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Otitis media in guinea pigs: Pathology

and bacteriology
ARTICLE in LABORATORY ANIMALS JULY 1986
Impact Factor: 1.12 DOI: 10.1258/002367786780865601 Source: PubMed

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242

Laboratory Animals (1986) 20, 242-248.

Otitis media in guineapigs: pathology and bacteriology

R. BOOT & H. C. WALVOORT2
I Department of Animal Supply and Laboratory for Parasitology and Mycology and 2 Laboratory for
Pathology, National Institute of Public Health and Environmental Hygiene, P.O. Box I, 3720 BA Bilthoven,
The Netherlands

Summary
In the course of post-mortem examination of conventional random-bred and inbred (immunosuppressed)
strain 2/N guinea pigs kept in separate quarters, otitis
media was diagnosed in 62 of 462 animals (13'4%)
and 18 of 66 animals (27,3%) respectively. Clinical
signs of otitis media were seen in only two randombred animals but in nearly 50% of affected inbred
animals. In random-bred guineapigs, purulent, often
bilateral, otitis media was associated mainly with the
isolation of Streptococcus zooepidemicus, Bordetella
bronchiseptica, Pasteurella and Actinobacillus spp.
and micrococci. In strain 2/N guineapigs serous or
purulent often bilateral otitis media was associated
mainly with the isolation of B. bronchiseptica and
Pseudomonas aeruginosa serotypes 10 and 11. The
simultaneous occurrence of similar pathogenic bac

teria in both ears of bilaterally affected animals and

in pneumonic lung tissue (in random-bred animals)

suggested ascending and descending infection
originating from the upper respiratory tract. It is
concluded that otitis media, associated with the isolation of a variety of respiratory bacterial species,
must be considered a major disease problem in
guineapigs.
Keywords: Otitis media; Guineapigs; Bacterial infections
Otitis media is an established disease entity in
conventional guineapigs. Responding to a questionnaire, five of 33 institutions considered otitis media
important in this animal species (Seamer & Chesterman, 1967) but only limited information has
appeared in the literature on the pathology and
bacteriology of this lesion. Kohn (1974) examined
31 guineapigs with torticollis from three different
commercial breeders and Streptococcus zooepidemicus (Lancefield group C) was isolated most
frequently, followed by S. pneumoniae. Rigby
(1976) stated that S. pneumoniae infection in
guineapigs was probably most commonly seen as
otitis media but data were not presented. Using
X-ray examination Wagner et al. (1976) diagnosed
otitis media in 13% of guineapigs and S. pneumoReceived 28 August 1985. Accepted 24 February 1986.

niae (20%), S. zooepidemicus (15%), Bordetella

bronchiseptica (12%) and Pseudomonas aeruginosa
(11 %) were isolated from animals showing
radiopacity of the tympanic bulla.
We report the pathology and bacteriology of
mostly asymptomatic cases of otitis media observed
in random-bred and inbred (strain 2/N) conventional guineapigs.
Materials and methods
Sources and methods of isolation
All animals originated from the random-bred or the
inbred (strain 2/N) colony in our Institute. The
colonies were kept in separate quarters under
conventional conditions. The animal technicians
supervising the inbred strain colony also worked
with conventional rabbits, rats and mice during part

of the study. The random-bred colony housed 2000

breeding females on average and showed a mortality
rate of about 5% per year. The inbred colony, the
production of which gradually replaced initially
imported animals, housed 50 breeding females on
average and showed a similar mortality rate. In both
colonies a variety of common bacterial pathogens
was present as has been described earlier for the
random-bred colony (Boot, Oosterom & Walvoort,
1983).
Most random-bred guinea pigs examined were
recently weaned animals or were from vaccine
control experiments (innocuity tests). Most inbred
animals had been subjected to immunosuppression
by cyclophosphamide treatment or sublethal whole
body irradiation. At post-mortem examination the
tympanic bullae were opened and samples from
grossly affected middle ears were taken using a
sterile bacteriological wire. Initially only one ear
was sampled in animals showing signs of bilateral
ear infection.
Samples were inoculated onto two plain sheepblood agars, a sheep-blood agar containing nalidixic
acid (40 flg/ml) and an Endo agar. One sheep-blood
agar was incubated anaerobically for 48 h at 37C.
All other media were incubated aerobically for 48 h
at 37C.
Growth on agar media was identified using
standard bacteriological procedures as described by

Otitis media in guinea pigs

243

Cowan (1974). P. aeruginosa isolates were typed as

described by Habs (1957).
Results
The guineapigs autopsied comprised 462 randombred and 66 strain 2/N animals (Table 1). Otitis
media was diagnosed in 62 (134%) random-bred
and in 18 (273%) strain 21N animals, with both ears
being affected in 40 (645%) and 14 (778%) animals
respectively.
Clinical signs of otitis media, such as
torticollis,
were noted in only two random-bred
guineapigs but in nearly 50% of affected animals in
the inbred strain, where these signs were the basis
for culling. In 33 random-bred
and 11 strain 2/N
animals otitis media was considered
the principal
disease but was considered an incidental finding in
the other cases, in which pneumonia and enteritis
were the major lesions. A characteristic
pattern of
post-mortem
findings was seen at necropsy of many
guinea pigs irrespective of whether otitis media was
considered
a major or an incidental finding. This
pattern consisted of weight loss, dehydration,
a
nearly empty gastrointestinal
tract with a strikingly
small caecum and an enlarged adrenal cortex.
Macroscopically,
otitis media presented
as an
exudative lesion of the tympanic bulla, the nature of
the exudate varying from serous to purulent (Table
1). Chronic lesions were characterized
by hyperostosis of the tympanic bulla, which in some cases
nearly obliterated
the lumen. In one random-bred
and three inbred guineapigs
with bilateral otitis
there was a purulent lesion in one ear and a serous
lesion in the other.

Table 1. Pathomorphological

Bacteriological
findings in 76 middle ear samples
from the outbred guineapigs are given in Table 2.
From 10 of these samples (132%) no bacterial
growth was obtained.
The remaining 66 samples
yielded 108 isolates which were assigned to 13
different bacterial species or genera. Eighty-eight of
the isolates (815%) were made up of the four most
common
bacterial
species
or genera,
i.e. S.
zooepidemicus (Lancefield group C) (45 or 417%),
B. bronchiseptica (20 or 185%), Pasteurella and
Actinobacillus spp. (14 or 13%) and Micrococcus
spp. (9 or 83%). S. zooepidemicus was found in all
12 chronic lesions. Other bacterial species or genera
isolated were each detected in less than 55% of all
samples examined by cultivation.
Pure cultures were obtained
in 32 of the 66
samples
(485%)
yielding bacterial
growth and
consisted of S. zooepidemicus (mostly from purulent
exudates), B. bronchiseptica, Proteus spp., Enterobacter cloacae and faecal streptococci.
Bacteriological
findings in 23 middle ear samples
from the inbred guineapigs are presented in Table 3.
From one serous sample no bacterial growth was
obtained but the remaining 22 samples yielded 48
isolates, assigned to 11 bacterial species or genera.
Twenty-nine
of these isolates (604%) were classified as B. bronchiseptica (18 or 375%) or P.
aeruginosa (11 or 229%). From the chronic lesions
B. bronchiseptica (three isolates) and S. aureus
(three
isolates)
were isolated.
Other
bacterial
species or genera were each cultivated from less
than 12-5% of all samples examined.
Pure cultures were obtained
from 6 of the 22

features of otitis media in guineapigs

Number of guineapigs
Random-bred
Inbred

Lesion
Otitis media
As major lesion,

unilateral
bilateral
unilateral
bilateral

62

18

8
25
14
15

Total examined

462

66

Nature of lesion
Mucosal hyperaemia

Number of lesions

As incidental
finding,

Serous

Mucopurulent
Purulent
Not specified
Total
'Numerals

32 (4)"

Seromucous

3
52 (20)
8
102

12 (4)

2
16 (8)
2

32

in parentheses indicate the number of chronic lesions.

244

Boot & Walvoort

Table 2. Bacteriological findings in otitis media in conventional random-bred

guineapigs

Bacteria

Nature of lesion
Mucosal
hyperaemia Serous

Seromucous

Mucopurulent

Purulent

Not
specified

Number of samples
No growth

2
1

3
2

36

28
7

S. zooepidemicus
B. bronchiseptica
Pasteurella-Actinobacillus spp.
Micrococci
1
Diphtheroids
E. coli
Proteus spp.
E. cloacae
Faecal streptococci
Neisseria spp.
Aeromonas spp.
S. aureus
P. aeruginosa

10 (2)*
7 (4)
5

Total number of isolates

35 (9)

*Numerals in parentheses

Total
76
10

4 (3)
1
1

29 (16)
11 (3)
5
6
1
4
1 (1)

2
1
2

3
1

2 (1)
2 (2)
2

45
20
14
9
4
4
3
2
2
2
1

(21)
(7)

(I)
(I)
(2)

1
2

7 (3)

57 (20)

108 (32)

indicate the number of isolates (pure cultures).

Table 3. Bacteriological findings in otitis media in conventional strain 21N guineapigs

Bacteria

Nature of lesion
Serous
Purulent

Number of cases

10

No growth

1
10 (2)

Total number of isolates

28 (2)

*Numerals in parentheses

Total

23

12

7 (1)*
B. bronchiseptica
P. aeruginosa
2 (2)
Pasteurella-Actinobacillus spp. I (I)
S. aureus
1
Bacteroides spp.
2
E. coli
1
Klebsiella spp.
2
Diphtheroids
1
Proteus spp.
Faecal streptococci
Peptostreptococcus spp.
18 (4)

Not specified

18 (3)
11 (2)
3 (1)
3
3
3
2

8
2
2
1
2

I
1

48 (6)

indicate the number of isolates (pure cultures).

samples
(273%) yielding bacterial growth and
consisted of B. bronchiseptica, P. aeruginosa and a
member of the Pasteurella-Actinobacillus group. P.
aeruginosa isolates were of serotype 10 (two isolates) and serotype 11 (nine isolates).
The bacteriological
findings in animals in which
both affected ears were sampled are presented
in
Fig.!. Of the 12 random-bred
guineapigs involved.

five animals showed similar bacteriological

infection
of both ears. In all but four animals mixed infections
were detected. All animals positive for S. zooepidemicus yielded this micro-organism from both ears.
In th~ seven inbred guineapigs
involved.
four
animals showed similar bacteriological
infection of
both ears. In all but two animals mixed infections
were found. Four of five animals positive for B.

245

Otitis media in guineapigs

random bred
5 6 7 8

B.brfYlCflis~plica
- Actinobacillus

spp,

0
0

micrococci
diphtheroids
E. coli
Prot~us
E. cloaca~

faecal streptococci
N~iss~ria

KI~bsi~lIa

12

inbred
3 4 5

D
0

P aeruginosa

sPP.

~plosl~plococcus

11

sPP.

S. auretJs

Bact~roid~s

10

spp,

0 0

S. zoo~pid~micus

Pasl~lla

spp.

spp.

o cultivated from one ear

Fig. 1. Bacteriological

findings

in bilateral

bronchiseptica contained this micro-organism in

both ears.
Bacteriological findings in animals simultaneously
suffering from otitis media and respiratory tract
infections are presented in Fig. 2. Of the 17
random-bred guinea pigs involved (nine with unilateral and eight with bilateral ear infection) six
showed similar bacteriological infection at both
sampling sites. In nine of 12 animals with streptococcal otitis media this micro-organism was also
recovered from pneumonic lung tissue. In four of
eight animals with B. bronchiseptica-associated
otitis media this species was also cultivated from the
respiratory tract. Escherichia coli was found at both
sites in one animal and Proteus spp. in another.
Only one inbred guineapig showed a similar infec-

tion of both the lung and the middle ear yielding B.

bronchiseptica and P. aeruginosa from both sites.
Discussion
Our findings support the view that otitis media is a
common disease in guineapigs (Rigby, 1976; Wagner, 1979). On the basis of pathological findings the
incidence of the condition in our random-bred
animals (134%) is equ!'.J to the incidence (13%)
reported by Wagner et al. (1976). The inbred strain

otitis media in conventional

cultivated from both ears

guineapigs.

2/N guineapigs showed a higher incidence of both

pathological lesions and clinical signs, possibly due
to the severe immunosuppression exerted on most
of these animals. Asymptomatic otitis media in
guineapigs was reported by Wagner (1979) to occur
frequently. However, Sea mer and Chesterman
(1967) and Rigby (1976) reported torticollis,
incoordination and circling to be commonly observed, presumably dependent on extension of the
infection to the inner ear or brain. The incidence of
otitis media in our study will be an underestimation
since exact clinical data were not recorded. The
importance of otitis media as a disease condition for
guineapigs is suggested by its being considered the
major lesion in more than 50% of the random-bred
animals and in nearly 70% of the inbred animals in

which affected ears were found (Table 1).

Of serous samples from random-bred animals,
25% did not yield bacterial growth (Table 2). This
type of lesion might have reflected an early stage of
infection, possibly by a virus, before bacteria
established a secondary infection. Serous exudation
yielded bacterial growth more frequently in the
inbred animals (Table 3) than in random-bred
animals but only a limited number of samples were
examined. Serous exudates from random-bred animals had a wider range of bacterial species than

246

Boot & Walvoort

random bred
234

inbred

r------------------------,---...,1

B. bronchi~tic9
Pasteurella-Actinobacillus

micrococci

S. zo~pid~micus

spp.

IE!

0
0

faecal streptococci
Neisseria

SPP.

S. au~us

00

13

14

15

16

17

0 0

0
0

SPP.

11 12

0
0

E.co/i
Prot~us

10

0
0

~
I:>iI

P. a~ruginosa

cultivated

from

o middle ear
~

respiratory

both sites

tract

Fig. 2. Bacteriological findings in conventional guineapigs suffering from respiratory tract and middle ear infections.

purulent exudates. The role of the less common

bacterial species in otitis media is not clear. The
isolation of small numbers of micrococci, diphtheroids and Neisseria spp. that are normally present on
the skin and on mucous membranes could result
from contamination during sampling. However, the
detection of large numbers of these species and of
Enterobacteriaceae and faecal streptococci, sometimes in pure culture, suggested a pathogenic role
for these organisms. Synergy of aerobic and facultatively anaerobic weak pathogens in mixed infections, which were frequently detected in this study,
is well known (MacDonald, 1962; Roberts, 1967;
Thore, Burman & Holm, 1982). Fulghum et al.
(1982) described a comparable effect of mixtures of
aerobic and anaerobic weak pathogens and the
much more pathogenic species S. pneumoniae in
experimental otitis media in gerbils and chinchillas.
Thore, Burman and Holm (1982) did not find severe
acute otitis media after application of Bacteroides
asaccharolyticus or Peptostreptococcus micros but
concluded that there was serious pathogenic potential for Propionibacterium acnes in guineapigs.
Overall findings in random-bred
guineapigs
showed the prevalence of purulent often bilateral
otitis media associated with the isolation of S.
zooepidemicus. B. bronchiseptica, Pasteurella and
Actinobacillus spp. and micrococci. These findings
differed clearly from the occurrence of serous or
purulent often bilateral ear infection in strain 2/N
animals from which B. bronchiseptica and P. aerugi-

nosa were the predominant isolates. Chronic lesions

were invariably associated with S. zooepidemicus in
the random-bred animals but with B. bronchiseptica
or S. aureus in strain 2/N animals.
In contrast with Kohn (1974), Wagner et al.
(1976), Rigby (1976) and Wagner (1979), we did not
detect S. pneumoniae in our guineapigs. Although
S. pneumoniae is considered fastidious, the apparent
absence of this micro-organism was not likely to be
due to inadequate isolation techniques since we
were able to grow S. pneumoniae from other
sources. The detection of S. zooepidemicus (Lancefield group C) as the predominant micro-organism
in the random-bred
guinea pigs stresses the
importance of this micro-organism as a cause of
otitis media as reported earlier (Kohn, 1974; Rigby,
1976; Wagner et al., 1976; Wagner, 1979). S.
zooepidemicus was not isolated from any lesions in
inbred guineapigs but susceptibility of the 2/N strain
to Lancefield group C streptococcal infections has
been reported, mainly as a chronic cervical
lymphadenitis ('lumps') and (pleuro )pneumonia
(Fraunfelter et al., 1971). The latter workers did not
examine the middle ear. Absence of group C
streptococcal infection in the 2/N strain might be
partly due to the separate housing of both groups.
However, more than eight distinct antigenic types
have been identified in S. zooepidemicus (Moore &
Bryans, 1969) which might show different abilities to
colonize different animal species and strains and
hence cause infection.

Otitis media in guineapigs

In spontaneous
and experimental
B. bronchiseptica infections in guineapigs, the middle ear has
nearly always been omitted as a sampling site. The
frequent isolation of B. bronchiseptica from cases of
otitis media in our random-bred
and inbred guineapigs (185% and 375% respectively of all isolates)
exceeded the yield (12% of all isolates) reported by
Wagner et al. (1976). Kohn (1974) detected
B.
bronchiseptica
only once, in a mixed infection,
among 31 cases of otitis media. Whether differences
in attack rates in animals depend on the bacteriological properties of B. bronchiseptica
is not fully
understood
(Bemis, Greisen & Appel, 1977a). B.
bronchiseptica isolates from different animal species
might show a different pathogenicity for guineapigs
as has been suggested
from results from experimental
infections in swine (Ross, Switzer &
Duncan,
1967). The pathogenicity
of various
guineapig strains for guineapigs was found to be
comparable,
regardless of the original site of isolation (Nakagawa
et al., 1971).
The isolation
of bacteria
of the PasteurellaActinobacillus
group from guineapigs
with otitis
media has been described
previously
for our
random-bred
colony (Boot, Oosterom & Walvoort,
1983). Pasteurella and Actinobacillus
spp. were also
isolated
from strain 2/N animals,
although
infrequently.
Experimental
infection,
preferably
in
gnotobiotic animals, will be necessary to assess the
pathogenicity
of members
of the PasteurellaActinobacillus
group more precisely.
The frequent
isolation of P. aeruginosa from
affected ears in strain 2/N guineapigs might partly
have resulted from the severe immunosuppression.
Indeed, P. aeruginosa is more frequently associated
with disease in immunocompromised
hosts than
other bacterial species. Several ceHular and extracellular products of P. aeruginosa have been implicated in pathogenicity
(Young, 1980) but no direct
correlation
has been reported between P. aeruginosa serotype and pathogenicity.
Our P. aeruginosa
isolates were serotypes 10 and 11. Both serotypes
are frequently found in the faeces of mice and rats
from different colonies (Batema et al., 1983). From
our other colonies, serotypes 10 and 11 have been
isolated only from the faeces of healthy rabbits
whereas various other serotypes were found in our
rodents
and rabbits (unpublished
observations).
Our findings suggest that P. aeruginosa serotypes 10
and 11 might show more pathogenic
potential in
strain 2/N guineapigs than other serotypes.
Several
bacterial
species isolated
from otitis
media are considered
to be normal inhabitants of
the upper respiratory
tract. Group C streptococci
are commonly present on the tonsils or pharynx of
apparently
healthy domestic
animals (Stamm &
Cobbs, 1980). Colonization
is possibly mediated

247

through surface antigens as has been found for S.

pyogenes (Lancefield group A) in humans (Gibbons
& van Houte, 1975). B. bronchiseptica
preferentially colonizes ciliated regions of the respiratory
tract (Bemis, Greisen & Appel, 1977b). Among the
members of the Pasteurella-Actinobacillus
group,
which in general show a marked degree of specificity
for localization
(Kilian & Frederiksen,
1981), P.
multocida type A has been shown to colonize the
nasopharynx
in rabbits through specific adhesins
interacting with receptors on the cell surface (Glorioso et al., 1982). The occurrence of S. zooepidemicus, B. bronchiseptica
and Pasteurella and Actinobacillus spp. in both ears in cases of bilateral otitis
media (Fig. 1) suggests ascending infection from the
nasopharynx
through
the Eustachian
tube. The
simultaneous occurrence of S. zooepidemicus
and B.
bronchiseptica
in pneumonic
lung tissue and ear
exudates (Fig. 2) suggests concomitant
descending
infection to the lower airways. Both ascending and
descending bacterial infection originating from the
upper respiratory tract might be triggered by viral
infections. Sendai virus infection occurs frequently
in guineapig colonies (Parker, Whiteman & Richter,
1978) and the interactions between Sendai virus and
bacterial pathogens in the lung are well recognized
(Jakab,
1981). Recently
adenovirus
infection in
guineapigs
has been observed
(Naumann
et al.,
1981; Brennecke,
Dreier & Stokes, 1983). The role
of viral infections in guineapig otitis media has not
been examined.
However,
in experimental
otitis
media in chinchillas, influenza A virus was shown to
enhance susceptibility to pneumococcal otitis media,
presumably
through bactericidal
and chemotactic
dysfunction
of polymorphonuclear
leucocytes and
damage to ciliated epithelium.
The incidence of
pneumococcal
otitis media increased as the time of
pneumococcus
inoculation approached
the time of
virus-induced
leucocyte
dysfunction
(Abramson,
Giebink & Ouie, 1982). The effects of experimental
ear infection with influenza A virus alone proved to
be limited compared with the effects of infection
with S. pneumoniae
alone (Giebink et al., 1980;
Giebink & Wright, 1983). The latter observations
suggest that the often used term secondary bacterial
infection reflects especially the time sequence of
processes in the development
of otitis media.
We conclude that otitis media. associated with the
isolation of a variety of respiratory bacterial species,
must be considered
a major disease problem in
gumeaplgs.
Acknowledgements
We would like to thank Mr A. E. Busschbach and
Mr C. Moolenbeek
for competent
technical assistance and Mrs A. E. Karsten for typing the manuscript.

248

Boot & Walvoort

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