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Correlation of Radiographic Changes after Tibial Tuberosity

Advancement in Dogs with Cranial Cruciate-Deficient Stifles


with Functional Outcome
Joe P. Morgan1, DVM, Diplomate ACVR, Katja Voss2, Dr med vet, Diplomate ECVS,
Daniel M. Damur3, Dr med vet, FVH, Diplomate ECVS, Tomás Guerrero2, Dr med vet, Diplomate ECVS,
Michael Haessig4, Prof. Dr med vet, and Pierre M. Montavon2, Prof. Dr med vet
1
Section of Diagnostic Imaging and Radio-Oncology, Vetsuisse Faculty University of Zurich, Zurich, Switzerland, 2Clinic for Small Animal Surgery
Vetsuisse Faculty University of Zurich, Zurich, Switzerland, 3Tierklinik Masans, Chur, Switzerland and 4Department for Farm Animals, Vetsuisse
Faculty University of Zurich, Zurich, Switzerland

Corresponding Author Objective: To (1) evaluate radiographic changes associated with osteoarthrosis
Katja Voss, Dr med vet, Diplomate ECVS, (OA) before and after tibial tuberosity advancement (TTA) and (2) determine if
University Veterinary Teaching Hospital these changes are indicative of limb function as determined by kinetic gait
Sydney, 65 Parramatta Road, Camperdown analysis.
2006 NSW, Australia
Study Design: Prospective clinical study.
E-mail: katja.voss@sydney.edu.au
Animals: Dogs (n=35) with cranial cruciate ligament (CCL) deficient stifles (38).
Methods: Variables recorded were: complete or partial CCL rupture, meniscal
Submitted April 2009
lesions, arthroscopically graded cartilage lesions, complications, and revision
Accepted January 2010
surgeries. Radiographic evaluation and kinetic gait analysis (vertical ground
DOI:10.1111/j.1532-950X.2010.00669.x reaction forces [GRFs]) were conducted pre- and 4–16 months postoperatively
(mean, 5.9 months). Radiographs were evaluated without knowledge of operative
findings and functional outcome. A score (0–3) based on new bone production at
11 specific sites was used to grade OA. Soft tissue changes were classified
separately as normal or excessive. Preoperative scores were correlated with clinical
variables. Postoperative scores and progression of OA scores were correlated with
clinical variables and GRFs.
Results: OA remained unchanged in 17 joints and progressed in 21 (55%). Dogs
with meniscal lesions had higher OA scores preoperatively, but not at follow-up.
Dogs with severe cartilage lesions at surgery had more progression of OA. GRFs
improved after surgery and were not correlated with any of the radiographic OA
scores.
Conclusion: Progression of OA was greater in the presence of severe cartilage
lesions at surgery. OA scores were not correlated with GRFs.
Clinical Relevance: Progression of OA is generally expected to occur after TTA
despite improvement of limb function.

Partial and complete rupture of the cranial cruciate liga- cyst formation, and joint space narrowing,7,14,15,18,21 gener-
ment (CCL) occurs frequently in dogs and results in insta- ally placing emphasis on presence and growth of marginal
bility and secondary osteoarthritis (OA).1–8 Presence and osteophytes. Patellar ligament thickening and patellar ten-
progression of radiographic changes of OA in the stifle dinosis have also been evaluated after TPLO.19,22,23
joint of the CCL-deficient dog has been reported after con- Surgical techniques that change the geometry of the
servative treatment 4,9 and after extracapsular or intracap- proximal aspect of the tibia, such as TPLO and TTA were
sular substitution techniques7,10–15; tibial plateau leveling developed to restore functional stability of the stifle, pre-
osteotomy (TPLO)15–19; and tibial tuberosity advancement vent deterioration of the medial meniscus, and reduce the
(TTA).20 Radiographic soft tissue changes include joint degree of secondary OA in the stifle joint with CCL rup-
effusion/capsular thickening, lateral and medial soft tissue ture.24 The initial hope that progression of OA could be
thickening, intraarticular osseous fragments, and meniscal minimized using these techniques has not been realized.
mineralization.14,18 Bony changes include osteophytosis Whereas progression of OA is less in dogs after TPLO than
and enthesiophytosis, subchondral sclerosis, subchondral after extracapsular stabilization,15 in general, progression

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c Copyright 2010 by The American College of Veterinary Surgeons 425
Radiographic Changes after TTA and Functional Outcome Morgan et al.

of OA has been observed after both TPLO and TTA.16–20 would not be an indicator for functional outcome as deter-
Radiographic progression of OA after TTA has not been mined by vertical ground reaction forces.
reported in detail, nor is it known whether certain clinical
factors correlate with development of degenerative
changes. MATERIALS AND METHODS
Outcome after surgery for CCL disease can be assessed
based on the radiographic progression of stifle joint OA Dogs
and by evaluating functional outcome, which is probably
the clinically more relevant outcome measure. Whereas ra- Dogs (n = 35; weighing Z20 kg) with a partial or complete
diographic changes have been used as a standard clinical CCL rupture that had TTA (n = 38) between May 2003
tool to evaluate progression of degenerative disease,7,18,25 and December 2004 were studied. These dogs were part of
their identification does not necessarily relate directly to the population of an earlier study of consecutive patients
clinical functional outcome.10,17 Several studies have re- with CCL disease that had been treated with TTA.32 Two
ported or suggested a lack of significant correlation be- of the original 37 dogs were excluded because of incom-
tween the radiographic appearance of OA and clinical plete radiographic studies.
evaluation of limb function.5,7,9,18,26 Postoperative clinical
status has been judged using lameness evaluation by a cli- Clinical Evaluation
nician or by an owner assessment at various intervals after
surgery.18,20,27,28 This type of assessment is subjective and All dogs had arthroscopic stifle examination before TTA.
may not necessarily reflect the effective functional out- Synovial membrane biopsies were taken at the beginning of
come. Force plate gait analysis is a more objective method the arthroscopy from the medial aspect of the joint capsule
to classify gait, and has been used to demonstrate clinical using 2.7 mm arthroscopic spoon forceps (Dr. Fritz Instru-
effectiveness of several treatment techniques in dogs with ments, Tuttlingen, Germany). Samples were stained with
CCL disease.29–32 hematoxylin and eosin and examined by light microscopy.
Our purpose was to record the presence and progres- The retropatellar fat pad was partially removed to increase
sion of both bony and soft tissue radiographic changes oc- visibility. The intraarticular structures were explored for
curring after TTA, and to evaluate potential risk factors for partial or complete CCL tears, meniscal lesions, and to
OA progression after surgery. The influence of the level classify femoropatellar joint cartilage lesions by a modified
and progression of radiographic OA on functional Outerbridge grading scale.33 Dogs with meniscal lesions
outcome was determined by force plate gait analysis. We had a medial parapatellar arthrotomy for partial meniscec-
hypothesized that severity and progression of stifle OA tomy. TTA was then performed as described.32,34

Table 1 Summary of Radiographic Results for New Bone Production and Soft Tissue Changes in 35 Dogs with 38 CCL-Deficient Stifles that had TTA
New Bone Production Soft Tissue Changes

Follow-Up Primary
Preoperative (Mean, 5.9 months) Progression Localization Progression
Global scores
0–3 13 7
4–10 18 16
11–33 7 15
OA progression
None 17
1–4 9
5–10 11
4 10 1
11 joint involved
Femoropatellar 11
Femoropatellar and femorotibial 16
Femorotibial 3
Soft tissue changes
None 5
None preoperatively, present on follow-up 4
Present preoperatively unchanged on follow-up 19
Present preoperatively, worse on follow-up 6
Present preoperatively, decreased on follow-up 4

Numbers = Stifle Joints.


CCL, cranial cruciate ligament; TTA, tibial tuberosity advancement; OA, osteoarthritis.

426 Veterinary Surgery 39 (2010) 425–432


c Copyright 2010 by The American College of Veterinary Surgeons
Morgan et al. Radiographic Changes after TTA and Functional Outcome

Radiographic Evaluation postoperative studies; and group 5, findings were positive


on preoperative studies and positive but regressive on post-
Mediolateral and caudocranial radiographic projections
operative studies.
were evaluated presurgically, immediately postoperatively,
and at a final follow-up study planned 4–6 months after
TTA. Mediolateral views were obtained with the stifle joint Force Plate Gait Analysis
in 120–1351 extension, Caudocranial radiographs were Force plate gait analysis (Force plate OR6-7 from Ad-
made with the central X-ray beam at 151 proximal/distal vanced Medical Technologies Inc., Watertown, MA) was
angle. Pre- and postoperative radiographs were taken with conducted preoperatively and at final follow-up examina-
dogs anesthetized and for follow-up studies, dogs were se- tion at trotting velocity, as reported earlier.32 Trial velocity
dated. Radiographic exposure was controlled by of use of a was within 1.85–2.15 m/s, with an acceleration/decelera-
digital system and hard copies were made of each exposure tion o  0.5 m/s2. Peak vertical forces (PVF) and vertical
for examination. Evaluations of the degree and progression impulses (VI) of 5 valid trials were recorded for each pelvic
of OA and soft tissue changes were made by a board cer- limb and were expressed in percent of bodyweight (%BW
tified radiologist (J.P.M.), aware of signalment of the dogs for PVF; %BW s for VI). PVF and VI were defined to be
and the time of follow-up, but unaware of the intraopera- zero in dogs not using the affected leg at a trotting gait.
tive findings and the functional outcome of the dogs.
New bone production, including enthesiophytes and
osteophytes, was noted at 11 specific anatomic locations: Statistical Analysis
apical patella, basilar patella, trochlear groove just proxi- Results from descriptive statistics are reported as mean  SEM.
mal to the patella, lateral femoral trochlear groove, medial Data were analyzed using statistical software (StatView
femoral trochlear groove, medial femoral condyle and ep- 5.1, SAS Inc., Wangen bei Dübendorf, Switzerland).
icondyle, lateral femoral condyle and epicondyle, inter- Normality test (StatView 5.1) was applied before paramet-
condyloid fossa, medial tibial plateau, lateral tibial plateau, ric test if used. Preoperative radiographic scores were com-
and caudal tibial plateau. New bone production at a spe- pared between dogs with partial and complete CCL
cific site was graded 0 when not identified, and 1–3 when rupture, between dogs with and without meniscal lesions,
present, based on the amount of new bone, as indicated by and between the different grades of cartilage lesions seen
bone density in addition to bone thickness. A total score of during arthroscopy using factorial ANOVA.
0 indicated no evidence of new bone production within the The influence of partial or complete CCL rupture,
joint, whereas 33 indicated extensive new bone at all 11 presence of meniscal lesions, grade of cartilage lesions at
sites. Three groups were formed based on scoring intervals: the time of surgery, and presence of complications and re-
0–3, 4–10, and 4 10 (Table 1). vision surgery on progression of OA was examined using
For evaluation, preoperative scores were compared ANOVA for the absolute bony radiographic scores, and
with final scores. For statistical analysis, data were treated w2-test for the progression categories of both bony and soft
individually as well as being divided in a manner that sep- tissue lesions. Linear regression analysis was used to de-
arated those with no progression, minimal progression (in- scribe the relationship between body weight and progres-
crease in score of 1–4), those with moderate progression sion of OA.
(increase in score of 4 5–10), and those with marked pro- Radiographic OA scores were compared with func-
gression in the new bone production during the study (in- tional outcome represented by PVF and VI at follow-up.
crease in score of 4 10; Table 1). Linear regression analysis evaluated the relationship be-
Soft tissue changes included joint effusion/capsular tween the bony OA scores determined on both the preop-
thickening, lateral and medial soft tissue thickening, intra- erative and follow-up radiographs, and PVF and VI at
articular osseous fragments, and meniscal mineralization. follow-up. Linear regression analysis was also used to eval-
Changes were scored as normal or excessive. Detection of uate the relationship between progression of bony OA
joint capsule distention and joint effusion was based on changes and PVF and VI at follow-up. Additionally,
caudal distention of the joint capsule as evident on the lat- ANOVA was sued for evaluation of bony progression cat-
eral view or displacement of the collateral ligaments on the egories and PVF and VI at follow-up, and for soft tissue
caudocranial view. Detection of joint capsule distention change categories and PVF and VI at follow-up. A post
and joint effusion was also determined as excessive if the hoc Bonferroni Dunn test was used for further evaluation if
retropatellar fat pad was o 1 cm in width, when measured significant differences were found between group means.
at its widest site on a mediolateral view. For statistical Significance was set at P  .05.
analysis 5 groups were formed (Table 1). In group 1, find-
ings were negative on pre- and postoperative studies; in RESULTS
group 2, findings were negative on preoperative studies and
positive on postoperative studies; in group 3, findings were
Clinical Results
positive on preoperative studies and positive unchanged on
postoperative studies; in group 4, findings were positive Mean body weight of the 35 dogs (38 TTA) enrolled in the
on preoperative studies and positive and progressive on study was 33.7 kg  1.19 kg (range, 21.4–53.3 kg). Complete

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Radiographic Changes after TTA and Functional Outcome Morgan et al.

Figure 1 Immediate postoperative (A and B) and 5-month follow-up (C and D) radiographs of a 9-year-old mixed-breed dog with a unilateral complete
cranial cruciate ligament rupture and medial meniscal lesion. This dog was classified to have no progression of new bone production.

CCL rupture was identified in 28 of 38 stifles, and partial in 2 stifles. Thirty-three synovial membrane biopsies were
rupture in 10 stifles. Meniscal lesions found in 21 stifles considered suitable for histologic examination. A predom-
were treated by partial meniscectomy. Femoropatellar car- inance of lymphoplasmacellular infiltrates was found in
tilage lesions were seen in 32 stifles and were graded33 20 biopsies (60.6%), and unspecific synovitis with villous
as chondromalacia in 20 stifles (grade 1), fibrillation in 8 hypertrophy and/or hyperemia in 10 (30.3%). Three
stifles (grade 2), and fissuring in 4 stifles (grade 3). Postop- biopsies (9.1%) had normal synovial tissue. The follow-
erative complications occurred in 10 joints. Revision up radiographic study and force plate analysis were con-
surgery was performed in 5, including second look ducted between 4 and 16 months (mean, 5.9 months) after
arthroscopy or arthrotomy in 3, and revision of implants TTA.

Figure 2 Immediate postoperative (A and B) and 4-month follow-up (C and D) radiographs of a 5-year-old Boxer with a complete cranial cruciate
ligament rupture without meniscal lesion. This dog had a 10-point progression of radiographic scores indicating new bone production.

428 Veterinary Surgery 39 (2010) 425–432


c Copyright 2010 by The American College of Veterinary Surgeons
Morgan et al. Radiographic Changes after TTA and Functional Outcome

Radiographic Findings BW (mean, 4.2  0.49% BW). PVF at follow-up were be-
tween 49.4% and 85.2% BW (mean, 65.0  1.27% BW)
Preoperative bony changes were scored between 0 and 3 in
and VI ranged from 6.4% to 10.9%BW (mean,
13 joints, between 4 and 10 in 18 joints, and 4 10 in 7
8.4  0.18% BW). One-way ANOVA revealed no differ-
joints (mean, 6.16  0.93). Bony changes on follow-up were
ence in ground reaction forces of 27 limbs that had a fol-
scored between 0 and 3 in 7 joints, between 4 and 10 in 16
low-up between 4 and 6 months, and 11 limbs that had a
joints, and 4 10 in 15 joints (mean, 9.63  1.06). There was
follow-up between 6 and 16 months.
no progression of new bone noted in 17 joints (Fig 1), pro-
gression between 1 and 4 points in 9 joints, progression be-
Statistical Results
tween 5 and 10 points in 11 joints (Fig 2), and progression
4 10 points in 1 joint. Mean progression of new bone pro- Preoperative bony radiographic OA scores were signifi-
duction was 3.34  0.73 (Table 1). cantly greater in dogs with meniscal lesions compared with
The radiographic patterns noted on the final study dogs without (P = .04), but did not differ between dogs
were: (1) new bone production around the femoropatellar with partial or complete CCL ruptures, and between differ-
joint, in particular, the abaxial surfaces of the trochlea, the ent cartilage lesion grades.
femur just proximal to the trochlea, and the distal apex of Bony radiographic OA scores at follow-up and pro-
the patella; (2) enthesiophytes at the attachment of the col- gression of bony radiographic scores did not depend on
lateral ligaments on the femoral epicondyles and the periar- presence of partial or complete CCL rupture, presence or
ticular area of the tibia plateau; (3) new bone from the absence of meniscal lesion, presence or absence of surgical
epicondylar region extending toward the abaxial surfaces of complications, or revision surgery. The grade of cartilage
the trochlear notch; and (4) minimal new bone at the inter- lesion at time of surgery was statistically associated with
condylar fossa. Distribution by principal joint involvement progression of bony OA scores (P o .01; Fig 3). Dogs with
was: femoropatellar joint (11), femoropatellar and femoro- grade III cartilage lesion had a significantly higher progres-
tibial joints (16) and femorotibial joint (3). In 8 joints, OA sion of OA scores compared with dogs with grade I
changes were not sufficiently prominent to place the joint (P = .001), and dogs with grade II (P = .0013) cartilage le-
into a distinct pattern (total score,  3). sions (Bonferroni/Dunn test, significance at P o .0083).
Soft tissue changes, in particular joint effusion or cap- None of the variables tested was statistically associated
sular thickening was less evident than bony change, but with presence and progression of radiographic soft tissue
was considered present in 29 joints before, and in 33 joints changes.
after, surgery. Progressive soft tissue change occurred in 10 Neither preoperative radiographic bony OA scores,
joints, while 19 had similar scores before and after TTA bony OA scores at follow-up, progression of bony scores
(Table 1). throughout the study, nor categories of soft tissue changes
were associated with functional outcome represented by
Force Plate Results PVF and VI at final follow-up examination.
Preoperative PVF ranged from 0% to 64.6% BW (mean,
DISCUSSION
31.5  3.67% BW) and preoperative VI from 0% to 9.4%
We found that 55% of treated stifles had progressive OA
within 4–16 months of TTA, which is similar to other re-
ports where approximately half of the treated dogs devel-
oped progressive OA after TPLO16,18 or TTA.20
Preoperative radiographic OA scores were significantly
greater in dogs with meniscal lesion than in dogs with intact
menisci in our study. Higher radiographic scores usually in-
dicate chronic disease and it is possible that meniscal lesions
were more common in chronic cases because they had more
time to develop. It is also possible that meniscal lesions re-
sulted in faster progression of OA. Preoperative radio-
graphic scores did not differ between dogs with partial and
complete CCL rupture. This is somewhat surprising, be-
cause when assuming that CCL disease in large-breed dogs
is degenerative in origin one would expect a higher degree of
OA in dogs with complete CCL rupture. However, some
Figure 3 Diagram showing the relation between progression of bony dogs with complete CCL rupture had no, or only minimal,
osteoarthritis (OA) scores and grades of cartilage lesions as determined signs of OA on admission, which suggests an acute, and
during arthroscopy. Dogs with grade III cartilage lesions (4 dogs) had
significantly greater progression of OA scores (P o .01) compared with
possibly traumatic CCL rupture in these dogs.
dogs with grade I (20 dogs), grade II (8 dogs), and no cartilage lesions Meniscal release and caudal pole hemimeniscectomy
(6 dogs). result in changes of pressure distribution and in increased

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Radiographic Changes after TTA and Functional Outcome Morgan et al.

stresses within the medial compartment of the stifle joint,35 ever, lymphoplasmacellular synovitis as observed in 60.6%
and this has been suggested as a potential risk factor for of the preoperative synovial membrane biopsies indicates a
development of OA in affected stifle joints. We did not ob- chronic inflammatory process that may not resolve after
serve statistically significant differences in degree of OA treatment. A similar incidence of lymphoplasmacellular
progression between dogs with meniscal lesions that were synovitis (47%) has been described38 and type and degree
treated by partial meniscectomy and dogs with intact men- of synovial membrane pathology were not associated with
isci. There was also no difference in OA progression degree of CCL degeneration.38
between dogs with partial or complete CCL rupture. These The type of surgery also can have an effect on radio-
findings could of course change with longer follow-up times. graphic appearance of effusion, for example when place-
Radiographic scoring systems may not necessarily re- ment of an intraarticular fascial graft disrupts the anatomy
flect the true severity of OA. The radiographic features of the infrapatellar fat pad and the cranial femorotibial
identified in OA have classically included new bone pro- joint space.14 The advancement of the tibial tuberosity dur-
duction, bone lysis, bone sclerosis, and soft tissue ing TTA may create more intracapsular volume, which
changes.7,14,15,36,37 Thus, scoring systems have been used could add to the radiographic signs of cranial joint effu-
in various ways. Usually each determinant within the sys- sion/capsular thickening. Additionally, removal of the in-
tem has been assigned an equal value with the score depen- frapatellar fat pad during arthroscopy decreases the size of
dent upon the severity of the change. Scores were then the fat pad, and may also create a radiographic appearance
totaled for a cumulative global score. This was carried out of joint effusion/capsular thickening.
without consideration of the ease in detection of the deter- The grade of cartilage lesion seen at surgery was the only
minant in OA or whether the determinants should in fact factor having an influence on progression of bony OA
have equal value. An unexpected decrease in score for ex- changes in this study. Dogs with severe cartilage changes at
ample could be the result of remodeling or maturation of surgery seem to have a higher probability of progression of
osteophytes that gave the impression of decreased level of OA as indicated by bony changes. Cartilage injury is not ev-
osteophytosis14 or the result of the use of soft tissue vari- ident on radiographs precluding prognostic information from
ables that were more evident postoperatively than later in the preoperative radiographs. In people, weight-bearing ra-
the study.14,15 In addition, radiographic studies are com- diographs show a decrease of the joint space caused by thin-
promised by morphologic distortion, geometric magnifica- ning of the cartilage layer, but these are difficult to perform
tion, and superimposition of bony changes. and to evaluate accurately in dogs, and are not used regularly
We made no attempt to produce a global score for soft in small animal surgery. Meniscectomy could also cause vari-
tissue changes and bony changes to indicate the level of OA ability in the width of the medial aspect of the joint space.
because of the lack of knowledge of appropriate weighting Much emphasis is placed on presence and degree of
of individual features. Rather, we chose to use a combina- osteophytosis in evaluation of the clinical status of canine
tion of scoring systems.7,14,15,36,37 We acknowledge that the joints.5,7,9,10,16,17,36,39 Presence and progression of OA has
score indicating the level of OA was biased toward features been suggested as a true test of the value of the treatment of
that were more prominent on radiographs. For stifle OA, injured CCL,7 and thus, control of OA has been listed as
this was radiodense osteophytosis. Subchondral sclerosis in one of the primary surgical goals of repair of CCL injury.9
the tibial plateau was not evaluated in our study because However, achieving this goal remains elusive and many re-
this evaluation has been shown to have a large intra- or in- ports note progression of OA after stabilization despite an
terobserver variability.14 Changes in the fabellae were also acceptable clinical outcome.5,7,8,10,11,13,18,27 The value of
not included because of the assumption that these changes treatment on clinical status of patients has usually been
were age dependent and their association with stifle OA judged from a lameness evaluation by a clinician or by a
was questionable.2 Notch stenosis has been described as an client questionnaire or owner’s assessment at various times
important feature of stifle OA7 but we did not observe this, after surgery.19–21,28 Force plate analysis is a more objec-
possibly because of a younger dog age or a more acute tive method to evaluate limb function, and has been used in
presentation. evaluation of treatment in cruciate ligament deficiency
Soft tissue changes were recorded separately from dogs.29–32 The marked increase in PVF and VI at follow-
bony changes. Statistical evaluation showed no correlation up compared with preoperative values demonstrated the
with clinical outcome or with other variables. Joint effu- clinical effectiveness of TTA in our study. The comparison
sion/capsular thickening were usually present at surgery of force plate with presence and progression of patterns of
and often failed to resolve. TTA, as well as TPLO, only new bone formation and soft tissue changes all failed to
provides functional stability of the stifle joint during weight show significance. Thus, our results continue to support the
bearing, and capsular thickening is probably an attempt contention that presence or progression of OA as deter-
of the body to stabilize the joint. In addition, synovial mined on radiographs has little influence on the clinical
inflammation and/or proliferation may add to the status of the joint.
radiographically visible soft tissue silhouette. Synovial Comparison of progression of OA in the stifle joint
membrane biopsies could not be taken at follow-up in our between studies is difficult because of differences in age,
clinical patients, so the degree of synovial inflammation size, athletic activity, level of meniscal injury, whether
during the course of the disease remains unknown. How- the injury to the CCL was partial or complete or whether

430 Veterinary Surgery 39 (2010) 425–432


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Morgan et al. Radiographic Changes after TTA and Functional Outcome

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