Rupture of the CCL is one of the most common causes of pelvic limb lameness in large-breed dogs and one of the most common causes of osteoarthritis of the stifle joint.1–3 In 2003, it was estimated that pet owners in the United States spent approximately $1.32 billion for treatment of this condition.4 A single etiology has not been identified for CCL rupture, although several factors, including trauma, immune-mediated disease, age-associated degeneration of the ligament, conformational abnormalities, breed, sex, and TPA, have been suggested to play a role.4,5-14
Several studies12,13 have examined the role TPA may play in CCL rupture, and controversy exists regarding its importance. In 1982, Read and Robins9 first inferred a relationship between high TPA and subsequent rupture of the CCL. In 1983, Slocum and Devine15 postulated that a cranially directed force in the canine stifle joint (cranial tibial thrust) was generated during weight bearing, with magnitude of this force dependent on the amount of tibial compression and the slope of the tibial plateau. Slocum and Slocum16 suggested that as TPA increased, the magnitude of the cranial tibial thrust increased, predisposing dogs to rupture of the CCL. Warzee et al17 and Reif et al18 demonstrated that transection of the CCL resulted in an increase in cranial tibial translation when axial loads were applied and that leveling of the tibial plateau reduced this cranial tibial translation. Warzee et al17 also speculated that an increase in TPA would result in greater tibial thrust and, presumably, greater strain on the CCL, which might contribute to its rupture.
Because of the large variability in TPA between dogs of different and the same breeds,12,19 a true reference range for TPA in dogs has not been defined. Nevertheless, there is some evidence that dogs with higher TPAs may be predisposed to CCL rupture.9–12,15 Morris and Lipowitz,12 for instance, reported that mean TPA was higher in dogs with rupture of the CCL (23.76°) than in dogs without CCL rupture (18.1°) and hypothesized that TPA could be used as a screening test to identify dogs predisposed to CCL rupture. In contrast, Reif and Probst20 found no difference in TPA between Labrador Retrievers with and without CCL rupture. Similarly, Wilke et al13 found no difference in TPA between clinically normal Greyhounds (a breed not predisposed to CCL rupture) and clinically normal Labrador Retrievers (a breed predisposed to CCL rupture). In addition, they found that Labrador Retrievers with rupture of the CCL actually had lower TPAs than did Labrador Retrievers in which the CCL was intact.
If TPA does indeed play a role in CCL rupture and if, as has been suggested previously,19 TPAs in the right and left pelvic limbs of dogs are typically similar, then one would expect that TPAs in the right and left pelvic limbs of dogs with bilateral CCL rupture would be similar and that TPA in a dog with unilateral CCL rupture could be used to predict the likelihood of CCL rupture in the contralateral limb. The purposes of the study reported here were to compare TPAs in dogs with unilateral versus bilateral CCL rupture, to compare right versus left TPAs in dogs with bilateral CCL rupture, and to determine whether TPA could be used to predict whether a dog with unilateral CCL rupture would subsequently rupture the contralateral CCL.
Materials and Methods
Case selection criteria—Medical records of dogs examined at the Veterinary Centers of America, West Los Angeles Animal Hospital between January 2000 and June 2006 were reviewed. Dogs confirmed at surgery to have partial or complete rupture of the CCL were considered for inclusion in the study. Dogs were excluded if information on TPA in the affected limb (for dogs with unilateral CCL rupture) or limbs (for dogs with bilateral CCL rupture) was not available. In addition, to ensure that dogs with unilateral CCL rupture did not eventually rupture the contralateral ligament, dogs with unilateral CCL rupture were included in the study only if follow-up information was available for at least 2 years after the initial diagnosis of CCL rupture. Followup information was obtained through telephone calls to the owner or to the attending surgeon, if surgery had been performed elsewhere.
Medical records review—For dogs included in the study, information obtained from the medical record consisted of sex, breed, age, weight, orthopedic examination findings, and preoperative TPAs. Dogs were classified as having bilateral CCL rupture if both hind limbs were affected at the time of initial examination or, in dogs in which only 1 limb was affected at the time of initial examination, if rupture of the contralateral CCL was subsequently confirmed. For all dogs with bilateral CCL rupture, the time interval between diagnosis of the initial CCL rupture and diagnosis of CCL rupture in the contralateral limb was recorded. For dogs with bilateral CCL rupture at the time of initial examination, this time interval was recorded as 0.
Dogs were classified as having unilateral CCL rupture if only 1 limb was affected at the time of initial examination and there was no evidence of rupture of the contralateral CCL for at least 2 years after initial examination. Owners of dogs with unilateral CCL rupture were contacted a minimum of 2 years after initial examination, and follow-up examination to confirm that the contralateral CCL was intact was recommended. Owners who were unable or unwilling to return for a follow-up examination were specifically asked whether their dogs had had any signs of pain, discomfort, or lameness involving the contralateral limb and whether their dogs had undergone surgery for treatment of contralateral CCL rupture.
For dogs treated at the West Los Angeles Animal Hospital, TPAs had all been measured as described20 by 1 of 2 board-certified surgeons or by a veterinarian completing a surgical residency program. For dogs treated at other practices, TPAs had been measured by a board-certified surgeon and by a general practitioner.
Data analysis—The Wilcoxon signed rank test for paired data was used to compare right and left TPAs for dogs with bilateral CCL rupture and to compare, for dogs with bilateral CCL rupture in which there was an interval between initial and subsequent CCL rupture, TPA for the limb in which the CCL ruptured first with TPA in the contralateral limb. The Mann-Whitney test was used to compare TPAs for dogs with unilateral CCL rupture with TPAs for dogs with bilateral CCL rupture (ie, TPA for dogs with unilateral CCL rupture vs right TPA for dogs with bilateral CCL rupture, TPA for dogs with unilateral CCL rupture vs left TPA for dogs with bilateral CCL rupture, and TPA for dogs with unilateral CCL rupture vs TPA in the limb in which CCL rupture was first diagnosed for dogs with bilateral CCL) and to compare age and weight between groups. Mean time interval between diagnosis of the initial and subsequent CCL rupture and mean time interval between surgeries were calculated for dogs with bilateral CCL rupture. The Spearman rank correlation coefficient was used to determine whether right or left TPA was correlated with the time interval between diagnosis of the initial and subsequent CCL ruptures. The Cox proportional hazard regression method was used to determine whether age or initial TPA was associated with the time interval between diagnosis of the initial and subsequent CCL ruptures. The C2 test of homogeneity was used to test for differences in sex or breed distribution between dogs with unilateral CCL rupture and dogs with bilateral CCL rupture. All analyses were performed with standard software.a,b A value of P < 0.05 was considered significant.
Results
One hundred fifty dogs met the criteria for inclusion in the study. Fifty-eight of the 150 (38.7%) dogs were classified as having unilateral CCL rupture. Mean follow-up time for dogs classified as unilaterally affected was 3.4 years (range, 2 to 7 years). The remaining 92 (61.3%) dogs were classified as having bilateral CCL rupture. Twenty-five of the 92 (27%) dogs in this group had bilateral CCL rupture when initially examined, and 67 (73%) had unilateral CCL rupture when initially examined but subsequently had rupture of the contralateral CCL. An additional 250 dogs examined during the same period were excluded from the study.
Signalment—The 58 dogs with unilateral CCL rupture consisted of 38 females (36 spayed and 2 sexually intact) and 20 males (19 neutered and 1 sexually intact). The 92 dogs with bilateral CCL rupture consisted of 49 females (48 spayed and 1 sexually intact) and 43 males (41 neutered and 2 sexually intact). Sex distribution was not significantly (P = 0.59) different between groups.
Median age at the time of initial examination was 7.0 years for dogs with unilateral CCL rupture (mean, 6.8 years; range, 1.5 to 13 years) and 4.5 years for dogs with bilateral CCL rupture (mean, 4.8 years; range, 0.9 to 13.5 years). Median age at the time of initial examination of the 67 dogs with an interval between initial and subsequent CCL rupture was 4.5 years (mean, 5.0 years; range, 1.4 to 13.5 years). Median age was not significantly (P = 0.15) different between dogs with bilateral CCL rupture at the time of initial examination and dogs with bilateral CCL rupture in which there was an interval between ruptures. However, dogs with unilateral CCL rupture were significantly (P < 0.001) older than dogs with bilateral CCL rupture, and dogs < 4 years old at the time of initial examination were significantly (P = 0.018) more likely to have bilateral CCL rupture than were dogs ≥ 4 years old at the time of initial examination. For dogs with bilateral CCL rupture, there was a significant (P = 0.008) linear relationship between age at the time of initial examination and the time interval between ruptures, with the interval between ruptures increasing as age at initial examination increased.
Median body weight at the time of initial examination was 29.5 kg (64.9 lb; mean, 31.1 kg [68.4 lb]) for dogs with unilateral CCL rupture and 30.9 kg (68.0 lb; mean, 31.5 kg [69.3 lb]) for dogs with bilateral CCL rupture. Body weight was not significantly (P = 0.86) different between groups.
Nine of the 58 dogs with unilateral CCL rupture and 13 of the 92 dogs with bilateral CCL rupture were Labrador Retrievers. Seven dogs with unilateral CCL rupture and 12 dogs with bilateral CCL rupture were pitbull-type dogs. There was no significant (P = 0.75) difference in breed distribution between groups.
TPA—Median TPA in the affected limb for dogs with unilateral CCL rupture was 26° (mean, 26.3°; range, 20° to 36°). For dogs with bilateral CCL rupture, median TPA was 27° (mean, 26.9°; range, 19° to 50°) in the right hind limb and 27° (mean, 27.2°; range, 19° to 44°) in the left hind limb. Right and left TPAs were not significantly (P = 0.36) different in dogs with bilateral CCL rupture. In addition, TPA for dogs with unilateral CCL rupture was not significantly different from right TPA for dogs with bilateral CCL rupture (P = 0.36), left TPA for dogs with bilateral CCL rupture (P = 0.11), or TPA in the limb that was initially affected for dogs with bilateral CCL rupture (P = 0.17). Finally, for dogs with bilateral CCL rupture in which there was an interval between ruptures, median TPA for the limb that was affected first (27.0°; mean, 27.1°) was not significantly (P = 0.32) different from median TPA for the limb that was affected second (27.0°; mean, 26.8°).
Time interval between diagnosis of initial and subsequent CCL rupture—Median time interval between diagnosis of the initial and subsequent CCL rupture in the 92 dogs with bilateral CCL rupture was 32.0 weeks (mean, 39.9 weeks; range, 0 to 172 weeks). Median time interval between diagnosis of the initial and subsequent CCL rupture for the 67 dogs with unilateral CCL rupture at initial examination was 44.0 weeks (mean, 54.7 weeks; range, 5 to 172 weeks). Median time interval between surgeries for the 92 dogs with bilateral CCL rupture was 36.0 weeks (mean, 42.8 weeks; range, 4.5 to 168 weeks). Median time interval between surgeries for the 67 dogs with unilateral CCL rupture at initial examination was 44.0 weeks (mean, 52.5 weeks; range, 6 to 168 weeks).
There was no significant correlation between TPA and time interval between diagnosis of the initial and subsequent CCL rupture in dogs with bilateral CCL rupture. For the right TPA, the correlation coefficient was −0.12 (P = 0.34), and for the left TPA, the correlation coefficient was −0.13 (P = 0.28).
Discussion
In the present study, we did not identify any significant difference in TPA between dogs with unilateral CCL rupture and dogs with bilateral CCL rupture. In addition, TPAs in the present study were similar to those reported previously for dogs with and without CCL rupture.13,20-22 Taken together, these results suggest that there is no relationship between TPA and development of unilateral or bilateral CCL rupture in dogs. Previously, Caylor et al19 and Odders et al23 reported no significant difference between right and left TPAs in clinically normal dogs. Similarly, we found no significant difference between right and left TPAs in dogs with bilateral CCL rupture. We also did not identify any correlation between the TPA and the time interval between diagnosis of the initial and subsequent CCL ruptures in dogs with bilateral CCL rupture. This suggests that TPA in the range studied (mostly < 35°) does not appear to be a useful predictor of contralateral CCL rupture among dogs with unilateral CCL rupture. This is in contrast to the previous suggestion12 that dogs with unilateral CCL rupture and a high TPA may be predisposed to rupture of the contralateral CCL.
Mean time interval between diagnosis of initial and subsequent CCL ruptures in dogs with bilateral CCL rupture has previously been reported to be 48 to 64 weeks,2,14,24-26 and mean time interval in the present study (54.7 weeks) was in keeping with these reports. Given the previous range of times reported for mean time interval, we selected a minimum follow-up time of 2 years for dogs examined with unilateral CCL rupture to allow adequate time to document rupture of the contralateral ligament. Differences in follow-up times among studies may affect the distribution of unilateral versus bilateral CCL rupture, and a prospective study following dogs to the time of death will be necessary to differentiate dogs with true unilateral CCL rupture from dogs with bilateral rupture. The incidence of bilateral CCL rupture in dogs has been reported to range from 18% to 40%,14,24,27 whereas in the present study, the incidence was 61.3% (92/150). The higher percentage may be due to the longer follow-up time in the present study, and additional studies will be necessary to confirm these findings.
In the present study, there was a significant difference in age between dogs with unilateral CCL rupture and dogs with bilateral rupture, with dogs with bilateral CCL rupture being significantly younger. Bennett et al14 reported a higher incidence of CCL rupture among younger (< 4 years old) large-breed dogs, indicating that few of these young dogs had a history of trauma. Aiken et al7 reported that the intercondylar notch was narrow in young dogs (mean age, 3 years) with naturally occurring CCL rupture, but they could not determine whether the narrow intercondylar notch was a developmental or congenital anomaly or developed secondary to degenerative joint disease. Vasseur et al6 reported that microscopic degeneration of the CCL was apparent in dogs weighing ≥ 15 kg (33 lb) by 5 years of age, and Zeltzman et al28 reported no correlation between age at the time of diagnosis of CCL rupture and TPA. Thus, age at the time of initial examination may be a risk factor for development of bilateral CCL rupture. In particular, we found that for dogs with bilateral CCL rupture, there was a significant linear relationship between age at the time of initial examination and the time interval between ruptures, with the interval between ruptures increasing as age at initial examination increased. However, it should be considered that older patients may not live long enough to develop a contralateral CCL rupture, and additional studies are necessary to determine the relationship between age and the risk of bilateral CCL rupture.
Mean weights for dogs with unilateral and bilateral CCL rupture in the present study (31.1 and 31.5 kg, respectively) were less than mean weights reported in previous studies12,13,28 (37.9 to 40.9 kg). In part, this may be because previous studies tended to focus on specific dog breeds that generally are large (eg, Labrador Retriever, Rottweiler, Golden Retriever, and Greyhound). The inclusion of many smaller dogs in the present study resulted in lower mean weight.
The present study had several limitations because of its retrospective nature. Importantly, the inclusion criteria that were used resulted in the exclusion of a large number of dogs examined during the study period. Additionally, many of the dogs classified as having unilateral CCL rupture were not returned for follow-up examination at our hospital to confirm that they did not have a rupture of the contralateral ligament, and some of these dogs may have been misclassified.
Finally, it is possible that a real difference in TPA between dogs with unilateral versus bilateral CCL rupture exists but was obscured by the inherent variability associated with measuring TPA.19 The effect this variability in measurement of TPA could have had in the present study is not known.
ABBREVIATIONS
CCL | Cranial cruciate ligament |
TPA | Tibial plateau angle |
Egret for Windows, version 2.0.1. Cytel Software Corp, Cambridge, Mass.
StatXact-8, Cytel Software Corp, Cambridge, Mass.
References
- 1.
Powers MY, Martinez SA, Lincoln JD, et al. Prevalence of cranial cruciate ligament rupture in a population of dogs with lameness previously attributed to hip dysplasia: 369 cases (1994–2003). J Am Vet Med Assoc 2005;227:1109–1111.
- 2.↑
Johnson JM, Johnson AL. Cranial cruciate ligament rupture. Vet Clin North Am Small Animal Practice 1993;23:717–733.
- 3.
Vasseur P. Stifle joint. In: Slatter DH, ed. Textbook of small animal surgery. 3rd ed. Philadelphia: WB Saunders Co, 2002;2090–2133.
- 4.↑
Wilke VL, Robinson DA, Evans RB, et al. Estimate of the annual economic impact of treatment of cranial cruciate ligament injury in dogs in the United States. J Am Vet Med Assoc 2005;227:1604–1607.
- 5.
Niebauer GW, Wolf B, Bashey RI, et al. Antibodies to canine collagen types I and II in dogs with spontaneous cruciate ligament rupture and osteoarthritis. Arthritis Rheum 1987;30:319–327.
- 6.↑
Vasseur PB, Pool RR, Arnoczky SP, et al. Correlative biomechanical and histologic study of the cranial cruciate ligament in dogs. Am J Vet Res 1985;46:1842–1854.
- 7.↑
Aiken SW, Kass PH, Toombs JP. Intercondylar notch width in dogs with and without cranial cruciate ligament injuries. Vet Comp Orthop Traumatol 1995;8:128–132.
- 8.
Duval JM, Budsberg SC, Flo GL, et al. Breed, sex, and body weight as risk factors for rupture of the cranial cruciate ligament in young dogs. J Am Vet Med Assoc 1999;215:811–814.
- 10.
Macias C, Mckee WM, May C. Caudal proximal tibial deformity and cranial cruciate ligament rupture in small-breed dogs. J Small Anim Pract 2002;43:433–438.
- 11.
Selmi AL, Padilha Filho JG. Rupture of the cranial cruciate ligament associated with deformity of the proximal tibia in five dogs. J Small Anim Pract 2001;42:390–393.
- 12.↑
Morris E, Lipowitz AJ. Comparison of tibial plateau angles in dogs with and without cranial cruciate ligament injuries. J Am Vet Med Assoc 2001;218:363–366.
- 13.↑
Wilke VL, Conzemius MG, Besancon MF, et al. Comparison of tibial plateau angle between clinically normal Greyhounds and Labrador Retrievers with and without rupture of the cranial cruciate ligament. J Am Vet Med Assoc 2002;221:1426–1429.
- 14.↑
Bennett D, Tennant B, Lewis DG, et al. A reappraisal of anterior cruciate ligament disease in the dog. J Small Anim Pract 1988;29:275–297.
- 15.↑
Slocum B, Devine T. Cranial tibial thrust: a primary force in the canine stifle. J Am Vet Med Assoc 1983;183:456–459.
- 16.↑
Slocum B, Slocum TD. Tibial plateau leveling osteotomy for repair of cruciate ligament rupture in the canine. Vet Clin North Am Small Animal Practice 1993;23:777–795.
- 17.↑
Warzee C, Dejardin L, Arnoczky P, et al. Effect of tibial plateau leveling on cranial and caudal tibial thrust in canine cruciate-deficient stifles: an in vitro experimental study. Vet Surg 2001;30:278–286.
- 18.↑
Reif U, Hulse DA, Hauptman JG. Effect of tibial plateau leveling on stability of the canine cranial cruciate-deficient stifle joint: an in vitro study. Vet Surg 2002;31:147–154.
- 19.↑
Caylor KB, Zumpano CA, Evans LM, et al. Intraand interobserver measurement variability of tibial plateau slope from lateral radiographs in dogs. J Am Hosp Assoc 2001;37:263–268.
- 20.↑
Reif U, Probst CW. Comparison of tibial plateau angles in normal and cranial cruciate deficient stifles of Labrador Retrievers. Vet Surg 2003;32:385–389.
- 21.
Fettig AA, Rand WM, Sato AF, et al. Observer variability of tibial plateau slope measurement in 40 dogs with cranial cruciate ligament-deficient stifle joints. Vet Surg 2003;32:471–478.
- 22.
Reif U, Dejardin LM, Probst CW, et al. Influence of limb positioning and measurement method on the magnitude of the tibial plateau angle. Vet Surg 2004;33:368–375.
- 23.↑
Odders JW, Jessen CR, Lipowitz AJ. Sequential measurements of the tibial plateau angle in large-breed, growing dogs. Am J Vet Res 2004;65:513–518.
- 24.
Moore KW, Read RA. Cranial cruciate ligament rupture in the dog—a retrospective study comparing surgical techniques. Aust Vet J 1995;72:281–285.
- 25.
Doverspike M, Vasseur PB, Harb MF, et al. Contralateral cranial cruciate ligament rupture: incidence in 114 dogs. J Am Anim Hosp Assoc 1993;29:167–170.
- 26.
Pond MJ, Campbell JR. The canine stifle joint I. Rupture of the anterior cruciate ligament. An assessment of conservative and surgical treatment. J Small Anim Pract 1972;13:1–10.
- 27.
Lampman TJ, Lund EM, Lipowitz AJ. Cranial cruciate disease: current status of diagnosis, surgery, and risk for disease. Vet Comp Orthop Traumatol 2003;16:122–126.
- 28.↑
Zeltzman PA, Paré B, Johnson GM, et al. Relationship between age and tibial plateau angle in dogs with cranial cruciate rupture. J Am Anim Hosp Assoc 2005;41:117–120.