J. Vet. Med.

A 47, 283296 (2000) 2000 Blackwell Wissenschafts-Verlag, Berlin ISSN 0931184X

Department of Clinical Studies and Department of Animal Science and Animal Health, Royal Veterinary and Agricultural University, Copenhagen, Denmark

Mechanical Factors affecting the Occurrence of Intervertebral Disc Calcication in the Dachshund a Population Study
V. F. JENSEN1 and A. K. ERSBO LL2
Addresses of authors: 1Department of Clinical Studies and 2Department of Animal Science and Animal Health, Royal Veterinary and Agricultural University, Copenhagen, Denmark With 4 gures and 5 tables (Received for publication November 26, 1999)

Summary
In a population sample comprising 48 standard wirehaired dachshunds, the occurrence of intervertebral disc calcication was determined by plain spinal radiography. Body dimensions of the dogs were measured and information obtained from owners about exercise patterns, including stair climbing, and the relation of these variables to the number of calcied discs was analysed by logistic regression. In the Danish population of wirehaired dachshunds, the prevalence of disc calcication was estimated at 77 %. The spinal distribution of calcied discs is similar amongst different populations, while the prevalence varies signicantly. Most types of exercise included in the variable duration of exercise as well as moderate stair climbing seemed to reduce the rate of occurrence of disc calcication. The effects of moderate stair climbing (OR = 0.34) and duration of exercise (OR = 0.52) were statistically signicant and the effects appear to be additive. Running next to a bicycle was the only type of exercise with a positive association with the number of calcied discs. This was, however, not signicant. Effects of body conformation, including absolute and relative body measurements, were not found.

Introduction Herniation of intervertebral discs occurs in most breeds of dog, but a high incidence and a high relative risk are found in some hypochondroplastic (formerly chondrodystrophoid; Simpson, 1992) breeds characterized by rhizomelic dwarsm, for example dachshunds, Pekinese and French bulldog (Gage, 1975; Goggin et al., 1970; Priester, 1976). The relative risk is about 1012 times higher in the dachshund than in all other breeds (Goggin et al., 1970; Priester, 1976). Disc herniation in the hypochondroplastic breeds is generally accepted as being associated with a specic type of early disc degeneration. The degeneration is preceded by an early chondroid metaplasia macroscopically visible from 3 to 4 months of age. The degenerative changes are visible before 1 year of age and necrosis and dystrophic calcication appear in severely affected discs (Hansen, 1952; Hoerlein, 1978). Intervertebral disc calcication (IDC) is of particular interest as a crude indicator of severe disc degeneration as it can be demonstrated radiographically. Further, dogs with several calcied discs seem to be at particularly high risk of developing disc herniation, while herniation rarely occurs in dachshunds without IDC (Havranek-Balzaretti, 1980; Stigen, 1996). The incidence of disc herniation and IDC in the dachshund varies signicantly amongst the different hair coat varieties as well as amongst breeding lines, indicating some degree of genetic transmission (Funkquist and Henricson, 1969; Ball et al., 1982; Stigen, 1991). The occurrence of IDC in the offspring is signicantly correlated to its occurrence in both parents, which supports the hypothesis of a heritable component in the occurrence of the disease
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(Havranek-Balzaretti, 1980). However, the transmission pattern of IDC and disc herniation seems to be multifactorial (Ball et al., 1982; Stigen and Christensen, 1993) and an effect of unidentied environmental factors has been demonstrated (Stigen and Christensen, 1993). Several studies have described the biochemical and histological changes occurring in the degenerating disc of hypochondroplastic dogs, but the mechanisms responsible for the degenerative process are unknown (Cole et al., 1985a, 1985b, 1987; Ghosh, 1990; Ghosh et al., 1992). However, studies of degenerative processes in human and canine discs have identied a number of factors, including mechanical loading (Holm and Urban, 1987; Mirza and White, 1995; Buckwalter, 1995). Mechanical loading may inuence the nutrition of the disc and the composition of cartilage by numerous mechanisms, as follows. , A direct metabolic chondrocyte response to compressive or tensile forces initiates tissue remodelling with subsequent changes in the distribution of collagen types and the production of proteoglycan (PG) (Brichley-Parsons and Glimcher, 1984; Lipiello et al., 1985; Larsson et al., 1991; Parkkinen et al., 1993; Buschmann and Hunziker, 1995; Ohshima et al., 1995; Kim et al., 1995; Ishihara et al., 1996; Hutton et al., 1999). , Increased disc loading may increase the rate and severity of changes in the intervertebral disc indirectly by altering the diffusion of nutrients and metabolic waste (Andersson, 1993). Sustained load bearing (increased hydrostatic pressure) causes a constant ux of water from the disc and the subsequent dehydration may interfere with diffusion, thereby compromising cell nutrition and metabolism, particularly under prolonged external stress (Terahata et al., 1994; Buckwalter, 1995; McMillan et al., 1996). , Diffusion depends both on the osmotic pressure and the hydraulic permeability coefcient, both of which are largely determined by the PG content (Mankin and Lipiello, 1971; Urban and McMullin, 1988; Ishihara et al., 1997). Conversely, hydration (uid content and extracellular osmolality) inuences the synthesis of PG. Dehydration (as in the degenerated disc) compromises the diffusion of nutrients and metabolic waste, inuencing cell metabolism and pH. The declining pH further compromises cell metabolism and biosynthesis, and eventually causes necrosis (Ohshima and Urban, 1992; Buckwalter, 1995). , Alterations in the matrix, especially decreased hydration, affect stress distribution inside the vertebral disc. Stress concentration may lead to further alterations in chondrocyte metabolism (Adams et al., 1996a; Umehara et al., 1996). Experimental studies of the canine disc have demonstrated biochemical effects of different mechanical loads, including the effects of exercise and vertebral fusion; the latter causes diminished load on the fused segment and increased loading on the parafusion discs (Weinhoffer et al., 1995). The biochemical changes are age-dependent (Vasan et al., 1991) and discs in the hypochondroplastic breeds respond differently from those in non-hypochondroplastic breeds (Cole et al., 1987). In adult Labradors, which are non-hypochondroplastic dogs, daily moderate or violent exercise for extended periods (30 min/day for 3 months) had a benecial effect on the disc, increasing solute transport and metabolic rate (Holm and Nachemson, 1983). Accordingly, slightly increased metabolism was seen in parafusion discs while metabolism decreased in discs between the fused segments (Holm and Nachemson, 1982). In greyhounds, which are also nonhypochondroplastic, a decrease in catabolism of PG (diminished turnover) was demonstrated in the parafusion discs (Cole et al., 1987). In contrast with these ndings, spinal fusion in adult hypochondroplastic dogs caused disaggregation with loss of PGs both in the discs beneath the fusion and in the parafusion discs, followed at a later stage by evidence of stimulated biosynthesis of PG (Cole et al., 1985a). Cole et al. (1987) suggested that the difference in the response of the discs in hypochondroplastic and non-hypochondroplastic breeds is related to a difference in the matrix and cell type. In the nucleus pulposus (NP) of the beagle, a hypochondroplastic breed, chondrocyte-like cells are embedded in a hyalinized matrix, and these cells seem to become nutritionally compromised more easily than the notochordal cells embedded in the highly hydrated PG-rich gel of the non-hypochondroplastic disc in greyhounds (Cole et al., 1987). The hydromechanical size of PG is correlated to the xed charge density (i.e. composition) of the glycosaminoglycan (GAG) population, one of the major components of PG.

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The hydromechanical size of PG is greater in the greyhound disc than in the beagle disc (Ghosh et al., 1992). In relation to degeneration of the disc, a decrease in the xed charge density of the GAG occurs, with a subsequent decrease in hydrostatic pressure (dehydration). As diffusion depends on hydration, nutrition may readily be compromised in the degenerating disc (Urban and Maroudas, 1980; Cole et al., 1985a). Additionally, the cells of the chondrodystrophoid disc seem to be less metabolically adaptable to lower nutritional levels (Cole et al., 1987). In conclusion, the abnormal disc of the hypochondroplastic dog may be more sensitive to mechanical stress, and loading may indirectly accelerate the degenerative process. It appears that environmental factors imposing different mechanical loadings on the discs may either have a benecial effect or accelerate the degeneration process of the intervertebral discs in hypochondroplastic breeds. The objective of this study was to estimate the occurrence and distribution of IDC in the Danish population of wirehaired dachshunds and evaluate the signicance of a number of mechanical factors acting on the spine under eld conditions. In the present study, exercise pattern and body conformation were included as factors affecting the loading applied to the vertebral column. Material and Methods
Sampling The population study was conned to standard wirehaired dachshunds. A lower age limit of 2 years was dened because the number of calcied discs in the individual dog may increase considerably up to around 24 months of age (Jensen and Arnbjerg, 2000). As the vast majority of disc herniation in the dachshunds occurs at the age of 47 years (Hansen, 1952; Priester, 1976), an upper age limit of 4 years (49 months) was dened to avoid bias due to owners being more inclined to participate with dogs showing signs of spinal disease (e.g. pain or lameness). Dogs bred outside Denmark are represented in many of the pedigrees of the Danish dachshund population due to importation of dogs and breeding with populations in other Scandinavian countries and, in particular, Germany. To make the sample representative of the Danish population, litters with four Danish grandparents were preferred, but it was decided to allow a maximum of two foreign-registered grandparents in the individual pedigree. Breeding is dominated by a few sires, each producing offspring in the hundreds, constituting a large percentage of the population (Danish Kennel Club, personal communication). Consequently, there is a high risk of overrepresentation of a few ancestors in a convenience sample or even in a random sample. To obtain a minimum of kinship within the sample, it was decided to select the dogs by multistage sampling based on the criteria listed in Table 1. Due to selection criterion 4 (coefcient of kinship 1/16), the sample represents the genetic pool of the dogs used for breeding in the grandparents generation and, consequently, the genetic pool of the parental generation. Sampling was initiated by the inclusion of six unrelated, clinically healthy standard dachshunds aged 2 to 4 years, obtained by advertising. Subsequently, pedigrees of all registered litters at the relevant age, i.e. 383 litters born during the period of January 1994 to April 1996, were reviewed systematically (Danish Kennel Club, personal communication) and litters fullling the criteria were selected. Based on the owners postal number, one dog was selected from each litter. This selection is considered random as regards within-litter factors (genetic factors and environmental litter effects).

Table 1. Inclusion criteria for the population sample 1. 2. 3. 4. Wirehaired dachshunds, aged 2429 months. Registered with the Danish Kennel Club (DKK). Both parents and at least two grandparents should be registered with the DKK. (a) The coefcient of relationship between individuals should be 1/16. An ancestor should appear as grandparent no more than twice in the sample. (b) Exceptions from (a) were allowed when ancestors were used intensively* for breeding. These animals were allowed to appear in the pedigree 3 times as grandparents or once as parent and once as grandparent.

*Fatherhood of 15 litters or more; motherhood (one case) of more than ve litters or grandparenthood of more than 50 litters.

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Positive contact was made with the owners of 46 dogs out of a total of 50 dogs (50 litters) meeting the criteria. An additional two dogs aged 52 and 55 months but otherwise meeting the selection criteria were included to increase the sample size. All dogs (n = 48) were clinically healthy at presentation and none of them had previously been treated for spinal problems. Radiography The dogs were placed in right lateral recumbency and at least ve lateral radiographs of each dog were made, covering the vertebral column from the axis to the sacral bone (C2S2). Additional radiographs were made until all the intervertebral discs were visualized (Dennis, 1987). A Polydores XL 50 X-ray machine with Bucky-movable grid (Siemens A/S, Copenhagen, Denmark), 3M Trimax T16 intensifying screens (3M, Ferrania, Italy) and Fuji Super HR-L30 lm (Fuji Photo Film Co., Tokyo, Japan) were used (exposure: 5560 kV, 916mAs; lm focus distance: 1 m). The location of calcied discs was recorded according to the position in the cervical (C1T1), thoracic (T1L1) and lumbar (L1S1) regions. Every set of radiographs was evaluated twice, independently, at at least a 2-month interval. If differences were found, the discs in question were re-evaluated for a nal diagnosis. Environmental factors Information pertaining to exercise pattern was obtained through questionnaires, with additional interviews to complete or clarify the answers. Information on type and duration of exercise was obtained and information on climbing of staircases was included explicitly. The individual dog was assigned to one category (class) for each variable listed in Table 2. The duration of daily exercise was estimated, including the duration of free range activity in the yard (Table 2).

Table 2. Denition of variables for description of exercise patterns Variable (type of exercise) Activity in yard Class Denition a b c Hunting Active a b a b Bicycle Duration of exercise (min/day) Stair climbing a b a b Highly active in a yard most of the day with free range activities such as playing with other dogs, hunting birds, etc. ( 150 min exercise). Access to free range activity in a yard all day but not particularly active, or high activity (cf. class a) within a limited daily period (outside working hours) ( 90 min activity). Access to free range activity in a yard within a limited daily period (hours) but not very active ( 45 min activity), or no access to free range activity in a yard. Used for hunting. Not used for hunting. Highly active most of the day in a yard and/or used as hunting dog. Not highly active in a yard or free range activity within a limited daily period ( 90 min activity/day); not used for hunting. Exercised by running next to bicycle (regularly, 2 times per month). No running next to bicycle. All types of outdoor exercise included. Duration of free range activity in yard was estimated according to the above descriptions (cf. activity in yard). 6 steps, many times a day or 12 steps, twice a day or 24 steps at a time, once a day. No daily stair climbing or 6 steps.

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The measured body dimensions and relative measures for body length and leg length (Rel.1Rel.5) are dened in Table 3. Descriptive analysis of the population The occurrence of IDC in the population was described by the prevalence and sex distribution of IDC in the sample (n = 48). Further, the individual number of calcied discs and the distribution pattern of calcied discs in the spine were presented. Statistical analysis Forty-eight dogs (n = 48) were included in the statistical analysis of the environmental factors. Maximum-likelihood logistic regression analysis (Hosmer and Lemeshow, 1989) was performed to estimate effects on IDC of the categorical variables dened in Table 2 (i.e. sex, active, bicycle, activity in yard, hunting, and stair climbing) and for the following continuous variables: duration of exercise, Rel.1 Rel.5, breast width, leg length, body length, weight and height (Tables 2 and 3). The number of calcications in relation to the number of intervertebral discs was chosen as the response. Initially, bivariate logistic regression analyses were performed for all variables. Variables with a signicance level below 0.20 (P 0.20) (Hosmer and Lemeshow, 1989) were included in the further multivariate analysis. A signicance level of 0.05 was used for the nal multivariate models. Odds ratios (OR) and condence intervals for OR were calculated for the individual variables and the estimated variables in the nal models. OR for the relative body measures were calculated for 1/2 3 8 kg) for Rel.1 and Rel.4 and 1/10 scale unit (1 cm/10 cm) for Rel.2, Rel.3 and Rel.5. scale unit (1 cm/z The OR for the continuous variable duration of exercise was calculated for an increase in daily exercise by 1 h.

Results
Occurrence and distribution of calcied discs

The distribution of 48 wirehaired dachshunds by number of calcied discs in each individual is presented in Fig. 1. Calcied discs were identied in 77 % (37/48) of the 2455month-old dachshunds. The number of calcied discs in individual dogs ranged from zero to 19, with a mean 2 standard deviation (SD) of 3.5 2 3.8. In the group of affected dogs, the mean number of calcied discs was 4.5 2 3.7. A total of 166 calcied discs were found with a particularly high frequency (71 % of the calcications) in the thoracic region between T1 and rst lumbar (L1) vertebra (Fig. 2). Of 37 affected dogs, 92 % (34/37) had IDC in the thoracic region, 46 % (17/37) had IDC in the cervical region (C2T1), and 32 % (12/37 dogs) had IDC in the lumbar region (L1S1). The sample comprised 20 males (42 %) and 38 (58 %) females. The occurrence of IDC

Table 3. Measured body dimensions and calculated relative measures Body measure Body weight (W) Thorax (T) Height (H) Leg length (L) Body length (B) Rel.1Rel.3 Rel.4Rel.5 Denition Circumference of thorax immediately caudal to the front limbs. Height (over shoulders). Distance from the proximal extremity of the olecranon* to the distal extremity of the footpad of the third digit. Distance from the external occipital protuberance to the cranio-dorsal part of the illiac crest, positioning the cranial axis perpendicular to the vertebral axis. 3 W; Rel.2 = L/T; Rel.3 = L/H Relative leg length: Rel.1 = L/z 3 W); Rel.5 =B/L Relative body length: Rel.4 = B/(z

*Anatomical site located by palpation.

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Fig. 1. Forty-six wirehaired dachshunds distributed by number of calcied intervertebral discs. The dogs were all between 24 and 49 months of age, except two dogs aged 52 and 55 months.

Fig. 2. Spinal distribution of disc calcication in 48 wirehaired dachshunds aged 2455 months.

was higher in males (90 % affected) than in females (68 % affected). However, a signicant association between sex and occurrence of IDC could not be demonstrated (cf. bivariate analysis below).
Environmental factors: statistical analysis

The number of intervertebral discs between C2 and S3 varied from 25 to 27 discs due to the occurrence of block vertebrae (cervical, one case) and lumbarization of S1 (ve cases). The results from analysis of the individual categorical and continuous variables are presented in Table 4. The odds ratio was 1 for most types of exercise, i.e. the number of calcied discs decreased with increasing amount or duration of exercise; the only exception was the effect of bicycle, which tended towards an association with high numbers of calcied discs. However, stair climbing was the only statistically signicant variable (P = 0.049); the exercise variables were not statistically signicant in the bivariate analysis. None of the absolute body measures had a signicant effect (P = 0.530.78) (not shown). Higher signicance levels were found for some of the relative measures, but none of these variables were signicant (Table 4). Stair climbing, duration of exercise, Rel.1 and Rel.3 had signicance levels below 0.20 (P 0.20) and these variables were included in the multivariate analysis (Table 5). Due to the close relation to duration of exercise, the variable active was included. Correction for confounding between stair climbing and duration of exercise increased the signicance level

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Table 4. Bivariate analysis of the effect of exercise variables and relative body measures on the occurrence of intervertebral disc calcication. (a) Bivariate logistic regression analysis of the categorical variables; (b) bivariate logistic regression analysis of the continuous variables (a) 95% condence interval for OR 0.472.0 0.211.8 0.502.3 0.372.1 0.321.4 0.575.3 0.181.0

Variable Sex

Class

Number of dogs 28 20 10 20 18 11 37 18 30 4 44 15 33

Mean SD (calc/dar)* (calc/dar)* P 0.13 0.14 0.09 0.15 0.10 0.12 0.14 0.11 0.15 0.20 0.13 0.08 0.16 0.16 0.12 0.10 0.18 0.12 0.11 0.16 0.10 0.17 0.16 0.14 0.10 0.16 0.92 0.54 0.76 0.29 0.35 0.049

Odds ratio 0.96 0.62 1.09 1.00 0.88 1.00 0.67 1.00 1.74 1.00 0.44 1.00

female male Activity in yard a b c Hunting a b Active a b Bicycle a b Stair climbing a b (b)

Variable Duration of exercise 3 W) Rel.1 (L/z Rel.2 (L/T) Rel.3 (L/H) 3 W) Rel.4 (B/z Rel.5 (B/L)

Scale unit min/day 3 cm/z kg cm/cm cm/cm 3 cm/z kg cm/cm

Mean 2 SD of variable 111 2 39 N N N N N

Mean SD (calc/dar)* (calc/dar)* P 0.13 0.13 0.13 0.13 0.13 0.13 0.14 0.14 0.14 0.14 0.14 0.14 0.12 0.20 0.88 0.054 0.83 0.30

Odds ratio 0.64 1.4 1.1 3.6 1.0 0.87

95% condence interval for OR 0.361.1 0.842.3 0.393.0 0.9713.7 0.741.2 0.651.14

*Dependent variable: calcied discs/intervertebral discs at risk. OR relative to 60 min exercise/day. 3 kg)1]. OR relative to 1/2 unit increase [i.e. (1/2cm/z OR relative to 1/10 unit increase (i.e. 1 cm/10 cm). Further descriptions of the different variables are given in Table 2.

of both variables, revealing a signicant effect of duration of exercise at the 5 % signicance level (Table 5 and Fig. 3). Figure 3 illustrates the effect of duration of exercise on the probability of calcication of the discs in dogs exposed to stair climbing and in those not exposed to stair climbing. The latter group is evidently more affected by disc calcication. Interaction between stair climbing and duration of exercise could not be demonstrated. The signicance level for these exercise variables did not increase by further adjustment for relative measures. Adjustment for stair climbing and duration of exercise did not reveal signicant effects of any of the relative measures. In general, the signicance level of relative measures increased slightly when corrected for confounding stair climbing; however, the signicance level of Rel.3 decreased (Table 5). Rel.1 was almost signicant when corrected for confounding with the exercise variables (Table 5 and Fig. 4). Again, the curves describing the effect of Rel.1 were mutually displaced as the dogs exposed to stair climbing were less affected.

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Table 5. Multivariate analysis of the effect of exercise variables and relative body measures on the occurrence of intervertebral disc calcication 95% condence interval for OR 0.140.82 0.161.1 0.191.14 0.241.1 0.290.92 0.341.2 0.361.3 0.280.98 0.291.1 0.892.4 0.562.2 0.802.2 0.9213 0.711 0.508.3

Variable Stair climbing

Confounder (corrected for)

P* 0.01 0.05 0.08 0.07 0.02 0.15 0.22 0.04 0.07 0.14 0.37 0.28 0.07 0.14 0.31

Odds ratio (OR)* 0.34 0.42 0.47 0.51 0.52 0.64 0.68 0.52 0.55 1.4 1.3 1.3 3.5 2.8 2.0

Duration of exercise Rel.1 Rel.3 Active Stair climbing Stair climbing Duration of exercise Rel.1 Rel.3 Rel.1 and stair climbing Rel.3 and stair climbing Stair climbing Rel.1 Duration of exercise Stair climbing and duration of exercise Stair climbing Rel.3 Duration of exercise Stair climbing and duration of exercise

Dependant variable: calcied discs/discs at risk. *P value and OR for the variable in the rst column. OR relative to an increase of 60 min exercise/day. 3 kg)1]. OR relative to 1/2 unit increase [i.e. (1/2cm/z OR relative to 1/10 unit increase (i.e. 1 cm/10 cm). Further descriptions of the different variables are given in Table 2.

Discussion The prevalence of IDC in the Danish population of wirehaired dachshunds was estimated at 77 % in the present study. The Norwegian population prevalence in mature wirehaired dachshunds can be estimated at 52 % in mature dogs (5 years old), based on a relative risk of 1.9 in mature dogs relative to young wirehaired dachshunds (1218 months) with a prevalence of 27.1 % (Stigen, 1991, 1996), which is considerably lower than the Danish population prevalence. As the occurrence of IDC varies signicantly amongst families (Havranek-Balzaretti, 1980), the prevalence would be expected to vary between populations, even related populations such as the Norwegian and Danish populations. Variation is unsurprising as interaction between the Norwegian and Danish dachshund populations has been restricted by the Norwegian rabies policy, with tight regulations on the import of dogs to Norway. Furthermore, the prevalence may alter considerably within a few generations due to the intensive use of a few studs in breeding. The mean number of calcications in the affected dogs was 4.5 (SD = 3.7) as compared to a mean of 3.7 calcied discs in affected dogs in the Norwegian population (Stigen, 1995). This difference, though non-signicant, is probably related to the higher prevalence of IDC in the Danish population. Two dogs included in the study were 2 and 6 months above the upper age limit set in the selection criteria (Table 1). This age limit was set to limit disappearance of disc calcications (asymptomatic or clinical herniation) before examination. As both dogs were affected and the mean number of calcied discs in these dogs was 4.5, the inclusion of these dogs is not thought to have caused bias in this study. The majority (71 %) of the calcications were observed in the thoracic region, in particular the caudal thoracic region (Fig. 2), in agreement with the ndings of Stigen (1991) and Hansen (1952). The canine spinal cord is protected from dorsal disc herniation by the intercostal

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Fig. 3. Probability of disc calcication in relation to duration of exercise in dogs exposed to stair climbing and dogs not exposed to stair climbing. The upper and lower limits of a 95 % condence interval and mean probability of disc calcication are calculated separately for each group (2 stair climbing).

ligaments in the region T1T9 (Hansen, 1952; Breit and Kunzel, 1997). Approximately 55 % of the disc herniations are located between T9 and L1 (65 % between T11 and L2) (Hoerlein, 1987). In the present study, 45 % (40/88) of the calcications found outside the region T1T9, were located in the region T9L1, and 32 % (32/88) were located in the region T10L2. This suggests an association between the localization of IDCs and disc herniations, supporting the hypothesis (Hansen, 1952; Havranek-Balzaretti, 1980) that the occurrence of IDC reects the disposition (risk) of disc herniation to some degree; other factors seem to be responsible to the high frequency of disc herniation in the cranial lumbar region (T13L2), possibly mechanical factors, as this area is highly mobile and affected by high loads (Hansen, 1952; Braund et al., 1977). No association was found between sex and IDC, whether evaluated as a binominal or a binary (either/or) variable. This is in accordance with previous studies on the occurrence of IDC (Hansen, 1952; Havranek-Balzaretti, 1980; Stigen, 1991; Stigen and Christensen, 1993). In conclusion, the population sample in the present study is comparable to samples used in other studies, although the estimated population prevalence is higher than that of the Norwegian population.
Body conformation (relative measures)

In the present study, signicant effects of the relative or absolute measures could not be demonstrated. The OR for Rel.2, Rel.4 and Rel.5 were close to 1 (within range of normal physiognomy) and not statistically signicant (Table 4). The OR values for the relative leg length (Rel.1 and Rel.3) were greater than 1 and the effect of leg length relative to height (Rel.3) was almost signicant (Table 4). In theory, the effect of Rel.3 (i.e. leg-length/height) may either be a mechanical effect (i.e. variations in loading on the discs) or an effect of different degrees of rhizomelic dwarsm, affecting both the length of the tubular bones and the predisposition to

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Fig. 4. Probability of disc calcication in relation to Rel.1 (relative leg length) within dogs exposed to stair climbing and dogs not exposed to stair climbing. The upper and lower limits of a 95 % condence interval and mean probability of disc calcication are calculated separately for each group 3 3 W (cm/z kg). (2 stair climbing). Rel.1 =L/z

disc degeneration. However, the association appears to be positive, i.e. the number of calcied discs increases with increasing leg length (relative to height). This implies that an increasing severity of rhizomelia (dwarsm) appears to be associated with a decreasing number of calcied discs the opposite of what may be expected. Furthermore, Rel.3 did not have a signicant effect (P = 0.31) when corrected for confounding with the signicant variables for exercise (duration of exercise and stair climbing). In conclusion, what at rst appeared to be a signicant effect of Rel.3 was probably due to confounding with the exercise variables in the present sample. Many breeders argue that breeding towards a shorter type would solve the problem of disc herniation. However, signicant effects on disc degeneration could not be demonstrated for the relative measures for body length (Rel.4 and Rel.5). This does not prove that there is not an effect of body length. However, the (non-signicant) relation between body length/leg length (Rel.5) and severity of disc degeneration was negative (OR = 0.87; P = 0.30), i.e. the risk of IDC tended to decrease with increasing spinal length or decreasing leg length, making it highly unlikely that breeding towards shorter spines would decrease the severity of disc degeneration. The effect of one relative measure, Rel.1, was almost signicant (P = 0.05), when corrected for confounding with stair climbing, indicating that increasing body size (weight) relative to leg length may have a benecial effect on the discs (decreasing number of calcications) (Fig. 4). This may be interpreted as a benecial effect of short limbs or a benecial effect of a large trunk (including long trunks).
Exercise variables

A signicant correlation between stair climbing and the relative number of calcied discs was demonstrated by logistic regression. The relation was negative, i.e. the number of calcied

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discs was lower in dogs exposed to stair climbing (OR = 0.44, Table 4). Multivariate analysis with correction for confounding with stair climbing demonstrated a statistically signicant effect of duration of exercise, as illustrated in Fig. 3. Duration of exercise was negatively correlated with IDC, with OR = 0.52 (Table 5); that is, the odds of developing calcication of the intervertebral disc were halved by increasing the daily exercise by 1 h, within the spectrum (111 2 39 min/day) represented in the present study. None of the exercise variables included in duration of exercise had signicant effects individually. Active almost had a signicant (P = 0.07) effect when corrected for confounding with stair climbing. This was not surprising as the variables (hunting and activity in yard) included in active make up a major part of the daily exercise. A positive effect of using dogs for hunting has been suggested in other studies (Havranek-Balzaretti, 1980); however, these ndings were not signicant. This is in accordance with the present study, as none of the exercise variables had a signicant effect individually. Stair climbing was not included in the variable duration of exercise, but the biological effects are related (response to mechanical loadings). Confounding was demonstrated, but there was no interaction between the two variables, i.e. the effects appear to be additive. The present study indicates a benecial effect of moderate exercise, in accordance with the published experimental ndings in non-hypochondroplastic dogs, i.e. that moderate daily exercise is benecial for the nutrition of the disc. In contrast with the present ndings, studies of the effect of daily exercise on discs in the Labrador demonstrated a biochemical response that did not depend on the duration of daily exercise (Holm and Nachemson, 1983). This may indicate differences in the response of discs in hypochondroplastic and non-hypochondroplastic dogs. Other studies have indicated an upper limit to the benecial effect of exercise; in young hypochondroplastic dogs (beagles), long-distance running (40 km/day from 15 to 70 weeks of age) caused signicant alterations in PG synthesis and PG concentration, and decreased hydration (Puustja rvi et al., 1993). In rats, non-physiological strenuous daily exercise for a prolonged period disturbs the metabolism, thereby inducing disc degeneration (Holm and Rosenquist, 1986). These studies indicate that monotone vigorous exercise may be detrimental to the disc in hypochondroplastic dogs. The experimental conditions (Puustja rvi et al., 1993) were extreme compared to eld conditions; nevertheless, in the present study, a positive association (not signicant) was found between the occurrence of IDC and running next to a bicycle (OR = 1.74), a relatively vigorous type of exercise dominated by cyclic (monotonous) motion. However, the number of dogs (four dogs) exposed to this type of exercise (bicycle) was much too low for any conclusion concerning the effect under eld conditions. In theory, stair climbing may also be a monotone vigorous type of exercise when many oors are climbed at a time, but in the present study, only two of 15 dogs exposed to stair climbing were climbing more than 15 steps at a time. A likely explanation of the benecial effect of moderate daily exercise may be a stimulating effect on cell metabolism, possibly with increased production of PG. Insufcient nutritional levels and diffusion of metabolic waste due to increasing metabolic demand may occur due to vigorous, persistent loading. Excessive stresses may also cause dehydration and thereby compromise diffusion. In the present study, few of the variables had a statistically signicant effect on the number of calcied discs. In particular, none of the body measures was signicant, possibly because other factors (including genetic factors) are of major signicance and the sample size was too small to demonstrate minor effects. With respect to the exercise variables, a major problem was the difculty in obtaining exact measures for the amount of exercise for private pets due to very broad variability in exercise pattern there was not only variation between dogs, but also weekly and seasonal variations. Therefore, the mean daily duration of exercise is a rough estimate. Estimation of duration of activity in yard is particularly rough as time of access to the yard does not correspond directly to the duration or level of free range activity. Thus, the estimates presented of the benecial effect (OR) of exercise are rough. In spite of these problems, this study indicates that moderate exercise is benecial for the intervertebral disc, but the magnitude of this benecial effect needs to be studied under more standardized conditions.

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Loss of hydromechanical pressure of the NP causes higher mechanical stress on the annulus, thereby increasing the risk of tearing of the outer innervated annulus (Buckwalter, 1995; Adams et al., 1996a). Therefore, with regard to stair climbing, one source of error that should be considered is that the dogs may not climb stairs due to pain secondary to severe disc degeneration. However, not having access to staircases was the most common cause for not climbing stairs in the present study; only two dogs refused to climb stairs, but these dogs had never previously climbed stairs, indicating that spinal pain was not the cause. It should be emphasized that the effect of stair climbing demonstrated here was an inhibitory effect on dystrophic calcication, suggesting a retardation of the degenerative process. Despite these ndings, stair climbing should still be considered a potential risk factor for development of disc herniation in dogs that have already developed severe disc degeneration, due to higher stress peaks on the annulus of the degenerated disc (Adams et al., 1996b). This is the rst study of vertebral disc degeneration in hypochondroplastic dogs demonstrating a signicant effect of spinal motion induced by differences in exercise patterns in the eld. The ndings are consistent with the available results of biochemical studies on the effect of mechanical loading on the canine disc. In conclusion, a benecial effect of moderate daily exercise, of up to 150 min/day, has been demonstrated, although the effect needs to be quantied under more standardized conditions. In particular, the effect of exercise by running next to a bicycle should be investigated thoroughly; the effect was questionable in the present study, but this type of exercise may represent a vigorous, monotonous type of exercise with deleterious effects on the disc. On the basis of these ndings, it seems advisable to exercise a dachshund for several hours a day, at moderate intensity. Furthermore, until further investigations have been performed, running next to bicycles should probably be avoided. On the other hand, there seems to be no reason to avoid moderate daily stair climbing. The widespread myth that it is deleterious for dachshunds in general to climb staircases was rejected, as moderate stair climbing was a statistically signicant benecial factor. Signicant effects of body conformation could not be demonstrated. References
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