonexistent. Analgesia has been
shown to be good after low-dose morphine administration (0.2 mg/kg),42 and MAC
reduction has been determined as significant at high (1.0 mg/kg) but not low (0.1
mg/kg) doses.6 Morphine as a CRI is not likely to be suitable in cats, however, because
of concerns for excitement with overdosing. If a m-agonist is required, fentanyl would
be the preferred drug because of its short duration of effect, thus reducing concerns
for overdosing and excitement. Low doses of hydromorphone as a CRI can be used in
the cat with assessment of effectiveness of the infusion, adjustment as needed, and
monitoring for hyperthermia, however. An infusion based on a 6-hour duration of
effect43 rather than 4 hours, unless proved otherwise by individual response, may
be a practical approach in cats (0.005–0.01 mg/kg/h). In general, butorphanol selec-
tion as a CRI would be a safe alternative for mild to moderate pain.

Lidocaine Continuous Rate Infusion


Lidocaine has been shown to reduce MAC in dogs, provide analgesia, and act as an
antiarrhythmic. It is an excellent choice in cases in which these benefits are of value
(eg, animals presented with gastric dilation/torsion, splenic tumors, chest trauma, car-
diac disease). Such critical patients can be induced with the addition of 2 mg/kg as
a bolus in advance of the induction agent, a second bolus of 2 mg/kg after intubation
and stabilization onto an inhalant, and a CRI started at 120 mg/kg/min (7 mg/kg/h). This
recommendation achieves immediate therapeutic levels for antiarrhythmic effects and
an expectation for a MAC reduction of approximately 43%. This approach is extrap-
olated from studies performed in normal and cardiovascular-compromised
patients.44,45 Plasma levels from this method are similar to those achieved in longer
than 30 minutes from a single 2-mg/kg dose followed by a 200-mg/kg/min (12 mg/
kg/h) CRI. This second method would be suitable for dogs with no evidence of cardio-
vascular compromise, arrhythmia concern (requiring an immediate antiarrhythmic
level), or possibly liver compromise (although lidocaine accumulation depends more
on flow than on liver function). It is a simple method for intraoperative MAC reduction
and analgesia in other cases (10 mg/kg/h simplifies calculations even more so with
likely little difference), however. Before recovery or after 1 hour in long surgical proce-
dures, the CRI should be reduced to 40 to 80 mg/kg/min (2–5 mg/kg/h) to reduce the
chance of mildly toxic plasma levels. The infusion can simply be stopped if not needed
for postoperative analgesia or arrhythmia management. At lower infusions, the MAC
may be reduced by approximately 20%. Analgesia can be achieved with as little as
1 to 3 mg/kg/h, however. The effective loading dose for analgesia in the awake patient
is similar to that during anesthesia (1–4 mg/kg).
Although MAC reduction has been measured in cats during lidocaine infusion, sig-
nificant cardiovascular depression has been shown.46 It has been suggested as an
analgesic in the awake cat at a loading dose of 0.25 to 1 mg/kg followed by a CRI
at 0.5 to 2 mg/kg/h.47 At the Ontario Veterinary College, however, the author and
her colleagues have no experience in this setting.
1320 Dyson

Ketamine Continuous Rate Infusion


Ketamine has been studied as a CRI in dogs and shown to provide an approximately
25% MAC reduction at 10 mg/kg/min (0.6 mg/kg/h).35 Intraoperative CRI administra-
tion is suggested at 2 to 10 mg/kg/min (0.1–0.6 mg/kg/h) after a loading dose provided
by ketamine in the induction or 2 mg/kg administered intravenously. At these doses,
MAC reduction and somatic analgesia are expected without evidence of significant
sympathetic drive. Doses between 0.1 and 2 mg/kg have been used for analgesia in
the postoperative setting when other analgesics alone are not effective. CNS depres-
sion, muscle rigidity, and sympathetic drive may occur with higher doses, depending
on coinciding drug use.

Morphine/Lidocaine/Ketamine Continuous Rate Infusion


A single report on the use of an MLK cocktail has been published.35 Analgesia and
MAC reduction are achieved with a mixture of morphine (12 mg), lidocaine
(150 mg), and ketamine (30 mg) in surgical fluid (500 mL) dripped at the standard
surgical fluid rate (10 mL/kg/h). This provides morphine at a rate of 4 mg/kg/min
(0.24 mg/kg/h), lidocaine at 50 mg/kg/min (3 mg/kg/h), and ketamine at 10 mg/kg/
min (0.6 mg/kg/h). The mixture produced the same MAC reduction (45%) and cardio-
vascular effects as morphine alone (same dose as in mixture). A multimodal approach
to analgesia was suggested as the benefit of this cocktail. This view may not be taken
by all anesthetists, however. If there is no measurable advantage, a simpler approach
may be more appropriate.48 The lack of benefit with the addition of ketamine along
with opioids during orthopedic surgery was similar35 to that shown in the study by
Muir and colleagues. This MLK cocktail is not simpler to use and shows no clear ad-
vantage when compared with using higher lidocaine infusions or opioid infusions.
Although no advantage has been shown at this point, it does not cause harm if mixed
properly and inhalant adjustments are made appropriately. For severe postoperative
pain, the concentrations of each drug in this mixture, and their combined potential
effect, are unlikely to confer adequate analgesia.

PREPARATION FOR RECOVERY

Appropriate analgesia should be achieved in advance of recovery. This may require


lowering or stopping infusions (as previously addressed), adding additional analgesics
(eg, NSAIAs delayed for concerns about hypotension or those only used for postop-
erative administration), or bringing single-dose opioid injections up to therapeutic
levels based on timing of last administration. There is no reason to avoid additional
opioids until after recovery if the patient is expected to require more than the level
on board. Delay in recovery associated with analgesia administration is more likely
attributable to poor drug or dose selection. Calculate the dose required to produce
the desired effect as described in the section on repeated intraoperative dosing during
maintenance, and administer just before turning off the inhalant. If the drugs on board
are likely to provide adequate analgesia, however, recovery can proceed with plans to
provide more analgesia only if the patient seems to need such.
Sedatives should be preemptively administered if thought to be useful in recovery.
The primary concern about acepromazine relates to intraoperative hypotension; how-
ever, a low dose in the premedication prevents this. Also, administration of low doses
(0.01–0.02 mg/kg) at recovery does not seem to affect blood pressure adversely at this
time. In hard-to-handle or stress-sensitive patients that were given acepromazine as
part of their premedication, additional dosing before recovery may be appropriate
to achieve significant sedation. The dose chosen depends on the residual
Perioperative Pain Management 1321

premedication dose effect expected, but 0.01 to 0.02 mg/kg in dogs and 0.02 to
0.1 mg/kg in cats are suggested. In some cases, medetomidine may be preferred
(1–2 mg/kg given as the patient is extubated). This is more likely to be chosen for
the extremely aggressive animal.

POSTOPERATIVE ANALGESIA

Need for further analgesia is assessed after recovery. The patient must be carefully
assessed to determine if excitement, whining, or agitation is pain, dysphoria, or disori-
entation. When in doubt, pain should be assumed, and the response to treatment
defines if this judgment was correct. When pain is suspected or clearly displayed,
rapid administration of hydromorphone, fentanyl, or butorphanol, as appropriate,
should be performed. Morphine must be given intramuscularly or slowly intravenously.
If necessary, propofol (0.5–1-mg/kg increments) can be used to return the animal to an
anesthetized state until morphine is fully effective. Diazepam (0.2 mg/kg administered
intravenously) is also effective in the short term to deepen the plane of sedation in
a recovering animal that is showing signs of pain and provides time for the opioid to
take effect. It is important to recognize that some dogs can become quite excited after
benzodiazepine administration in the fully awake animal requiring analgesia. The opi-
oid should always be given first in this circumstance.
Low doses of acepromazine (0.01–0.02 mg/kg for dogs, 0.02–0.05 mg/kg for cats)
can be given if an animal is appearing only mildly uncomfortable or mildly dysphoric.
Response to treatments (acepromazine or more opioid) may be the best method of
diagnosis when uncertain. Occasionally, the treatment selected may be a reversal
agent. If the patient is clearly dysphoric or returns to a whining state shortly after
additional opioid administration, or if suspicion exists related to the use of high doses
of opioid during surgery, a slow titration of naloxone can be given to effect (4 mg/kg
diluted to 10 mL and given in 1-mL increments every minute).
For the animal that is thrashing and difficult to assess, medetomidine (1–2 mg/kg)
can be helpful. Some analgesia is achieved, and when recovery occurs in 15 to 20 min-
utes, it is usually smooth if the initial recovery behavior was disorientation. This is an
excellent approach in the ‘‘husky syndrome,’’ wherein disorientation in this breed is
associated with dramatic behavioral responses that are difficult to differentiate from
pain.
After stabilization of the patient in an analgesic state at recovery, regular
assessment is required to maintain this comfortable state. The patient may need no
more analgesia, occasional single-dose injections of opioid, or CRI administration of
one or more drugs to manage the pain.

ADVICE FOR SPECIFIC CASES

Not every case can be considered in this article, but a few special situations are
discussed.

PEDIATRICS

Much evidence exists that human babies experience pain.49,50 Responses to typical
analgesics are not always as expected. A study in puppies revealed that newborn
pups have a reduced requirement for analgesia and that, overall, puppies may be
more sensitive to opioid-associated respiratory depression.51 By 1 month of age,
puppies have a significantly increased analgesic requirement. Based on this evidence,
we must not ignore analgesia but must be cautious to monitor the effects of it.
1322 Dyson

Our primary analgesic choices for these cases include opioids and local anesthesia.
Ketamine may be a consideration as well and seems to be a reasonable choice for
short procedures in human infants,52 although neonates may be less responsive to
NMDA antagonists and ketamine is thus ineffective in providing analgesia.53
Opioids alone provide good restraint and sedation in addition to analgesia. In most
situations, sedatives are not required in pediatric patients. The dose of opioid selected
for premedication in healthy pediatric patients is often at the higher end of the range
related to patient size, but redosing may be less frequent, and if profound sedation is
associated with doses given, lower doses should be chosen. In sick patients or those
younger than 1 month of age, low doses should be administered. The patient can be
induced with propofol, diazepam/ketamine, or mask inhalant and then maintained on
inhalant.
Local anesthesia is an excellent choice when possible. Eutectic mixture of local
anesthetics (EMLA) cream is effective for local analgesia if given 30 minutes to
penetrate the skin. The weight of the animal must be used to calculate a safe volume
of injectable local anesthesia (2% lidocaine or 0.5% bupivicaine at approximately 0.4
mL/kg). Dilution to half strength with saline can be performed to allow more volume
without risking toxicity. If laryngeal desensitization is performed, the use of 2% lido-
caine drops rather than the 10% spray reduces the lidocaine dose by this route, allow-
ing for a larger volume to be used in other specific local blockade.
NSAIAs are not recommended in patients younger than 8 weeks of age because of
their effect on kidney development.

COMMON ELECTIVE SURGICAL PROCEDURES

Premade mixtures containing meperidine or butorphanol for premedication provide


a low level of analgesia conferred by the opioid and are capable of producing
a short-term mild to moderate analgesic effect. These mixtures are also dosed at
the lowest end of the analgesic range, again making them most suitable for mild
pain. With this in mind, further analgesia is required in many situations. NSAIAs are
useful in these cases. In any elective procedure, the NSAIA loading dose (initial
dose as double the maintenance dose) is usually not needed. The approved dosing
of meloxicam at 0.3 mg/kg in cats (United States) is not recommended, because
a dose of 0.1 or 0.2 mg/kg (orthopedic procedures) is adequate. Effective analgesia
is common with use of the maintenance dose (0.1 mg/kg) for elective procedures, be-
cause wind-up is not established with any associated increased analgesic demands.
If, however, the animal seems to be slightly uncomfortable later in the evening, a sec-
ond dose can be given because this does not exceed label dosing.
Cat castrations are associated with mild pain and may not require more analgesia
than that in the premedication period, provided that the procedure is performed within
15 to 30 minutes of administration. The administration of an NSAIA is a responsible
approach to avoid any painful experience, however. Dog castrations should be man-
aged adequately with an NSAIA, even if administered postoperatively, given the same
conditions as for the cat. Ovariohysterectomies in dogs and cats may require an
additional opioid dose for recovery if the NSAIA is withheld until the operation is
over, however. The opioid dose should be calculated in the premedication period,
and additional opioid should be added during or after surgery to achieve a total
dose of butorphanol at 0.2 to 0.4 mg/kg or meperidine at 5 to 10 mg/kg. A more
profound opioid dosed at the lower end of the range may be selected as part of the
premedication (usually given with acepromazine), however. The use of NSAIAs for 1
to 3 days is a reasonable option for postoperative analgesia in these cases. If the
Perioperative Pain Management 1323

NSAIA is given 30 minutes or more before recovery, additional or more profound opi-
oid administration is less likely to be required. Onychectomy in cats is best managed
with buprenorphine or hydromorphone as part of the premedication and the addition
of local blocks using bupivacaine or a lidocaine-bupivacaine mixture in advance of
surgery (see the article by Lemke elsewhere in this issue). Postoperative NSAIA anal-
gesia is indicated for 2 to 3 days. This technique seems to be effective, although fen-
tanyl patches have also been applied for pain associated with the declawing
procedure. In this case, because the fentanyl patch usually is removed on discharge
and the effect quickly dissipates, analgesia can be continued with an NSAIA for 1 to 2
more days.

EMERGENCY CASES

The reader is referred to the article by Dyson elsewhere in this issue.

CESAREAN SECTION

There is little concern related to the use of opioids for premedication in patients re-
quiring a cesarean section. If puppies or kittens are sedated or have respiratory
depression from the expected placental transfer of the opioid, 1 drop of naloxone
(0.4 mg/mL from a 1-mL syringe) can be administered under the tongue, and repeat
doses can be sent home with the owner if longer acting opioids are involved. Doxap-
ram may be helpful during resuscitation of the newborn if the response to naloxone is
poor or if no opioids were used. Because of the analgesic effect of progesterone,
which is at high levels at this time in the bitch or queen, butorphanol may be adequate
as a premedication. Its short duration of effect can result in mild and short-duration
respiratory depression on neonates but provides short-term analgesia in the bitch at
recovery. A single dose of an NSAIA is often administered after surgery. Concerns
for milk transfer and the impact on the neonate ’s kidney development dictate the
use of one dose only, however. If low-dose butorphanol is given for the premedication,
the bitch could be provided a dose of hydromorphone for discharge, which can then
provide several hours of analgesia. The antagonistic effect of the butorphanol is likely
to be minimal when a m-agonist is given approximately 1 hour after butorphanol.
Although hydromorphone or morphine is suitable as a premedication in these cases,
low-end doses should be given initially, with more given after removal of the puppies if
deemed necessary (based on other analgesia present). There is a greater need to
reverse the neonate when profound m-agonists are selected, even when low doses
are used. Local analgesia is also a reasonable choice, especially in cases in which
inhalant use must be minimized because of cardiovascular instability. A local line block
is quick and easy; epidural local analgesia can provide a longer duration of effect but
involves more time and expertise.

GERIATRICS

In general, typical doses of analgesia are selected for the geriatric patient. Because of
the slower elimination, however, redosing may be required less frequently. As in the
pediatric patient, if excessive sedation is associated with the dose selected, lower
doses would be administered thereafter. Partial reversal by careful titration with nalox-
one and saline, as previously described, can also be considered if an excessive effect
of the opioid is noted.
1324 Dyson

SUMMARY

Pain exists; however, we can prevent it, and we can treat it. The fallacy that pain is pro-
tective and must be allowed to avoid risk for damage after surgery needs to be erad-
icated. Preoperative and postoperative analgesia is directed at aching pain, whereas
sharp pain associated with inappropriate movements persists. Analgesia provides
much more benefit than concern. Preoperative and intraoperative analgesia reduces
wind-up and postoperative demands for analgesia, and during general anesthesia,
it creates a more balanced plane associated with less cardiovascular depression.
The advice given in this article provides guidelines for the veterinarian that can be
adjusted according to the patient ’s needs and responses. Suggestions are provided
from the point of admission to discharge to give a starting point for individual tailoring
of an analgesic plan.

REFERENCES

1. American Animal Hospital Association, American Association of Feline Practi-


tioners, AAHA/AAFP Pain Management Guidelines Task Force Members,
Hellyer P, Rodan I, Brunt J, et al. AAHA/AAFP pain management guidelines for
dogs and cats. J Am Anim Hosp Assoc 2007;43:235–48.
2. de Jong AE, Middelkoop E, Faber AW, et al. Non-pharmacological nursing inter-
ventions for procedural pain relief in adults with burns: a systematic literature
review. Burns 2007;33:811–27.
3. Golianu B, Krane E, Seybold J, et al. Non-pharmacological techniques for pain
management in neonates. Semin Perinatol 2007;31:318–22.
4. Yackey M, Ilkiw JE, Pascoe PJ, et al. Effect of transdermally administered fentanyl
on the minimum alveolar concentration of isoflurane in cats. Vet Anaesth Analg
2004;31:183–9.
5. Wilson D, Pettifer GR, Hosgood G. Effect of transdermally administered fentanyl
on minimum alveolar concentration of isoflurane in normothermic and hypother-
mic dogs. J Am Vet Med Assoc 2006;228:1042–6.
6. Ilkiw JE, Pascoe PJ, Tripp LD. Effects of morphine, butorphanol, buprenorphine,
and U50488H on the minimum alveolar concentration of isoflurane in cats. Am
J Vet Res 2002;63:1198–202.
7. Kay-Mugford PA, Grimm KA, Weingarten AJ, et al. Effect of preoperative admin-
istration of tepoxalin on hemostasis and hepatic and renal function in dogs. Vet
Ther 2004;5:120–7.
8. Crandell DE, Mathews KA, Dyson DH. Effect of meloxicam and carprofen on renal
function when administered to healthy dogs prior to anesthesia and painful stim-
ulation. Am J Vet Res 2004;65:1384–90.
9. Bergmann HM, Nolte IJ, Kramer S. Effects of preoperative administration of car-
profen on renal function and hemostasis in dogs undergoing surgery for fracture
repair. Am J Vet Res 2005;66:1356–63.
10. Fresno L, Moll J, Peñalba B, et al. Effects of preoperative administration of me-
loxicam on whole blood platelet aggregation, buccal mucosal bleeding time,
and haematological indices in dogs undergoing elective ovariohysterectomy.
Vet J 2005;170:138–40.
11. Borer LR, Peel JE, Seewald W, et al. Effect of carprofen, etodolac, meloxicam, or
butorphanol in dogs with induced acute synovitis. Am J Vet Res 2003;64:
1429–37.
Perioperative Pain Management 1325

12. Leece EA, Brearley JC, Harding EF. Comparison of carprofen and meloxicam for
72 hours following ovariohysterectomy in dogs. Vet Anaesth Analg 2005;32:
184–92.
13. Mathews KA, Pettifer G, Foster R, et al. Safety and efficacy of preoperative
administration of meloxicam, compared with that of ketoprofen and butorphanol
in dogs undergoing abdominal surgery. Am J Vet Res 2001;62:882–8.
14. Lascelles BD, Cripps PJ, Jones A, et al. Efficacy and kinetics of carprofen,
administered preoperatively or postoperatively, for the prevention of pain in
dogs undergoing ovariohysterectomy. Vet Surg 1998;27:568–82.
15. Welsh EM, Nolan AM, Reid J. Beneficial effects of administering carprofen before
surgery in dogs. Vet Rec 1997;141:251–3.
16. Tobias KM, Harvey RC, Byarlay JM. A comparison of four methods of analgesia in
cats following ovariohysterectomy. Vet Anaesth Analg 2006;33:390–8.
17. Gassel AD, Tobias KM, Egger CM, et al. Comparison of oral and subcutane-
ous administration of buprenorphine and meloxicam for preemptive analgesia
in cats undergoing ovariohysterectomy. J Am Vet Med Assoc 2005;227:
1937–44.
18. Carroll GL, Howe LB, Peterson KD. Analgesic efficacy of preoperative administra-
tion of meloxicam or butorphanol in onychectomized cats. J Am Vet Med Assoc
2005;226:913–9.
19. Dobbins S, Brown NO, Shofer FS. Comparison of the effects of buprenorphine,
oxymorphone hydrochloride, and ketoprofen for postoperative analgesia after
onychectomy or onychectomy and sterilization in cats. J Am Anim Hosp Assoc
2002;38:507–14.
20. Turner PV, Kerr CL, Healy AJ, et al. Effect of meloxicam and butorphanol on
minimum alveolar concentration of isoflurane in rabbits. Am J Vet Res 2006;67:
770–4.
21. Ko JC, Lange DN, Mandsager RE, et al. Effects of butorphanol and carprofen on
the minimal alveolar concentration of isoflurane in dogs. J Am Vet Med Assoc
2000;217:1025–8.
22. Romans CW, Gordon WJ, Robinson DA, et al. Effect of postoperative analgesic
protocol on limb function following onychectomy in cats. J Am Vet Med Assoc
2005;227:89–93.
23. Menigaux C, Guignard B, Fletcher D, et al. Intraoperative small-dose ketamine
enhances analgesia after outpatient knee arthroscopy. Anesth Analg 2001;93:
606–12.
24. Stubhaug A. A new method to evaluate central sensitization to pain following sur-
gery. Effect of ketamine. Acta Anaesthesiol Scand Suppl 1997;110:154–5.
25. Chen HC, Sinclair MD, Dyson DH. Use of ephedrine and dopamine in dogs for
the management of hypotension in routine clinical cases under isoflurane anes-
thesia. Vet Anaesth Analg 2007;34:301–11.
26. Pypendop BH, Verstegen JP. Hemodynamic effects of medetomidine in the dog:
a dose titration study. Vet Surg 1998;27:612–22.
27. Slingsby I, Lane E, Mears E, et al. Postoperative pain after ovariohysterectomy in
the cat: a comparison of two anaesthetic regimens. Vet Rec 1998;143:589–90.
28. Kuo WC, Keegan RD. Comparative cardiovascular, analgesic, and sedative
effects of medetomidine, medetomidine-hydromorphone, and medetomidine-
butorphanol in dogs. Am J Vet Res 2004;65:931–7.
29. Sammarco JL, Conzemius MG, Perkowski SZ, et al. Postoperative analgesia for
stifle surgery: a comparison of intra-articular bupivacaine, morphine, or saline.
Vet Surg 1996;25:59–69.
1326 Dyson

30. Day TK, Pepper WT, Tobias TA, et al. Comparison of intra-articular and epidural
morphine for analgesia following stifle arthrotomy in dogs. Vet Surg 1995;24:
522–30.
31. Sekar C, Rajasekaran S, Kannan R, et al. Preemptive analgesia for postopera-
tive pain relief in lumbosacral spine surgeries: a randomized controlled trial.
Spine J 2004;4:261–4.
32. Martinez V, Belbachir A, Jaber A, et al. The influence of timing of administration
on the analgesic efficacy of parecoxib in orthopedic surgery. Anesth Analg
2007;104:1521–7.
33. Onal SA, Kelesx E, Toprak GC, et al. Preliminary findings for preemptive analgesia
with inhaled morphine: efficacy in septoplasty and septorhinoplasty cases.
Otolaryngol Head Neck Surg 2006;135:85–9.
34. Lucas AN, Firth AM, Anderson GA, et al. Comparison of the effects of morphine
administered by constant-rate intravenous infusion or intermittent intramuscular
injection in dogs. J Am Vet Med Assoc 2001;218:884–91.
35. Muir WW 3rd, Wiese AJ, March PA. Effects of morphine, lidocaine, ketamine, and
morphine-lidocaine-ketamine drug combination on minimum alveolar concentra-
tion in dogs anesthetized with isoflurane. Am J Vet Res 2003;64:1155–60.
36. Guedes AG, Papich MG, Rude EP, et al. Pharmacokinetics and physiological
effects of two intravenous infusion rates of morphine in conscious dogs. J Vet
Pharmacol Ther 2007;30:224–33.
37. Robinson EP, Faggella AM, Henry DP, et al. Comparison of histamine release
induced by morphine and oxymorphone administration in dogs. Am J Vet Res
1988;49:1699–701.
38. Guedes AG, Papich MG, Rude EP, et al. Comparison of plasma histamine levels
after intravenous administration of hydromorphone and morphine in dogs. J Vet
Pharmacol Ther 2007;30:516–22.
39. Steagall PV, Teixeira Neto FJ, Minto BW, et al. Evaluation of the isoflurane-sparing
effects of lidocaine and fentanyl during surgery in dogs. J Am Vet Med Assoc
2006;229:522–7.
40. Schwieger IM, Hall RI, Hug CC Jr. Less than additive antinociceptive interaction
between midazolam and fentanyl in enflurane-anesthetized dogs. Anesthesiology
1991;74:1060–6.
41. Murphy MR, Hug CC Jr. The anesthetic potency of fentanyl in terms of its reduc-
tion of enflurane MAC. Anesthesiology 1982;57:485–8.
42. Steagall PV, Carnicelli P, Taylor PM, et al. Effects of subcutaneous methadone,
morphine, buprenorphine or saline on thermal and pressure thresholds in cats.
J Vet Pharmacol Ther 2006;29:531–7.
43. Lascelles BD, Robertson SA. Antinociceptive effects of hydromorphone, butor-
phanol, or the combination in cats. J Vet Intern Med 2004;18:190–5.
44. Valverde A, Doherty TJ, Herna ndez J, et al. Effect of lidocaine on the minimum
alveolar concentration of isoflurane in dogs. Vet Anaesth Analg 2004;31:264–71.
45. Nunes de Moraes A, Dyson DH, O ’Grady MR, et al. Plasma concentrations and
cardiovascular influence of lidocaine infusions during isoflurane anesthesia in
healthy dogs and dogs with subaortic stenosis. Vet Surg 1998;27:486–97.
46. Pypendop BH, Ilkiw JE. Assessment of the hemodynamic effects of lidocaine
administered IV in isoflurane-anesthetized cats. Am J Vet Res 2005;66(4):661–8.
47. Gaynor JS, Muir WW. Handbook of veterinary pain management. St. Louis (MO):
Mosby; 2002.
Perioperative Pain Management 1327

48. Reuben SS, Buvanendran A. Preventing the development of chronic pain after
orthopaedic surgery with preventive multimodal analgesic techniques. J Bone
Joint Surg Am 2007;89:1343–58.
49. Anand KJ, Johnston CC, Oberlander TF, et al. Analgesia and local anesthesia
during invasive procedures in the neonate. Clin Ther 2005;27:844–76.
50. Taddio A, Katz J, Ilersich AL, et al. Effect of neonatal circumcision on pain
response during subsequent routine vaccination. Lancet 1997;349:599–603.
51. Luks AM, Zwass MS, Brown RC, et al. Opioid-induced analgesia in neonatal
dogs: pharmacodynamic differences between morphine and fentanyl. J Pharma-
col Exp Ther 1998;284:136–41.
52. Herd D, Anderson BJ. Ketamine disposition in children presenting for procedural
sedation and analgesia in a children ’s emergency department. Paediatr Anaesth
2007;17:622–9.
53. Gibbs LM, Kendig JJ. Substance P and NMDA receptor-mediated slow potentials
in neonatal rat spinal cord: age-related changes. Brain Res 1992;595:236–41.
J Vet Intern Med 2008;22:525–533

P o s t ope r at iv e Ble e ding i n Re t i r e d R a c i n g G r e y h o u n d s


A. Lara-Garcı́a, C.G. Couto, M.C. Iazbik, and M.B. Brooks

Background: Some retired racing Greyhounds (RRG) that undergo surgery bleed excessively.
Hypothesis: Greyhounds that bleed excessively will have one or more preoperative hemostatic abnormalities that can be
used to predict the risk and severity of postoperative bleeding.
Animals: Eighty-eight RRG undergoing ovariohysterectomy or castration.
Methods: All dogs were evaluated preoperatively with a physical exam, CBC, platelet count, OSPT, APTT, platelet func-
tion with PFA-100a; fibrinogen, D-dimer, plasminogen (Plmg), antiplasmin (AP), antithrombin (AT), and vWF concentration
(vWF:Ag); vWF collagen binding assay (vWF:CBA), and Factor XIII assay. Assays were repeated in the dogs that bled, and in
an age- and sex-matched control group of RRG.
Results: Twenty-six percent of the dogs had bleeding 36–48 hours after surgery. AP (P o.0001) and AT concentration
(P 5 .007) were significantly lower, and vWF:CBA (P 5 .0284) was higher preoperatively in the dogs with excessive hemorrhage. A
lower platelet count (P 5 .001) and hematocrit (P 5 .002), shorter OSPT (P 5 .0002) and higher plasma fibrinogen (P o.0001), and
AP (P 5 .001) concentration were detected at the time of bleeding compared with preoperative values in the dogs that bleed exces-
sively. The same findings were observed postoperatively for the control group, except for the decrease in hematocrit.
Conclusions and Clinical Importance: The results indicate that this excessive postoperative bleeding is not attributable to a
primary or secondary hemostatic defect, but could result from altered fibrinolysis.
Key words: Antiplasmin; Fibrinolysis; Hemostasis; Surgery; von Willebrand factor.

reyhounds have physiologic and hematologic documenting or investigating this phenomenon in the
G peculiarities specific for the breed.1–5 The mean
packed cell volume (PCV), hemoglobin concentration,
breed.
Recently, a website-based survey documented the
red blood cell (RBC) count, and whole blood viscosity prevalence of diseases and major causes of death in 747
are higher, whereas the white blood cell count, neutrophil RRG in the United States in 2006.6 The mortality rate
count, and platelet count1–3 are lower than in other during a 2-year period was 15%; and bleeding disorders
breeds of dogs. The serum total protein, globulin, a-glob- were one of the 4 most prevalent causes of death
ulin, and b-globulin concentrations are also lower than in reported, accounting for 8% of all deaths. Hematologic
non-Greyhound dogs.1,3–5 In addition, platelet aggrega- diseases had a prevalence of 3.3%, with thromboembolic
tion under high shear as determined with PFA-100a is disease and spontaneous and postoperative bleeding
significantly shorter in retired racing Greyhounds (RRG) accounting for 46% of these.6
than in non-Greyhound dogs.5 Intra-operative and immediate postoperative bleeding
We have observed a tendency for RRG to develop can be attributed to surgical technique (surgical bleeding)
bleeding after minor trauma or a simple surgical proce- or systemic abnormalities (nonsurgical bleeding).7 The lat-
dure, including ovariohysterectomy, orchiectomy, ter includes primary hemostatic defects such as thrombo-
dewclaw removal, or laparotomy. In the majority of the cytopenia, platelet dysfunction, or von Willebrand disease
dogs, one-stage prothrombin time (OSPT), activated (vWD), and secondary hemostatic defects such as hypo-
partial thromboplastin time (APTT), and platelet counts fibrinogenemia, hypoprothrombinemia, hemophilia A or
(PLT) were within the reference ranges. Although anec- B, factor VII deficiency, or combined clotting factor defi-
dotal references to excessive bleeding can be found ciencies.7 Delayed postoperative bleeding is more likely
in some Greyhound websites or Greyhound health man- caused by abnormal fibrin stabilization, factor XI defi-
uals, there are no published controlled studies ciency, or enhanced fibrinolysis.8 Finally, systemic
endothelial damage or dysfunction after postoperative
From the Department of Veterinary Clinical Sciences and Veteri- septic complications or hypertensive crises can result in
nary Teaching Hospital (Lara-Garcı´a, Couto, Iazbik), the OSU thrombocytopenia and generalized bleeding, as described
Comprehensive Cancer Center (Couto), The Ohio State University, in women with HELLP (elevated liver enzymes, low plate-
Columbus, OH; and the Comparative Coagulation Section the Animal let count) syndrome associated with preeclampsia and in
Health Diagnostic Laboratory, Cornell University, Ithaca, NY children with hemolytic-uremic syndrome.9–10
(Brooks). This work was performed at The Ohio State University
In our experience, limb amputation for osteosarcoma
Veterinary Teaching Hospital, Columbus, OH. Preliminary data were
presented in abstract form at the 25th ACVIM Forum, Seattle, June (OSA) also frequently results in severe postoperative
2007. bleeding in Greyhounds. In the past 3 years, 36% (10/
Corresponding author: Ana Lara Garcia, DVM, MS, PhD, 38) of the RRG that underwent limb amputation for
Department of Veterinary Clinical Sciences, College of Veterinary OSA at The Ohio State University Veterinary Teaching
Medicine, The Ohio State University, 601 Vernon L Tharp, 43210 Hospital (OSU-VTH) had severe delayed postoperative
Columbus, OH; e-mail: lara-garcia.3@osu.edu. bleeding that required intensive care management.b In six
Submitted July 10, 2007; Revised October 15, 2007; Accepted
of these dogs, the severity of the bleeding required trans-
January 30, 2008.
Copyright r 2008 by the American College of Veterinary Internal fusion of packed RBCs and fresh frozen plasma, leading
Medicine to a transient poor quality of life postamputation,
10.1111/j.1939-1676.2008.0088.x lengthy hospitalization, and high medical bills.
526 Lara-Garcı́a et al

Our hypothesis was that Greyhound ‘‘bleeders’’ would Table 1. Scale for severity of bleeding.
have one or more preoperative abnormalities in primary Score 0 Definitely no new bleeding
or secondary hemostasis or in the fibrinolytic pathway Score 1 Questionable new petechiae or bruising
that could be used to predict the risk and severity of Score 2 Definite new cutaneous hemorrhagic lesions
postoperative bleeding. To test this hypothesis, primary Score 3 Moderate to severe cutaneous bleeding without
and secondary hemostasis were prospectively evaluated measurable decline in hemoglobin concentration
preoperatively in RRG who underwent routine ovario- Score 4 Severe external bleeding of sufficient magnitude
hysterectomy or castration at OSU-VTH. The hemosta- to decrease hematocrit by 46%
sis assays were repeated in those RRG who developed
Adapted from the system for children with idiopathic thrombo-
bleeding complications at the time of the event, and in an cytopenic purpura.11
age- and sex-matched control group of RRG that under-
went ovariohysterectomy or castration at the same time
and did not bleed. Sampling
Twenty milliliters of blood were collected from the jugular vein
Material and Methods by atraumatic direct venipuncture, and placed in a 3 mL siliconized
tube containing sodium ethylenediaminetetraacetate and in 4.5 mL
Animals and Blood Samples tubes containing 3.8% sodium citrate.j
This study was approved by the Hospital Executive Committee One tube of blood collected in sodium citrate was placed in a rack
of The Ohio State University Veterinary Teaching Hospital. Eighty- at room temperature for at least 10 minutes (and for no longer than
eight RRG from Greyhound Adoption of Ohio (Chagrin Falls, 3 hours); this sample was used to evaluate platelet function with the
OH—www.greyhoundadoptionofoh.org) were spayed or neutered PFA-100.a The other tubes of citrated blood were immediately cen-
at the OSU-VTH between November 2004 and February 2006 as trifuged at 1,380  g for 10 minutes, and the plasma was transferred
part of a 3rd-year veterinary student teaching laboratory. A phys- to several polypropylene transfer tubes. One tube with plasma was
ical examination was performed on each dog, and blood was drawn used for immediate determination of OSPT, APTT, and fibrinogen
preoperatively for a CBC and hemostasis assessment. The following concentration, and the rest of the tubes were stored in a freezer at
tests were used to evaluate primary hemostasis: PLT, platelet func- 31C for 1–2 weeks. Frozen plasma was shipped for the additional
tion with PFA-100a closure time (CT), von Willebrand factor assays to the Comparative Coagulation Section laboratory (Animal
antigen concentration (vWF:Ag), and von Willebrand factor activity Health Diagnostic Laboratory, Cornell University, Ithaca, NY).
with collagen binding assay (vWF:CBA). Secondary hemostasis was
evaluated with APTT, OSPT, fibrinogen concentration, anti- Platelet Count and Platelet Function Assays
thrombin (AT) activity, and Factor XIII (FXIII). The fibrinolytic
pathway was evaluated by measuring plasminogen activity (Plmg), Platelet counts were performed using automated counters (Cell-
antiplasmin activity (AP), and D-dimer concentration. Dyn 3500k or LaserCytel) or a manual hand count for those samples
Before surgery, all RRG were premedicated with buprenorphinec below the reference ranges. Whole blood (800 mL) platelet function
(0.05 mg/kg) and acepromazined (0.05 mg/kg) intramuscularly, and a assays were done by means of the PFA-100.a The PFA-100a simu-
prophylactic dose of intravenous cefazolin sodiume (22 mg/kg IV) was lates primary hemostasis after injury to a small vessel under high
administered. Anesthesia was induced with ketaminef (5 mg/kg) and shear stress. Disposable cartridges with collagen and either epineph-
diazepamg (0.25 mg/kg) IV, and maintained using isofluraneh in oxy- rine (10 mg) (COL/EPI) or adenosindiphosphate (ADP—50 mg)
gen. Respiration was supported with intermittent positive-pressure (COL/ADP) were used as platelet activating reagents. The test was
ventilation, and intra-operative fluid therapy consisted of lactated Ring- performed twice with each type of reagent as described previously,
er’s solution (10 mL/kg/hours IV). The dogs were monitored during and the closure times (CT) were recorded.12,13 Greyhound-specific
surgery with electrocardiography, pulse oximetry, respirometry, capno- reference intervals were used for hematocrit, PLT, and CT with
graphy, measurement of peripheral arterial pressure, and body PFA-100.a5
temperature. After surgery, analgesia was continued with one single in-
tramuscular injection of carprofeni (4 mg/kg). The dogs were monitored Routine Hemostasis Assays
postoperatively until recovery and then transferred to a boarding area.
After the surgical procedure (spay or neuter), dogs were kept at OSPT, APTT, and plasma fibrinogen concentration were deter-
the OSU-VTH for a minimum of 4 days. All dogs underwent daily mined by means of the automated analyzer ACL-200m and
physical examination, their bleeding score was recorded once a day, commercially available reagents,n as described previously.14
and the areas of hemorrhage were photographed digitally. Although
there is no standardized scale to evaluate the severity of bleeding in Antithrombin
dogs, a system with scores ranging from 0 to 4 was adapted from the
one proposed by Buchanan and Adix for children with idiopathic Plasma AT activity was measured with a synthetic chromogenic
thrombocytopenic purpura (Table 1).11 The final bleeding score as- substrate kito following the manufacturer’s recommendations for
signed to each RRG corresponded with the highest score recorded assay conditions and instrumentation.p The assay detects AT activ-
during the postoperative period. ity based on inhibition of a thrombin reagent (anti-IIa activity) and
In dogs with clinical evidence of bleeding (ie, bleeding score 1–4), was modified by the substitution of pooled normal canine plasma,
the assays of hemostatic function performed at baseline were repeated rather than human plasma, as the calibration standard. The AT ac-
when the bleeding was detected. These assays were also performed in a tivities of test plasma were reported as the percentage of the
group of age- and gender-matched Greyhounds who underwent sur- standard, which had an assigned value of 100%.15
gery at the same time and did not have postoperative bleeding (ie,
bleeding score 0). The results of the hemostasis assays in this ‘‘control’’ Von Willebrand Factor Assays
group were used to assess which hemostatic changes developed post-
operatively as a result of the surgical procedure performed and for Plasma vWF concentration [vWF antigen (vWF:Ag)] was mea-
comparison with the postoperative results of the ‘‘bleeder’’ group. sured by enzyme-linked immunosorbent assay (ELISA) configured
Bleeding in Greyhounds 527

with monoclonal anticanine vWF antibodies.16 The biologic activity of the variables before using parametric methods. The Student’s
of vWF was evaluated in a collagen-binding assay (vWF:CBA).17 t-test for independent variables was used to compare hemostatic
Deficiency of the high molecular-weight vWF multimers impairs the variables between groups (‘‘non-bleeders,’’ ‘‘bleeders,’’ or control
ability of vWF to effectively bind collagen. Determination of the group). Comparisons within groups (‘‘bleeders’’ and control group)
ratio of vWF:Ag to vWF:CBA differentiates type 1 from type 2 were done using the Student’s t-test for paired samples. Contingen-
vWD, based on the disproportionate lack of vWF:CBA in the latter. cy tables were used to compare categorical variables between
A ratio of vWF:Ag to vWF:CBA greater than 2:1 is considered to be groups. Differences were considered statistically significant
diagnostic of type 2 vWD.17–18 when P o.05.

Fibrinolysis Assays Results


The activities of Plmg and AP were measured using synthetic Signalment and Prevalence of Postoperative
chromogenic substrate kits and the manufacturer’s recommended Bleeding in RRG
instrument.q,r,s The Plmg assay was modified by substitution of
urokinase, rather than streptokinase, to activate Plmg.19 Standard Eighty-eight Greyhounds were evaluated. There were
curves for the Plmg and AP assays were derived from dilutions of a 36 intact males and 52 intact females, with ages that
canine plasma standard, and the results were reported as a percent- ranged from 1 to 11 years (mean 4 years). Although none
age of the standard. Plasma D-dimer concentration was measured of the dogs experienced intra-operative or immediate
using a semiquantitative latex agglutination assay,t as described postoperative bleeding, 26% of the dogs (23/88) had de-
previously.20 The results of this assay were expressed semiquanti- layed postoperative bleeding 36 to 48 hours after surgery.
tatively within 4 ranges: o250, 250–500, 500–1,000, and 1,000–
The bleeding was scored as grade 1 in 2 dogs, grade 2 in
2,000 ng/dL.
14 dogs, grade 3 in 5 dogs, and grade 4 in 2 dogs. The
observed signs of bleeding consisted of cutaneous bruis-
Factor XIII Deficiency Screen ing that extended from the area of the surgical incision
toward the periphery (Fig 1). There was no bleeding from
A screening test to detect the presence of cross-linked fibrin was mucosal surfaces or in areas distant from the surgical
performed by comparing the urea solubility of fibrin from control site. None of the dogs required transfusion of blood
dogs and test plasma.21 Briefly, 2 volumes of citrated plasma were
components and the bleeding was self-limiting; bruising
combined in a glass tube with 1 volume of an imidazole buffer and
was still present at the time the dogs were discharged, 4
1/10th volume of 0.25 M CaCl2. After incubation for 1 hour at
37 1C, the resultant fibrin clot was transferred to a 5 M urea solu- days after the surgery.
tion, and the presence or absence of residual clot was recorded at There was no significant difference for sex between
5-minute intervals. In the absence of Factor XIII, complete clot lysis ‘‘bleeders’’ and ‘‘non-bleeders.’’ The age of the ‘‘bleed-
should occur within 5 minutes. Cross-linked fibrin, formed by ers’’ (range 1–11 years, mean 3 years) was significantly
the action of Factor XIII, is insoluble in urea and remains intact. lower than in the ‘‘non-bleeders’’ (range 2–11 years,
Results are reported as normal or abnormal.22 mean 4 years) (P 5 .02). On physical examination, we
found that the prevalence of a left basilar systolic mur-
mur in the ‘‘non-bleeder group’’ was 69%, and it was
Statistical Analysis significantly higher than in the ‘‘bleeder’’ group, where it
Graph Pad Prism softwareu was used for statistical analysis. De- was 52% (P 5 .013). The murmurs were graded as I
scriptive statistics were performed for all the variables. The or II/VI in all dogs, except for 1 RRG from the ‘‘non-
Kolmogorov-Smirnoff test was used to assess normal distribution bleeder group’’ that had a III/VI murmur.

Fig 1. (A) Image of the surgical incision in one of the Greyhounds of the control group 36 hours post-surgery (bleeding score 0). (B) Image of
the surgical incision in one of the Greyhounds of the ‘‘bleeder’’ group 36 hours postsurgery (bleeding score 3).
528 Lara-Garcı́a et al

Comparison of Hemostatic Parameters between Comparison of Preoperative and Postoperative Values


‘‘Bleeders’’ and ‘‘Non-Bleeders’’ Preoperatively within ‘‘Bleeders’’ and within Control Group
Preoperatively, there were no significant differences When the hemostatic variables were compared before
between ‘‘bleeders’’ and ‘‘non-bleeders’’ for any of the surgery and after surgery within the ‘‘bleeders,’’ and
following factors: PLT, hematocrit, OSPT, APTT, before and after surgery within the control group, the
fibrinogen, vWF:Ag, platelet function using the PFA- PLT was significantly lower in both groups (P 5 .001,
100a with COL/EPI and COL/ADP, Plmg, D-dimer, and P 5 .03), the OSPT was significantly shorter (P 5 .0002,
F-XIII (Table 2). The D-dimer concentration was P 5 .048), and the fibrinogen (P o.0001, P 5 .002) con-
o250 ng/dL in all but two of the ‘‘non-bleeders,’’ which centration and AP (P 5 .01, P 5 .04) activity were
had values of 250–500 and 500–1,000 ng/dL, respectively; significantly higher postoperatively in both groups
all ‘‘bleeders’’ had values of o250 ng/dL, except 1 dog (Table 2; Figs 3 and 4). Concentration of the D-dimer
that had 250–500 ng/dL before surgery. Factor XIII ac- was significantly increased after surgery in both groups.
tivity was normal for all the dogs in both groups. In 2 dogs within the control group (25%), the D-dimer
In the ‘‘non-bleeder’’ group, AP and AT activities were concentration increased to between 250 and 2,000 ng/dL
above the reference range in 20% and 23% of the dogs, (P o.001), whereas in 3 dogs within the ‘‘bleeder’’ group
respectively. The AP and AT activities, although within (13%), it increased to between 250 and 1,000 ng/dL
the normal range, were significantly lower in the ‘‘bleed- (P 5 .0238). The hematocrit was the only variable that
er’’ group than in the ‘‘non-bleeders’’ (P o.001 and P 5 was significantly lower at the time of bleeding in the
.007, respectively). The vWF:Ag was below the reference ‘‘bleeder’’ group (P 5 .002), but not in the control group
interval in 21% of the ‘‘bleeders’’ and in 50% of the (P 5 .4533); the hematocrit decreased more than 6%
‘‘non-bleeders’’ without significant differences between (ie, grade 4 bleeding) in 2/23 ‘‘bleeders’’ (10%) (Table 2,
groups (P 5 .9614), and the vWF:CBA was below the Figs 3 and 4).
reference range in 8% of the ‘‘bleeders’’ and in 30% of
the ‘‘non-bleeders’’ and was significantly higher in the Comparison of Postoperative Values between
‘‘bleeders’’ (P 5 .0284). The ratio between the vWF:Ag ‘‘Bleeders’’ and Control Group
concentration and the vWF:CBA was significantly lower
in the ‘‘bleeder’’ group (P o.0001) (Table 2, Fig 2). There were no significant postoperative differences be-
tween ‘‘bleeders’’ and the control group for any of the
hemostatic parameters evaluated, except for the ratio
vWF:Ag/vWF:CBA, which was lower in the ‘‘bleeder’’
Control Group group (P 5 .0389).

The control group consisted of 8 Greyhounds who Discussion


underwent spaying or neutering and had no signs
of bleeding (ie, Score 0). Before surgery, there were no In this prospective study, we documented the develop-
significant differences for any of the parameters evaluat- ment of delayed postoperative bleeding after spaying or
ed between the control dogs and the rest of the neutering in RRG, with a prevalence of 26%. In 10%
Greyhounds of the ‘‘non-bleeder’’ group. of the bleeders, there was a decrease in the hematocrit of

Table 2. Results of hemostatic parameters in ‘‘non-bleeder,’’ ‘‘bleeder,’’ and control group.


Laboratory Non-bleeder Pre-Sx Bleeder Pre-Sx Bleeder Post-Sx Control Post-Sx
Reference Ranges Mean (SD) n565 Mean (SD) n523 Mean (SD) n523 Mean (SD) n58
Hematocrit (%) 46–64 52.3 (4.3) 53.7 (3.7) 50.6 (4.4)a 53.7 (7.8)
PLT (109/L) 125–397 218 (51) 198 (46) 169 (49)a 181 (43)b
COL–ADP (seconds) 63–92 88.7 (22) 82 (13.6) 80 (11.4) 84.5 (21.9)
COL–EPI (seconds) 87–238 207 (71.3) 180 (59.1) 206.5 (82.5) 174 (64.8)
APTT (seconds) 9–21 14.4 (2.6) 13.7 (1.6) 13.7 (2.3) 15.6 (4.2)
OSPT (seconds) 6–7.5 6.8 (0.4) 6.8 (0.47) 6.3 (0.23)a 6.37 (0.48)b
Fibrinogen (g/L) 100–384 118 (29.7) 130 (40.8) 215 (37.5)a 200 (54.7)b
vWF:Ag (%) 70–180 73.7 (23) 74 (14) 81.4 (22.7) 71 (27.8)
vWF:CBA (%) 450 62 (20) 72.7 (16.5)c 80 (26.8) 62.2 (24.1)
Ratio vWF:Ag/vWF:CBA o2 1.2 (0.14) 1.03 (0.12)c 1.03 (0.13) 1.15 (0.11)
Antiplasmin (%) 65–120 107 (35.8) 82 (20)c 94 (26.4)a 108 (36.5)b
Antithrombin (%) 65–145 100.8 (36.4) 78.3 (17.2)c 74.8 (24.3) 95.6 (32.4)
Plasminogen (%) 60–170 71.6 (16.9) 65 (19.4) 62.3 (15.2) 71.1 (20.8)

PLT, platelet count; COL-ADP, closure time with collagen-adenosindiphosphate; COL-EPI, closure time with collagen-epinephrine;
APTT, activated partial thromboplastin time; OSPT, one stage phrothrombine time; vWF:Ag, von Willebrand Factor antigen concentration;
vWF:CBA, von Willebrand Factor collagen binding assay activity; Pre-Sx, preoperative; Post-Sx, postoperative.
a
Hemostatic parameters significantly differ within the ‘‘bleeder’’ group.
b
Hemostatic parameters significantly differ within the ‘‘control’’ group.
c
Hemostatic parameters significantly differ preoperatively between ‘‘bleeders’’ and ‘‘non-bleeders.’’
Bleeding in Greyhounds 529

Fig 2. Scatter dot plots of the hemostatic parameters that differ significantly between the ‘‘bleeder’’ group (n 5 23) and ‘‘non-bleeder’’ group
(n 5 65) preoperatively (P o.05). The dotted lines represent the reference range limits for a given parameter, and the solid line represents the
mean of the values obtained for that parameter in each group of RRG.

more than 6% (ie, grade 4 bleeding) but blood compo- in platelet aggregation at high shear using PFA-100a
nent therapy was not required by these dogs. In both after treatment with carprofen for 5 days.
groups, platelet counts and platelet function were within vWF is a large molecule composed of low-, intermedi-
the reference ranges for the breed5 and were not signifi- ate-, and high-molecular weight (MW) multimers. The
cantly different between ‘‘bleeders’’ and ‘‘non-bleeders.’’ high-MW multimers are vital for platelet adhesion to the
Selective or combined clotting factor deficiencies were subendothelium in areas of high shear.26 In this study,
ruled out on the basis of normal fibrinogen concentra- the vWF:Ag concentration was below the reference rang-
tion, OSPT, and APTT in the ‘‘bleeders.’’ Factor XIII es in 21% of the ‘‘bleeders’’ (range 43–63%; mean
deficiency was also ruled out on the basis of normal 54.8%) and 50% of the dogs from the ‘‘non-bleeder’’
Factor XIII assay. group (range 36–68%, mean 56%), without significant
All the RRG received the same analgesic and anesthet- differences between the groups. Paradoxically, the ‘‘non-
ic protocol pre- and postoperatively; therefore, it is bleeder’’ group had significantly lower levels of high-
unlikely that differences between the groups are caused MW vWF than the ‘‘bleeder’’ group measured by
by the drugs administered perioperatively. The delayed vWF:CBA (P 5 .0284); this unexplained phenomenon
bleeding makes drug-associated thrombocytopenia or should have made the ‘‘non-bleeders’’ more predisposed
platelet dysfunction unlikely as a cause of bleeding. Fur- to develop perioperative bleeding.
thermore, in a previous study, acepromazine caused Greyhounds are not one of the breeds with a reported
thrombocytopenia and platelet dysfunction that lasted high prevalence of vWD.26 In a recent 2-year period
o200 minutes.23 Although all the Greyhounds in this (July 2002 to July 2004), approximately 10% (22 of 216)
study received carprofen perioperatively, the platelet of the Greyhounds screened at the Comparative Coagu-
function with PFA-100a was within normal limits in both lation Section had plasma vWF concentration of
groups at the time of bleeding. Previous studies reported 30%.v In a previous study of platelet function with
decreased platelet aggregation by aggregometry in dogs PFA-100a in Greyhounds, we also found that 13% (3/23)
that underwent surgery and received multiple doses of of the dogs had vWF:Ag concentrations below reference
carprofen, but there was no clinical evidence of bleeding range, but normal CT with the PFA-100.a5
attributable to this drug in the postoperative period.24 Greyhounds commonly have a high velocity aortic
Another study by Gaal et al25 demonstrated no changes murmur because of relative aortic stenosis.27 Type 2 von
530 Lara-Garcı́a et al

Fig 3. Scatter dot plots for the preoperative and postoperative values of the hemostatic parameters that differ significantly within the
‘‘bleeder’’ group (n 5 23; P o.05). The dotted lines represent the reference range limits for a given parameter, and the solid line represents the
mean of the group of values obtained for that parameter in the ‘‘bleeder’’ group before or after surgery.

Willebrand’s syndrome (vWS), a depletion of high-MW Although vWF has always been seen as a platelet
vWF multimers secondary to high shear, has been adhesion molecule that is involved in only the primary
described in humans with aortic valve mineralization, hemostatic process, recent evidence in humans has doc-
and recently in dogs with aortic and subaortic stenosis.28 umented that plasma vWF:Ag is higher in hypertensive
Interestingly, the prevalence of a left basilar systolic mur- than in normotensive human patients.29 Greyhounds
mur in the ‘‘non-bleeder’’ group was significantly higher have high arterial blood pressure compared with mixed
than in the ‘‘bleeder’’ group (P 5 .013). Type 2 vWS was breed dogs30,31; therefore, the vWF:Ag in this breed may
ruled out because the vWF:Ag/vWF:CBA ratio was be- be artificially increased because of endothelial cell dam-
low 2. Because the decreases in vWF:Ag were moderate age secondary to hypertension. It is possible that the
and the platelet function assays were normal in the ‘‘non- ‘‘bleeders’’ had higher vWF:Ag concentrations than the
bleeder’’ group, it is possible that the ‘‘non-bleeder’’ ‘‘non-bleeders’’ because they were hypertensive, and that
group had lower vWF:CBA activity than the ‘‘bleeder’’ the high blood pressure contributed to the delayed bleed-
group owing to depletion of high-MW vWF multimers ing (ie, increased hydrostatic pressure dislodging the
associated with the higher prevalence of a high-velocity hemostatic plug). Although this study did not examine
aortic murmur. arterial blood pressure as a potential contributing factor
Bleeding in Greyhounds 531

Fig 4. Scatter dot plots for the preoperative and postoperative values of the hemostatic parameters that differ significantly within the control
group (n 5 8; P o.05). The dotted lines represent the reference range limits for a given parameter, and the solid line represents the mean of the
group of values obtained for that parameter in the ‘‘control’’ group before or after surgery.

to the bleeding, a prospective study evaluating this pos- and PAI-1 or ELT.32,33 In this study, we did not measure
sibility is under way. tissue-plasminogen activator (tPA) or PAI-1, which are
It is possible that the delayed onset of bleeding (ie, more specific fibrinolysis parameters whose results
36–48 hours) in the affected Greyhounds would be could have supported or ruled out this possible explana-
caused by enhanced fibrinolysis, because ‘‘bleeders’’ had tion for the postoperative bleeding in RRG. To our
lower AP than ‘‘non-bleeders’’ before surgery, suggesting knowledge, assays for tPA in canine plasma have not
activated fibrinolysis and, hence, a hypocoagulable state. been validated; we are currently evaluating an ELISA for
D-dimer concentrations in the ‘‘bleeder’’ group were PAI-1 in dogs (Marjory B Brooks, unpublished observa-
increased in only 3 dogs postoperatively, although theo- tions, Animal Health Diagnostic Laboratory, Cornell
retically D-dimer concentrations are expected to be high University, Ithaca, NY). At this moment, we are evalu-
in patients with hyperfibrinolysis. Several studies in hu- ating this assay in RRG plasma at our institution as a
mans have shown that bleeding patients with increased next step of the present study.
fibrinolysis diagnosed by low plasminogen activator in- Aminocaproic acid is a prohemostatic agent that is
hibitor type 1 (PAI-1) or short euglobulin lysis time beneficial not only in patients with hyperfibrinolysis but
(ELT) can have normal D-dimer concentrations, and that also in those with a variety of primary and secondary
there was no correlation between D-dimer concentration hemostatic defects.34 Although the data in this study do
532 Lara-Garcı́a et al

not confirm hyperfibrinolysis as the primary cause of play a role in the development of this complication. Fur-
postoperative bleeding in RRG, further clinical investi- ther investigation is needed in order to determine its
gation of the role of perioperative administration of cause.
aminocaproic acid to decrease the prevalence or severity
of this complication is warranted.
We propose that values for hemostatic assays in Grey-
hounds may differ from those of the general dog Footnotes
population, as it occurs with other clinicopathologic a
PFA-100, Dade Behring, West Sacramento, CA
analytes in the breed,1–5 and reference ranges for b
Marin L, Couto CG, Iazbik MC, et al. Hemostatic complications
vWF:Ag, vWF:CBA, AT, AP in RRG should be gener- after limb amputation in retired racing Greyhounds. J Vet Intern
ated. Med 2007;21:573 (abstract)
c
In a previous study in dogs undergoing elective ova- Buprenorphine HCL, Bedford Laboratories, Bedford, OH
d
riohysterectomy, there were no differences in the Aceproject, Butler Animal Health Supply, Dublin, OH
e
hemostatic profiles before and after the procedure.35 In f
Cephazolin sodium, Sandoz Inc, Princetown, NJ
our study, the hemostatic changes observed in both Ketaset, Fort Dodge Animal Health, Fort Dodge, IA
g
‘‘bleeder’’ and control groups after surgery were identi- Diazepam, Hospira Inc, Lake Forest, IL
h
Isosol, Vedco Inc, St Joseph, MO
cal, with the exception of the expected decrease in the i
Rymadil, Pfizer Inc, New York City, NY
hematocrit for the ‘‘bleeders.’’ The shortening in OSPT j
Blue stopper tubes, Monoject, Sherwood, St Louis, MO
and the increase in fibrinogen and D-dimer concentra- k
Cell-Dyn 3500 R, Abbott Laboratories, Abbott Park, IL
tions observed postoperatively within the ‘‘bleeder’’ l
LaserCyte, IDEXX Laboratories, Westbrook, MD
group and within the control group support the hyper- m
ACL-200, Instrumentation Laboratory, Lexington, MA
n
coagulable state that has been widely described in IL Test APTT-C Activated Partial Thromboplastin Time and IL
humans after surgery attributable to release of TF intra- Test PT-Fibrinogen, Instrumentation Laboratory
o
operatively.36,37 The postoperative hypercoagulable state p
Stachrom AT III, Diagnostica Stago, Parsippany, NJ
is most likely responsible for the increase in AP in the StaCompact, Diagnostica Stago
q
‘‘bleeders’’ compared with their baseline values, support- StaCompact, Diagnostica Stago
r
Stachrom Plasminogen, Diagnostica Stago
ing the fact that these dogs, regardless of the initial s
Stachrom Antiplasmin, Diagnostica Stago
hemostatic profile, are capable of generating a compen- t
Minutex D-dimer latex, Biopool, Wicklow, Ireland
satory response after surgical tissue trauma. This was u
Prism version 4.0, GraphPad Software Inc, San Diego, CA
clinically evident by the fact that the bleeding was self- v
Spectrolyse/pL PAI-1, DiaPharma, West Chester, OH
limiting and the blood components were not required in
any of the ‘‘bleeders.’’ This will also most likely explain
the lack of differences in AP after surgery between the
‘‘bleeders’’ and the control group. Acknowledgment
The low vWF:Ag, high AT, and high AP in RRG
could be an adaptational mechanism to racing or an evo- Supported in part by the ACVIM Foundation and the
lutionary trait designed to prevent clotting of blood with Savannah and Barry French Poodle Memorial Fund.
high viscosity (ie, Greyhounds have high hematocrit and
whole blood viscosity) that circulates through large mus-
cle masses, as it has been reported in human athletes.38 A
References
recent study in transgenic polycythemic mice with HCT 1. Porter J, Canaday WR Jr. Hematologic values in mongrel and
of 85% reported thrombocytopenia, with platelet Greyhound dogs being screened for research use. J Am Vet Med
counts that did not differ from those in wild type mice Assoc 1971;159:1603–1606.
when corrected for plasma volume, increased nitric oxide 2. Sullivan PS, Evans HL, McDonald TP. Platelet concentration
concentration, and hypocoagulability based on comput- and hemoglobin function in Greyhounds. J Am Vet Med Assoc
erized thromboelastography and plasmatic coagulation 1994;205:838–841.
3. Steiss JE, Brewer WG, Welles E, Wright JC. Hematologic and
activity.39 It is very tempting to think that a similar
serum biochemical reference values in retired Greyhounds. Com-
phenomenon may occur in sight hounds and that pend Cont Educ 2000;22:243–248.
they have evolved to be ‘‘hypocoagulable’’ in order 4. Fayos M, Couto CG, Cline Iazbik MC, Wellman M. Serum
to prevent intravascular thrombosis during strenuous protein electrophoresis in retired racing Greyhounds. Vet Clin
exercise. Pathol 2005;34:397–400.
We did not evaluate the pedigrees of the ‘‘bleeders’’ 5. Couto CG, Lara A, Iazbik MC, Brooks M. Evaluation of
and the ‘‘non-bleeders’’; it is possible that because racing platelet aggregation using a point-of-care instrument in retired
Greyhounds are derived from a relatively small genetic racing Greyhounds. J Vet Intern Med 2006;20:365–370.
pool, genetic disorders of clotting or fibrinolysis could be 6. Lord L, Jaissle J, Marin L, Couto CG. Results of a web-based
partially responsible for this disorder. health survey of retired racing greyhounds. J Vet Intern Med
2007;21:1243–1250.
In conclusion, approximately 25% of RRG develop
7. Adams GL, Manson RJ, Turner I, et al. The balance of
delayed postoperative bleeding 36–48 hours after a sim- thrombosis and hemorrhage in surgery. Hematol Oncol Clin N Am
ple surgical procedure; this bleeding does not seem to be 2007;21:13–27.
attributable to a primary or secondary hemostatic disor- 8. Hoffman M, Monroe DM. Coagulation 2006: A modern view
der. Our data suggest that enhanced fibrinolysis could of hemostasis. Hematol Oncol Clin N Am 2007;21:1–11.
Bleeding in Greyhounds 533

9. Moake JL. Mechanisms of disease: Thrombotic microangio- dogs undergoing surgery for fracture repair. Am J Vet Res
pathies. N Eng J Med 2000;347:589–600. 2005;66:1356–1363.
10. Martin JN, Rose CH, Briery CM. Understanding and man- 25. Gaal T, Halmay D, Kocsis R, Abonyi-Toth Z. Evaluation of
aging HELLP syndrome: The integral role of aggressive the effect of ketoprofen and carprofen on platelet function in dogs
glucocorticoids for mother and child. Am J Obstet Gynecol studied by PFA-100 point-of-care analyser. Acta Vet Hung
2006;195:914–934. 2007;55:287–294.
11. Buchanan GR, Adix L. Grading for hemorrhage in children 26. Brooks M. Von Willebrand disease. In: Feldman BF, Zinkl
with idiopathic thrombocytopenic purpura. J Pediatr 2002;141:683– JG, Jain NC, eds. Schalm’s Veterinary Hematology, 5th ed. Phila-
688. delphia, PA: Lippincott Williams and Wilkins; 2000:509–515.
12. Kundu SK, Heilmann EJ, Sio R, et al. Description of an in 27. Fabrizio F, Baumwart R, Cline MC, et al. Functional sys-
vitro platelet function analyzer PFA-100TM. Semin Throm Hae- tolic murmur in retired racing Greyhounds. J Vet Intern Med
most 1995;21(Suppl 2):106–112. 2006;20:78–82.
13. Mammen EF, Comp PC, Gosselin R, et al. PFA-100TM sys- 28. Tarnow I, Kristensen AM, Olsen LH, et al. Dogs with heart
tem: A new method for assessment of platelet dysfunction. Semin diseases causing turbulent high-velocity blood flow have changes in
Thromb Hemost 1998;24:195–202. platelet function and von Willebrand multimer distribution. J Vet
14. Iazbik MC, Couto CG, Gray TL, Kociba G. Hemostatic Intern Med 2005;19:515–522.
evaluation of canine plasma collected for transfusion and stored 29. Blann AD, Naqvi T, Waite M, McCollum CN. Von Wille-
under different conditions. Am J Vet Res 2001;62:734–735. brand factor and endothelial damage in essential hypertension.
15. Otto CM, Rieser TM, Brooks MB, et al. Evidence of hyper- J Hum Hypertens 1993;7:107–111.
coagulability in dogs with parvoviral enteritis. J Am Vet Med Assoc 30. Cox RX, Peterson LH, Detweiler DK. Comparison of arte-
2005;10:1500–1504. rial hemodynamics in the mongrel dog and the racing Greyhound.
16. Benson RE, Catalfamo JL, Brooks M, Dodds WJ. A sensi- Am J Physiol 1976;230:211–218.
tive immunoassay for von Willebrand factor. J Immunoassay 31. Couto CG, Iazbik MC. Effects of blood donation on arterial
1991;12:371–390. pressure in retired racing Greyhounds. J Vet Intern Med
17. Sabino EP, Erb HN, Catalfamo JL. Development of a colla- 2005;19:845–848.
gen-binding activity assay as a screening test for type II von 32. Agren A, Wiman B, Schulman S. Laboratory evidence of
Willebrand disease in dogs. Am J Vet Res 2006;67:242–249. hyperfibrinolysis in association with low plasminogen activator in-
18. Favaloro EJ. Collagen binding assay for von Willebrand fac- hibitor type 1 activity. Blood Coagul Fibrinolysis 2007;18:657–660.
tor (VWF:CBA): Detection of von Willebrands disease (VWD), and 33. Hu KO, Yu AS, Tiyyagura L, et al. Hyperfibrinolytic activity
discrimination of VWD subtypes, depends on collagen source. in hospitalized cirrhotic patients in a referral liver unit. Am J
Thromb Haemost 2000;83:127–135. Gastroenterol 2001;96:1581–1586.
19. Lanevschi A, Kramer JW, Greene SA, Meyers KM. Evalu- 34. Ross J, Dallap BL, Dolente BA, Sweeney RW. Pharmacoki-
ation of chromogenic substrate assays for fibrinolytic analytes in netics and pharmacodynamics of e-amicocaproic acid in horses. Am
dogs. Am J Vet Res 1996;57:1124–1130. J Vet Res 2007;68:1016–1021.
20. Stokol T, Brooks MB, Erb HN, Mauldin GE D-dimer con- 35. Millis DL, Hauptman JG, Richter M. Preoperative and post-
centrations in healthy dogs and dogs with disseminated operative hemostatic profiles of dogs undergoing ovariohysterectomy.
intravascular coagulation. Am J Vet Res 2000;61:393–398. Cornell Vet 1992;82:465–470.
21. Triplett DA, Harms CS. Factor XIII deficiency screen. In: 36. Siemens HJ, Brueckner S, Hagekberg S, et al. Course of mo-
Triplett DA, ed. Procedures for the Coagulation Laboratory. Chi- lecular hemostatic markers during and after different surgical
cago, IL: Educational Products Division; 1981:67–68. procedures. J Clin Anesth 1999;11:622–629.
22. Lorand L. Sol Sherry lecture in thrombosis: Research on clot 37. Lippi G, Montagnana M, Regis D, et al. Plasma D-dimer
stabilization provides clues for improving thrombolytic therapies. variation following elective orthopaedic surgery. Blood Coagul
Arterioscler Thromb Vasc Biol 2000;20:2–9. Fibrinolysis 2006;17:87–88.
23. Barr SC, Ludders JW, Looney AL, et al. Platelet aggregation 38. Cerneca E, Simeone R, Bruno G, Gombaci A. Coagulation
in dogs after sedation with acepromazine and atropine and during parameters in senior athletes practicing endurance activity. J Sports
subsequent general anesthesia and surgery. Am J Vet Res Med Phys Fitness 2005;45:576–579.
1992;53:2067–2070. 39. Shibata J, Hasegawa J, Siemens HJ, et al. Hemostasis and
24. Bergmann HM, Nolte IJ, Kramer S. Effects of preoperative coagulation at a hematocrit level of 0.85: Functional consequences
administration of carprofen on renal function and hemostasis in of erythrocytosis. Blood 2003;101:4416–4422.
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Dewclaws in wolves as evidence of admixed ancestry with dogs

Article  in  Canadian Journal of Zoology · February 2011


DOI: 10.1139/z03-183

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Dewclaws in wolves as evidence of admixed


ancestry with dogs
Paolo Ciucci, Vittorio Lucchini, Luigi Boitani, and Ettore Randi

Abstract: Vestigial first toes (dewclaws) on the hind legs are common in large dog (Canis lupus familiaris) breeds but
are absent in wild canids, including wolves (Canis lupus). Based on observational criteria, dewclaws in wolves have
been generally regarded as a clue of hybridization with dogs, although this was not substantiated by molecular evi-
dence. By means of population assignment and genetic admixture analysis, we investigated individual genotypes of
three dewclawed wolves from Tuscany (central Italy, 1993–2001). Based on 18 microsatellite markers, dewclawed
wolves were not uniquely assigned to the Italian wolf population but appeared to be second or later generation back-
crosses of wolf–dog hybrids. Alleles uniquely shared with dogs, and mitochondrial DNA and Y haplotypes identical to
those of Italian wolves, further supported their admixed ancestry. Although patterns of dewclaw inheritance in wolf–
dog hybrids and backcrosses have not been ascertained, we conclude that dewclaws in wolves, when present, are a
clue of admixed ancestry, probably originating in areas where large dog breeds are involved in cross-matings. Other
“atypical” morphological traits (e.g., white nails, atypical color patterns or body proportions, dental anomalies) as well
might be reliable clues of admixed ancestry, and they deserve careful monitoring and molecular investigation.

Résumé : Des premiers orteils vestigiaux (ergots) existent fréquemment sur les pattes postérieures des races de chiens
(Canis lupus familiaris) de grande taille, mais sont absents chez les canidés sauvages, y compris les loups (Canis lu-
pus). En se basant sur des critères visuels, on a généralement considéré la présence d’ergots chez les loups comme un
indice d’une hybridation avec les chiens, bien que les données moléculaires n’aient pas appuyé cette conclusion. Nous
avons étudié les génotypes individuels de trois loups de Toscane (Italie centrale, 1993–2001) qui possèdent des ergots
au moyen d’une méthode d’assignation de population et d’une analyse de mélange génétique. D’après 18 marqueurs
microsatellites, les loups à ergots ne se regroupent pas exclusivement avec la population italienne de loups, mais ils
semblent être des hybrides loups–chiens issus de rétrocroisements de seconde génération ou de génération précédente.
Des allèles communs avec seulement les chiens, d’une part, et des haplotypes ADN mitochondrial et Y identiques à
ceux des loups italiens, d’autre part, viennent confirmer leur ascendance mixte. Bien que les patterns de transmission
des ergots chez les hybrides loups–chiens et chez les animaux issus de rétrocroisements n’aient pas été déterminés,
nous croyons que la présence d’ergots chez les loups est un indice d’une ascendance mixte, provenant de régions où
des chiens de races de grande taille sont impliqués dans les accouplements mixtes. D’autres caractères morphologiques
« particuliers » (e.g., tels que les ongles blancs, les patterns de couleur ou les proportions corporelles inusités et les
anomalies dentaires) peuvent aussi s’avérer être des indices fiables d’ascendance mixte; ils méritent un suivi attentif et
devraient donner lieu à une analyse moléculaire.
[Traduit par la Rédaction] Ciucci et al. 2081

Introduction (Boitani 1983, 1984; Bibikov 1985; Blanco et al. 1992;


Andersone et al. 2002). However, until recently wolf–dog
Hybridization between wolves (Canis lupus) and domestic hybrids have been diagnosed solely on the basis of atypical
dogs (Canis lupus familiaris) has often been feared in Eur- or anomalous morphological characters (i.e., size, propor-
asia in areas where human-induced low wolf densities, habi- tions, color patterns, etc.; Kronit 1971 cited in Andersone et
tat fragmentation, and large number of free-ranging dogs al. 2002; Boitani 1983; Bibikov 1985), a method whose reli-
increase the chances of nonpredatory wolf–dog encounters ability is limited because it is essentially observational and

Received 3 October 2002. Accepted 7 October 2003. Published on the NRC Research Press Web site at http://cjz.nrc.ca on
23 January 2004.
P. Ciucci1 and L. Boitani. Università di Roma “La Sapienza”, Dipartimento di Biologia Animale e dell’Uomo, Viale
dell’Università, 32-00185 Roma, Italy.
V. Lucchini and E. Randi. Istituto Nazionale per la Fauna Selvatica, Via Cà Fornacetta, 9-40064 Ozzano Emilia, Italy.
1
Corresponding author (e-mail: paolo.ciucci@uniroma1.it).

Can. J. Zool. 81: 2077–2081 (2003) doi: 10.1139/Z03-183 © 2003 NRC Canada

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2078 Can. J. Zool. Vol. 81, 2003

subjective. In addition, not all morphological variation has a tional maternal and paternal genetic markers, to assess the
genetic basis, and hybrids are not always morphologically individual genotypes of dewclawed wolves and compared
distinguishable from the parental taxon (Allendorf et al. them with Italian wolves and dogs.
2001).
Although recent DNA population-level studies failed to
Methods
reveal large-scale introgression of dog genes in European
wolf populations (Vilà and Wayne 1999; Randi et al. 2000; In 1993–2001 we closely examined six wolves from the
Randi and Lucchini 2002), molecular genetic markers did al- Tuscany region (central Italy), four of which were illegally
low detection of some wolf–dog hybrids in Europe (Vilà et or accidentally killed and two were livetrapped as part of a
al. 1997, 2003; Randi et al. 2000; Andersone at al. 2002; radiotelemetry study. Three of these wolves displayed the
Randi and Lucchini 2002; Lucchini et al. 2004). In addition, dewclaw on both hind legs, representing the first and only
rare backcrosses of wolf–dog hybrids into the parental wolf wolves observed in Italy with this character out of 206 car-
population were already reported in Italy by Randi and casses examined from 1986 to 2001 (V. Guberti, personal
Lucchini (2002) who called for the development of a suite of communication), and 19 wolves livetrapped since the 1970s
morphological, behavioral, and molecular traits to aid in the (Ciucci and Boitani 1998). Age of dead or livetrapped
distinction of pure wolf populations and areas of potential wolves was estimated from patterns of dentition consump-
introgression. However, limited molecular evidence is cur- tion (Gipson et al. 2000). All dewclawed wolves (W520,
rently available on the admixed nature of anomalous W535, W587) were from an area in south-central Tuscany,
morphological characters, which are generally considered which composes a secondary branch of the main wolf distri-
“atypical” in wolves. bution in Italy. The area consists of semiagricultural land-
The dewclaw, a vestigial first toe on the hind leg, is never scapes at about 300 m a.s.l. with extensive sheep production
found in wolves but can be common in large dog breeds. and large numbers of maremma-type guard dogs, most of
Dewclaws in wolves were never observed by several North which display dewclaws.
American and Eurasian wolf biologists, and were not found Wolf W535 was a 32-kg 6-month-old male livetrapped
in the large wolf-pelt collections from Spain, Portugal, and and radio-collared in November 1993 in an area of the Prov-
Italy (J.C. Blanco, L.D. Mech, F. Petrucci–Fonseca, S. Reig, ince of Siena where a wolf pack was being monitored by ra-
C. Vilà, personal communications). A case was reported from diotelemetry. W535 showed a high degree of association
Extremadura (Spain), in an area where wolves, large mastiff with W390, the radio-collared alpha male of the pack and
dogs, and putative wolf–dog hybrids were known to occur potential father of W535, and displayed ecological and be-
(Teruelo and Valverde 1992: 261). Similarly, from a large havioral attitudes typical of wolves (P. Ciucci, L. Boitani,
collection of dingo (Canis lupus dingo) skins in the Natural E. Tedesco, and L. Artoni, unpublished data). Although
History Museum of London, only one specimen displayed W390 did not display dewclaws and matched the phenotypic
dewclaws; however, its skin did not conform to the standard standard of wolves, we never closely observed W535’s
of purebred dingoes (J. Clutton-Brock, personal communica- mother or siblings. W535 died, apparently in good health,
tion). In coyotes (Canis latrans), dewclaws are commonly from a vehicle collision in February 1994 at 9 months,
believed by some researchers to be a sign of hybridization whereas W390 was illegally shot 1 month later. W520 was a
with dogs (L.D. Mech, personal communication), and the 28-kg 9-month-old male poisoned in February 1999 also in
same anecdotal evidence appears to hold for wolves. A com- the Province of Siena, and W587 was an unaged female ille-
pilation of observational material reviewed by wolf special- gally shot in November 2001 in the Province of Grosseto (N.
ists from the Great Lakes area in North America suggested Cini, personal communication). Distances between the local-
that dewclaws in wolves indicated hybridization with dogs ities where the three wolves were found ranged 20–60 km.
(Duman 2001), although no molecular investigation sup- Phenotypically, the three dewclawed wolves were judged by
ported this conclusion. More recently, Andersone et al. experienced observers to fall within the standard variability
(2002) found dewcalws in a litter of seven mongrel pups of Italian wolves, with the exception of W520’s skull, which
from northern Latvia whose individual genotypes (16 micro- at later inspection was, on average, smaller and displayed a
satellites) showed that most of the alleles were common with pronounced prognathism. W587 was found decapitated.
dogs, whereas their mitochondrial DNA (mtDNA) haplotype All dewclawed wolves were tissue-sampled for genetic
was typical of other Latvian wolves. analyses, and DNA extraction and microsatellite genotyping
In contrast to wolves, dewclaws can be quite common in followed protocols by Randi and Lucchini (2002). We also
large domestic dogs. Although in some breeds the character included in the analysis a set of 100 Italian wolves and 95
is maintained through artificial selection (e.g., Great Pyre- domestic and feral dogs as reference populations. Individual
nees, St. Bernard), in others (Bernese, Newfoundland) it keeps genotypes of the dewclawed wolves were determined at 18
reappearing in the population despite being consistently se- loci assigned to 16 different chromosomes (Neff et al. 1999)
lected against (Alberch 1985). Both developmental (Alberch as described in Randi and Lucchini (2002). Wolves and dogs
1985) and genetic (Galis et al. 2001) arguments have been have distinct multilocus microsatellite genotypes, and hy-
used to explain the occurrence of dewclaws in dogs (see Dis- brids can be identified by assignment procedures (Randi and
cussion). Based on these theoretical grounds, we hypothe- Lucchini 2002; Vilà et al. 2003). Multilocus genotypes of
sized that dewclaws in wolves represent a trait inherited dewclawed wolves were assigned to the Italian wolf or dog
through cross-mating with dogs rather than an expression of populations using two procedures: a factorial correspondence
phenotypic variation in wolves. To test this hypothesis we analysis (FCA; Benzécri 1973) of individual multilocus
analyzed 18 canine microsatellite loci, supported by addi- scores computed using GENETIX version 4.02 (Belkhir et

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Ciucci et al. 2079

Fig. 1. Scores of individual wolf (Canis lupus) and dog (Canis lupus familiaris) microsatellite genotypes plotted on the first two axes
of a factorial correspondence analysis (FCA) performed using GENETIX.

Table 1. Alleles (size given as base pairs, including primers) of six microsatellite loci that were observed in
the dewclawed wolves (Canis lupus), which are shared with dogs (Canis lupus familiaris) but are absent in
the Italian wolf population (cf. Randi and Lucchini 2002).
CPH2 CPH6 CPH7 CPH12 C20.253 FH2132
W520 — — — — — —
W535 94 (0.34) — — — — —
W587 — 122 (0.15) 170 (0.32) 196 (0.09) 106 (0.76) 327 (0.05)
Note: Values in parentheses are the frequency of the allele in the dog population.

al. 1996–2001) and a Bayesian admixture analyses imple- 0.60–0.92), providing further evidence of their admixed an-
mented in STRUCTURE version 1.0 (Pritchard et al. 2000). cestry with dogs. Males W535 and W520 shared a unique Y
We used STRUCTURE with 100 000 iterations following a haplotype that is very common in the Italian wolf population
burn-in period of 10 000 iterations to identify the number of but absent in the dogs that we analyzed (V. Lucchini and E.
genetically distinct clusters that maximize the likelihood of Randi, unpublished data). W520’s microsatellite alleles were
the data and to assign the individuals to the clusters using also found in Italian wolves, but W535 and W587 shared
only genetic information (Randi and Lucchini 2002; Luc- with dogs alleles that were absent from the Italian wolf pop-
chini et al. 2004). The amount of dog ancestry of the three ulation (Table 1). All three dewclawed wolves shared the
dewclawed wolves up to the second generation in the past unique mtDNA haplotype of the Italian wolf population
was estimated using STRUCTURE (options Usepopinfo = 1 (Randi et al. 2000).
and Genesback = 2), whereas their relatedness (r) was calcu- Estimates of the amount of dog ancestry up to the second
lated using the program KINSHIP version 1.3.1 (Goodnight generation in the past revealed that W587 had a high compo-
and Queller 1999). To check for male wolf ancestry in nent of dog ancestry (q = 0.99) at the second generation,
W535 and W520, we also investigated Y markers using four whereas W535 and W520 had lower values (q = 0.014 and
microsatellites that map on Y chromosomes (Sundqvist et al. q = 0.122, respectively), suggesting that their hybridization
2001). Further methodological details are provided in Randi origin could only be older than two generations. Kinship
and Lucchini (2002) and Lucchini et al. (2004). analysis suggested that W535 and W520 could be first-
degree relatives (r = 0.31; cf. Lucchini et al. 2002), which is
further supported (p = 0.95) by a simulation using 1000 rep-
Results licates (Goodnight and Queller 1999). W390 was assigned to
Italian wolves by Bayesian admixture analyses.
The FCA split the dog and Italian wolf populations into Individual heterozygosities (H; Nei 1987) of W535,
two clearly separated clusters, and the three dewclawed W520, and W587 ranged from 0.32 to 0.52, and only W535
wolves were marginal to the Italian wolf genotype distribu- (H = 0.32) was lower than the average heterozygosity for all
tion (Fig. 1). In addition, the Bayesian procedure assigned Italian wolves (H = 0.44; Randi and Lucchini 2002;
each wolf and dog to the correct populations with high q Lucchini et al. 2004).
values (>0.99) and small 90% confidence intervals (dog:
0.97–1; wolf: 0.99–1), where the q value represents the pro-
portion of the genome that originate from that particular Discussion
population. In contrast, dewclawed wolves were assigned to
the Italian wolf population with lower q values (W535: q = It has long been recognized that the occurrence of
0.95; W520: q = 0.90; W587: q = 0.76) and larger 90% con- dewclaws in dogs is correlated with body size and is more
fidence intervals (W520: 0.58–1; W535: 0.75–1; W587: frequent in large breeds (Darwin 1868: 35; Alberch 1985).

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2080 Can. J. Zool. Vol. 81, 2003

From a developmental point of view, the phenotypic varia- traits), which indicated hybridization, but there was no men-
tion necessary for the development of extra toes appears to tion of dewclaws (Andersone et al. 2002).
be linked with the size (number of cells) of the embryonic Relatedness values among the three dewclawed wolves
limb bud, which is larger in large dog breeds (Alberch suggest that at least two different hybridization events oc-
1985). By exceeding a minimum threshold value in the num- curred in this restricted area of Tuscany, reflecting local-
ber of limb-bud cells necessary to specify for extra toes ly predisposing conditions (i.e., widespread, large-livestock
during morphogenesis, dog breeders cannot eliminate the ap- guard dogs; low density and social disruption of local wolf
pearance of the trait by continuously selecting for large size packs; highly fragmented landscape). In addition, they share
(Alberch 1985). On the other hand, although mutations for the unique mtDNA haplotype of Italian wolves (Randi et al.
polydactyly are quite common in amniotes, they are not 2000), confirming the previously described directionality of
evolutionarily stable owing to the strong negative pleiotropic wolf–dog (and wolf–coyote) hybridization (i.e., female wolves
effects present during the phylotypic stage (Lande 1978; mating with male dogs or coyotes; Boitani 1983; Lehman et
Galis et al. 2001). In line with this theory, there are no pub- al. 1991; Gottelli et al. 1994; Roy et al. 1994; Vilà and
lished reports of dewclaws in wild canids except for a red Wayne 1999; Randi et al. 2000; Randi and Lucchini 2002;
fox (Vulpes vulpes) shot in 1913 on the island of Biskops- Vilà et al. 2003).
Arnö in Sweden (Lönnberg 1916). Being evolutionarily con- Although introgression of dog genes into the Italian wolf
strained in amniotes, polydactyly in large dog breeds could population is apparently very limited and wolves and dogs
have been fostered by intense artificial selection, whereas are genetically differentiated (Randi and Lucchini 2002), our
the expected negative pleiotropic effects might be responsi- results provide additional evidence that wolves and dogs do
ble for the shorter life, higher incidence of locomotory dis- hybridize in the wild and that, at least occasionally, hybrids
eases, and higher mortality rates reported for polydactylous can be successfully reintegrated into the wolf population
dogs (Galis et al. 2001: 639). (Andersone et al. 2002; Randi and Lucchini 2002; Vilà et al.
Although possible in principle, it is therefore quite un- 2003; Lucchini et al. 2004). Following Allendorf et al.’s
likely that polydactyly could stochastically appear and be (2001) categorization, these findings suggest that the Italian
maintained in wolves, even at the level of the local, inbred wolf population might represent an intermediate case be-
populations. Accordingly, the heterozygosity observed in the tween type 4 and type 5 anthropogenic hybridization, with a
three dewclawed wolves we collected did not reveal high widespread pure wolf parental population interspersed with
levels of inbreeding compared with the Italian wolf popula- few, localized areas of very limited introgression. In this re-
tion. Alternatively, the extreme rarity of dewclawed wolves spect, as quantitative assessment of anthropogenic hybridiza-
and their exclusive occurrence in an area with high densities tion is crucial to evaluate conservation scenarios (Allendorf
of large dog breeds suggest that the trait represents a charac- et al. 2001), intensive genetic sampling and monitoring are
ter possibly displayed by wolf–dog hybrids and backcrosses. urgently needed in areas of suspected hybridization. Map-
Although we did not investigate patterns of genetic inheri- ping these areas on a regional scale would benefit from
tance of the dewclaws either in dogs or in wolf–dog hybrids, screening diagnostic morphological traits that are reliable
our results confirmed that the dewclawed wolves we col- clues of admixed ancestry (Randi and Lucchini 2002).
lected in Tuscany were wolves of admixed ancestry, which Among these, dewclaws on wolves are expected to be lim-
supported our original hypothesis. Since they shared the ited to cross-matings involving some large dog breeds. Other
mtDNA and Y haplotypes of the Italian wolf population, but presumptive morphological traits might be reliable as well
their Bayesian assignment probabilities were not intermedi- (e.g., white nails, atypical color patterns or body propor-
ate between dogs and wolves as expected for F1 hybrids tions, dental anomalies; cf. Duman 2001), provided that their
(Randi and Lucchini 2002), they were most likely back- molecular correlates are further investigated.
crosses of wolf–dog hybrids into the Italian wolf population.
The amount of dog ancestry estimated up to the second gen- Acknowledgments
eration in the past revealed that the dewclawed wolves we
sampled might represent second (W587) or later (W520, This study was funded by the Region of Tuscany and by
W535) generation backcrosses, with the number of alleles the Italian National Institute of Wildlife. We thank L. Artoni
uniquely shared with the dog population increasingly diluted and E. Tedesco for field assistance, and an anonymous ref-
by the number of generations since the origin of the hybrid- eree for comments on an earlier draft of the manuscript.
ization. C.D. Soulsbury kindly reviewed the English style of the text.
It is noteworthy that according to observational criteria
alone, and with the notable exception of dewclaws, experi- References
enced observers would not have distinguished the three Alberch, P. 1985. Developmental constraints: why St. Bernard of-
wolves from pure wolves. Unfortunately, in all three cases ten have extra digit and poodles never do. Am. Nat. 126: 430–
we could not examine parents or siblings for the presence of 433.
dewclaws. The case reported by Andersone et al. (2002) Allendorf, F.W., Leary, R.F., Spruell, P., and Wenburg, J.K. 2001.
supported our findings that dewclaws in wolves originated The problems with hybrids: setting conservation guidelines.
from cross-mating with dogs, even though the dewclawed Trends Ecol. Evol. 16: 613–622.
pups they analyzed were obviously different from the Andersone, ð., Lucchini, V., Randi, E., and OzoliÚ, J. 2002. Hy-
phenotypic standard of Latvian wolves. As successively con- bridization between wolves and dogs in Latvia as documented
firmed by molecular markers, both presumptive parents of using mitochondrial and microsatellite DNA markers. Mamm.
these pups shared some dog-like traits (color patterns, skull Biol. 67: 79–90.

© 2003 NRC Canada

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Ciucci et al. 2081

Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., and Bonhomme, F. Lucchini, V., Fabbri, E., Marucco, F., Ricci, S., Boitani, L., and
1996–2001. GENETIX 4.02, logiciel sous WINDOWS TM pour Randi, E. 2002. Non-invasive molecular tracking of colonizing
la génétique des populations. Laboratorie Génome, Populations, wolf (Canis lupus) packs in the western Alps. Mol. Ecol. 11:
Interactions, Centre National de la Recherche Scientifique – 857–868.
Unité Mixte de la Recherche (CNRS–UMP) 5000, Université Lucchini, V., Galov, A., and Randi, E. 2004. Evidence of genetic
de Montpellier II, Montpellier, France. Available from http:// distinction and long-term population decline in wolves (Canis
www.univ-montp2.fr/~genetix/genetics.htm [accessed 10 May 2002]. lupus) in the Italian Apennines. Mol. Ecol. In press.
Benzécri, J.P. 1973. L’analyse des donnèes: T.2, L’analyse des cor- Neff, M.W., Broman, K.W., Mellersh, C.S., Ray, K., Acland, G.M.,
respondences. Dunoud, Paris, France. Aguirre, G.D., Ziegle, J.S., Ostrander, E.A., and Rine, J. 1999.
Bibikov, D.I. 1985. The wolf. History, systematics, morphology, A second-generation linkage map of the domestic dog, Canis
ecology. Nauka, Moscow. [In Russian.] familiariz. Genetics, 151: 803–820.
Blanco, J.C., Reig, S., and de la Cuesta, L. 1992. Distribution, sta- Nei, M. 1987. Molecular evolutionary genetics. Columbia Univer-
tus and conservation problems of the wolf Canis lupus in Spain. sity Press, New York.
Biol. Conserv. 60: 73–80. Peterson, R.O. 1977. Wolf ecology and prey relationship on Isle
Boitani, L. 1983. Wolf and dog competition in Italy. Acta Zool. Royale. Nat. Park Serv. Sci. Monogr. Ser. No. 11.
Fenn. 174: 259–264. Pritchard, J.K., Stephens, M., and Donnelly, P.J. 2000. Inference of
Boitani, L. 1984. Genetic considerations on wolf conservation in population structure using multilocus genotype data. Genetics,
Italy. Boll. Zool. 51: 367–373. 155: 945–959. Available from http://pritch.bds.uchicago.edu
Boitani, L. 1992. Wolf research and conservation in Italy. Biol. [accessed 2 May 2002].
Conserv. 61: 125–132. Randi, E., Lucchini, V., Christensen, M.F., Mucci, N., Funk, S.M.,
Ciucci, P., and Boitani, L. 1998. Il lupo. Elementi di biologia, Dolf, G., and Loeschke, V. 2000. Mitochondrial DNA variability
gestione e ricerca. Istituto Nazionale della Fauna Selvatica in Italian and east European wolves: detecting the consequences
“Alessandro Ghigi”, Documenti Tecnici no. 23. [In Italian.] of small population size and hybridization. Conserv. Biol. 14:
Darwin, C. 1868. The variation of animals and plants under domes- 464–473.
tication. Vol. I. J. Murray, London. Randi, E., and Lucchini, V. 2002. Detecting rare introgression of
Duman, B. 2001. Differentiating Great Lakes area native wild domestic dog genes into wild wolf (Canis lupus) populations by
wolves from dogs and wolf–dog hybrids. Earth Voices, LLC, Bayesian admixture analyses of microsatellite variation. Conserv.
Howell, Mich. Genet. 3: 31–45.
Galis, F., Alphen, J.J.M., and Metz, J.A.J. 2001. Why five fingers? Roy, M.S., Geffen, E., Smith, D., Otsrander, E.A., and Wayne,
Evolutionary constraints on digits numbers. Trends Ecol. Evol. R.K. 1994. Patterns of differentiation and hybridization in North
16: 637–646. American wolflike canids, revealed by analysis of microsatellite
Gipson, P.S., Ballard, W.B., Nowak, R.M., and Mech, L.D. 2000. loci. Mol. Biol. Evol. 11: 553–570.
Accuracy and precision of estimating age of gray wolves by Sundqvist, A.K., Ellegren, H., Olivier, M., and Vilà, C. 2001. Y
tooth wear. J. Wildl. Manag. 64: 752–758. chromosome haplotyping in Scandinavian wolves (Canis lupus)
Goodnight, K.F., and Queller, D.C. 1999. Computer software for based on microsatellite markers. Mol. Ecol. 10: 1959–1966.
performing likelihood tests of pedegree relationship using ge- Teruelo, S., and Valverde, J.A. 1992. Los lobos de Morla. Circulo
netic markers. Mol. Ecol. 8: 1231–1234. de Bibliofilia Venatoria, Madrid, Spain.
Gottelli, D., Sillero–Zubiri, C., Applebaum, G.D., Roy, M.S., Vilà, C., and Wayne, R.K. 1999. Hybridization between wolves
Girman, D.J., García–Moreno, J., Ostrander, E.A., and Wayne, and dogs. Conserv. Biol. 13: 195–198.
R.K. 1994. Molecular genetics of the most endangered canid: Vilà, C., Savolainen, P., Maldonado, J.E., Amorim, I.R., Rice, J.E.,
the Ethiopian wolf Canis simensis. Mol. Ecol. 3: 301–312. Honeycutt, R.L., Crandall, K.A., Lunderberg, J., and Wayne,
Lande, R. 1978. Evolutionary mechanism of limb loss in tetrapods. R.K. 1997. Multiple and ancient origins of the domestic dog.
Evolution, 32: 73–92. Science (Wash., D.C.), 276: 1687–1689.
Lehman, N., Eisenhawer, A., Hansen, K., Mech, L.D., Peterson, Vilà, C., Walker, C., Sundqvist, A-K., Flagstad, Ø., Andersone, ð.,
R.O., and Wayne, R.K. 1991. Introgression of coyote mitochon- Casulli, A., Kojola, I., Valdmann, H., Halverson, J., and
drial DNA into sympatric North American gray wolf popula- Ellegren, H. 2003. Combined use of maternal, paternal and bi-
tions. Evolution, 45: 104–119. parental genetic markers for the identification of wolf–dog hy-
Lönnberg, E. 1916. A remarkable occurrence of the first hind toe brids. Heredity, 90: 17–24.
in the common fox (Vulpes vulpes). Ark. Zool. 10: 1–5.

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