Radiographic and ultrasonographic diagnostic imaging of feet is performed routinely now on lame horses, and many conditions can be identified with these imaging modalities.1–5 However, when DIP-PDJD (a chronic condition characterized by slow onset, gradual cartilage degeneration, and reactive changes in the joint margins not secondary to a major conformational defect, acute trauma, infection, or developmental locomotor disease related to the DIPJ1,6) is diagnosed or suspected, evaluation of articular cartilage status remains a difficult task. Radiographic evidence of DIP-PDJD is frequently limited and generally only observed in the most advanced and severe cases.1,6 Ultrasonographic assessment of DIPJ articular cartilage can be performed in a non–weight-bearing limb by placing the joint in flexion; however, only the most dorsal and proximal aspects of the articular surface of the MP are visible.7 High-field MRI and CT arthrography are the best available noninvasive modalities for cartilage imaging in horses8–11; however, these techniques are only performed on anesthetized horses. The diagnostic value of low-field MRI to evaluate DIPJ cartilage has been studied mainly in isolated limbs of cadavers or on limbs of anesthetized horses.12,13 The diagnostic usefulness of standing low-field MRI for DIPJ cartilage injuries in horses is still questionable.14
The purposes of the study reported here were to report history, findings from clinical examinations and diagnostic imaging, treatment, and outcomes associated with DIP-PDJD in horses and to evaluate diagnostic usefulness and limitations of standing low-field MRI, relative to radiography and ultrasonography, for diagnosis of DIP-PDJD in horses.
Materials and Methods
Case selection
Medical records of horses that had been examined and underwent standing low-field MRI at the CIRALE because of lameness involving 1 or both front feet between January 2010 and January 2014 were reviewed. The criteria for inclusion were availability of complete clinical history and examination results, comprehensive radiographic and ultrasonographic examination of the affected foot or feet prior to MRI, and DIP-PDJD diagnosed as the cause of lameness on the basis of findings from clinical examination and diagnostic imaging. Horses with degenerative joint disease secondary to a major conformational defect, acute trauma, infection, or developmental locomotor disease related to the DIPJ were not included.
Data collection
Data collected from the records of each horse included age, breed, sex, work discipline, history, severity and duration of lameness, results of physical and lameness examinations, response to diagnostic anesthesia, findings from diagnostic imaging, management, and outcome. Long-term follow-up information was obtained through reassessment of horses; communication with owners, trainers, or referring veterinarians; and consultation of official websites that provided results of sport and racing competitions in which included horses participated.
Examination protocol
Each horse underwent a complete and detailed clinical examination. The degree of lameness was graded from 0 to 5 in accordance with the lameness scale of the American Association of Equine Practitioners.15 In addition to diagnostic images obtained of the lame or lamer forefoot, comparative images of the contralateral foot were systematically acquired with the same diagnostic imaging modalities.
Radiographic examination of the lame or lamer forefoot included D60°Pr-PaDiO, lateromedial, weight-bearing dorsopalmar, and palmaroproximalpalmarodistal oblique views.1 The D60°Pr-PaDiO view was performed with a horizontal radiographic beam and the foot placed on a wooden block with a 60° slope.16,17 Care was taken to place limbs perpendicular to the ground for dorsopalmar weight-bearing views to avoid artifactual lateromedial imbalance and associated joint space narrowing.18
Ultrasonographic examinations of feet were conducted with dorsal, medial, lateral, and distal approaches to the DIPJ.2–4,7 When feasible, transcuneal images that were dedicated mainly to the infrasesamoidean region were acquired.5
A standing low-field (0.27 T) MRI systema was used for image acquisition. Our standard protocol for foot image sequences (Appendix) included T1W GRE 3-D TRA and T2W TRA FSE perpendicular to the suprasesamoidean region of the DDFT, T2W 3-D FRO HR perpendicular to the infrasesamoidean portion of the DDFT, STIR FSE SAG, T1W GRE 3-D TRA HR perpendicular to the flexor surface of the DSB, and T1W GRE 3-D FRO HR parallel to the suprasesamoidean region of the DDFT. Other sequences were added depending on clinical abnormalities, routine imaging findings, and standard MRI protocol results. In horses with suspected or diagnosed DIP-PDJD, additional sequences included at least a STIR GRE TRA perpendicular to the suprasesamoidean region of the DDFT and a T1W GRE 3-D SAG HR.
Statistical analysis
Abnormal findings from diagnostic imaging were recorded for the DIPJ articular cartilage and space, periarticular margins and soft tissues, dorsal proliferations of the MP, and subchondral and trabecular bone of the MP, DP, and DSB. Abnormal findings were graded on a scale from 1 to 3, with 1 = mild, 2 = moderate, and 3 = severe (Supplementary Table S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.254.2.257). The criteria used in the grading system were adapted from a previous study.19
All images were reviewed separately by individuals (TR and FA) blinded to the identity of the horses, and mean grade was calculated for each parameter. Data were evaluated for normality with a Shapiro-Wilk analysis. For all horses, normally distributed data were analyzed with the Student t test to compare mean grade of joint space narrowing evident by radiography versus MRI, mean grade of periarticular bone remodeling and osteophytes evident by radiography and ultrasonography versus MRI, and mean grade of subchondral and trabecular bone abnormalities between the MP, DP, and DSB evident by MRI. Statistical analyses were performed with available software,b and values of P < 0.05 were considered significant.
Results
Animals
Between January 2010 and January 2014, 176 horses were referred to the CIRALE with a foot-related condition as the main cause of a locomotor disorder. Among these 176 horses, a diagnosis of DIP-PDJD was established for 12 (6.8%), including 6 mares, 4 stallions, and 2 geldings. Mean ± SD age was 8.2 ± 2.7 years (range, 3.0 to 12.5 years), and breeds included French warmblood (n = 7), Belgian warmblood (1), French Trotter (1), Hanoverian (1), Holsteiner (1), and Zangersheide (1). Horses were mainly show jumpers (n = 10), with 1 dressage horse and 1 racing trotter. Before onset of lameness, all horses had been trained in their respective activity. Mean duration of lameness was 7 months (range, 1 week to 32 months). All horses had a unilateral forelimb lameness (left, n = 7; right, 5) associated with unilateral DIP-PDJD.
Before referral, DIPJ arthropathy was unsuspected in 8 horses. Nine of the 12 horses had been restricted to rest, 2 horses had reduced activity on the flat track or exercise pen, and 1 horse had unrestricted activity. Eight horses were known to have received intra-articular corticosteroid injections (mean, 1.5 injections; range 1 to 3 injections) into the DIPJ of the lame limb and had temporary improvement in lameness; however, no horse had received a DIPJ injection in the 6 months immediately before referral.
Clinical examination results
All 12 horses had forefoot-related abnormalities or mild conformational defects, including foot atrophy (ie, the affected foot was smaller, contracted, and more upright in comparison with the contralateral foot; n = 7), dorsosagittal soft tissue thickening just proximal to the coronary band (7), toed in (3), digital varus (3), or positive results on a DIPJ extension test (2). On initial examination at the CIRALE, the most frequent lameness grade was 3 (n = 7; range, 2 to 4) on a scale from 0 to 5. The severity of lameness for 7 horses was exacerbated by exercising the affected horse on a lunge line on hard ground with the lame limb on the inside of the circle. Also on hard ground at a walk and when exercised in a circle at a trot, 7 and 3 horses had reduction in the caudal or cranial phases of their steps, respectively. All digital flexion tests performed on lame limbs had positive results with mild exacerbation of lameness. Flexion tests were not conducted on 2 horses because of the severity of their lameness at a walk. All 12 horses had proper digital nerve blocks (eg, palmar digital nerve blocks) performed, and results were positive with complete resolution of lameness in all horses, 8 by distal digital nerve block, and 4 by proximal digital nerve block. No lameness was observed in the contralateral limbs.
Diagnostic imaging results
Comparative images of the contralateral foot were systematically acquired with the same diagnostic imaging modalities. Prior to each MRI examination, a diagnosis of DIP-PDJD was confirmed at the CIRALE on the basis of radiographic and ultrasonographic findings in 3 horses, suspected in 8, and unsuspected in 1. For these last 9 horses, abnormal findings from MRI examination confirmed DIP-PDJD and excluded other foot-related conditions.
Joint space—From radiographic examinations, mean ± SD grade for DIPJ space thinning was 1.7 ± 0.8 (range, 0 to 3). Ten horses had diffuse and homogeneous thinning of the joint space that was more conspicuous on D60°Pr-PaDiO views, compared with weight-bearing dorsopalmar views. Only 1 horse had an asymmetric narrowing (thinner medially) of the joint space evident on the D60°Pr-PaDiO view of the affected foot. One horse had no narrowing of the joint space.
Articular cartilage—MRI examination revealed that all horses had diffuse thinning of the DIPJ articular cartilage of the MP, DP, or both. Mean ± SD grade for articular cartilage thinning determined from images obtained by MRI was 2.4 ± 0.7 (range, 1 to 3), which was significantly (P = 0.02) greater than the mean ± SD grade for thinning of 1.7 ± 0.8 (range, 0 to 3) determined from radiographic images (Figure 1). Only 1 horse had grade 1 cartilage thinning evident from MRI examination. Homogenous thinning of articular cartilage was present in 8 horses, whereas overall diffuse thinning combined with asymmetric thinning (more pronounced medially than laterally) was observed in the remaining 4 horses (Figure 2). Articular cartilage thinning between the articular surfaces of the DSB and the DP was noticed in only 2 of 12 horses.
Features of MRI examination results associated with cartilage thinning were loss of visible separation of the 2 cartilage layers between the MP and DP for all horses in the study and articular cartilage signal abnormalities (decreased SI on T1W GRE 3-D HR sequences) observed in images obtained from 8 horses. For the nonlame contralateral limbs, however, both cartilage layers were identified clearly on the medial and lateral aspects of the joints on T1W GRE 3-D HR sequences in all horses of the study (Figure 3).
Synovial effusion, periarticular bone remodeling, and osteophytes—None of the horses in the study had alterations in synovial invaginations of the distal articular surface of the DSB evident on images from any of the diagnostic imaging modalities. Four horses had absent to mild (grade 1) synovial effusion, osteophytes, and periarticular bone remodeling evident by all diagnostic imaging modalities. Mean rest period prior to referral was 2.8 months for the 4 horses with absent to mild synovial effusion detected by all diagnostic imaging modalities, compared with 2.1 months for the other 8 horses. These 8 remaining horses had osteophytes and bone remodeling that were moderate (grade 2) to severe (grade 3; mean ± SD grade, 2.4 ± 0.5) when determined from radiographic and ultrasonographic images, compared with mild (grade 1) to moderate (grade 2; mean ± SD grade, 1.3 ± 0.6) when determined from images obtained by MRI. For these 8 horses, the mean ± SD grade of synovial effusion was not significantly (P = 0.127) different when determined from radiographic and ultrasonographic images (1.6 ± 0.8; range, 1 to 3) than when determined from images obtained by MRI (1.7 ± 0.8; range, 1 to 3). For all 12 horses, the mean ± SD grade of osteophytes and periarticular bone remodeling was significantly (P = 0.03) greater when determined from radiographic and ultrasonographic images (1.8 ± 1.1) than when determined from images obtained by MRI (1.1 ± 0.7; Figure 4).
Subchondral and trabecular bone—In 11 horses, no signs of increased bone opacity was evident on images obtained by radiography or MRI. However, the remaining horse did have radiographic and MRI evidence of increased opacity of trabecular bone on the medial and proximal aspects of the DP (Figure 2).
Results from STIR sequences indicated that 8 horses had an increased SI of the spongiosa of the bones related to the DIPJ, with at least 2 of the 3 bones affected. The DSB was always affected, whereas the MP and the DP were affected in 5 and 4 horses, respectively. In 5 of these 8 horses that had either the MP (n = 3) or the DP (2) involved, signal abnormalities of the DSB were more pronounced close to the articular (dorsal) aspect, compared with the palmar aspect (Figure 5). The STIR signal abnormalities of the MP were more frequently localized distodorsally around the SAG of the MP, whereas signal abnormalities of the DP varied (diffuse [n = 2] or localized either in the extensor process [1] or in the glenoid cavity [dorsomedial aspect, 1; palmaromedial aspect, 1; or palmarosagittal aspect 1] alone or in combination). Mean ± SD MRI grades of subchondral and trabecular bone abnormalities were not significantly (P > 0.08) different between the DSB (1.8 ± 1.2), the MP (1.7 ± 0.8), and the DP (1.6 ± 1.1).
Collateral ligaments—Seven horses had mild thickening of 1 of the collateral ligaments of the DIPJ with mild heterogeneous echogenicity and SI evident on images obtained by MRI. The lateral collateral ligament was affected in 4 horses, and the medial collateral ligament was affected in 3 horses (Figure 2).
Management
Management included corrective shoeing of both forefeet with commercially available shoesc that provided wide cover, onion heels, and a bevel covering all of the outer rim of the shoe; administration of tiludronate disodium as a regional distal limb perfusion (0.1 mg/kg [0.045 mg/lb]) or IV (1 mg/kg [0.45 mg/lb]); and intra-articular injections of interleukin 1 receptor antagonist protein (2 to 4 mL/joint) or sodium hyaluronan (2 to 4 mL/joint) alone, or in combination. The proportion of horses receiving each of these treatments was not known. Corticosteroid injections in the DIPJ were discouraged and such injections were not known to have been given by the referring veterinarian after the examination at the CIRALE.
Outcome
Follow-up information was available for all 12 horses in the study. Ten horses did not recover and were unable to compete again. Only 2 show jumpers returned to competition, but at a lower level with fewer competitions per year. For these 2 show jumpers, mean number of competitions per year over a 2-year period before the initial episode of lameness was 12.4 competitions per year, compared with 3.1 competitions per year over an approximate 2-year period after the referral.
Discussion
The present study described findings for 12 horses with advanced DIP-PDJD selected from among 176 horses with foot-related locomotor disorders referred to the CIRALE. For each of these 12 horses, the diagnosis of DIP-PDJD was established after considering findings from clinical examination, diagnostic analgesia, and diagnostic imaging, including ruling out other potential causes on the basis of MRI results. Diagnostic nerve blocks were used instead of DIPJ intra-articular analgesia because the former represented less invasive procedures that would not have interfered with MRI examination of the DIPJ. Moreover, intra-articular DIPJ analgesia is not specific to pain arising from the DIPJ as signs of pain arising from the sole and associated soft tissue structures as well as from the navicular region can also be relieved by this procedure.20,21 Results of the present study provided an evaluation of the diagnostic value of standing low-field MRI for the detection of DIP-PDJD and described associated abnormal diagnostic imaging findings. The main limitation was the lack of a gold standard method (eg, postmortem or high-field MRI examinations) for detection of DIP-PDJD in the horses studied. Another limitation was the absence of a repeatability study for the image interpretations by the 2 observers.
Standing low-field MRI systems have a lower spatial resolution, compared with high-field MRI systems that require general anesthesia of patients.9,10 This could explain why only 1 horse in the present study had grade 1 cartilage thinning, whereas the others had more severe thinning (grades 2 and 3). Nevertheless, the present study was useful because most MRI procedures performed on horses are undertaken with standing low-field (0.27 T) units.22 Images from standing MRI are useful to identify joint space narrowing, but because of potential influence by positioning, including by the horse, care must be taken when interpreting lateromedial asymmetrical thinning.9 In our experience, mild abduction of the examined limb frequently induced a medial DIPJ space narrowing with the possibility of differentiating the 2 cartilage layers between the MP and the DP on T1W GRE 3-D HR sequences in sound horses. In contrast, a diffuse thinning with a lack of differentiation of the articular cartilage layers of the MP and the DP on T1W GRE 3-D HR sequences was observed in all horses in which DIP-PDJD was diagnosed in the present study. Whenever possible, it would be useful to confirm such abnormal findings through comparison with the contralateral limb as was done in the present study. These results were consistent with a previous study23 on the appearance of DIPJ articular cartilage in images obtained by MRI of weight-bearing limbs of sound horses. In addition, the asymmetry of cartilage signal abnormalities and cartilage thickness observed between the 2 forelimbs of each horse in the present study was very helpful in creating a more reliable diagnostic study and reducing the risk of over- or underinterpretation of cartilage abnormalities observed.
Because the DIPJ has curved articular surfaces,24–26 the T1W GRE 3-D FRO HR and T1W GRE 3-D SAG HR sequences with thin slices (2 mm) used in the present study for cartilage assessment as high spatial resolution sequences were helpful to minimize partial volume averaging associated with the anatomic conformation of the DIPJ.10,13,27 Moreover, T1W GRE 3-D sequences have been reported as the most accurate low-field pulse sequences for cartilage evaluation.13,14 Cartilage thinning was always identified between the MP and the DP in the present study but was detected between the DSB and the DP in only 2 horses. We hypothesized that the cartilage between the DSB and DP was less frequently affected because of biomechanical reasons.
Following radiographic and ultrasonographic examinations, MRI was useful to diagnose or confirm DIP-PDJD in the present study. Mean ± SD grade for thinning of the joint space or articular cartilage was substantially greater when determined from images obtained by MRI, compared with images obtained radiographically, possibly because MRI allowed for a 3-D representation of the articular cartilage, whereas radiography did not. Moreover, there is a limited ultrasonographic examination window for evaluation of the DIPJ cartilage.
In addition to the diffuse cartilage thinning in affected feet of all horses of the present study, another MRI result associated with DIP-PDJD in these horses was an increased SI in STIR sequences in at least 2 of the 3 bones related to the DIPJ. The DSB was always affected, and STIR signal abnormalities increased toward its articular surface. This result was pertinent to differentiate DIP-PDJD from podotrochlear apparatus–related causes of lameness in which STIR signal abnormalities would have been expected to increase toward the flexor surface of the DSB.8 Increased SI in STIR or fat saturation sequences has been reported as bone marrow edema–like lesions in the human literature,28,29 and this finding has been associated with a myriad of tissue changes. Histologic studies have shown osteonecrosis, osteofibrosis, bone marrow edema, hyperemia, and hemorrhage as the main causes of bone marrow edema–like lesions in both humans28,29 and horses.30,31 Subchondral bone marrow edema has been associated with cartilage loss in human patients with osteoarthrosis.32,33
Increased SI in STIR sequences of bones of the DIPJ has also been reported in association with infection of the DIPJ.34 Differentiation between DIP-PDJD and infection can be challenging on the basis of diagnostic imaging results alone; therefore, the combined results of patient history, clinical signs, and other complementary examinations (eg, synovial fluid analysis) should also be considered.
Synovial effusion is frequently associated with arthropathy of the DIPJ35; however, it represents a nonspecific finding that is not necessarily associated with degenerative changes of the DIPJ.9,36 Although the synovial invaginations of the distal articular surface of the DSB communicate with the DIPJ,37 4 of the 12 horses in the present study had absent to mild synovial effusion and periarticular new bone formation evident by all imaging modalities, and no horse had an increased number or size of synovial invaginations in the distal articular surface of the DSB. These findings were important and indicated that the absence of periarticular remodeling or synovial effusion evident by routine diagnostic imaging did not rule out DIP-PDJD. Nevertheless, the number of such cases may have been overrepresented among the horses studied because the group was comprised of only referral cases, including horses for which routine imaging had been performed and for which DIP-PDJD had not yet been diagnosed. In addition, such findings could have been attributable to previous DIPJ treatments and the extensive rest periods of horses studied. Nevertheless, no horse had received a DIPJ injection in a period of at least 6 months prior to referral, and mean rest period prior to referral was relatively similar for the 4 horses with absent to mild synovial effusion detected by all diagnostic imaging modalities and the remaining 8 horses (2.8 months and 2.1 months, respectively).
The absence of flexed oblique radiographic views was another limitation of the present study. Consequently, the diagnostic value of radiography to diagnose remodeling of the articular margins of the DIPJ was underestimated. Nevertheless, the DIPJ margins were assessed ultrasonographically in all horses, and the grade of osteophytes and periarticular bone remodeling was notably greater when determined from radiographic and ultrasonographic images, compared with when graded from MRI images.
We hypothesized that the collateral ligament alterations noted in 7 horses were consequences of DIP-PDJD, as this condition may lead to incongruity of articular surfaces, joint instability,1 and secondary collateral ligament relaxation. A degenerative joint disease of the DIPJ secondary to a collateral ligament injury or development of a collateral ligament injury concurrently with degenerative joint disease could not be excluded in these horses. However, we judged such unlikely because none of these horses had a history of trauma or collateral ligament injury, there was no evidence on images obtained by any of the diagnostic imaging modalities that a bone abnormality at the ligament's insertion existed, and the heterogeneous signal and echogenicity as well as the thickening of the ligaments were graded as mild and were only present on the side where the joint space was the thinnest.
In the present study, there was a significant difference between mean grade of periarticular osteophytes and new bone formation evident on images obtained with MRI, compared with that evident by ultrasonography and radiography. These changes were underestimated by MRI, compared with ultrasonography and radiography. This may have been a consequence of the lower spatial resolution of standing low-field MRI, compared with the resolution of ultrasonography and radiography. When compared with ultrasonography, another limitation of MRI was its inability to detect with accuracy synovial membrane proliferations and articular debris floating in the synovial cavity.7,38
Results of the present study suggested that DIP-PDJD has a poor prognosis in advanced cases, in that 10 of the 12 horses did not go back to work despite periods of rest. However, other horses with less advanced DIP-PDJD may have a better prognosis.
Acknowledgments
Supported by the Conseil Régional de Normandie and the European Regional Development Funds (FEDER).
The authors declare that there were no other conflicts of interest.
ABBREVIATIONS
CIRALE | Centre for Imaging and Research in Locomotor Affections in Equines |
DDFT | Deep digital flexor tendon |
DIPJ | Distal interphalangeal joint |
DIP-PDJD | Distal interphalangeal primary degenerative joint disease |
DP | Distal phalanx |
DSB | Distal sesamoid bone |
D60°Pr-PaDiO | Dorsal 60° proximal-palmarodistal oblique |
FRO | Frontal plane |
FSE | Fast spin-echo |
GRE | Gradient recalled echo |
HR | High resolution |
MP | Middle phalanx |
SAG | Sagittal plane |
SI | Signal intensity |
STIR | Short tau inversion recovery |
TRA | Transverse plane |
T1W | T1-weigh t ed |
T2W | T2-weighted |
Footnotes
Hallmarq Equine Standing MRI, Hallmarq Veterinary Imaging Ltd, Guildford, England.
SPSS Statistics, Version 23, International Business Machines, Ar monk, N Y.
Arthropathix ND, Michel Vaillant, Cluses, France.
References
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Appendix
Technical parameters of standing low-field MRI sequences used for diagnosis of DIP-PDJD in horses (n = 12) of the present study.
Sequence | No. of slices | TR (ms) | TE (ms) | Flip angle (°) | Acquisition time (s) | Matrix (pixels) | FOV (mm) | Thickness (mm) | Interslice distance (mm) |
---|---|---|---|---|---|---|---|---|---|
T1W GRE 3-D TRA | 26 | 24 | 7 | 43 | 132 | 256 × 256 | 170 | 5 | – |
T2W FSE TRA FAST | 9 | 1,737 | 88 | 90 | 114 | 256 × 256 | 175 | 5 | 1 |
T2W 3-D FRO HR | 48 | 33 | 13 | 25 | 304 | 512 × 512 | 170 | 2 | – |
STIR FSE SAG | 12 | 3,042 | 27 | 90 | 219 | 256 × 256 | 170 | 5 | 1 |
T1W GRE 3-D FRO HR | 48 | 24 | 8 | 43 | 221 | 512 × 512 | 170 | 2 | – |
T1W GRE 3-D TRA HR | 48 | 24 | 8 | 43 | 221 | 512 × 512 | 170 | 2 | – |
T1W GRE 3-D SAG HR | 48 | 24 | 8 | 43 | 221 | 512 × 512 | 170 | 2 | – |
STIR FSE TRA FAST | 8 | 2,336 | 22 | 90 | 161 | 256 × 256 | 170 | 5 | 1 |
FAST = Fourier acquired steady state. FOV = Field of view. TE = Time of echo. TR = Time of repetition.