Intervertebral disk disease is one of the most common neurologic disorders in dogs,1 with approximately 15% of all dogs with IVDH having cervical IVDH.1–3 The predominant clinical signs in dogs with cervical IVDH are neck pain, root signature (ie, referred pain causing lameness), tetraparesis, and tetraplegia. Clinical signs depend on the location of the degenerative lesion and the severity and direction of compression.
Various studies have investigated epidemiological factors potentially associated with the occurrence of cervical IVDH, including age, trauma, nutrition, and genetics, and several investigators have suggested that the incidence of cervical IVDH varies according to dog breed. In particular, studies4–6 have suggested that small-breed dogs and dogs of chondrodystrophoid breeds tend to be the most commonly affected. The C2–3 disk is reportedly the most commonly affected site, with more caudal cervical disks less frequently affected.2,7 However, dogs of nonchondrodystrophoid medium or large breeds reportedly tend to more often have herniation of caudal cervical disks.8
Although multiple reports of cervical IVDH in dogs have been published, little information is available on variations in affected disk spaces among dog breeds or on breed differences related to age of onset, duration or severity of neurologic signs, or recovery time. Therefore, the purpose of the study reported here was to identify characteristics of chondrodystrophoid and nonchondrodystrophoid small-breed dogs with cervical IVDH. The authors have previously reported on IVDH in dogs,9 and the database used in that study was also used in the present study.
Materials and Methods
Case selection criteria—Medical records of the Nippon Veterinary Life Science University were reviewed to identify small-breed dogs (ie, dogs weighing ≤ 15 kg [33 lb]) examined between April 1993 and April 2013 because of cervical IVDH. Dogs were included in the study if cervical IVDH had been diagnosed on the basis of clinical signs and results of myelography, CT, a,b or MRIc,d and if the diagnosis had been confirmed at the time of surgery.
Medical records review—Information obtained from medical records of dogs included in the study consisted of breed, sex, neuter status, age and body weight at the time of surgery, number and location of affected intervertebral disks, duration and severity of neurologic signs, and recovery time. Location of affected intervertebral disks was determined by means of myelography, CT, or MRI and was confirmed at the time of surgery.
Myelography was performed with iohexol (240 or 300 mg of I/mL) injected at the L5–6 space or cisterna magnum. For both myelography and CT, affected disks were identified on the basis of compression of the spinal cord. For MRI, sagittal T2-weighted images were used to identify the affected disks. When dynamic spinal cord compression was suspected on MRI, affected sites were confirmed by means of myelography.
Severity of neurologic signs was graded on a scale from 1 to 3,10 where grade 1 was defined as signs of neck pain with normal ambulation, grade 2 was defined as ambulatory tetraparesis with or without signs of neck pain, and grade 3 was defined as nonambulatory tetraparesis. Duration of neurologic signs was defined as the time from the onset of clinical signs to surgery. Recovery time was defined as the time from surgery to maximum improvement after surgery.
Data analysis—To compare chondrodystrophoid and nonchondrodystrophoid breeds, 7 dog breeds (Beagle, Dachshund, Shih Tzu, Pekingese, English Bulldog, French Bulldog, and American Cocker Spaniel) were categorized as chondrodystrophoid breeds and other breeds were categorized as nonchondrodystrophoid breeds.11 Only breeds represented by ≥ 6 dogs were included in the analyses.
Statistical analysis—Associations between breed and age at the time of surgery were examined by means of ANOVA followed by the Tukey-Kramer test (parametric methods). Associations between breed and number of affected disks, severity of neurologic signs, duration of neurologic signs, and recovery time were examined by means of the Kruskal-Wallis test (nonparametric methods). Statistical analyses were performed with standard software.e For all tests, values of P < 0.05 were considered significant.
Results
One hundred eighty-seven dogs met the criteria for inclusion in the study. Of the 187 dogs, 108 (57.8%) were male (82 sexually intact and 26 castrated), and 79 (42.2%) were female (38 sexually intact and 41 spayed; Table 1). Mean ± SD age at the time of surgery was 8.1 ± 2.7 years (range, 1.0 to 16.0 years). Mean weight at the time of surgery was 7.5 ± 3.4 kg (16.5 ± 7.5 lb; range, 1.5 to 15.0 kg [3.3 to 33 lb]). Sixty-two (33.2%) dogs had grade 1 neurologic signs, 80 (42.8%) had grade 2 neurologic signs, and 45 (24.1%) had grade 3 neurologic signs. Median time from onset of clinical signs to surgery (ie, duration of neurologic signs) was 32.5 days (range, 2 to 306; n = 174 dogs), and median time from surgery to maximum improvement after surgery (ie, recovery time) was 14 days (range, 1 to 180; 137 dogs). Three dogs (2 Beagles and 1 Yorkshire Terrier) required a second surgical procedure because of continued spinal cord compression at the same site. Five dogs (1 Beagle, 1 Dachshund, and 3 Shih Tzus) required a second surgical procedure because of cervical IVDH involving other sites.
Characteristics of small-breed (≤ 15 kg [33 lb]) dogs (n = 187) that underwent surgery for treatment of cervical IVDH.
| Neurologic grade | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Breed | No. of dogs (%) | Age at surgery (y) | Body weight (kg) | No. of males | No. of females | 1 | 2 | 3 | Duration of signs (d)* | Recovery time (d)† |
| Chondrodystrophoid breeds | 133 (71.1) | 8.1 ± 2.7 | 8.4 ± 3.1 | 73 | 60 | 48 | 53 | 32 | 42.4 ± 34.9 | 18.6 ± 18.8 |
| Beagle | 55 (29.4) | 8.1 ± 2.9 | 11.0 ± 2.2 | 28 | 27 | 27 | 18 | 10 | 43.2 ± 31.7 | 16.5 ± 17.1 |
| Dachshund | 35 (18.7) | 8.0 ± 2.0 | 6.2 ± 1.9 | 19 | 16 | 13 | 13 | 9 | 37.6 ± 37.2 | 21.2 ± 24.6 |
| Shih Tzu | 29 (15.5) | 9.6 ± 2.3 | 6.1 ± 1.3 | 15 | 14 | 5 | 15 | 9 | 42.7 ± 29.8 | 17.8 ± 14.5 |
| Pekingese | 7 (3.7) | 6.1 ± 2.9 | 5.4 ± 0.8 | 6 | 1 | 0 | 4 | 3 | 74.9 ± 59.6 | 30.2 ± 18.1 |
| French Bulldog | 5 (2.7) | 4.5 ± 2.0 | 11.0 ± 1.6 | 4 | 1 | 2 | 2 | 1 | 23.3 ± 13.3 | 21.5 ± 16.3 |
| American Cocker Spaniel | 2 (1.1) | 4.8 ± 0.2 | 10.3 ± 2.0 | 1 | 1 | 1 | 1 | 0 | 21.5 ± 12.0 | 2.5 ± 2.1 |
| Nonchondrodystrophoid breeds‡ | 54 (28.9) | 8.0 ± 2.6 | 5.3 ± 3.1 | 35 | 19 | 14 | 27 | 13 | 63.5 ± 70.0 | 26.8 ± 31.2 |
| Yorkshire Terrier | 12 (6.4) | 9.5 ± 2.3 | 3.4 ± 1.2 | 6 | 6 | 2 | 8 | 2 | 128.9 ± 108.7 | 36.7 ± 13.0 |
| Pomeranian | 10 (5.3) | 6.2 ± 2.5 | 3.1 ± 0.7 | 5 | 5 | 6 | 3 | 1 | 46.1 ± 29.0 | 22.3 ± 18.6 |
| Chihuahua | 8 (4.3) | 8.1 ± 2.5 | 3.6 ± 1.2 | 6 | 2 | 1 | 5 | 2 | 46.4 ± 39.9 | 12.2 ± 7.2 |
| Pug | 5 (2.7) | 9.0 ± 1.5 | 8.3 ± 0.7 | 4 | 1 | 0 | 2 | 3 | 49.4 ± 31.2 | 9.3 ± 6.2 |
| Toy Poodle | 4 (2.1) | 5.8 ± 2.4 | 5.3 ± 2.0 | 3 | 1 | 0 | 2 | 2 | 20.7 ± 18.4 | 30.0 ± 36.8 |
| Shiba Inu | 3 (1.6) | 10.0 ± 2.0 | 12.0 ± 1.1 | 2 | 1 | 2 | 1 | 0 | 25.0 ± 8.2 | 6.0 |
| Maltese Terrier | 3 (1.6) | 7.8 ± 1.4 | 4.1 ± 0.5 | 3 | 0 | 0 | 1 | 2 | 17.0 ± 15.6 | 30.7 ± 11.8 |
| Miniature Pinscher | 2 (1.1) | 6.3 ± 2.5 | 4.3 ± 1.8 | 1 | 1 | 1 | 1 | 0 | 39.0 ± 29.7 | 8.0 |
| Shetland Sheepdog | 2 (1.1) | 9.5 ± 6.4 | 12.3 ± 3.3 | 1 | 1 | 0 | 2 | 0 | 35.5 ± 29.0 | 21.0 |
| All breeds | 187 (100) | 8.1 ± 2.7 | 7.5 ± 3.4 | 108 | 79 | 62 | 80 | 45 | 48.4 ± 48.2 | 20.7 ± 22.8 |
Data are given as mean ± SD or number of dogs. For neurologic grade, grade 1 was defined as signs of neck pain with normal ambulation, grade 2 was defined as ambulatory tetraparesis with or without signs of neck pain, and grade 3 was defined as nonambulatory tetraparesis.
Defined as the time from the onset of clinical signs to surgery; data were available for 174 dogs.
Defined as the time from surgery to maximum improvement after surgery; data were available for 137 dogs.
Includes 5 additional breeds represented by 1 dog each.
Of the 187 dogs, 133 (71.1%) represented 6 chondrodystrophoid breeds, and 54 (28.9%) represented 14 nonchondrodystrophoid breeds. Beagles were the most common (n = 55 [29.4%]), followed by Dachshunds (35 [18.7%]), Shih Tzus (29 [15.5%]), Yorkshire Terriers (12 [6.4%]), Pomeranians (10 [5.3%]), Chihuahuas (8 [4.3%]), and Pekingese (7 [3.7%]). Mean age at the time of surgery was not significantly (P = 0.867) different between chondrodystrophoid and nonchondrodystrophoid breeds. However, mean number of affected disks was significantly (P < 0.001) higher and mean recovery time was significantly (P = 0.037) longer in nonchondrodystrophoid than in chondrodystrophoid breeds.
A total of 253 disks were affected in the 187 dogs (Table 2). Mean ± SD number of affected disks was 1.4 ± 0.6. The most commonly affected disk was C2–3 (n = 81 [32.0%]), followed by C3–4 (40 [15.8%]), C4–5 (58 [22.9%]), C5–6 (46 [18.2%]), and C6–7 (28 [11.1%]).
Distribution of affected disks for the dogs in Table 1.
| No. (%) of affected disks | |||||||
|---|---|---|---|---|---|---|---|
| Breed | No. of dogs | C2–3 | C3–4 | C4–5 | C5–6 | C6–7 | No. of affected disks/dog* |
| Chondrodystrophoid breeds | 133 | 64 (39.3) | 24 (14.7) | 35 (21.5) | 25 (15.3) | 15 (9.2) | 1.2 ± 0.5 |
| Beagle | 55 | 29 (43.9) | 11 (16.7) | 11 (16.7) | 9 (13.6) | 6 (9.1) | 1.2 ± 0.4 |
| Dachshund | 35 | 13 (35.1) | 5 (13.5) | 9 (24.3) | 7 (18.9) | 3 (8.1) | 1.1 ± 0.3 |
| Shih Tzu | 29 | 16 (39.0) | 4 (9.8) | 10 (24.4) | 6 (14.6) | 5 (12.2) | 1.4 ± 0.6 |
| Pekingese | 7 | 3 (30.0) | 1 (10.0) | 3 (30.0) | 2 (20.0) | 1 (10.0) | 1.4 ± 0.8 |
| Nonchondrodystrophoid breeds | 54 | 17 (18.9) | 16 (17.8) | 23 (25.6) | 21 (23.3) | 13 (14.4) | 1.7 ± 0.8 |
| Yorkshire Terrier | 12 | 2 (8.3) | 3 (12.5) | 6 (25.0) | 7 (29.2) | 6 (25.0) | 2.0 ± 0.9 |
| Pomeranian | 10 | 3 (16.7) | 5 (27.8) | 7 (38.9) | 3 (16.7) | 0 (0) | 1.8 ± 1.0 |
| Chihuahua | 8 | 1 (7.7) | 1 (7.7) | 2 (15.4) | 5 (38.5) | 4 (30.8) | 1.6 ± 0.7 |
| All breeds | 187 | 81 (32.0) | 40 (15.8) | 58 (22.9) | 46 (18.2) | 28 (11.1) | 1.4 ± 0.6 |
Data are given as mean ± SD.
The most frequently affected disk was C2–3 in Beagles (29/66 [43.9%] affected disks), Dachshunds (13/37 [35.1%]), Shih Tzus (16/41 [39.0%]), and Pekingese (3/10 [30.0%]), but not in Yorkshire Terriers (2/24 [8.3%]), Pomeranians (3/18 [16.7%]), and Chihuahuas (1/13 [7.7%]). A total of 163 disks were affected in dogs of chondrodystrophoid breeds. The most frequently affected disk was C2–3 (64/163 [39.3%]), followed by C4–5 (35 [21.5%]), C5–6 (25 [15.3%]), C3–4 (24 [14.7%]), and C6–7 (15 [9.2%]). In dogs of nonchondrodystrophoid breeds, the most frequently affected disk was C4–5 (23 [25.6%]), followed by C5–6 (21 [23.3%]), C2–3 (17/90 [18.9%]), C3–4 (16 [17.8%]), and C6–7 (13 [14.4%]).
The 7 breeds represented by ≥ 6 dogs (ie, Beagle, Dachshund, Shih Tzu, Yorkshire Terrier, Pomeranian, Chihuahua, and Pekingese) were compared on the basis of age at the time of surgery, number of affected disks, severity of neurologic signs, duration of neurologic signs, and recovery time, and significant differences among breeds were found for age at the time of surgery, number of affected disks, and recovery time. Shih Tzus (P = 0.006) and Yorkshire Terriers (P = 0.047) were significantly older than Pomeranians, and Shih Tzus were significantly (P = 0.022) older than Pekingese, but other significant differences between breeds were not identified. Mean number of affected disks was significantly (P < 0.001) higher in Yorkshire Terriers than in Dachshunds, but other significant differences between breeds were not identified. Mean recovery time was significantly longer in Yorkshire Terriers (n = 9) than in Beagles (42; P = 0.015) or Shih Tzus (24; P = 0.023), but other significant differences between breeds were not identified.
Mean recovery time was significantly (P = 0.047) longer for dogs with 3 affected disks (32.9 ± 10.5 days; n = 9) than for dogs with only 1 affected disk (17.9 ± 18.4 days; 100). Mean recovery time for dogs with 2 affected disks (21.0 ± 18.2 days; n = 27) did not differ significantly from times for dogs with 3 affected disks or only 1 affected disk.
Discussion
Results of the present study suggested that there may be breed-specific differences in the characteristics of cervical IVDH in small-breed dogs. Specifically, mean number of affected disks was significantly higher and mean recovery time was significantly longer in dogs of nonchondrodystrophoid breeds than in dogs of chondrodystrophoid breeds. Also, when dogs of the most commonly represented breeds were considered, significant differences among breeds were found in regard to age at the time of surgery, number of affected disks, and recovery time.
Beagle (55/187 [29.4%]) was the most commonly affected of 20 chondrodystrophoid and nonchondrodystrophoid breeds in the present study, followed by Dachshund (35 [18.7%]), Shih Tzu (29 [15.5%]), Yorkshire Terrier (12 [6.4%]), Pomeranian (10 [5.3%]), Chihuahua (8 [4.3%]), and Pekingese (7 [3.7%]). However, breed distribution was not compared with overall breed distribution for the study period. Therefore, our results do not allow us to conclude whether these breeds were particularly prone to cervical IVDH or were more commonly represented simply because they were popular breeds. Previous studies12,13 have found Dachshund to be the most commonly affected breed, but at least 1 other study5 has suggested that Beagles are more commonly affected.
In the present study, C2–3 was the most commonly affected disk (81/253 [32.0%]), and C2–3 and C3–4 accounted for approximately half of the affected disks (121/253 [47.8%]). Reportedly, the cranial cervical disks are more frequently affected in small-breed dogs.8,14 In contrast, C5–6 and C6–7 represented 46 (18.2%) and 28 (11.1%) of the affected disks, respectively, which was consistent with previous reports2,7 that prevalence of cervical disk herniation decreases as one moves caudally.
There were more than twice as many dogs of chondrodystrophoid breeds (133/187 [71.1%]) as nonchondrodystrophoid breeds (54/187 [28.9%]) in the present study. According to previous reports, intervertebral disk degeneration occurs earlier and faster in dogs of chondrodystrophoid breeds than in dogs of nonchondrodystrophoid breeds,11 and the cervical intervertebral disk morphology differs between chondrodystrophoid and nonchondrodystrophoid breeds.15 In addition, C2–3 accounted for 64 of the 163 (39.3%) affected disks in dogs of chondrodystrophoid breeds, but only 17 of the 90 (18.9%) affected disks in dogs of nonchondrodystrophoid breeds. To our knowledge, no previous studies have shown that the C2–3 disk is more frequently affected in dogs of chondrodystrophoid breeds than in dogs of nonchondrodystrophoid breeds.
In the present study, caudal cervical disks (ie, C5–6 or C6–7) were more frequently affected in Yorkshire Terriers (13/24 [54.2%]) and Chihuahuas (9/13 [69.2%]) than were more cranial cervical disks. A previous study8 found that nonchondrodystrophoid medium to large breeds were more likely to be affected in the caudal cervical region; however, to our knowledge, there are no studies investigating nonchondrodystrophoid small-breed dogs. In the present study, the caudal cervical disks accounted for 34 of the 90 (37.8%) affected disks in dogs of nonchondrodystrophoid breeds and 40 of the 163 (24.6%) affected disks in dogs of chondrodystrophoid breeds. These findings suggested that nonchondrodystrophoid small-breed dogs are more frequently affected in the caudal cervical region. However, because dogs of these breeds accounted for only a limited number of cases, this relationship remains controversial and should be reexamined as additional cases accumulate.
When data for the 7 breeds represented by ≥ 6 dogs were analyzed, there were significant differences among breeds in regard to age at the time of surgery, number of affected disks, and recovery time. Specifically, Shih Tzus and Yorkshire Terriers were significantly older than Pomeranians, and Shih Tzus were significantly older than Pekingese. Generally, the mean age at diagnosis in dogs with cervical IVDH is reported to be 6 to 8 years,3,6–8 but mean age for both Shih Tzus and Yorkshire Terriers in the present study was > 9 years, suggesting dogs of these breeds may be prone to developing cervical IVDH at an older age. Reportedly, there is a difference between chondrodystrophoid and nonchondrodystrophoid breeds in regard to peak age of occurrence because chondrodystrophoid breeds differ from nonchondrodystrophoid breeds in the mechanism of intervertebral disk degeneration.5 In the present study, Yorkshire Terriers were classified as a nonchondrodystrophoid breed, but Shih Tzus were classified as a chondrodystrophoid breed. Taken together, our findings seem to have suggested that variations in the mechanism of intervertebral disk degeneration are not always associated with variations in age of development of clinical signs.
Mean number of affected disks per dog was significantly higher in nonchondrodystrophoid breeds than in chondrodystrophoid breeds in the present study, and mean number of affected disks per dog was significantly higher in Yorkshire Terriers than in Dachshunds.
Finally, mean recovery time was more than twice as long in Yorkshire Terriers as it was in Beagles, Shih Tzus, and Chihuahuas in the present study. Because Yorkshire Terriers were more likely to have multiple affected disks, several lesions needed to be treated simultaneously, which may have influenced recovery time. In general, recovery time increased as the number of affected disks increased, with mean recovery time for dogs with 3 affected disks significantly longer than recovery time for dogs with only 1 affected disk. Further, it has been reported that IVDH in the caudal cervical region is associated with a worse prognosis than IVDH in the cranial cervical region.14 Yorkshire Terriers were more likely to have caudal cervical disks affected than cranial cervical disks, which may have influenced recovery time.
ABBREVIATIONS
| IVDH | Intervertebral disk herniation |
Asteion-TSX-021B, Toshiba Medical Systems, Tochgi, Japan.
Aquilion PRIME, Toshiba Medical Systems, Tochgi, Japan.
Visart, Toshiba Medical Systems, Tochgi, Japan.
Signa EXCITE 3.0 T, GE Healthcare Japan, Tokyo, Japan.
SPSS for Windows, version 16.0, SPSS Inc, Chicago, Ill.
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