Hip dysplasia is a leading cause of disease in the hip joints of dogs and humans, and HD in dogs is an accepted condition used to study DDH in humans.1–5 The precise pathophysiologic processes by which apparently normal neonatal hip joints become malformed, osteoarthritic joints by the time of adulthood have not been determined in dogs or humans.4,6,7 Early diagnosis, prevention, and treatment of osteoarthritis of the hip joints characteristic of HD in dogs and DDH in humans have been the focus of intensive research efforts for some time.8–13 Radiography is the standard imaging modality used to diagnose HD in dogs.3,14,15 However, radiographically evident joint changes are not representative of cartilage degeneration characteristic of osteoarthritis.16–18 Standard radiographs do not permit quantification of existing joint disease at the cartilage level and therefore lack necessary sensitivity for early diagnosis or to monitor disease progression without bony changes.3,14,17
Computed tomography is routinely used to image hip joints of immature and mature humans for diagnostic purposes, surgical planning, and evaluation of therapeutic interventions.19–23 The use of 2-D and 3-D CT imaging has substantially advanced detection of minor conformational abnormalities of the hip joints associated with the initiation and progression of DDH-associated osteoarthritis.8,23-25 Computed tomography of the hip joints of dogs has been used to assess joint changes mediated by surgical treatment10,11 and to detect joint laxity and dorsolateral femoral subluxation for diagnosis of HD in dogs.26,27 Pelvic limbs are typically abducted10,11 or subjected to simulated weight bearing26,27 during CT, and measurements are performed on images for comparative purposes. Computed tomography is not routinely used on dogs to assess degenerative joint changes.
Hip joint articulation can be quantified with standard measures on radiographic and CT images. The DI is a measure of passive laxity in the hip joints of dogs determined by use of a distraction radiographic technique.28,29 The NA is used to measure femoral head subluxation, and RPC is a measure of the percentage of femoral head covered by the acetabulum on standard ventrodorsal joint-extended radiographs of dogs.30 Personnel at PennHIPa and the OFAb score hip joint confirmation and degenerative joint disease of dogs by use of independent standardized systems.12 The CEA, VASA, DASA, HASA, HTEA, and AI are standard measures used to evaluate human 2-D CT hip joint images.22 Similarly, femoral headto-acetabulum ratios are measured on SCT and TCT images of hip joints in humans.31 To our knowledge, these CT measures have not been routinely used in canine patients.
The study reported here was designed to test the hypothesis that measures obtained from CT images have stronger correlations with articular cartilage microstructural changes than with measures obtained from radiographs. The hypothesis was tested by evaluating relationships among established canine radiographic measures and standard human CT measures with microstructural cartilage changes in canine hip joints with moderate to severe joint laxity characteristic of HD. The objective was to determine a combination of imaging modalities and measures that reflect microstructural changes in canine hip joints with the highest accuracy.
Materials and Methods
Animals—Twelve 30-month-old mixed-breed hounds (progeny of 2 dams and 1 sire) were used for the study. There were 5 males and 7 females with a mean ± SEM body weight of 25.6 ± 1.38 kg (range, 20.0 to 35.0 kg). For inclusion in the study, the DI of both hip joints of each dog had to be ≥ 0.45. One hip joint from each dog was selected for evaluation in accordance with a randomized block design. The study was performed in accordance with institutional and National Institutes of Health regulations governing the treatment of vertebrate animals. Procedures were initiated after approval by a university animal care committee.
Radiography—Each dog was anesthetized, and hipextended and distraction radiographs were obtained via established techniques.29 Radiographs were submitted to PennHIP and the OFA for objective evaluation. For purposes of statistical evaluation, the numeric PennHIP DI score was used as reported, and the degenerative joint disease classification29,32 was assigned a numeric score (none = 0; mild = 1; moderate = 2; and severe = 3). Numeric scores were similarly assigned to OFA grades (excellent, good, fair, or borderline = 0; mild = 1; moderate = 2; and severe = 3).
CT evaluation—Immediately after radiography, CT images of the pelvis were obtained. Dogs were placed in dorsal recumbency with the hip joints extended, in accordance with established standards.29 Positioning was maintained by the use of tape and sandbags and confirmed with a survey scan. Transverse pelvic imagingc was performed by use of 1.5-mm slice widths. Images were stored on optical disksd and transferred to a computer workstatione where 3-D images were reconstructed in both transverse and sagittal planes. Both 2-D and 3-D images were printed on radiographic film.
Radiography and CT measurements—Radiographic and CT images were digitized at 400 × 400 dots/inch and an 8-bit depth of gray scale by means of a transparent scan bed of a high-resolution scannerf at full size. Images were exported as uncompressed tagged-image file format files and implemented in a graphics software program.g The software measuring tool was used to obtain all measurements.
The NA and RPC were measured 3 times for the selected hip joint of each dog (Figure 1).30 Computed tomography measurements were obtained from 3 contiguous slices, which were selected on the basis that each image contained a clearly defined acetabular fossa, sourcil, fovea capitis, and round femoral heads.8,24 The mean of all measurements was used for statistical analysis.
The center of the femoral head on 2-D CT images was assumed to be the midpoint of a line drawn perpendicular to a straight line that connected the caudal articular cartilage margins on the dorsal and ventral articular surfaces (Figure 2). All measurements were performed in accordance with methods routinely used for images obtained from human patients.8,33
CEA—The CEA is used to assess dorsolateral coverage of the femoral head by the bony acetabulum.34 It was measured between a line that extended from the center of the femoral head to the dorsolateral point of the labrum and a line perpendicular to the horizontal axis of the pelvis that extended dorsally through the labrum from the center of the femoral head. The horizontal axis of the pelvis was defined as a line through the center of both femoral heads (Figure 3).
VASA, DASA, and HASA—Ventral, dorsal, and global acetabular coverage of the femoral head is quantified with the VASA, DASA, and HASA, respectively8,22 (Figure 3). To measure the VASA and DASA, a line was drawn on the aforementioned horizontal pelvic axis. The VASA was then measured between the horizontal pelvic axis and a line that extended ventrally from the center of the femoral head to the lateral edge of the acetabular rim. The DASA was measured between a line that extended dorsally from the center of the femoral head to the lateral edge of the acetabular rim and horizontal pelvic axis. The HASA was measured between the ventral line of the VASA and dorsal line of the DASA.
HTEA—The HTEA is used to evaluate the lateral slope of the acetabular roof.22,23 The angle was measured between a line that extended from the medial edge of the sourcil to the lateral edge of the dorsal acetabular rim and a line that extended laterally from the medial edge of the sourcil parallel to the horizontal pelvic axis (Figure 4). The sourcil is a curved area of dense bone on the weight-bearing surface of the acetabulum, and it is recognized by its sclerotic, arched appearance that resembles an eyebrow.34
AI—The AI is the ratio of acetabular depth to acetabular width multiplied by 100.33 The width was measured on a line drawn between the dorsolateral and ventrolateral points of the acetabulum, and the depth was measured from the medial edge of the sourcil to the width line (Figure 4).
CPC—The CPC is the ratio of width of the dorsal acetabular shelf to width of the femoral head. It was measured on 2-D CT images, with 3 vertical lines drawn perpendicular to the horizontal pelvic axis (Figure 4). The first line passed along the medial edge of the acetabulum, the second along the lateral edge of the acetabulum, and the third along the lateral edge of the femoral head. The ratio of the distance between the first and second and first and third lines was multiplied by 100 to yield the CPC.
3-D CT images—Measurements were performed on SCT and TCT images to assess the ratio of the exposed femoral head to the acetabular shelf (Figure 5). The distance between the dorsolateral edge of the acetabulum to the most lateral edge of the femoral head was divided by the distance between the ilium and dorsolateral edge of the acetabulum at the same level. Ratios were multiplied by 100 to yield femoral head–acetabular shelf percentages for the SCT and TCT.
Histologic examination—Dogs were euthanized immediately after radiography and CT by IV administration of sodium pentobarbitalh (200 mg/kg). Hip joints were harvested from each dog, and sections for light microscopy were prepared from the joint used for the radiography and CT measurements. Femoral heads and corresponding acetabulae were sectioned in a coronal plane at the level of the ligamentum teres by use of a precision saw with a diamond wafering bladei (Figure 6). Sections were fixed in neutral-buffered 10% formalin and decalcified in citric-buffered formic acid. Sections were embedded in paraffin, and 6-Mm-thick sections were then stained with H&E and safranin-O. Stained sections were viewed with light microscopy and graded by use of a revised Mankin scoring method35,36 (Appendix). Evaluations were based on histologic changes in 6 categories (structure of articular cartilage, uptake of safranin-O stain, number of chondrocyte clones, extent of fibrocartilage, number of osteophytes, and condition of subchondral bone). Investigators were not aware of radiographic or CT measurements. Mean scores for each femoral head and corresponding acetabulum were used for statistical analyses. Acetabular and femoral head scores were combined to yield a single score for each hip joint.
Statistical analysis—The mean, SEM, median, and range for all measurements were calculated. Relationships of OFA confirmation and PennHIP osteoarthritis scores with radiography, CT, and cartilage variables were evaluated with Spearman rank correlations. Relationships of cartilage scores with radiography and CT measurements were also evaluated with Spearman rank correlations. The Pearson correlation was used to assess relationships of DI with radiography, CT, and cartilage variables. Histologic scores for the femoral head and acetabulum were compared by use of least-squares linear regression. Analyses were performed with commercially available software programs.j,k For all analyses, values of P < 0.05 were considered significant. Results were reported as mean ± SEM.
Results
Twelve hip joints were included in the study. Five joints had no osteoarthritis, 2 had mild osteoarthritis, 2 had moderate osteoarthritis, and 3 had severe osteoarthritis on the basis of PennHIP osteoarthritis scores. Four joints had no disease, 3 joints had mild disease, 3 joints had moderate disease, and 2 joints had severe disease on the basis of OFA grades. Mean ± SEM DI score for all hip joints was 0.75 ± 0.09 (range, 0.48 to 1.25; Table 1). Ranges for CT and radiography measurements for each dog were consistent with ranges for DI and radiographically evident joint disease scores.
Mean ± SEM values for radiographic and microstructur-al osteoarthritis scores as well as radiography and CT measurements in adult mixed-breed hounds with laxity of the hip joints
Variable | Mean ± SEM | Range |
---|---|---|
PennHIP osteoarthritis score | 1.25 ± 0.37 | 0 – 3.00 |
OFA confirmation score | 1.25 ± 0.33 | 0 – 3.00 |
Cartilage score | 11.80 ± 2.92 | 1.00 – 34.00 |
DI | 0.75 ± 0.09 | 0.48 – 1.25 |
NA (0) | 97.20 ± 4.65 | 59.30 – 113.00 |
RPC (%) | 42.3 ± 0.07 | 0 – 63.00 |
CEA (0) | -11.96 ± 6.86 | –62.20 – 5.23 |
HTEA (0) | 32.70 ± 8.08 | 11.40 – 83.90 |
VASA (0) | 49.4 ± 3.18 | 27.6 – 61.2 |
DASA (0) | 75.9 ± 6.13 | 28.2 – 91.4 |
HASA (0) | 125.0 ± 6.5 | 88.1 – 144.0 |
AI | 26.10 ± 2.58 | 11.10 – 35.30 |
CPC (%) | 46.90 ± 8.25 | 6.78 – 94.10 |
Femoral head–acetabular shelf percentage for SCT (%) | 0.57 ± 0.08 | 0.30 – 1.00 |
Femoral head–acetabular shelf percentage for TCT (%) | 0.75 ± 0.06 | 0.48 – 0.99 |
A strong linear correlation (r2 = 0.73; P < 0.001) was detected between femoral and acetabular cartilage scores. The PennHIP osteoarthritis score had significant positive correlations with cartilage score, HTEA, and femoral head–acetabular shelf percentage on TCT (r, 0.70 to 0.92), whereas it had significant negative correlations with CEA, DASA, AI, and CPC (r, −0.71 to −0.92; Table 2). The OFA confirmation score had significant positive correlations with cartilage score, HTEA, and femoral head–acetabular shelf percentage on TCT (r, 0.79 to 0.97) and significant negative correlations with NA, RPC, CEA, DASA, AI, and CPC (r, −0.60 to −0.88). Significant positive correlations were evident between cartilage score, HTEA, and femoral head–acetabular shelf percentage on TCT (r, 0.76 to 0.92), whereas significant negative correlations were evident between cartilage score and NA, RPC, CEA, DASA, HASA, and AI (r, −0.73 to −0.91). The DI was significantly and positively correlated with cartilage score and HTEA (r, 0.65 to 0.81), whereas it was significantly and negatively correlated with CEA, DASA, HASA, AI, and CPC (r, −0.72 to −0.81).
Correlation coefficients of osteoarthritis and DI scores with cartilage scores as well as with CT and radiography measurements in adult mixed-breed hounds with laxity of the hip joints.
Variable | PennHIP osteoarthritis score Spearman | OFA confirmation score Spearman | Cartilage score Spearman | DI Pearson | ||||
---|---|---|---|---|---|---|---|---|
r | P | r | P | r | P | r | P | |
Cartilage score | 0.89 | < 0.001 | 0.79 | 0.004 | — | — | 0.65 | 0.030 |
NA | –0.47 | 0.120 | –0.60 | 0.040 | –0.73 | 0.010 | –0.47 | 0.120 |
RPC | –0.42 | 0.180 | –0.62 | 0.030 | –0.80 | 0.003 | –0.55 | 0.070 |
CEA | –0.80 | 0.006 | –0.87 | 0.001 | –0.89 | 0.001 | –0.78 | 0.008 |
HTEA | 0.92 | < 0.001 | 0.97 | < 0.001 | 0.92 | < 0.001 | 0.81 | 0.005 |
VASA | 0.34 | 0.340 | 0.34 | 0.330 | –0.37 | 0.320 | –0.04 | 0.910 |
DASA | –0.92 | < 0.001 | –0.88 | < 0.001 | –0.91 | < 0.001 | –0.77 | 0.010 |
HASA | –0.64 | 0.050 | –0.59 | 0.070 | –0.77 | 0.010 | –0.75 | 0.010 |
AI | –0.83 | 0.003 | –0.88 | < 0.001 | –0.82 | 0.007 | –0.81 | 0.005 |
CPC | –0.71 | 0.020 | –0.84 | 0.002 | –0.61 | 0.080 | –0.72 | 0.020 |
Femoral head–acetabular shelf percentage for SCT | –0.05 | 0.900 | 0.03 | 0.930 | 0.40 | 0.290 | 0.19 | 0.600 |
Femoral head–acetabular shelf percentage for TCT | 0.70 | 0.030 | 0.80 | 0.010 | 0.76 | 0.020 | 0.44 | 0.200 |
Discussion
Hip dysplasia in dogs has been a focus of research in pelvic imaging for a number of years.5,6,29,30,33,37,38 Computed tomography of the pelvis is routinely used for diagnosis, prognosis, and treatment of DDH in humans, but it has had limited application in dogs for the same purposes with regard to HD.19–23 Results of studies8,10,11,31 support the advantages of CT over standard radiography to assess early joint conformational changes characteristic of DDH in humans and HD in dogs. Despite major technologic advances, assessment of joint surface changes remains limited with either modality.16–18,21 Therefore, standardized measurements designed to quantify conformational changes are used to predict whether there is disease of the hip joints and progression of disease characteristic of HD on radiographic and CT images.8,10,11,23-25,30,33 Results of the study reported here supported the use of measurements obtained from both 2- and 3-D CT images of canine hip joints in a standard extended-hip position in combination with established procedures to predict microstructural changes in articular cartilage characteristic of HD.
The acetabular labrum plays an important role in mechanical stability and lubrication of the hip joint.21 There is a high frequency of acetabular labral tears in the period preceding disease or the early stages of osteoarthritis in humans with HD.21 Cartilage degeneration generally originates in the dorsocranial weightbearing region of the femoral head and acetabulum in dogs.4 Measurements that correlated most highly with cartilage degeneration in the study reported here were the CEA, HTEA, and DASA, which is consistent with information known about progression of hip joint disease. The range of CEA values in this study reflected the laxity of the hip joints in the dogs; the value for CEA was negative when the femoral head was lateral to the bony acetabulum, whereas it was positive when the femoral head was within the acetabulum. The CEA is a fairly sensitive indicator of DDH, and it decreases drastically as disease progresses.39 Humans whose hip joints are affected by DDH have higher HTEA values than do humans with normal hip joints because of insufficient coverage of the femoral head by the acetabulum,33 which is similar to the degenerative changes characteristic of HD in dogs illustrated by the results of our investigation. Similarly, DASA and AI values are decreased relative to reference values in human patients with HD,33 which are also consistent with the findings for the dogs reported here. The significant but less pronounced correlation between HASA and cartilage score was likely attributable to the poor correlation of the VASA with cartilage damage because HASA is the sum of both angles. The strong correlation between 2-D measurements with the PennHIP osteoarthritis score, OFA confirmation score, and DI further indicated their potential to provide an additional amount of information about health of hip joints in dogs.
The PennHIP osteoarthritis score had the strongest correlation with cartilage score of the radiographic scoring systems, with a correlation coefficient within the top 3 of all outcome measures evaluated. Notably, both radiographic scoring systems evaluated in this study had good correlations with cartilage changes. This was not surprising because both systems are designed to detect subtle joint changes characteristic of osteoarthritis through comprehensive evaluations of joint congruity and conformation as well as bony changes. Results of another report40 support a combination of radiographic measures to predict macroscopic cartilage lesions in young dogs. In the study reported here, CEA, HTEA, and DASA measurements on 2-D CT images and PennHIP radiographic osteoarthritis score were the best predictors of cartilage degeneration. It is possible that a combination of measurements may provide the best representation of the condition of the articular surface in the hip joints of dogs.
The fact that lower NA and RPC corresponded strongly with poorer OFA confirmation and greater microstructural changes in this study is consistent with results of other reports,12,30,37,40 although microstructural changes were not included in those earlier investigations. An NA ≥ 105° and RPC ≥ 50% are considered to indicate normal hip joint confirmation, but the cutoff values are not applicable to all breeds of dogs.30 The wide range of NA and RPC values in our study included values within and outside of the reference ranges for most midsize dog breeds.30 Lack of correlation of the RPC with DI in our study was not necessarily unexpected because DI was measured on distraction radiographs, whereas RPC was not.29,30 Lack of correlation between NA measurements with DI and PennHIP osteoarthritis scores contrasts with results of another study28 in which there was a good correlation in similarly aged dogs. Differences in study populations and designs as well as the methods used complicate direct comparisons among studies.
Measurements on 3-D CT images to evaluate hip joints of dogs is a relatively new concept, although it is established for use in human patients.19–23 Three-dimensional imaging provides information that is unavailable on 2-D images, including, but not limited to, joint congruency as well as acetabular and femoral shape.31 The femoral head–acetabular shelf percentage for TCT had strong positive correlations with articular cartilage damage, PennHIP osteoarthritis scores, and OFA confirmation scores in the study reported here. Given that the femoral head–acetabular shelf percentage for TCT is a measurement of dorsal femoral head coverage similar to the CEA, HTEA, and DASA, this result was not surprising. The advantages of 3-D imaging for purposes of preoperative planning and assessment of complex DDH have been established,19–23 and it is possible that the same may be true for canine patients. The strong correlation of the femoral head–acetabular shelf percentage for TCT with articular cartilage damage supports the use of this measure to predict articular cartilage damage; however, the additional step necessary to generate and measure the femoral head–acetabular shelf percentage for TCT may not necessarily be warranted in all cases.
A homogenous canine population was selected for this study to assess the relationship between the outcome measures selected. The DI range included was consistent with a moderate to high likelihood that the dogs would have degenerative joint changes characteristic of HD.12 Images were obtained from dogs of the same age to limit potential age effects and to increase the potential that dogs in the study population would have a wide range of degenerative changes, rather than advanced disease in all joints. Fulfillment of this objective was supported by the fact that radiographic and microstructural evidence of joint disease ranged from unaffected to severely affected. Although the study population was selected for purposes of specific evaluation, it was not necessarily representative of all dog breeds. Additionally, prognostic value of specific radiographic measurements varies among breeds of dog and on the basis of age.5,38 It is possible that the correlations between the measurements used in this study and microstructural articular cartilage changes may vary among dog breeds. Validation steps will be necessary to confirm the relationships in a heterogenous population of dogs.
Computed tomography for evaluation of hip joints in dogs has been reported, with images obtained with the hind limbs in a typical standing position with or without weight-bearing forces. Dogs were placed in a standard hip-extended position for the study reported here to permit measurements routinely performed on CT images of hip joints of humans. Extensive research within the field of CT imaging of human hip joints22,23 has permitted the determination of sex-specific cutoff values for the measurements described for the dogs of our study. Additional studies will be necessary to determine similar values for dogs with consideration given to sexand breed-specific differences.
A number of techniques to assess the condition of articular cartilage have been described for dogs and humans. Arthroscopy, magnetic resonance imaging, and synovial fluid markers of osteoarthritis reportedly are potential diagnostic tools with which to assess early degenerative joint disease that is not radiographically evident.41–43 In 1 study,42 moderate articular cartilage lesions were detected during arthroscopy in hip joints without radiographic evidence of joint disease. Synovial fluid markers of osteoarthritis have been used in dogs and humans as a fairly sensitive mechanism by which to assess changes in articular cartilage.41 Magnetic resonance imaging is considered an accurate method to assess pathologic changes within the acetabular labrum and adjacent acetabular articular cartilage in humans with HD.43 It is possible that this imaging modality will be useful for the same application in canine patients. Advances in imaging and molecular methods to assess joint disease continue to provide additional information about a condition shared by numerous species.
Osteoarthritis of the hip joints is chronic and progressive, and it is typically diagnosed in relatively advanced stages when clinical and radiographic signs become evident. Methods to predict the condition of articular cartilage and disease progression will substantially enhance therapeutic options for affected animals by permitting early initiation of treatment. For research purposes, accurate methods to monitor disease progression at the microstructural level may reduce the number of required tissue harvests and facilitate assessment of therapeutic interventions. Additionally, the measurements assessed in the study reported here may provide an additional mechanism to elucidate the complex pathophysiologic processes of HD in dogs. Computed tomographic imaging is an imaging modality that may result in new standards by which hip joints of dogs are evaluated.
ABBREVIATIONS
HD | Hip dysplasia |
DDH | Developmental dysplasia of the hip |
2-D | Two-dimensional |
3-D | Three-dimensional |
CT | Computed tomography |
DI | Distraction index |
NA | Norberg angle |
RPC | Radiographic percentage of femoral head coverage |
OFA | Orthopedic Foundation for Animals |
CEA | Center-edge angle |
VASA | Ventral acetabular sector angle |
DASA | Dorsal acetabular sector angle |
HASA | Horizontal acetabular sector angle |
HTEA | Horizontal toit externe angle |
AI | Acetabular index |
SCT | Sagittal 3-dimensional computed tomography |
TCT | Transverse 3-dimensional computed to-mography |
CPC | Computed tomography percentage femoral head coverage |
PennHIP, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pa.
Orthopedic Foundation for Animals, Columbia, Mo.
GE Hilight Advantage, General Electric Medical Systems, Milwaukee, Wis.
DC-502A, Pioneer Communications of America Inc, Upper Saddle River, NJ.
Sun Sparc 10, Sun Microsystems Inc, Santa Clara, Calif.
Agfa HiD dual-bed flatbed scanner, Agfa Corp, Wilmington, Mass.
Adobe Photoshop, version 5.5, Adobe Systems Inc, Seattle, Wash.
Beuthanasia-D Special, Schering-Plough Animal Health, Union, NJ.
Model 11-2480 Isomet, Buelher Ltd, Lake Bluff, Ill.
SAS, version 8.2, SAS Institute Inc, Cary, NC.
GraphPad Prism, version 3.0, GraphPad Software Inc, San Diego, Calif.
References
- 1.
Endo H, Mitani S, Senda M, et al. Three-dimensional gait analysis of adults with hip dysplasia after rotational acetabular osteotomy. J Orthop Sci 2003;8:762–771.
- 2.↑
Pedersen EN, Simonsen EB, Alkjaer T, et al. Walking pattern in adults with congenital hip dysplasia: 14 women examined by inverse dynamics. Acta Orthop Scand 2004;75:2–9.
- 3.
Powers MY, Biery DN, Lawler DE, et al. Use of the caudolateral curvilinear osteophyte as an early marker for future development of osteoarthritis associated with hip dysplasia in dogs. J Am Vet Med Assoc 2004;225:233–237.
- 4.↑
Riser WH. The dog as a model for the study of hip dysplasia. Growth, form, and development of the normal and dysplastic hip joint. Vet Pathol 1975;12:234–334.
- 5.
Smith GK. Advances in diagnosing canine hip dysplasia. J Am Vet Med Assoc 1997;210:1451–1457.
- 6.
Lust G, Rendano VT, Summers BA. Canine hip dysplasia: concepts and diagnosis. J Am Vet Med Assoc 1985;187:638–640.
- 7.
Novacheck TF. Developmental dysplasia of the hip. Pediatr Clin North Am 1996;43:829–848.
- 8.
Anda S, Terjesen T, Kvistad KA, et al. Acetabular angles and femoral anteversion in dysplastic hips in adults: CT investigation. J Comput Assist Tomogr 1991;15:115–120.
- 9.
Anda S, Terjesen T, Kvistad KA. Computed tomography measurements of the acetabulum in adult dysplastic hips: which level is appropriate? Skeletal Radiol 1991;20:267–271.
- 10.
Dueland RT, Adams WM, Fialkowski JP, et al. Effects of pubic symphysiodesis in dysplastic puppies. Vet Surg 2001;30:201–217.
- 11.
Patricelli AJ, Dueland RT, Lu Y, et al. Canine pubic symphysiodesis: investigation of electrocautery dose response by histologic examination and temperature measurement. Vet Surg 2001;30:261–268.
- 12.↑
Puerto DA, Smith GK, Gregor TP, et al. Relationships between results of the Ortolani method of hip joint palpation and distraction index, Norberg angle, and hip score in dogs. J Am Vet Med Assoc 1999;214:497–501.
- 13.
Todhunter RJ, Casella G, Bliss SP, et al. Power of a Labrador Retriever-Greyhound pedigree for linkage analysis of hip dysplasia and osteoarthritis. Am J Vet Res 2003;64:418–424.
- 14.
Fujita Y, Hara Y, Nezu Y, et al. Direct and indirect markers of cartilage metabolism in synovial fluid obtained from dogs with hip dysplasia and correlation with clinical and radiographic variables. Am J Vet Res 2005;66:2028–2033.
- 15.
Todhunter RJ, Bertram JE, Smith S, et al. Effect of dorsal hip loading, sedation, and general anesthesia on the dorsolateral subluxation score in dogs. Vet Surg 2003;32:196–205.
- 16.
Miosge N, Hartmann M, Maelicke C, et al. Expression of collagen type I and type II in consecutive stages of human osteoarthritis. Histochem Cell Biol 2004;122:229–236.
- 17.
Messner K, Fahlgren A, Persliden J, et al. Radiographic joint space narrowing and histologic changes in a rabbit meniscectomy model of early knee osteoarthrosis. Am J Sports Med 2001;29:151–160.
- 18.
Lorenz H, Richter W. Osteoarthritis: cellular and molecular changes in degenerating cartilage. Prog Histochem Cytochem 2006;40:135–163.
- 19.
Lattanzi R, Baruffaldi F, Zannoni C, et al. Specialised CT scan protocols for 3-D pre-operative planning of total hip replacement. Med Eng Phys 2004;26:237–245.
- 20.
Nishii T, Sugano N, Sato Y, et al. Three-dimensional distribution of acetabular cartilage thickness in patients with hip dysplasia: a fully automated computational analysis of MR imaging. Osteoarthritis Cartilage 2004;12:650–657.
- 21.↑
Nishii T, Tanaka H, Sugano N, et al. Disorders of acetabular labrum and articular cartilage in hip dysplasia: evaluation using isotropic high-resolutional CT arthrography with sequential radial reformation. Osteoarthritis Cartilage 2007;15:251–257.
- 22.↑
Tallroth K, Lepisto J. Computed tomography measurement of acetabular dimensions: normal values for correction of dysplasia. Acta Orthop 2006;77:598–602.
- 23.
Lin CJ, Romanus B, Sutherland DH, et al. Three-dimensional characteristics of cartilaginous and bony components of dysplastic hips in children: three-dimensional computed tomography quantitative analysis. J Pediatr Orthop 1997;17:152–157.
- 24.
Peterson HA, Klassen RA, McLeod RA, et al. The use of computerised tomography in dislocation of the hip and femoral neck anteversion in children. J Bone Joint Surg Br 1981;63:198–208.
- 25.
Weiner LS, Kelley MA, Ulin RI, et al. Development of the acetabulum and hip: computed tomography analysis of the axial plane. J Pediatr Orthop 1993;13:421–425.
- 26.
Farese JP, Todhunter RJ, Lust G, et al. Dorsolateral subluxation of hip joints in dogs measured in a weight-bearing position with radiography and computed tomography. Vet Surg 1998;27:393–405.
- 27.
Fujiki M, Misumi K, Sakamoto H. Laxity of canine hip joint in two positions with computed tomography. J Vet Med Sci 2004;66:1003–1006.
- 28.↑
Smith GK, Biery DN, Gregor TP. New concepts of coxofemoral joint stability and the development of a clinical stress-radiographic method for quantitating hip joint laxity in the dog. J Am Vet Med Assoc 1990;196:59–70.
- 29.↑
Smith GK, Gregor TP, Rhodes WH, et al. Coxofemoral joint laxity from distraction radiography and its contemporaneous and prospective correlation with laxity, subjective score, and evidence of degenerative joint disease from conventional hipextended radiography in dogs. Am J Vet Res 1993;54:1021–1042.
- 30.↑
Tomlinson JL, Johnson JC. Quantification of measurement of femoral head coverage and Norberg angle within and among four breeds of dogs. Am J Vet Res 2000;61:1492–1500.
- 31.↑
Roach JW, Hobatho MC, Baker KJ, et al. Three-dimensional computer analysis of complex acetabular insufficiency. J Pediatr Orthop 1997;17:158–164.
- 32.
Smith GK, Mayhew PD, Kapatkin AS, et al. 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 2001;219:1719–1724.
- 33.↑
Delaunay S, Dussault RG, Kaplan PA, et al. Radiographic measurements of dysplastic adult hips. Skeletal Radiol 1997;26:75–81.
- 34.↑
Kim HT, Kim JI, Yoo CI. Diagnosing childhood acetabular dysplasia using the lateral margin of the sourcil. J Pediatr Orthop 2000;20:709–717.
- 35.
Edinger DT, Hayashi K, Hongyu Y, et al. Histomorphometric analysis of the proximal portion of the femur in dogs with osteoarthritis. Am J Vet Res 2000;61:1267–1272.
- 36.
Edinger DT, Hayashi K, Hongyu Y, et al. Histomorphometric analysis of the proximal portion of the femur in healthy dogs. Am J Vet Res 2000;61:268–274.
- 37.
Lust G, Todhunter RJ, Erb HN, et al. Comparison of three radiographic methods for diagnosis of hip dysplasia in eight-monthold dogs. J Am Vet Med Assoc 2001;219:1242–1246.
- 38.
Smith GK, Hill CM, Gregor TP, et al. Reliability of the hip distraction index in two-month-old German shepherd dogs. J Am Vet Med Assoc 1998;212:1560–1563.
- 39.↑
Murphy SB, Ganz R, Muller ME. The prognosis in untreated dysplasia of the hip. A study of radiographic factors that predict the outcome. J Bone Joint Surg Am 1995;77:985–989.
- 40.↑
Todhunter RJ, Grohn YT, Bliss SP, et al. Evaluation of multiple radiographic predictors of cartilage lesions in the hip joints of eight-month-old dogs. Am J Vet Res 2003;64:1472–1478.
- 41.↑
Chu Q, Lopez M, Hayashi K, et al. Elevation of a collagenase generated type II collagen neoepitope and proteoglycan epitopes in synovial fluid following induction of joint instability in the dog. Osteoarthritis Cartilage 2002;10:662–669.
- 42.↑
Holsworth IG, Schulz KS, Kass PH, et al. Comparison of arthroscopic and radiographic abnormalities in the hip joints of juvenile dogs with hip dysplasia. J Am Vet Med Assoc 2005;227:1087–1094.
- 43.↑
James S, Miocevic M, Malara F, et al. MR imaging findings of acetabular dysplasia in adults. Skeletal Radiol 2006;35:378–384.
Appendix
Scoring system used for histologic examination of articular cartilage.
Variable | Score | Description |
---|---|---|
Structure of cartilage | 0 | No abnormalities |
1 | Surface irregularities | |
2 | Pannus and surface irregularities | |
3 | Clefts from surface to transitional zone and superficial disorganization; loss of boundary between tangential and transitional zones | |
4 | Clefts from surface to radial zone with or without disorganization of radial zone and with or without loss of superficial layers | |
5 | Progression of loss of cartilage into radial zone with or without clefts to radial zone or the mineralized zone | |
6 | Cartilage eroded down to the mineralized zone | |
Cells | 0 | Typical number |
1 | Diffuse hypercellularity | |
2 | Cloning | |
3 | Hypocellularity | |
4 | Severe hypocellularity and cartilage loss | |
Staining | 0 | Typical |
1 | Slight reduction in staining with or without reduction of staining in radial zone | |
2 | Moderate reduction in staining with or without reduction in interterritorial matrix | |
3 | Staining only in pericellular matrix | |
4 | Staining not evident with or without occasional rim of staining in pericellular matrix | |
5 | Staining not evident and severe cartilage loss | |
Integrity of mineralized zone | 0 | Intact |
1 | Crossed by blood vessels | |
2 | Tidemark not evident and severe cartilage loss |