Effects of osteoarthritis on radiographic measures of laxity and congruence in hip joints of Labrador Retrievers

Randi M. Gold Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Thomas P. Gregor Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Jennifer L. Huck Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Pamela J. McKelvie Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Gail K. Smith Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Abstract

Objective—To determine effects of hip joint osteoarthritis on radiographic measures of hip joint laxity and congruence.

Design—Longitudinal study.

Animals—40 Labrador Retrievers.

Procedures—Dogs were assigned to 2 groups based on radiographic evidence of osteoarthritis. Dogs in the osteoarthritis group were free of osteoarthritis at initial radiographic evaluation (t1) and developed osteoarthritis by a subsequent radiographic evaluation (t2). Dogs in the nonosteoarthritis group had no radiographic osteoarthritis at either evaluation. Hip joint laxity was quantified by use of the distraction index (DI) from a distraction radiographic view and use of the Norberg angle (NA) from a ventrodorsal hip-extended radiographic view. The compression index (CI) from a compression radiographic view was used as a measure of joint congruence (concentricity).

Results—Hip joint laxity (NA or DI) did not change over time in the nonosteoarthritis group. Mean hip joint laxity (NA and DI) for the osteoarthritis group was greater at t1 than for the nonosteoarthritis group. With the onset of osteoarthritis, mean NA decreased significantly and mean CI increased significantly, but mean DI remained unchanged.

Conclusions and Clinical Relevance—No radiographic evidence for compensatory hip joint tightening associated with osteoarthritis was detected. Hip-extended radiography revealed that hip joints got looser with osteoarthritis and NA decreased. Hip joint laxity (DI) on distraction radiographs was unchanged by the onset of osteoarthritis and remained constant in the osteoarthritis and nonosteoarthritis groups at both evaluations. However, the CI increased with osteoarthritis, as reflected in nonzero indices (incongruence). The CI may be a valid marker for early hip joint osteoarthritis.

Abstract

Objective—To determine effects of hip joint osteoarthritis on radiographic measures of hip joint laxity and congruence.

Design—Longitudinal study.

Animals—40 Labrador Retrievers.

Procedures—Dogs were assigned to 2 groups based on radiographic evidence of osteoarthritis. Dogs in the osteoarthritis group were free of osteoarthritis at initial radiographic evaluation (t1) and developed osteoarthritis by a subsequent radiographic evaluation (t2). Dogs in the nonosteoarthritis group had no radiographic osteoarthritis at either evaluation. Hip joint laxity was quantified by use of the distraction index (DI) from a distraction radiographic view and use of the Norberg angle (NA) from a ventrodorsal hip-extended radiographic view. The compression index (CI) from a compression radiographic view was used as a measure of joint congruence (concentricity).

Results—Hip joint laxity (NA or DI) did not change over time in the nonosteoarthritis group. Mean hip joint laxity (NA and DI) for the osteoarthritis group was greater at t1 than for the nonosteoarthritis group. With the onset of osteoarthritis, mean NA decreased significantly and mean CI increased significantly, but mean DI remained unchanged.

Conclusions and Clinical Relevance—No radiographic evidence for compensatory hip joint tightening associated with osteoarthritis was detected. Hip-extended radiography revealed that hip joints got looser with osteoarthritis and NA decreased. Hip joint laxity (DI) on distraction radiographs was unchanged by the onset of osteoarthritis and remained constant in the osteoarthritis and nonosteoarthritis groups at both evaluations. However, the CI increased with osteoarthritis, as reflected in nonzero indices (incongruence). The CI may be a valid marker for early hip joint osteoarthritis.

Hip dysplasia in dogs is a developmental orthopedic disease in which abnormal development of a hip joint leads to functional laxity. This results in cartilage degradation, osteophyte formation, subchondral sclerosis, and ultimately osteoarthritis.1–5 It is empirically believed that fibrotic thickening of the joint capsule associated with osteoarthritis in dogs with HD causes a tightening effect on a hip joint, thereby making the joint more stable.3,4,6 However, in humans, osteoarthritis does not influence subluxation and will affect position within the hip joint only when the femoral head is malformed.7 It is further proposed that tightening and increased stability of the hip joints of affected dogs are associated with less pain. For the most seriously affected dogs, this reduction in pain is usually evident by the time dogs are 18 months old.6 In addition, it has been theorized that a large active muscle mass may inhibit transformation of passive laxity into functional laxity as a dog ambulates and thus decrease the stresses on articular cartilage that lead to degenerative changes.8,9

Several methods have been proposed to measure passive laxity of the hip joints in humans and dogs. However, 2 radiographic methods (ie, NA and DI) are used most commonly in dogs.9–20 The NA measurement method is applied to ventrodorsal hip-extended radiographs as a means of quantifying hip joint laxity.12,21 Throughout the world, the NA has been incorporated into several screening systems as a measure of joint laxity. In the United States, the NA is not measured; rather, joint laxity is subjectively estimated and represented as subluxation.

The PennHIPa method consists of 3 separate radiographs (ie, distraction view, compression view, and ventrodorsal hip-extended view) for full assessment of the spatial relationships of the femoral head to the acetabulum. With the hip joints in a neutral, stance-phase position, the distraction radiographic view permits quantifying maximum passive hip joint laxity by use of the DI.9,11,17,18,22 The compression radiographic view is also obtained with the hind limbs in a neutral, stance-phase position; however, instead of distraction, the femoral heads are compressed into the acetabula to reveal the extent of joint congruence represented by the CI.18 For a perfectly congruent joint, the CI is zero (or within-measurement error of 0). Joints that deviate substantially from zero represent grades of incongruence. The ventrodorsal hip-extended view is included in the PennHIP evaluation to obtain supplementary information regarding the existence of osteoarthritis in a hip joint as conventionally described.

Irrespective of animal positioning and measurement method (NA, DI, or CI), the authors are not aware of any studies conducted to examine the change in laxity or congruence of a hip joint associated with the development of osteoarthritis. The purpose of the study reported here was to examine the effects of osteoarthritis on laxity and congruence of hip joints.

Materials and Methods

Animals—Labrador Retrievers that had at least 2 PennHIP radiographic evaluations were identified in the PennHIP database. Inclusion criteria required that all dogs were ≥ 16 weeks old, dogs had no evidence of radiographic osteoarthritis at t1, and the minimum interval between radiographic sessions (ie, t1 and t2) was 2 months. The existence of radiographic evidence of osteoarthritis of the hip joints was determined by 1 investigator (PJM), who performed the evaluation in accordance with the standard radiographic protocol based on Orthopedic Foundation for Animals–type scoring.5,12,23 None of the dogs used in the study had prior injuries, surgery, or evidence of cavitation.

From this initial sample of dogs, 2 groups were selected. Twenty dogs were identified that had radiographic evidence of osteoarthritis at a subsequent evaluation (ie, at t2); these 20 dogs constituted the osteoarthritis group. A larger number of dogs were identified that did not have radiographic evidence of osteoarthritis at t2 (nonosteoarthritis dogs); the nonosteoarthritis dogs were matched with dogs in the osteoarthritis group on the basis of sex and age (± 2 months). Thus, there were 20 dogs in the nonosteoarthritis group.

Procedures—Distraction, compression, and ventrodorsal hip-extended radiographs from t1 and t2 were used in the measurement of DI, CI, and NA, respectively (Figure 1). The NA and DI are measures of hip joint laxity, whereas the CI is a measure of joint congruity (Figure 2). For statistical analysis, the worst hip in each dog (ie, hip with the greater DI) was determined at t1. The same hip was then measured again at t2.

Figure 1—
Figure 1—

Ventrodorsal hip-extended (A), compression (B), and distraction (C) radiographic projections of the hip joint of a representative dog. A—The NA is derived from the ventrodorsal hip-extended projection. It is the angle between a line connecting the femoral head centers and a line from the femoral head center to the craniodorsal acetabular rim. B—Circle gauges are used to determine the CI from the compression projection. In this example, the CI is equal to 0. C—Circle gauges are used to determine the DI from the distraction projection. The DI and CI are calculated by dividing the measured distance between the femoral head center and acetabular center (d) by the radius (r) of the femoral head.

Citation: Journal of the American Veterinary Medical Association 234, 12; 10.2460/javma.234.12.1549

Figure 2—
Figure 2—

Compression radiographic projections of the hip joints of representative dogs illustrating a CI equal to zero (A) and a CI not equal to zero (B).

Citation: Journal of the American Veterinary Medical Association 234, 12; 10.2460/javma.234.12.1549

The DI measurements were obtained from the PennHIP database. However, CI and NA were not included in the PennHIP database; therefore, measurements for those variables9 were generated by an experienced evaluator (TPG) for use in the study.

Statistical analysis—A repeated-measures ANOVA with post hoc pairwise comparisons (least significant difference) was used to test for mean differences in NA, DI, and CI measurements within subjects at t1 and t2 and for differences between the nonosteoarthritis and osteoarthritis groups for all measurement methods at each time period (time was the repeated measure within subjects). A repeated-measures ANOVA was performed separately for each measurement method. In addition, Student t tests were used to compare mean age and body weight between groups at each radiographic evaluation (t1 and t2).

For all analyses, significance was set at values of P < 0.05. All analyses were performed with statistical software.b,c

Results

Animals—Mean age did not differ significantly between the nonosteoarthritis (0.47 years) and osteoarthritis (0.46 years) groups at t1 (Table 1). There was a significant (P = 0.002) difference in mean age between the nonosteoarthritis (1.41 years) and osteoarthritis (1.00 years) groups at t2. The mean difference for the interval from t1 to t2 was 0.94 years for the nonosteoarthritis group and 0.54 years for the osteoarthritis group. The longer interval for the nonosteoarthritis group was intentional to allow additional time for osteoarthritis to develop in those dogs.

Table 1—

Descriptive statistics for age of the nonosteoarthritis (n = 20 dogs) and osteoarthritis (20) groups at t1 and t2 and the difference in age of dogs between the 2 time periods (t2 − t1).

Groupt1t2t2 − t1
MinMaxMean ± SDMinMaxMean ± SDMinMaxMean ± SD
Nonosteoarthritis0.350.680.47 ± 0.081.002.201.41 ± 0.500.511.840.94 ± 0.50
Osteorarthritis0.390.680.46 ± 0.090.591.501.00 ± 0.200.200.970.54 ± 0.18

Values are reported in number of years.

Min = Minimum. Max = Maximum.

Mean body weight did not differ significantly between the nonosteoarthritis and osteoarthritis groups at t1 (17.30 and 18.00 kg, respectively) or t2 (25.50 and 26.34 kg, respectively; Table 2). Mean weight gain in the interval from t1 to t2 was 8.20 kg for the nonosteoarthritis group and 8.76 kg for the osteoarthritis group.

Table 2—

Descriptive statistics for body weight of the nonosteoarthritis (n = 20 dogs) and osteoarthritis (20) groups at t1 and t2 and the difference in body weight of dogs between the 2 time periods (t2 − t1).

Groupt1t2t2 − t1
MinMaxMean ± SDMinMaxMean ± SDMinMaxMean ± SD
Nonosteoarthritis12.2725.4517.30 ± 3.7818.6432.7325.50 ± 3.40−1.3615.918.20 ± 4.22
Osteoarthritis12.2726.8118.00 ± 4.7019.55*40.91*26.34 ± 5.92*−2.27*19.55*8.76 ± 5.30*

Values are reported in kilograms.

Represents results for only 19 dogs.

See Table 1 for remainder of key.

Evaluation of the NA—Mean NA for the nonosteoarthritis group did not differ significantly between t1 and t2 (102.20° and 102.28°, respectively). For the osteoarthritis group, mean NA at t2 (90.85°) was significantly (P < 0.001) less than the mean NA at t1 (96.43°). Mean NA for the nonosteoarthritis group was significantly (P < 0.001) greater than the mean NA for the osteoarthritis group at t1 and at t2 (Table 3).

Table 3—

Descriptive statistics for each measurement method within each treatment group (n = 20 dogs/group) at each time period (t1 and t2) and the difference in values between the 2 time periods (t2 − t1).

Measurement methodGroupt1t2t2 − t1
MinMaxMean ± SDMinMaxMean ± SDMinMaxMean ± SD
NA (°)Nonosteoarthritis90113102.20 ± 5.05*89112102.28 ± 5.51*−1111−0.08 ± 5.38
Osteoarthritis8410496.43 ± 6.357510490.85 ± 8.84−13195.58 ± 7.36
DINonosteoarthritis0.330.620.50 ± 0.09*0.230.680.48 ± 0.14*−0.100.200.09 ± 0.09
Osteorarthritis0.480.920.70 ± 0.010.420.860.72 ± 0.10−0.300.20−0.03 ± 0.14
CINonosteoarthritis0.000.040.00 ± 0.0030.000.090.01 ± 0.028*−0.090.00−0.01 ± 0.024
Osteoarthritis0.000.170.03 ± 0.0470.000.250.12 ± 0.080−0.250.08−0.09 ± 0.090

Within a time period for each measurement method, value differs significantly (P < 0.05) from the value for the osteoarthritis group.

Evaluation of the DI—Mean DI did not differ significantly between t1 and t2 for the nonosteoarthritis (0.50 vs 0.48, respectively) or osteoarthritis (0.70 vs 0.72, respectively) groups (Table 3). Mean DI for the nonosteoarthritis group was significantly (P < 0.001) less than the mean DI for the osteoarthritis group at t1 and t2.

Evaluation of the CI—Mean CI for the nonosteoarthritis group did not differ significantly between t1 and t2 (0.00 and 0.01, respectively; Table 3). For the osteoarthritis group, mean CI at t2 (0.12) was significantly (P < 0.001) greater than the mean CI at t1 (0.03). No significant difference in mean CI was found between the osteoarthritis and nonosteoarthritis groups at t1; however, the mean CI of the nonosteoarthritis group at t2 was significantly (P < 0.001) less than the mean CI of the osteoarthritis group at t2.

Discussion

The common belief that hip joints tighten as a result of progressing osteoarthritis could not be confirmed in the study reported here. Joint laxity (as measured by the use of various methods) can precede hip joint remodeling and osteoarthritis.1,18,20,24 Joint laxity is also a function of coxofemoral position, with measured laxity decreasing for hip joints in extreme extended positions and maximal for hip joints in more neutral positions.25 Two methods for radiographic measurement of laxity were used in this study (NA from the hip-extended radiographic projections and DI from the hip-neutral distraction radiographic projections), each of which revealed a different result. The NA is a method to quantify laxity in ventrodorsal hip-extended radiographs; scores > 105° represent tight hip joints, whereas lower scores represent looser hip joints.12 For the nonosteoarthritis group, 5 (25%) dogs had an NA ≥ 105° at t1, and 8 (40%) dogs had an NA ≥ 105° at t2. For the osteoarthritis group, none of the dogs had an NA ≥ 105° at either time point. The NA decreased over time in the osteoarthritis group, which indicated that hip joints loosened with the onset of osteoarthritis.

The DI quantifies hip joint laxity as measured by the PennHIP DI. Scores range from 0 to > 1, with 0 representing full congruence (tight hip joints) and 1 representing complete luxation (loose hip joints). In this study, the DI as a measure of joint laxity did not change significantly over time in the nonosteoarthritis or osteoarthritis groups, which is consistent with results in another report.9 This result can be interpreted to mean that in the neutral distraction position, the DI is unaffected by mild or moderate osteoarthritis. This would give the DI more clinical value (ie, the magnitude of the DI can reflect the inherent susceptibility of a dog to osteoarthritis by remaining constant despite osteoarthritis, whether evaluated prospectively or retrospectively9,19). Another important consideration is that the more constant a trait is over time, the higher its genetic determination and estimate of heritability.26

The NA from the hip-extended radiographs and the DI from the distraction radiographs are both accepted measures of hip joint laxity, but these measures behaved differently in response to the onset of osteoarthritis in this study. A consistency was that both NA and DI indicated that the nonosteoarthritis dogs had tighter hip joints than did the dogs that ultimately developed osteoarthritis. This is consistent with the current understanding that joint laxity makes hip joints susceptible to osteoarthritis.9,11,17–20,27 Interestingly, the nonosteoarthritis group had a mean DI of 0.50, which was typical for Labrador Retrievers in the PennHIP database, whereas the osteoarthritis group had a mean DI of 0.70, which was markedly greater (ie, more lax). However, both DI values were within the osteoarthritis susceptibility range, which suggested that most of the dogs in this study may have developed osteoarthritis if they had been monitored for a sufficient period, as reported elsewhere.28 No similar comparisons of the predictive value of NA can be made because, to the authors' knowledge, such studies directly relating NA to osteoarthritis susceptibility in the long term have not been published. Another consistency was the observation that both NA and DI remained relatively constant for the nonosteoarthritis group between t1 and t2.

In contrast, the magnitude of NA and DI differed with regard to osteoarthritis onset. Analysis of the NA revealed that hip joints got looser with osteoarthritis onset. However, hip joint laxity as measured by the DI did not reveal changes over time in the nonosteoarthritis or osteoarthritis group, consistent with results in another report.9 Of the 3 radiographic measurements, the DI was least affected by mild osteoarthritis, which provided the DI with greater clinical value as a metric reflecting susceptibility to developing osteoarthritis.18 In contrast, the NA derived from hip-extended radiographs can have greater variability as a measure of hip joint laxity as young dogs age, which makes it a less reliable metric.9 In the study reported here, a change in mean NA of 5.6° at t2 was associated with the onset of osteoarthritis. This was a significant change. On the basis of the literature, it is known that a change of this magnitude is also clinically relevant. A difference in NA of 5° (ie, greater laxity) correlates with a higher likelihood of the development of HD in dogs.9,29,30 It is not known which of the 2 NA scores (before or after onset of osteoarthritis) is a more accurate indication of the genotype and, therefore, the breeding value of a dog.

The mean CI for the nonosteoarthritis group did not change significantly over time, which indicated that hip joint congruence was maintained throughout the time course of the study. On the other hand, the CI for the osteoarthritis group increased with progressing osteoarthritis. A nonzero CI indicates that the joint is no longer concentric and therefore that femoral head-to-acetabular congruence has decreased. For the nonosteoarthritis group, the mean CI difference remained close to (but not exactly equal to) zero. The small nonzero variability likely represented measurement error rather than a biological phenomenon, and it indicated that basic congruence was maintained over time. In comparison, within the osteoarthritis group, the CI measurements were greater at t2 with development of osteoarthritis, compared with the values at t1 when there was no osteoarthritis; this indicated that hip joints lost congruence with development of osteoarthritis. Specifically, as the hip joints were remodeled, the center of rotation of the femoral head moved away laterally from the center of rotation of the acetabulum as an effect of the development of osteoarthritis. The change over time for the nonosteoarthritis group was smaller, compared with results for the osteoarthritis group, which indicated consistent congruence between time points. The small but nonzero CI measurements at t1 for the osteoarthritis group (CI, 0.03) may suggest there is mild hip joint incongruity before osteoarthritis is radiographically evident. A theory has been advanced that HD develops only if a young, growing dog has instability and incongruity of the hip joints.3 The study reported here may have clinical importance and lend support to that theory, and the CI may be useful as a metric (in combination with the DI measurement) for predicting susceptibility to developing osteoarthritis in growing dogs before the overt onset of radiographic evidence of osteoarthritis.

The study reported here had some limitations. Dogs were matched on the basis of age and sex but not on the basis of body weight or body condition score. However, body weight did not differ significantly between the groups. Investigators in another study30 reported that body weight and body condition score have relevance and can exacerbate osteoarthritis and cause it to develop sooner and with greater severity. Lifestyle of the dogs in our study was also not controlled. Environmental factors, including diet and exercise, can substantially affect the incidence and severity of osteoarthritis in dogs with HD.5,16

Another potential concern was that the study was based on whether a dog had overt radiographic signs of osteoarthritis discovered at a second radiographic examination. Accordingly, this was not a randomized population, as exemplified by the finding (learned after initial assignment) that nonosteoarthritis dogs had tighter hip joints than did their osteoarthritis counterparts. Also, owners were not surveyed as to motivation for having > 1 PennHIP evaluation, so the study was limited in its ability to achieve broader epidemiologic conclusions about HD in dogs.

The DI and CI at t1 and t2 always had less variability for the nonosteoarthritis group than for the osteoarthritis group. However, although dogs in the nonosteoarthritis group did not have obvious radiographic evidence of osteoarthritis, it is a possibility that osteoarthritis may have been detected had the joints been evaluated by histologic examination, which is more sensitive than radiography for the diagnosis of osteoarthritis.3,4 Dogs with radiographic evidence of osteoarthritis definitely had osteoarthritis, but those without radiographic evidence of osteoarthritis could conceivably have been in the early stages of osteoarthritis. This uncertainty as to actual disease status could add to the variability in dogs not having overt radiographic evidence of osteoarthritis.

Another consideration is that the results apply to dogs 2 years old or younger. The results may not be the same for dogs that develop osteoarthritis at later stages of life. An additional possible source of concern may be the difference in the interval between t1 and t2 and the age of osteoarthritis and nonosteoarthritis dogs (1 year vs 1.4 years, respectively). However, it could be argued that a longer interval between radiographs of the hip joints for dogs in the nonosteoarthritis group would have had the effect of allowing more time for the development of osteoarthritis changes. In other words, allowing the nonosteoarthritis dogs more time to develop osteoarthritis gave greater assurance that the nonosteoarthritis dogs had an inherent lower susceptibility to development of osteoarthritis.

Results of the study reported here challenge the popular belief that there is compensatory tightening of the hip joints with progressive osteoarthritis. On the contrary, radiographic evidence of osteoarthritis was associated with measured loosening of the hip joints (as determined by evaluation of the NA) and incongruence (as determined by evaluation of the CI) because the femoral head no longer resided in its normal position within the acetabulum. The DI was the most repeatable of the 3 metrics used in this study. As reported in another study,9 it had the lowest variability over time, regardless of mild osteoarthritis. Nonosteoarthritis dogs appeared to have hip joints that were tighter and more congruent, compared with the hip joints of osteoarthritis dogs, which is consistent with current beliefs about HD. The results of this study may indicate use of the CI measurement to correlate with degenerative changes, perhaps even before such changes are radiographically apparent; thus, the CI may be an early radiographic indicator of osteoarthritis. Additional longitudinal studies are needed to examine whether nonzero CI values represent a valid early measure for the development of osteoarthritis.

ABBREVIATIONS

CI

Compression index

DI

Distraction index

HD

Hip dysplasia

NA

Norberg angle

t1

Time of the first radiographic evaluation

t2

Time of the second radiographic evaluation

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a.

PennHIP, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pa.

b.

SPSS 12.0 for Windows, SPSS, Chicago, Ill.

c.

SAS, version 9.1, SAS Institute Inc, Cary, NC.

  • Figure 1—

    Ventrodorsal hip-extended (A), compression (B), and distraction (C) radiographic projections of the hip joint of a representative dog. A—The NA is derived from the ventrodorsal hip-extended projection. It is the angle between a line connecting the femoral head centers and a line from the femoral head center to the craniodorsal acetabular rim. B—Circle gauges are used to determine the CI from the compression projection. In this example, the CI is equal to 0. C—Circle gauges are used to determine the DI from the distraction projection. The DI and CI are calculated by dividing the measured distance between the femoral head center and acetabular center (d) by the radius (r) of the femoral head.

  • Figure 2—

    Compression radiographic projections of the hip joints of representative dogs illustrating a CI equal to zero (A) and a CI not equal to zero (B).

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