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Lumbosacral Transitional Vertebrae, Canine Hip Dysplasia, and Sacroiliac Joint Degenerative Changes on Ventrodorsal Radiographs of the Pelvis in Police Working German Shepherd Dogs
Topics in Compan An Med ] (2015) ]]]–]]]
Topical Review
Lumbosacral Transitional Vertebrae, Canine Hip Dysplasia, and Sacroiliac Joint Degenerative Changes on Ventrodorsal Radiographs of the Pelvis in Police Working German Shepherd Dogs Renata Komsta, DVM, PhDn, Anna Łojszczyk-Szczepaniak, DVM, PhD, Piotr Dębiak, DVM, PhD Keywords: lumbosacral transitional vertebrae canine hip dysplasia sacroiliac joint degenerative changes working dogs Laboratory for Radiology and Ultrasonography, Department and Clinic of Animal Surgery, University of Life Science in Lublin, Lublin, Poland
Lumbosacral transitional vertebrae (LTV) frequently occur in German shepherd dogs. The aim of the study was to evaluate the prevalence and interdependence between LTV and canine hip dysplasia (CHD) as well as sacroiliac joint degenerative changes visualized on ventrodorsal radiographs of the pelvis in both working and companion German shepherd dogs. The presence of LTV was found in 12% of working dogs and in 33% of companion dogs. Similar incidence of hip dysplasia in both the groups was found. It has been shown that dogs with LTV have a higher frequency of severe CHD. A higher percentage of sacroiliac joint degenerative changes was observed in dogs with no signs of LTV and in working dogs. & 2015 Elsevier Inc. All rights reserved.
n
Address reprint requests to: Renata Komsta, DVM, PhD, Laboratory for Radiology and Ultrasonography, Department and Clinic of Animal Surgery, University of Life Science in Lublin, Głęboka 30 Street, 20-612 Lublin, Poland E-mail: [email protected], renata. [email protected] (R. Komsta)
Introduction The term “lumbosacral transitional vertebrae” (LTV) means the abnormally formed vertebra between the last normal lumbar vertebra and the first normal sacral vertebra.1 This disorder is classified as congenital and has morphologic characteristics of both lumbar and sacral vertebrae.1,2 A hereditary predisposition to LTV is also suggested.2-4 LTV may be responsible for weakening of the sacroiliac attachment and lead to premature intervertebral disk degeneration in the lumbosacral segment as well as occurrence of cauda equina syndrome.2-5 Moreover, asymmetric transitional vertebrae may hinder the correct positioning of the dog for hip dysplasia evaluation.2,6 Canine hip dysplasia (CHD) is considered to be a heritable developmental disease, which leads to the development of osteoarthritis.7-11 Studies by Smith et al.12 revealed that, when compared with rottweilers, Labrador retrievers, and golden retrievers, the risk of the development of degenerative joint disease associated with hip dysplasia in German shepherd dogs is almost 5 times higher. Both CHD and LTV were often described in German shepherd dogs.3,8,10,13-15 It is postulated to eliminate breeding of affected individuals and exclude them from expensive long-term trainings.2,8,14,16 The problem of sacroiliac joint degenerative changes in dogs is mentioned less frequently. Currently, it is suggested that sacroiliac joint disease may be responsible for pain at the gluteal region of the proximal thigh.17 The aim of the retrospective studies was to evaluate the prevalence and interdependence between LTV and hip dysplasia as well as sacroiliac joint degenerative changes visible on http://dx.doi.org/10.1053/j.tcam.2015.02.005 1527-3369/ & 2015 Topics in Companion Animal Medicine. Published by Elsevier Inc.
ventrodorsal radiographs in both working and companion German shepherd dogs.
Material and methods The retrospective studies have been conducted based on the pelvic radiographs of 205 German shepherd dogs in order to confirm or exclude hip dysplasia. Collected data came from the Faculty of Veterinary Medicine at the University of Life Sciences in Lublin. The dogs were divided into 2 groups: (A) police working dogs that were subjected to physical agility tests and radiographic examinations of hip joints and (B) companion dogs, the control group, which never underwent physical agility tests. For the radiographic examination, all animals were sedated intramuscularly with a combination of 2 mg/kg of xylazine (Sedazin, Biowet Puławy Sp. z o.o., Puławy, Poland), 0.25 mg/kg of diazepam (Relanium, Warszawskie Zakłady Farmaceutyczne, Polfa S.A., Warszawa, Poland), and 0.05 mg/kg of atropine sulfate (AtropinumSulfuricum, WZF Warszawskie Zakłady Farmaceutyczne, Polfa S.A., Warszawa, Poland). Ventrodorsal radiographs of the pelvis with pelvic limbs extended in accordance with the Orthopedic Foundation for Animals and Federal Cynologique Internationale regulations were performed.18 The following 3 quantitative traits were evaluated: LTV (divided into types with particular emphasis on the type of transverse process: symmetric or asymmetric), hip dysplasia (each joint was assessed separately), as well as degenerative changes of the sacroiliac joints, separately for each joint (right and left), recording their presence (1) or absence (0) in the binary system.
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R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]]
The LTV was considered the one that had at least one of the morphologic features visible on the ventrodorsal radiographs3: the spinous process of the first sacral vertebra separated from the median sacra crest, distinct morphologic changes in the transverse processes of the presacral vertebra or contact of at least one of these processes with the iliac bone, rotation of the presacral vertebra or the sacral bone over their long axes, or the lack of symmetry in the length and position of the sacroiliac attachment. Based on the shape and their attachment to the ilium, the transverse processes of LTV were divided into 3 types. Type 1 (lumbar type) is not attached to the ilium or sacral bone (Fig 1). Type 2 (intermediate type) is partially attached to the ilium or sacral bone, but the tip remains always free (Fig 2). Type 3 (sacral type) has characteristics of a sacral wing: it has a broad attachment to the ilium and often to the wing of the sacrum and does not have a free tip (Fig 1). It is considered that LTV is symmetric if it has the same type of transverse processes (1/1, 2/2, and 3/3), whereas asymmetric LTV has a different type of transverse processes, for example, type 1 on the right side and type 3 on the left side (1/3).3,16 Hip dysplasia was evaluated in accordance with regulations of the Federal Cynologique Internationale.18 The CHD score includes A (no signs of hip dysplasia) (Fig 3), B (near-normal hip joints) (Fig 4) (free of CHD), and C (mild hip dysplasia) (Fig. 5), D (moderate hip dysplasia), E (severely affected by CHD) (Fig 6). Features indicating sacroiliac joint degenerative changes visible in a ventrodorsal radiograph of pelvis7,17 included osteophyte formation, calcification of the sacroiliac ligaments or sclerosis at the site of their insertion, and ankylosis or increased opacity of the synovial joint (Fig 7). To evaluate the correlation between selected changes in the skeletal system in working and companion German shepherd dogs and exposure of facilitating factors, the odds ratio (OR) parameter was used. Counted interactions created the data table with dimensions of 2 2, based on which Mantel-Haenszel statistics and chi-square of homogeneity were calculated (P o 0.05 considered statistically significant). Statistical calculations were performed using the R Statistical Software with the “EPIR” module.
Fig. 2. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There is symmetric LTV (2/2): both transverse processes are partially attached to the ilium, whereas their tips remain free (small arrows).
Imaging findings on ventrodorsal radiographs of the pelvis in the working German shepherd dogs and the control dogs are shown in Table 1. Prevalence of morphologic traits in working German shepherd dogs and control dogs is shown in Table 2. LTV was found in 47 (22.9%) animals. In the German shepherd dogs from the group of companion animals, LTV was more frequent. The risk of its occurrence was more than 3 times greater
Results The working dogs group (group A) included 99 German shepherd dogs (10 females and 89 males) aged 1.2-12 years (an average age of 5 years). The companion animals group (group B) included 106 German shepherd dogs (14 females and 94 males) aged from 0.5-11 years (an average age of 2.6 years).
Fig. 1. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There is asymmetric LTV (1/3). The transverse process on the right is not attached to the ilium bone (black arrow), whereas the one on the left is fully attached to the ilium and the sacrum.
Fig. 3. A ventrodorsal hip-extended radiograph in the dog with no signs of dysplasia (CHD A) in both the joints. The femoral heads and the acetabulums are congruent, the joint spaces are narrow and even, and the craniolateral rims are sharp and slightly rounded. The acetabular angles according to Norberg are approximately 1051.
R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]]
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on the increased risk of the severe hip dysplasia (CHD E) in one or both the hip joints is not shown either. There was a significantly higher prevalence of bilateral sacroiliac joint degenerative changes in dogs with no symptoms of LTV (Table 5). A similar correlation was found for the degenerative changes only in the right sacroiliac joint. The similar correlation was recognized for degenerative changes in the left hip joint, but the conclusions are not statistically significant. A small population of studied animals with asymmetric LTV and degenerative changes in one or both the sacroiliac joints did not allow to statistically confirm correlation between them (Table 6). Discussion The prevalence of LTV in the German shepherd dogs, according to different studies, varies from 3.5%-40%.3,8,14,15,19 Such a big discrepancy is explained by the difference in inclusion criteria. In the our observations, this anomaly was revealed in 22.9% of the German shepherd dogs in the whole group of the studied animals. There was a significant variation in the prevalence of LTV between a group of working dogs (12.0%) and the control group (33.0%), with a similar incidence of hip dysplasia in both the groups (77.7% in group A and 77.4% in group B). Such results may be explained by the fact that, in Poland, all dogs pass physical ability tests before employment in the police. All animals that reveal abnormalities of gait or refuse to jump over the obstacle up to 1.5-m high are disqualified. Studies by Scharf et al.8 concerning only working dogs showed lower incidence of the transitional
Fig. 4. A ventrodorsal hip-extended radiograph in the dog with near-normal hip joints (CHD B) in both the joints. The femoral heads and the acetabulums are slightly incongruent, and the acetabular angles according to Norberg are approximately 1051.
than in the police working dogs. The ratio between the symmetric and asymmetric LTV was not balanced. The symmetric form constituted 68.1% of all recognized transitional vertebrae. Asymmetric types of the transverse processes were more frequent in group A. Hip dysplasia was found in 158 (77.1%) animals: 76 German shepherd dogs in group A (which constitutes 77.7% of the group) and 82 in group B (77.4% of the group). In both the groups, the degree of severity of the disease was different (Table 1). Degenerative changes in at least one sacroiliac joint were found in 175 (85.4%) German shepherd dogs. The changes were recognized in 85 police dogs (which is 85.9% of this group), of which, in 23 (27.1%) animals the changes were unilateral. Degenerative sacroiliac joint abnormalities were found in 90 dogs in group B (which is 84.9% of this group), of which, in 43 (47.8%) animals the changes were unilateral. The correlation between the method of use of German shepherd dogs and the number of sacroiliac joints affected by degenerative changes was shown (Table 2). Statistical analysis showed no statistically significant correlation between the occurrence of LTV and hip dysplasia (C, D, and E) in any of the joints (right, left, or both). A strong and statistically significant correlation between the occurrence of LTV and the most severe form of unilateral or bilateral hip dysplasia (E) is shown in Table 3. There was no correlation between the presence of symmetric or asymmetric LTV and increased risk of unilateral or bilateral hip dysplasia (Table 4). The influence of asymmetric LTV
Fig. 5. A ventrodorsal hip-extended radiograph in the dog with mild hip dysplasia (CHD C) in both the joints. The femoral heads and the acetabulums are incongruent, the acetabular angles according to Norberg are approximately 1001, and there are osteoarthritic changes at margo acetabularis cranialis and femoral necks.
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R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]] Table 1 Imaging Findings on Ventrodorsal Radiographs of Pelvis in the Working German Shepherd Dog (A) Group (n ¼ 99) and the Control (B) Group (n ¼ 106) Variable
A Group (%) B Group (%) Total
LTV 12 Symmetric type 4 Asymmetric type 8 CHD A or B* 75 CHD C* 72 CHD D* 35 CHD E* 16 Sacroiliac joint degenerative changes* 147 n
(12.0) (4.0) (8.0) (37.9) (36.4) (17.7) (8.0) (76.6)
35 28 7 75 53 58 26 137
(33.0) (26.4) (6.6) (35.4) (25) (27.3) (12.3) (64.9)
47 32 15 150 125 93 42 284
(22.9) (15.6) (7.3) (36.6) (30.5) (22.7) (10.2) (69.3)
Each joint counted separately.
Table 2 Prevalence of Morphologic Traits Reported as Number of Dogs (%) for the Working German Shepherd Dog (A) Group (n ¼ 99) and the Control (B) Group (n ¼ 106) Variable
A Group (%) B Group (%) OR (CI)
LTV CHD C, D or E† Sacroiliac joint degenerative changes†
12 (12.0) 123 (62.1) 147 (76.6)
33 (33.0) 137 (64.6) 137 (64.9)
P Value
3.57 (1.73-7.39) 0.0004* 0.9 (0.6-1.34) 0.599 1.76 (1.14-2.73) 0.0106*
OR, odds ratio. n
†
Level of significance at P o 0.05. Each joint counted separately.
Table 3 Odds Ratios (OR) for CHD Associated With LTV CHD
LTV
OR (CI)
With
Fig. 6. A ventrodorsal hip-extended radiograph in the dog with moderate dysplasia of the left joint and severe dysplasia of the right joint. In the left joint, there are obvious incongruence between femoral head and the acetabulum, acetabular angle according to Norberg more than 901, and osteoarthritic signs. In the right joint there are distinct subluxation, acetabular angle according to Norberg less than 901, flattening of the margo acetabularis cranialis, and deformation of the femoral head and neck. There are osteoarthritis changes at margo acetabularis.
vertebra (3.5%) than it was shown in the present study. Moreover, despite the fact that dogs with degenerative changes of the hip, knee, or elbow joints should be disqualified already in preliminary
Bilateral C, D or E Bilateral E C, D or E in either one hip joint or both E in either one hip joint or both C, D or E in left hip joint E in left hip joint C, D or E in right hip joint E in right hip joint n
P Value
Without
28 (59.6%) 74 (46.8%) 1.67 (0.86-3.24) 0.125 7 (14.9%) 9 (5.7%) 2.9 (1.02-8.26) 0.039* 38 (80.9%) 120 (75.9%) 1.34 (0.59-3.01) 0.483 10 (21.3%) 33 8 33 9
16 (10.1%)
2.4 (1.01-5.72) 0.044*
(70.2%) 94 (59.5%) 1.6 (0.8-3.24) 0.184 (17.0%) 11 (7.0%) 2.74 (1.03-7.28) 0.0368* (70.2%) 100 (63.3%) 1.37 (0.68-2.76) 0.3828 (19.1%) 14 (8.9%) 2.44 (0.98-6.05) 0.0498*
Level of significance at P o 0.05.
Table 4 Odds Ratios (OR) for CHD Associated With Asymmetric LTV CHD
LTV
OR (CI)
P Value
Asymmetric Symmetric Bilateral C, D or E Bilateral E C, D or E in left hip joint E in left hip joint C, D or E in right hip joint E in right hip joint
Fig. 7. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There are sacroiliac joint degenerative changes, such as calcified dorsal and ventral sacroiliac ligaments (black arrow), sclerosis at the site of attachment of the sacroiliac ligaments at the sacral margin (white arrow), osteophytes bridging the synovial space (stars), and osteophytes on the caudal aspect of synovial sacroiliac joint (arrowhead).
11 (73.3%) 1 (6.7%) 12 (80.0%)
17 (53.1%) 6 (18.8%) 21 (65.6%)
2.43 (0.64-9.25) 0.188 3.23 (0.35-29.58) 0.278 2.1 (0.49-9.03) 0.315
1 (6.7%) 12 (80.0%)
7 (21.9%) 21 (65.6%)
3.92 (0.44-35.2) 1.08 (0.23-5.08)
0.196 0.919
3 (20.0%)
6 (18.7%)
1.08 (0.23-5.08)
0.919
radiographic examinations, dogs with mild dysplasia may be accepted.20 According to our study, lesions characteristic for mild hip dysplasia (CHD C) prevailed in the hip joints of the police working dogs, while in group B dominated moderate changes (CHD D), although the dogs from group B had lower average age.
R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]] Table 5 Odds Ratios (OR) for Sacroiliac Joint Degenerative Changes Associated With LTV Sacroiliac Joint Degenerative Changes
LTV With
Bilateral Left Right n
OR (CI)
P Value
Without
17 (36.2%) 94 (59.5%) 2.59 (1.32-5.09) 0.005* 28 (60.9%) 114 (72.6%) 1.7 (0.86-3.39) 0.127 26 (55.3%) 116 (75.8%) 2.53 (1.28-5.02) 0.0067*
Level of significance at P o 0.05.
Table 6 Odds Ratios (OR) for Sacroiliac Joint Degenerative Changes Associated With Asymmetric LTV Sacroiliac Joint LTV Degenerative Changes Asymmetric Symmetric
OR (CI)
Bilateral Left Right
2.92 (0.82-10.44) 0.094 2.26 (0.59-8.7) 0.228 2.00 (0.56-7.18) 0.284
8 (53.3%) 11 (73.3%) 10 (66.7%)
9 (28.1%) 17 (54.8%) 16 (46.9%)
P Value
Observations of the military working dogs11,21 did not reveal any significant differences in the length of time worked between normal and dysplastic dogs. This is probably because working dogs have professional and careful medical care. Contrary to other studies,3,14,16 our studies clearly demonstrate that symmetric LTV (15.6%) is more frequent than asymmetric LTV is (7.3%). This uneven distribution was intensified especially in the control group (Table 1). According to the Rosenberg hypothesis, it is facilitated by the presence of contact points between the pelvis and the vertebrae at the same level on both the sides during the development of the animal.22 To date, it was a disputable issue to establish the correlation between the presence of LTV and a hip joint development. Larsen6 and Wigger et al.14 did not find such a correlation. Conversely, Olsson and Kasstrom,9 and Morgan and Stevens23 suggested that the presence of LTV could affect uneven hip joint development. It is possible that our studies will help to explain the apparent lack of consistency in the results of different studies. The detailed analysis revealed the correlation between LTV and the development of the severe hip dysplasia (E), but not mild forms (C and D) (Table 1). This correlation is stronger for the bilateral severe dysplasia than in the case of the unilateral (separately right or left) severe dysplasia. This can at least in part explain the distinctly lower incidence of CHD E in working dogs when compared with companion animals (Table 1). Indication of the relation between the influence of symmetric and asymmetric form of LTV on the increased risk of bilateral or unilateral hip dysplasia requires further study. Results of our studies revealed that, in the working dogs, the risk of sacroiliac joint degenerative changes increases (Table 2). The result was consistent with the expectations of the authors. The average age of dogs in group A was higher than that of the dogs in group B. The relation between the age of dogs and the development of degenerative changes in the mentioned joints was proved by Knaus et al.17 Moreover, Breit et al.24 suggest that one of the causes of the new bone formation in the sacroiliac joint may be vigorous exercise. It is interesting that our studies revealed that the degenerative changes in the sacroiliac joints develop more often in animals with no LTV. The risk of bilateral sacroiliac joint degenerative changes is 2.5 times greater than in a group of dogs that have LTV. Asymmetric sacroiliac attachments occurring with asymmetric LTV is described quite often.2,3,16 However, the
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authors have not found any work confirming the correlation between the presence of LTV and the development of the sacroiliac joint degenerative changes. Thus, this issue needs to be further studied. The retrospective nature of the present study makes the presented study restricted. The presented research was based solely on the ventrodorsal radiograph of the pelvis. There is the possibility of overlooking some types of the transitional vertebra (symmetric type 1 LTV). As both the groups of dogs were evaluated on the same basis, the error should be comparable and should not affect the results of this work.
Conclusion Dogs with LTV have a higher frequency of CHD E. Hence, it is recommended to exclude dogs with LTV from expensive specialized trainings and from breeding. Simultaneously, our studies revealed that in the group of dogs that underwent physical agility tests, the defect is almost 3 times less frequent than in companion animals. The risk of sacroiliac joint degenerative changes is greater in dogs that do not have LTV. It is also more frequent in working dogs. References 1. Morgan JP. Congenital anomalies of the vertebral column of the dog: a study of the incidence and significance based on a radiographic and morphologic study. J Am Vet Radiol Soc 9:21–29, 1968 2. Morgan JP. Transitional lumbosacral vertebral anomaly in the dog: a radiographic study. J Small Anim Pract 40:167–172, 1999 3. Damur-Djuric N, Steffen F, Hässing M, et al. Lumbosacral transitional vertebrae in dogs: classification, prevalence, and association with sacroiliac morphology. Vet Radiol Ultrasound 47:32–38, 2006 4. Morgan JP, Bahr A, Franti CE, et al. Lumbosacral transitional vertebrae as a predisposing cause of cauda equine syndrome in German shepherd dogs: 161 cases (1987–1990). J Am Vet Med Assoc 202:1877–1882, 1993 5. Steffen F, Berger M, Morgan JP. Asymmetrical, transitional, lumbosacral vertebral segments in six dogs: a characteristic spinal syndrome. J Am Anim Hosp Assoc 40:338–344, 2004 6. Larsen JS. Lumbosacral transitional vertebrae in the dog. J Am Vet Radiol Soc 18:76–79, 1977 7. Graeme SA. Radiographic signs of joint disease in dogs and cats. In: Thrall DE, editor. Textbook of Veterinary Diagnostic Radiology. 5th ed. Philadelphia, PA: W. Elsevier Saunders; 2007. p. 317–358 8. Scharf G, Steffen F, Grünenfelder F, et al. The lumbosacral junction in working German shepherd dogs—neurological and radiological evaluation. J Vet Med A 51:27–32, 2004 9. Olsson SE, Kasstrom H: Etiology and pathogenesis of canine hip dysplasia. Proceedings on Canine Hip Dysplasia Symposium and Workshop. St. Luis, MO: Orthopedic Foundation of Animals; 24, 1972 10. Coopman F, Verhoeven G, Saunders J, Duchateau L, Van Bree H. Prevalence of hip dysplasia, elbow dysplasia and humeral head osteochondrosis in dog breeds in Belgium. Vet Rec 29:654–658, 2008 11. Zorko B, Ivanuša T, Pelc R. Progression of hip dysplasia in 40 police working dogs: a retrospective study. Slovenian Vet Res 42:71–76, 2005 12. Smith GK, Mayhew PD, Kapatkin AS, McKelvie PJ, Shofer FS, Gregor TP. Evaluation of risk factors for degenerative joint disease associated with hip dysplasia in German Shepherd Dogs, Golden Retrievers, Labrador Retrievers and Rottweilers. J Am Vet Med Assoc 219:1719–1724, 2001 13. Breit S, Knaus I, Künzel W. Differentiation between lumbosacral Transitional Vertebrae, Pseudolumbarisation, and lumbosacral osteophyte formation in ventrodorsal radiographs of the canine pelvis. Vet J 165:36–42, 2003 14. Wigger A, Julier-Franz C, Telhelm B, et al. Lumbosacral transitional vertebrae in the German shepherd dog: prevalence, classification, genetics, and association with canine hip dysplasia. Tierärztliche Praxis. Ausgabe Kleintiere Heimtiere 37:7–13, 2009 15. Lappalainen AK, Salomaa R, Junnila J, et al. Alternative classification and screening protocol for transitional lumbosacral vertebra in German shepherd dogs. Acta Vet Scand 54:1–10, 2012 16. Flückiger MA, Damur-Djuric N, Hässing M, et al. A lumbosacral transitional vertebra in the dog predisposes to cauda equine syndrome. Vet Radiol Ultrasound 47:39–44, 2006 17. Knaus I, Brett S, Künzel W, Mayrhofer E. Appearance and incidence of sacroiliac joint disease in ventrodorsal radiographs of canine pelvis. Vet Radiol Ultrasound 45:1–9, 2004
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18. Federation Cynologique Internationale (AIBL). Radiographic Procedure for Hip Dysplasia Evaluation. www.fci.be/circularizes/46-2009-annex2-eu.pdf 19. Ondreka N, Amort KH, Stock KF, et al. Skeletal morphology and morphometry of the lumbosacral junction in German shepherd dogs and an evaluation of the possible genetic basis for radiographic findings. Vet J 196: 64–70, 2013 20. Moore GE, Burkman KD, Carter MN, et al. Causes of death or reasons for euthanasia in police working dogs: 927 cases (1993–1996). J Am Vet Med Assoc 219:209–214, 2001
21. Banfield CM, Bartles JE, Huson JA, et al. A retrospective study of canine hip dysplasia in 116 police working dogs. Part II: clinical signs and performance data. J Am Anim Hosp Assoc 32:423–430, 1996 22. Rosenberg E. Bemerkungen über den Modus des Zustandekommens der Regionen an der Wirbesäule des Menschen. Morph Jahrb 36:609–659, 1907 23. Morgan JP, Stevens M. Radiographic diagnosis and control of canine hip dysplasia. Ames, IA: Iowa State University Press; 1985 24. Breit S, Knaus I, Künzel W. The gross and radiographic appearance of sacroiliac ankylosis capsularis ossea in the dog. Res Vet Sci 74:85–92, 2003
Topical Review
Lumbosacral Transitional Vertebrae, Canine Hip Dysplasia, and Sacroiliac Joint Degenerative Changes on Ventrodorsal Radiographs of the Pelvis in Police Working German Shepherd Dogs Renata Komsta, DVM, PhDn, Anna Łojszczyk-Szczepaniak, DVM, PhD, Piotr Dębiak, DVM, PhD Keywords: lumbosacral transitional vertebrae canine hip dysplasia sacroiliac joint degenerative changes working dogs Laboratory for Radiology and Ultrasonography, Department and Clinic of Animal Surgery, University of Life Science in Lublin, Lublin, Poland
Lumbosacral transitional vertebrae (LTV) frequently occur in German shepherd dogs. The aim of the study was to evaluate the prevalence and interdependence between LTV and canine hip dysplasia (CHD) as well as sacroiliac joint degenerative changes visualized on ventrodorsal radiographs of the pelvis in both working and companion German shepherd dogs. The presence of LTV was found in 12% of working dogs and in 33% of companion dogs. Similar incidence of hip dysplasia in both the groups was found. It has been shown that dogs with LTV have a higher frequency of severe CHD. A higher percentage of sacroiliac joint degenerative changes was observed in dogs with no signs of LTV and in working dogs. & 2015 Elsevier Inc. All rights reserved.
n
Address reprint requests to: Renata Komsta, DVM, PhD, Laboratory for Radiology and Ultrasonography, Department and Clinic of Animal Surgery, University of Life Science in Lublin, Głęboka 30 Street, 20-612 Lublin, Poland E-mail: [email protected], renata. [email protected] (R. Komsta)
Introduction The term “lumbosacral transitional vertebrae” (LTV) means the abnormally formed vertebra between the last normal lumbar vertebra and the first normal sacral vertebra.1 This disorder is classified as congenital and has morphologic characteristics of both lumbar and sacral vertebrae.1,2 A hereditary predisposition to LTV is also suggested.2-4 LTV may be responsible for weakening of the sacroiliac attachment and lead to premature intervertebral disk degeneration in the lumbosacral segment as well as occurrence of cauda equina syndrome.2-5 Moreover, asymmetric transitional vertebrae may hinder the correct positioning of the dog for hip dysplasia evaluation.2,6 Canine hip dysplasia (CHD) is considered to be a heritable developmental disease, which leads to the development of osteoarthritis.7-11 Studies by Smith et al.12 revealed that, when compared with rottweilers, Labrador retrievers, and golden retrievers, the risk of the development of degenerative joint disease associated with hip dysplasia in German shepherd dogs is almost 5 times higher. Both CHD and LTV were often described in German shepherd dogs.3,8,10,13-15 It is postulated to eliminate breeding of affected individuals and exclude them from expensive long-term trainings.2,8,14,16 The problem of sacroiliac joint degenerative changes in dogs is mentioned less frequently. Currently, it is suggested that sacroiliac joint disease may be responsible for pain at the gluteal region of the proximal thigh.17 The aim of the retrospective studies was to evaluate the prevalence and interdependence between LTV and hip dysplasia as well as sacroiliac joint degenerative changes visible on http://dx.doi.org/10.1053/j.tcam.2015.02.005 1527-3369/ & 2015 Topics in Companion Animal Medicine. Published by Elsevier Inc.
ventrodorsal radiographs in both working and companion German shepherd dogs.
Material and methods The retrospective studies have been conducted based on the pelvic radiographs of 205 German shepherd dogs in order to confirm or exclude hip dysplasia. Collected data came from the Faculty of Veterinary Medicine at the University of Life Sciences in Lublin. The dogs were divided into 2 groups: (A) police working dogs that were subjected to physical agility tests and radiographic examinations of hip joints and (B) companion dogs, the control group, which never underwent physical agility tests. For the radiographic examination, all animals were sedated intramuscularly with a combination of 2 mg/kg of xylazine (Sedazin, Biowet Puławy Sp. z o.o., Puławy, Poland), 0.25 mg/kg of diazepam (Relanium, Warszawskie Zakłady Farmaceutyczne, Polfa S.A., Warszawa, Poland), and 0.05 mg/kg of atropine sulfate (AtropinumSulfuricum, WZF Warszawskie Zakłady Farmaceutyczne, Polfa S.A., Warszawa, Poland). Ventrodorsal radiographs of the pelvis with pelvic limbs extended in accordance with the Orthopedic Foundation for Animals and Federal Cynologique Internationale regulations were performed.18 The following 3 quantitative traits were evaluated: LTV (divided into types with particular emphasis on the type of transverse process: symmetric or asymmetric), hip dysplasia (each joint was assessed separately), as well as degenerative changes of the sacroiliac joints, separately for each joint (right and left), recording their presence (1) or absence (0) in the binary system.
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R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]]
The LTV was considered the one that had at least one of the morphologic features visible on the ventrodorsal radiographs3: the spinous process of the first sacral vertebra separated from the median sacra crest, distinct morphologic changes in the transverse processes of the presacral vertebra or contact of at least one of these processes with the iliac bone, rotation of the presacral vertebra or the sacral bone over their long axes, or the lack of symmetry in the length and position of the sacroiliac attachment. Based on the shape and their attachment to the ilium, the transverse processes of LTV were divided into 3 types. Type 1 (lumbar type) is not attached to the ilium or sacral bone (Fig 1). Type 2 (intermediate type) is partially attached to the ilium or sacral bone, but the tip remains always free (Fig 2). Type 3 (sacral type) has characteristics of a sacral wing: it has a broad attachment to the ilium and often to the wing of the sacrum and does not have a free tip (Fig 1). It is considered that LTV is symmetric if it has the same type of transverse processes (1/1, 2/2, and 3/3), whereas asymmetric LTV has a different type of transverse processes, for example, type 1 on the right side and type 3 on the left side (1/3).3,16 Hip dysplasia was evaluated in accordance with regulations of the Federal Cynologique Internationale.18 The CHD score includes A (no signs of hip dysplasia) (Fig 3), B (near-normal hip joints) (Fig 4) (free of CHD), and C (mild hip dysplasia) (Fig. 5), D (moderate hip dysplasia), E (severely affected by CHD) (Fig 6). Features indicating sacroiliac joint degenerative changes visible in a ventrodorsal radiograph of pelvis7,17 included osteophyte formation, calcification of the sacroiliac ligaments or sclerosis at the site of their insertion, and ankylosis or increased opacity of the synovial joint (Fig 7). To evaluate the correlation between selected changes in the skeletal system in working and companion German shepherd dogs and exposure of facilitating factors, the odds ratio (OR) parameter was used. Counted interactions created the data table with dimensions of 2 2, based on which Mantel-Haenszel statistics and chi-square of homogeneity were calculated (P o 0.05 considered statistically significant). Statistical calculations were performed using the R Statistical Software with the “EPIR” module.
Fig. 2. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There is symmetric LTV (2/2): both transverse processes are partially attached to the ilium, whereas their tips remain free (small arrows).
Imaging findings on ventrodorsal radiographs of the pelvis in the working German shepherd dogs and the control dogs are shown in Table 1. Prevalence of morphologic traits in working German shepherd dogs and control dogs is shown in Table 2. LTV was found in 47 (22.9%) animals. In the German shepherd dogs from the group of companion animals, LTV was more frequent. The risk of its occurrence was more than 3 times greater
Results The working dogs group (group A) included 99 German shepherd dogs (10 females and 89 males) aged 1.2-12 years (an average age of 5 years). The companion animals group (group B) included 106 German shepherd dogs (14 females and 94 males) aged from 0.5-11 years (an average age of 2.6 years).
Fig. 1. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There is asymmetric LTV (1/3). The transverse process on the right is not attached to the ilium bone (black arrow), whereas the one on the left is fully attached to the ilium and the sacrum.
Fig. 3. A ventrodorsal hip-extended radiograph in the dog with no signs of dysplasia (CHD A) in both the joints. The femoral heads and the acetabulums are congruent, the joint spaces are narrow and even, and the craniolateral rims are sharp and slightly rounded. The acetabular angles according to Norberg are approximately 1051.
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on the increased risk of the severe hip dysplasia (CHD E) in one or both the hip joints is not shown either. There was a significantly higher prevalence of bilateral sacroiliac joint degenerative changes in dogs with no symptoms of LTV (Table 5). A similar correlation was found for the degenerative changes only in the right sacroiliac joint. The similar correlation was recognized for degenerative changes in the left hip joint, but the conclusions are not statistically significant. A small population of studied animals with asymmetric LTV and degenerative changes in one or both the sacroiliac joints did not allow to statistically confirm correlation between them (Table 6). Discussion The prevalence of LTV in the German shepherd dogs, according to different studies, varies from 3.5%-40%.3,8,14,15,19 Such a big discrepancy is explained by the difference in inclusion criteria. In the our observations, this anomaly was revealed in 22.9% of the German shepherd dogs in the whole group of the studied animals. There was a significant variation in the prevalence of LTV between a group of working dogs (12.0%) and the control group (33.0%), with a similar incidence of hip dysplasia in both the groups (77.7% in group A and 77.4% in group B). Such results may be explained by the fact that, in Poland, all dogs pass physical ability tests before employment in the police. All animals that reveal abnormalities of gait or refuse to jump over the obstacle up to 1.5-m high are disqualified. Studies by Scharf et al.8 concerning only working dogs showed lower incidence of the transitional
Fig. 4. A ventrodorsal hip-extended radiograph in the dog with near-normal hip joints (CHD B) in both the joints. The femoral heads and the acetabulums are slightly incongruent, and the acetabular angles according to Norberg are approximately 1051.
than in the police working dogs. The ratio between the symmetric and asymmetric LTV was not balanced. The symmetric form constituted 68.1% of all recognized transitional vertebrae. Asymmetric types of the transverse processes were more frequent in group A. Hip dysplasia was found in 158 (77.1%) animals: 76 German shepherd dogs in group A (which constitutes 77.7% of the group) and 82 in group B (77.4% of the group). In both the groups, the degree of severity of the disease was different (Table 1). Degenerative changes in at least one sacroiliac joint were found in 175 (85.4%) German shepherd dogs. The changes were recognized in 85 police dogs (which is 85.9% of this group), of which, in 23 (27.1%) animals the changes were unilateral. Degenerative sacroiliac joint abnormalities were found in 90 dogs in group B (which is 84.9% of this group), of which, in 43 (47.8%) animals the changes were unilateral. The correlation between the method of use of German shepherd dogs and the number of sacroiliac joints affected by degenerative changes was shown (Table 2). Statistical analysis showed no statistically significant correlation between the occurrence of LTV and hip dysplasia (C, D, and E) in any of the joints (right, left, or both). A strong and statistically significant correlation between the occurrence of LTV and the most severe form of unilateral or bilateral hip dysplasia (E) is shown in Table 3. There was no correlation between the presence of symmetric or asymmetric LTV and increased risk of unilateral or bilateral hip dysplasia (Table 4). The influence of asymmetric LTV
Fig. 5. A ventrodorsal hip-extended radiograph in the dog with mild hip dysplasia (CHD C) in both the joints. The femoral heads and the acetabulums are incongruent, the acetabular angles according to Norberg are approximately 1001, and there are osteoarthritic changes at margo acetabularis cranialis and femoral necks.
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R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]] Table 1 Imaging Findings on Ventrodorsal Radiographs of Pelvis in the Working German Shepherd Dog (A) Group (n ¼ 99) and the Control (B) Group (n ¼ 106) Variable
A Group (%) B Group (%) Total
LTV 12 Symmetric type 4 Asymmetric type 8 CHD A or B* 75 CHD C* 72 CHD D* 35 CHD E* 16 Sacroiliac joint degenerative changes* 147 n
(12.0) (4.0) (8.0) (37.9) (36.4) (17.7) (8.0) (76.6)
35 28 7 75 53 58 26 137
(33.0) (26.4) (6.6) (35.4) (25) (27.3) (12.3) (64.9)
47 32 15 150 125 93 42 284
(22.9) (15.6) (7.3) (36.6) (30.5) (22.7) (10.2) (69.3)
Each joint counted separately.
Table 2 Prevalence of Morphologic Traits Reported as Number of Dogs (%) for the Working German Shepherd Dog (A) Group (n ¼ 99) and the Control (B) Group (n ¼ 106) Variable
A Group (%) B Group (%) OR (CI)
LTV CHD C, D or E† Sacroiliac joint degenerative changes†
12 (12.0) 123 (62.1) 147 (76.6)
33 (33.0) 137 (64.6) 137 (64.9)
P Value
3.57 (1.73-7.39) 0.0004* 0.9 (0.6-1.34) 0.599 1.76 (1.14-2.73) 0.0106*
OR, odds ratio. n
†
Level of significance at P o 0.05. Each joint counted separately.
Table 3 Odds Ratios (OR) for CHD Associated With LTV CHD
LTV
OR (CI)
With
Fig. 6. A ventrodorsal hip-extended radiograph in the dog with moderate dysplasia of the left joint and severe dysplasia of the right joint. In the left joint, there are obvious incongruence between femoral head and the acetabulum, acetabular angle according to Norberg more than 901, and osteoarthritic signs. In the right joint there are distinct subluxation, acetabular angle according to Norberg less than 901, flattening of the margo acetabularis cranialis, and deformation of the femoral head and neck. There are osteoarthritis changes at margo acetabularis.
vertebra (3.5%) than it was shown in the present study. Moreover, despite the fact that dogs with degenerative changes of the hip, knee, or elbow joints should be disqualified already in preliminary
Bilateral C, D or E Bilateral E C, D or E in either one hip joint or both E in either one hip joint or both C, D or E in left hip joint E in left hip joint C, D or E in right hip joint E in right hip joint n
P Value
Without
28 (59.6%) 74 (46.8%) 1.67 (0.86-3.24) 0.125 7 (14.9%) 9 (5.7%) 2.9 (1.02-8.26) 0.039* 38 (80.9%) 120 (75.9%) 1.34 (0.59-3.01) 0.483 10 (21.3%) 33 8 33 9
16 (10.1%)
2.4 (1.01-5.72) 0.044*
(70.2%) 94 (59.5%) 1.6 (0.8-3.24) 0.184 (17.0%) 11 (7.0%) 2.74 (1.03-7.28) 0.0368* (70.2%) 100 (63.3%) 1.37 (0.68-2.76) 0.3828 (19.1%) 14 (8.9%) 2.44 (0.98-6.05) 0.0498*
Level of significance at P o 0.05.
Table 4 Odds Ratios (OR) for CHD Associated With Asymmetric LTV CHD
LTV
OR (CI)
P Value
Asymmetric Symmetric Bilateral C, D or E Bilateral E C, D or E in left hip joint E in left hip joint C, D or E in right hip joint E in right hip joint
Fig. 7. Ventrodorsal projection of the lumbosacral area in the dog with the pelvic limb extended. There are sacroiliac joint degenerative changes, such as calcified dorsal and ventral sacroiliac ligaments (black arrow), sclerosis at the site of attachment of the sacroiliac ligaments at the sacral margin (white arrow), osteophytes bridging the synovial space (stars), and osteophytes on the caudal aspect of synovial sacroiliac joint (arrowhead).
11 (73.3%) 1 (6.7%) 12 (80.0%)
17 (53.1%) 6 (18.8%) 21 (65.6%)
2.43 (0.64-9.25) 0.188 3.23 (0.35-29.58) 0.278 2.1 (0.49-9.03) 0.315
1 (6.7%) 12 (80.0%)
7 (21.9%) 21 (65.6%)
3.92 (0.44-35.2) 1.08 (0.23-5.08)
0.196 0.919
3 (20.0%)
6 (18.7%)
1.08 (0.23-5.08)
0.919
radiographic examinations, dogs with mild dysplasia may be accepted.20 According to our study, lesions characteristic for mild hip dysplasia (CHD C) prevailed in the hip joints of the police working dogs, while in group B dominated moderate changes (CHD D), although the dogs from group B had lower average age.
R. Komsta et al. / Topics in Companion An Med ] (2015) ]]]–]]] Table 5 Odds Ratios (OR) for Sacroiliac Joint Degenerative Changes Associated With LTV Sacroiliac Joint Degenerative Changes
LTV With
Bilateral Left Right n
OR (CI)
P Value
Without
17 (36.2%) 94 (59.5%) 2.59 (1.32-5.09) 0.005* 28 (60.9%) 114 (72.6%) 1.7 (0.86-3.39) 0.127 26 (55.3%) 116 (75.8%) 2.53 (1.28-5.02) 0.0067*
Level of significance at P o 0.05.
Table 6 Odds Ratios (OR) for Sacroiliac Joint Degenerative Changes Associated With Asymmetric LTV Sacroiliac Joint LTV Degenerative Changes Asymmetric Symmetric
OR (CI)
Bilateral Left Right
2.92 (0.82-10.44) 0.094 2.26 (0.59-8.7) 0.228 2.00 (0.56-7.18) 0.284
8 (53.3%) 11 (73.3%) 10 (66.7%)
9 (28.1%) 17 (54.8%) 16 (46.9%)
P Value
Observations of the military working dogs11,21 did not reveal any significant differences in the length of time worked between normal and dysplastic dogs. This is probably because working dogs have professional and careful medical care. Contrary to other studies,3,14,16 our studies clearly demonstrate that symmetric LTV (15.6%) is more frequent than asymmetric LTV is (7.3%). This uneven distribution was intensified especially in the control group (Table 1). According to the Rosenberg hypothesis, it is facilitated by the presence of contact points between the pelvis and the vertebrae at the same level on both the sides during the development of the animal.22 To date, it was a disputable issue to establish the correlation between the presence of LTV and a hip joint development. Larsen6 and Wigger et al.14 did not find such a correlation. Conversely, Olsson and Kasstrom,9 and Morgan and Stevens23 suggested that the presence of LTV could affect uneven hip joint development. It is possible that our studies will help to explain the apparent lack of consistency in the results of different studies. The detailed analysis revealed the correlation between LTV and the development of the severe hip dysplasia (E), but not mild forms (C and D) (Table 1). This correlation is stronger for the bilateral severe dysplasia than in the case of the unilateral (separately right or left) severe dysplasia. This can at least in part explain the distinctly lower incidence of CHD E in working dogs when compared with companion animals (Table 1). Indication of the relation between the influence of symmetric and asymmetric form of LTV on the increased risk of bilateral or unilateral hip dysplasia requires further study. Results of our studies revealed that, in the working dogs, the risk of sacroiliac joint degenerative changes increases (Table 2). The result was consistent with the expectations of the authors. The average age of dogs in group A was higher than that of the dogs in group B. The relation between the age of dogs and the development of degenerative changes in the mentioned joints was proved by Knaus et al.17 Moreover, Breit et al.24 suggest that one of the causes of the new bone formation in the sacroiliac joint may be vigorous exercise. It is interesting that our studies revealed that the degenerative changes in the sacroiliac joints develop more often in animals with no LTV. The risk of bilateral sacroiliac joint degenerative changes is 2.5 times greater than in a group of dogs that have LTV. Asymmetric sacroiliac attachments occurring with asymmetric LTV is described quite often.2,3,16 However, the
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authors have not found any work confirming the correlation between the presence of LTV and the development of the sacroiliac joint degenerative changes. Thus, this issue needs to be further studied. The retrospective nature of the present study makes the presented study restricted. The presented research was based solely on the ventrodorsal radiograph of the pelvis. There is the possibility of overlooking some types of the transitional vertebra (symmetric type 1 LTV). As both the groups of dogs were evaluated on the same basis, the error should be comparable and should not affect the results of this work.
Conclusion Dogs with LTV have a higher frequency of CHD E. Hence, it is recommended to exclude dogs with LTV from expensive specialized trainings and from breeding. Simultaneously, our studies revealed that in the group of dogs that underwent physical agility tests, the defect is almost 3 times less frequent than in companion animals. The risk of sacroiliac joint degenerative changes is greater in dogs that do not have LTV. It is also more frequent in working dogs. References 1. Morgan JP. Congenital anomalies of the vertebral column of the dog: a study of the incidence and significance based on a radiographic and morphologic study. J Am Vet Radiol Soc 9:21–29, 1968 2. Morgan JP. Transitional lumbosacral vertebral anomaly in the dog: a radiographic study. J Small Anim Pract 40:167–172, 1999 3. Damur-Djuric N, Steffen F, Hässing M, et al. Lumbosacral transitional vertebrae in dogs: classification, prevalence, and association with sacroiliac morphology. Vet Radiol Ultrasound 47:32–38, 2006 4. Morgan JP, Bahr A, Franti CE, et al. Lumbosacral transitional vertebrae as a predisposing cause of cauda equine syndrome in German shepherd dogs: 161 cases (1987–1990). J Am Vet Med Assoc 202:1877–1882, 1993 5. Steffen F, Berger M, Morgan JP. Asymmetrical, transitional, lumbosacral vertebral segments in six dogs: a characteristic spinal syndrome. J Am Anim Hosp Assoc 40:338–344, 2004 6. Larsen JS. Lumbosacral transitional vertebrae in the dog. J Am Vet Radiol Soc 18:76–79, 1977 7. Graeme SA. Radiographic signs of joint disease in dogs and cats. In: Thrall DE, editor. Textbook of Veterinary Diagnostic Radiology. 5th ed. Philadelphia, PA: W. Elsevier Saunders; 2007. p. 317–358 8. Scharf G, Steffen F, Grünenfelder F, et al. The lumbosacral junction in working German shepherd dogs—neurological and radiological evaluation. J Vet Med A 51:27–32, 2004 9. Olsson SE, Kasstrom H: Etiology and pathogenesis of canine hip dysplasia. Proceedings on Canine Hip Dysplasia Symposium and Workshop. St. Luis, MO: Orthopedic Foundation of Animals; 24, 1972 10. Coopman F, Verhoeven G, Saunders J, Duchateau L, Van Bree H. Prevalence of hip dysplasia, elbow dysplasia and humeral head osteochondrosis in dog breeds in Belgium. Vet Rec 29:654–658, 2008 11. Zorko B, Ivanuša T, Pelc R. Progression of hip dysplasia in 40 police working dogs: a retrospective study. Slovenian Vet Res 42:71–76, 2005 12. Smith GK, Mayhew PD, Kapatkin AS, McKelvie PJ, Shofer FS, Gregor TP. Evaluation of risk factors for degenerative joint disease associated with hip dysplasia in German Shepherd Dogs, Golden Retrievers, Labrador Retrievers and Rottweilers. J Am Vet Med Assoc 219:1719–1724, 2001 13. Breit S, Knaus I, Künzel W. Differentiation between lumbosacral Transitional Vertebrae, Pseudolumbarisation, and lumbosacral osteophyte formation in ventrodorsal radiographs of the canine pelvis. Vet J 165:36–42, 2003 14. Wigger A, Julier-Franz C, Telhelm B, et al. Lumbosacral transitional vertebrae in the German shepherd dog: prevalence, classification, genetics, and association with canine hip dysplasia. Tierärztliche Praxis. Ausgabe Kleintiere Heimtiere 37:7–13, 2009 15. Lappalainen AK, Salomaa R, Junnila J, et al. Alternative classification and screening protocol for transitional lumbosacral vertebra in German shepherd dogs. Acta Vet Scand 54:1–10, 2012 16. Flückiger MA, Damur-Djuric N, Hässing M, et al. A lumbosacral transitional vertebra in the dog predisposes to cauda equine syndrome. Vet Radiol Ultrasound 47:39–44, 2006 17. Knaus I, Brett S, Künzel W, Mayrhofer E. Appearance and incidence of sacroiliac joint disease in ventrodorsal radiographs of canine pelvis. Vet Radiol Ultrasound 45:1–9, 2004
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18. Federation Cynologique Internationale (AIBL). Radiographic Procedure for Hip Dysplasia Evaluation. www.fci.be/circularizes/46-2009-annex2-eu.pdf 19. Ondreka N, Amort KH, Stock KF, et al. Skeletal morphology and morphometry of the lumbosacral junction in German shepherd dogs and an evaluation of the possible genetic basis for radiographic findings. Vet J 196: 64–70, 2013 20. Moore GE, Burkman KD, Carter MN, et al. Causes of death or reasons for euthanasia in police working dogs: 927 cases (1993–1996). J Am Vet Med Assoc 219:209–214, 2001
21. Banfield CM, Bartles JE, Huson JA, et al. A retrospective study of canine hip dysplasia in 116 police working dogs. Part II: clinical signs and performance data. J Am Anim Hosp Assoc 32:423–430, 1996 22. Rosenberg E. Bemerkungen über den Modus des Zustandekommens der Regionen an der Wirbesäule des Menschen. Morph Jahrb 36:609–659, 1907 23. Morgan JP, Stevens M. Radiographic diagnosis and control of canine hip dysplasia. Ames, IA: Iowa State University Press; 1985 24. Breit S, Knaus I, Künzel W. The gross and radiographic appearance of sacroiliac ankylosis capsularis ossea in the dog. Res Vet Sci 74:85–92, 2003