The etiopathogenesis of canine cranial cruciate ligament. Article. Comparison of tibial plateau angles in small and large breed dogs.

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1 Article Comparison of tibial plateau angles in small and large breed dogs Lillian Su, Katy L. Townsend, Jennifer Au, Thomas E. Wittum Abstract Cranial cruciate ligament (CCL) disease can affect dogs of all sizes. The literature describing tibial plateau angle (TPA) in small breed dogs is limited. A retrospective study was conducted in unselected dogs presented for stifle or tibial examination to compare TPA in small breed dogs (n = 146 dogs, 185 stifles) versus large breed dogs (n = 200 dogs, 265 stifles). Small breed dogs had a mean TPA higher than large breed dogs. There were higher TPAs in spayed females and castrated males for all dogs compared with intact males ( and , respectively). Dogs with unilateral and bilateral CCL disease had higher TPAs compared to dogs with intact CCLs ( and , respectively). Tibial morphology differs between large and small breed dogs; however, the significance of the impact of TPA on CCL disease in small breed dogs is unknown. Résumé Comparaison des angles du plateau tibial chez les chiens de petite et de grande races. La maladie du ligament cruciforme crânien (LCC) peut affecter les chiens de toutes les tailles. La littérature décrivant l angle du plateau tibial (APT) chez les chiens de petites races est limitée. Une étude rétrospective a été réalisée chez des chiens non sélectionnés présentés pour un examen du grasset ou du tibia pour comparer l APT chez les chiens de petite race (n = 146 chiens, 185 grassets) par rapport aux chiens de grande race (n = 200 chiens, 265 grassets). Les chiens de petite race présentait un APT moyen de 3,1 6 0,6 de plus que les chiens de grande race. Il y avait des APT supérieurs chez les femelles stérilisées et les mâles castrés pour tous les chiens comparativement aux mâles intacts (3,6 6 1,0 et 2,7 6 1,0, respectivement). Les chiens atteints d une maladie LCC unilatérale et bilatérale présentaient des APT supérieurs comparativement aux chiens avec des LCC intacts (2,0 6 0,7 et 2,5 6 0,8, respectivement). La morphologie tibiale diffère entre les chiens de grande et de petite race. Cependant, l importance de l impact de l APT sur la maladie LCC chez les chiens de petite race est inconnue. (Traduit par Isabelle Vallières) Can Vet J 2015;56: Introduction Department of Veterinary Clinical Sciences (Su, Townsend, Au) and Veterinary Preventive Medicine (Wittum), The Ohio State University College of Veterinary Medicine, Columbus, Ohio 43210, USA. Address all correspondence to Dr. Lillian Su; su.302@osu.edu Dr. Townsend s current address is Oregon State University College of Veterinary Medicine, Corvallis, Oregon 97331, USA. Dr. Au s current address is Charleston Veterinary Referral Center, Charleston, South Carolina 29414, USA. Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere. The etiopathogenesis of canine cranial cruciate ligament (CCL) disease has yet to be fully elucidated; however, it is recognized as a degenerative process within the extracellular matrix (ECM) that ultimately leads to partial or complete ligament rupture, instability, and secondary degenerative joint disease (1,2). Risk factors such as breed and genetics, increased body weight, neuter status, lack of consistent activity, alterations in cellular and ECM composition within the CCL, and conformational variation including a straight stifle angle, a narrowed intercondylar notch, and an elevated tibial plateau angle (TPA) have all been identified as potential contributors to CCL disease (3,4 10). Proximal tibial morphology, specifically caudal angulation of the proximal tibia resulting in an elevated TPA, has previously been evaluated in the veterinary literature. There is controversy with regard to the causal role of TPA in canine CCL disease. Some reports have shown that higher TPA was associated with a higher incidence of CCL disease and younger age at onset of lameness (10 13), but other reports have shown no effect of TPA on presence or progression of CCL disease (7,14 17). Tibial plateau angle as measured on a standard lateral radiographic projection of the tibia is defined as the angle between a line tangential to the central articular surface, or intersecting the cranial and caudal landmarks of the medial tibial plateau, and a line perpendicular to the mechanical long axis of the tibia (18,19). Average TPA in large breed dogs is reported to range from 23.5 to 28.0 (16,20,21); however, the TPA of individual dogs of various breeds has been reported to range from 12 to 59 (10,22). Unlike the case with large breed dogs, CCL disease and risk factors for CCL disease in small breed dogs have not been extensively studied. Small breed dogs with CCL disease have been described as having a mean TPA of 27.4 with individual 610 CVJ / VOL 56 / JUNE 2015

2 TPAs ranging from 21 to 40 (23 26). A recent study evaluating tibial conformation in normal Yorkshire terriers compared with Labrador retrievers found mean TPAs to be and , respectively (27). Despite evidence in large breed dogs (. 20 kg) that TPA does not play a role in clinical outcome following lateral suture stabilization (28), no equivalent evaluation has been performed in small breed dogs undergoing stifle stabilization surgery. Other than the recent evaluation of normal Yorkshire terriers and a case series describing tibial plateau leveling osteotomy (TPLO) in small breed dogs with excessive TPAs (. 30 ) (29), there are few peer-reviewed references documenting TPAs in small breed dogs. Tibial conformation in small breed dogs was described in a case series of 8 CCL-deficient dogs that underwent cranial tibial wedge ostectomy (CTWO) with TPAs ranging from 26 to 37 and radiographic evidence of caudal tibial angulation (26). The purpose of this study was to measure the TPA of small breed dogs and compare that to the TPA of large breed dogs. Our hypothesis was that small breed dogs would have a higher TPA compared with that of large breed dogs presented for stifle or tibial evaluation. Materials and methods Medical records of dogs examined at The Ohio State University Veterinary Medical Center between January 2005 and December 2012 were reviewed. An initial data trawl employed the Hospital Information System (Vetstar 9.0, Advanced Technology Corp., Ramsey, New Jersey, USA) with a search request for key words tibia or TPLO in the radiography request. Dogs confirmed by the medical record to have patellar instability, CCL rupture, or palpably normal stifles were included. In addition, age, breed, weight, and gender were noted. All dogs registered as small or toy breeds, defined as American Kennel Club recognized breeds with an expected adult body weight, 13 kg, with a documented stifle examination were eligible for inclusion in our study group (30). Radiographic studies were screened to ensure image quality was appropriate for the measurement of TPA. Lateral images (taken under sedation) were required to include the stifle and the tarsus with adequate superimposition of both the femoral and tibial condyles (, 4 mm separation) for measurement of TPA. Dogs were excluded if images were obtained for diagnosed fracture or angular deformity. In the control group, the 20 large breeds, defined as breeds with an expected adult body weight of. 25 kg, that most frequently had eligible radiographic images taken during the study period were considered for inclusion. The first 10 dogs from each large breed to meet the aforementioned imaging and medical records criteria were included. If any dog in either group had appropriate images available of the contralateral tibia, both stifles were included for TPA measurement. For all dogs, TPA was measured (E-film Workstation 3.2; Merge Healthcare, Chicago, Illinois, USA) using previously described techniques (18,19) by 1 veterinarian who had previously completed a surgical residency (LS) and 1 ACVS diplomate (KT). Each image was measured 3 times, non-sequentially, by each observer and observers were blinded to each other s measurements. Table 1. Unadjusted signalment variables, patella and cruciate status of small and large breed dogs Small breed dogs Large breed dogs Signalment (n = 146) (n = 200) Age (y) Mean 6 SD Median (range) 6.0 (0.6 to 13) 4.0 (0.5 to 12.5) Weight (kg) Mean 6 SD Median (range) 7.4 (1.9 to 23.3) 42.0 (16.5 to 90) Gender (Number of dogs) Intact female 5 6 Intact male Spayed female Castrated male Patellar Diagnosis Medial patella luxation Normal patella Lateral patella luxation 1 5 Patella luxation w/ccl rupture 44 7 CCL Unilateral CCL rupture Bilateral CCL rupture CCL intact Normal stifle SD standard deviation; CCL cranial cruciate ligament. Statistical analysis The TPA was calculated as a mean of the 6 measurements, 3 by each observer for each stifle. All statistical analyses were performed using SAS statistical software (SAS v. 9.3; SAS Institute, Cary, North Carolina, USA). The data were evaluated graphically to ensure that the assumption of normality was met (31). The difference between observer measurements was evaluated using a paired t-test. A multivariable linear mixed model was used to estimate the impact of breed size on TPA adjusted for potential confounding factors. Nominal variables indicating breed size of the dog (large or small), gender (male, female, castrated, spayed), CCL status (intact, unilateral rupture, bilateral rupture), and patellar stability (normal, medial patella luxation, lateral patella luxation) were included in the model as fixed effects, with the individual dog included as a random effect to account for repeated measurement. Multiple pairwise comparisons were accomplished using the Tukey-Kramer method. Values of P, 0.05 were considered significant. Results The small breed study group consisted of 146 dogs that met the inclusion criteria, for a total of 185 small breed stifles. The control group consisted of 200 large breed dogs that met the inclusion criteria for a total of 265 large breed stifles. Signalment, breed distribution, and mean TPA by breed are presented in Tables 1 and 2, respectively. The mean difference between observer measurements was (range: 27.3 to 9.3 ). The TPA (least squares means 6 SE) of small breed dogs was and was higher (P, 0.001) than the TPA of large breed dogs ( ). The TPA for all dogs with unilateral and bilateral CCL rupture was higher than for dogs with intact CCLs by CVJ / VOL 56 / JUNE

3 Table 2. Distribution and unadjusted mean tibial plateau angle of small and large dogs by breed Small breed dogs (Number of dogs, Large breed dogs (Number of stifles; Number of stifles) Mean TPA 6 SD 10 dogs per breed) Mean TPA 6 SD Australian terrier (1, 1) Akita (11) Bichon frise (20, 28) American bulldog (16) Boston terrier (6, 8) American pit bull terrier (12) Brussels griffon (1, 1) Australian shepherd (14) Cairn terrier (5, 7) Bernese mountain dog (11) Cavalier King Charles spaniel (6, 8) Boxer (13) Chihuahua (7, 7) Bull mastiff (16) English toy spaniel (1, 1) Doberman pinscher (11) Havanese (2, 2) English bulldog (16) Jack Russell terrier (10, 11) English mastiff (13) Lhasa apso (1, 1) German shepherd dog (11) Maltese dog (5, 7) Golden retriever (13) Miniature pinscher (1, 2) Great dane (12) Miniature poodle (2, 3) Great Pyrenees (13) Miniature schnauzer (4, 4) Labrador retriever (11) Norwich terrier (1, 1) Newfoundland (18) Papillon (2, 3) Rottweiler (12) Pekingese (1, 2) St. Bernard (16) Pomeranian (8, 12) Siberian husky (13) Pug (2, 2) Weimaraner (13) Rat terrier (1, 1) Shetland sheepdog (11, 12) Shiba inu (1, 1) Shih tzu (6, 9) Silky terrier (1, 2) Toy fox terrier (2, 2) Toy poodle (5, 6) West Highland white terrier (7, 7) Wire haired fox terrier (1, 2) Yorkshire terrier (25, 32) TPA tibial plateau angle; SD standard deviation. (P = 0.007) and (P = 0.004), respectively. Mean TPAs for large breed dogs with unilateral and bilateral CCL disease were and higher, respectively, compared to large breed dogs with intact CCLs. For small breed dogs, the mean TPA in dogs with bilateral CCL disease was higher than for dogs with intact CCLs (P = 0.053). Mean TPA for all dogs with normal patellae was higher than for dogs with medial patella luxation (MPL; P = 0.009). Patellar status did not affect TPA in large breed dogs; however, mean TPA for small breed dogs with normal patellae was higher than for small breed dogs with MPL (P = 0.001). Mean TPA for all dogs was higher when comparing castrated males to intact males, spayed females to intact males, and spayed females to intact females by (P = 0.045), (P = 0.003), and (P = 0.348), respectively. When separated by breed size, mean TPAs for castrated males and spayed females compared to intact males were (P = 0.022) and (P = 0.013) higher, respectively; and mean TPA for spayed females compared to intact females was (P = 0.998) in large breed dogs. Mean TPA for spayed females was higher than for intact males (P = 0.04) and higher than for intact females (P = 0.199) in small breed dogs. Discussion In our population of dogs presented for stifle or tibial examination, small breed dogs had a higher mean TPA compared to large breed dogs. This finding supports 1 previous study which compared proximal tibial conformation between Labrador retrievers and Yorkshire terriers (27) and 3 non-peer reviewed reports of small breed dogs having higher TPAs (23 25). Possible reasons for a higher TPA in small breed dogs include individual breed variation resulting in proximal tibial morphology that differs from large breed dogs, a higher likelihood for caudal angulation of the proximal tibia, or alterations in proximal tibial physeal growth due to size, conformation, or limb use. The role of TPA in CCL disease in small breed patients should be investigated further, particularly since higher TPA has been previously associated with incidence of CCL disease (10 13). Variations in proximal tibial and distal femoral morphology and joint angle can be breed- and individual-specific and result in variations of stifle mechanics that may play a role in the development of CCL rupture and stifle disease. Extracapsular stabilization is frequently the surgical method of choice for small breed dogs and differences in TPA and stifle mechanics may influence outcome following surgical stabilization. Havig et al (28) reported that TPA does not play a role in clinical outcome following lateral fabellar suture in large breed dogs but there were insufficient numbers of study animals with TPAs outside of the normal range (23 to 26 ) to draw meaningful conclusions regarding surgical outcome of dogs with elevated TPAs. As such, the literature lacks evidence to determine whether an elevated TPA may influence the quality of surgical outcome in dogs of any size. In our study population, we also observed a difference in mean TPA among altered status, diagnosis of normal, unilateral, or bilateral cruciate disease, and patellar stability, with higher 612 CVJ / VOL 56 / JUNE 2015

4 mean TPA noted in altered males and females, dogs with cruciate disease, and dogs with normal patellae. Differences in TPA for all dogs associated with altered status and presence of CCL disease appear to mirror previously documented differences in prevalence of CCL rupture in altered versus unaltered dogs (4,5,8) and correlation of excessive TPA with early neutering (10). The difference in TPA between spayed and intact females did not reach statistical significance, although there was a larger difference between altered and intact females for small breed dogs. This most likely represents a lack of adequate numbers of intact females in our study populations to detect a difference. However, an alternate explanation could be that sex hormones in female dogs play less of a role on limb length and physeal closure than in their male counterparts. A lack of difference in TPA between dogs with unilateral and bilateral CCL disease is consistent with previous findings (14). However, in our small breed group, the difference in TPA between dogs with CCL disease and dogs with intact CCLs was not statistically significant. This could be a result of our mixed population of small breed dogs or it may indicate that TPA has less influence on CCL disease in small breed dogs. Incidence of CCL disease has been linked to presence of MPL in small breed dogs (32); however, the TPA of dogs with patellar luxation in our study was lower than in dogs with normal patellae. This difference was more pronounced for the small breed dogs. Based on the observation that MPL was more prevalent in our small breed group and small breed dogs had a higher mean TPA, we may have expected mean TPA to be higher in dogs with MPL than in dogs with normal patellae. If CCL disease is viewed as a sequela of ligament overload, then any state that places excessive or repetitive strain on the CCL may contribute to rupture. Thus, while an elevated TPA is hypothesized to subject the CCL to additional strain in drawer, MPL will theoretically place additional strain on the CCL in internal rotation. A lower TPA in dogs with MPL may indicate a difference in proximal tibial physeal growth in small breed dogs when normal femoropatellar contact pressures are altered or it may indicate that the rotational stresses experienced by the CCL in dogs with MPL are equivalent, or possibly worse than, an elevated TPA in the context of progression of CCL disease. Further studies evaluating the role of MPL and TPA on CCL strain in small breed dogs are needed. There are several limitations to this study. Given the retrospective nature of this study, we were reliant on our medical records for completeness of information and accuracy of diagnosis. The study population was skewed toward patients with some degree of stifle disease (either CCL disease, patellar instability, or both) with only a small number of dogs having normal stifles. As a referral center, it is possible that our patient population does not accurately reflect TPAs and incidence of stifle disease in large and small breed dog populations as a whole. Therefore we are only able to relate our findings to small and large breed dogs presenting for stifle or tibial evaluation. The heterogeneity in our study groups may have influenced the data by having certain breeds and/or disease states overrepresented compared to others. While we had a robust number of small breed stifle radiographs to evaluate, the number of dogs per breed was often small with many small breeds represented by only a single dog; additional recruitment of specific breeds of dog or limiting our analysis to specific breeds may have allowed for direct breed comparisons. Despite the understanding that breed plays a large role in specific anatomic conformation, we opted to compare all large breed dogs and all small breed dogs rather than to stratify by breed in order to allow for appropriate statistical analysis in our unselected patient population. Data stratified by breed are made available to illustrate the variations we observed; however, small sample size for many of the breeds prevents conclusions from being made about TPA for individual breeds. Inclusion of giant breed dogs in our large breed control group could have introduced unintended variation in our control population, which may have influenced our findings. Two out of three of our large breed groups with mean TPAs $ 30 were giant breeds and 1 of the 2 large breeds with mean TPAs # 25 was a giant breed. If we excluded giant breed dogs from our control group, we may have found a larger difference between our study populations. Previous breed stratified data showed that mean TPA in German shepherd dogs was higher than in Labrador retrievers, boxers, and Rottweilers (33), which differs from our breed specific data where the mean TPA for German shepherd dogs ranked third compared with those same breeds. This may reflect regional differences in breed conformation. Also, while some small breeds were only represented by a single dog, it was noted that 15 of 30 small breeds had a mean TPA $ 28 and the small breed dogs identified as having mean TPAs $ 35 were all terrier breeds. This seems to reflect similar reports with terriers being overrepresented in case studies describing excessive TPA in small breed dogs (26,29) and raises questions regarding the role of TPA in the progression of stifle disease for those breeds. In summary, our data add to the evidence that in unselected patient populations, small breed dogs presenting for stifle or tibial evaluation have a higher mean TPA than large breed dogs presenting for similar evaluation. Altered dogs have a higher mean TPA than unaltered male dogs, small breed dogs with normal patellae have a higher mean TPA than dogs with MPL, and breed specific variations in TPA appear to exist but dogs of the same breed may show regional variation. This, in combination with the literature on stifle disease and tibial conformation, invites further investigation of the influence of TPA on CCL disease and surgical outcomes following stifle stabilization, as well as the role of breed, patellar stability, and altered status on the development of CCL disease in small breed dogs. Acknowledgment We acknowledge Dr. Turi Aarnes for editorial support. References 1. Comerford EJ, Smith K, Hayashi K. Update on the aetiopathogenesis of canine cranial cruciate ligament disease. 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