Subchondral cystic lesions, commonly described as SCLs, occur frequently and cause lameness in horses.1,2 While the femur poses the most represented site in a study of 703 SCLs,1 about 26.2% occur in the phalanges. Their etiopathogenesis is still incompletely understood. Two main explanations of how SCL formation occurs are being debated. One proposes a first occurring full-thickness defect in the cartilage, leading to synovial fluid being pressed into the subchondral bone. This in turn causes pressure necrosis and subsequent resorption of the bone.1,3–5 The second theory states that no connection to the joint is needed, as either a focal area of ischemia of the epiphyseal growth cartilage develops, leading to chondronecrosis or dilation of blood vessels and following SCL formation (osteochondrosis),3,6 or as a traumatic impact on subchondral bone leads directly to bone edema and necrosis (contusion theory).7,8
To this day, a relationship between SCLs and osteochondrosis is assumed,9–12 since both diseases may develop secondary to a disturbance of endochondral ossification.1,5,9,10,13 As osteochondrosis is initiated in skeletally immature individuals, it is classified as a developmental orthopedic disorder.3 This etiology fits the age distribution of many described SCL cases, in which the affected horses proved to be young (0 to 3 years) and show symptoms at the onset of training.14–16 It alone, however, does not explain the occurrence of SCLs in older horses, several years into training.2,9,17
Trauma, as well, has been acknowledged as a causing factor, since SCLs have been recognized to develop after acute articular trauma,7,18,19 intra-articular fractures,3,20 septic arthritis,2,21 and osteoarthritis.1,13 Experiments showed that primary damage to the articular cartilage, but also damage solely to subchondral bone, triggers the development of SCLs.22 One experimental study4 only showed a formation of SCLs, when combined trauma was applied to the cartilage and the subchondral bone. In a longitudinal study7 of subchondral cysts in the human knee, however, the contusion theory was supported. It proposes that bone necrosis occurs after a traumatic impact of two opposing articular surfaces, sometimes occurring with, but not in need of, a cartilage defect.
Meanwhile, the proximal phalanx is a predominant site of traumatic injury in equine athletes.23,24 Simple sagittal fractures of the proximal PP occur frequently. They have most commonly been described in the mid sagittal groove25 as a result of the compressive and torsional forces26 acting upon the metacarpophalangeal joint. Kümmerle et al24 have identified a correlation between short, incomplete, sagittal fractures and SCLs of the proximal phalanx. Fifty percent of the described fractures were accompanied by an SCL.
Morphology of SCLs has generally been described as radiolucent areas of the bone,1,2,27 which are well demarcated from the surrounding tissue by a peripheral zone of sclerosis and microfractures.1,3,28 They form a distinct cystic wall composed of fibrous connective tissue and their cavity is filled with either fibrous tissue or mucoid, gelatinous fluid.1 Depending on the anatomic location of the SCL, between 30% and 100%10,15,17, 27–29 exhibit a cloaca, meaning a connection to the adjacent articulation. SCLs vary vastly in shape and size. They may be shallow or deep and have a dome, conical, or spherical shape.1,30 Defects may occur as solitary or multiple lesions in a horse and, depending on location, about 9.4% to 42% of horses show them bilaterally.1,15,17,31–33
Due to low case numbers, many studies have summarized morphological and anatomical attributes of SCLs of any joint in the equine patient.1,9,23 Recognizing the loss of information with this approach, newer studies have focused on only one of the more represented sites, mainly the stifle15,28,32 and the distal phalanx.14,18 However, even though the phalanges constitute about a fourth of all occurrences, to the knowledge of the authors, no larger study on morphology on SCLs in the proximal phalanx (PP) has been performed.
For this reason, the purpose of the present study was to describe the morphology and characteristics of SCLs of the proximal phalanx. We hypothesized that proximal SCLs mirrored development after chronic, repetitive stress put on the articular cartilage and/or the subchondral bone, while distal SCLs showed the morphological markers of SCLs derived from osteochondrotic processes.
Materials and Methods
Case selection
Medical records of all cases presented to an equine referral center between 2005 and 2015 were included in the present study, if a single SCL or multiple SCLs were diagnosed in the proximal phalanx of a fore- or hindlimb with standard radiographs or CT. Horses represented either outpatients scheduled for an orthopedic examination or referral cases with a preceding lameness work-up of the referral veterinarian. To assess the lameness, the scoring system of Ross and Dyson34 (grades 1 to 5) was used. To locate the pathology of the lameness, flexion tests and diagnostic anesthesia (perineural and/or joint anesthesia) were conducted, after which radiographs and/or CT scans were obtained. All available medical information was collected retrospectively for each case.
Radiographic and CT evaluation
All radiographic studies were performed with a digital system (FCR Profect CS; Fujifilm). In all distal interphalangeal, metacarpophalangeal, and proximal interphalangeal joints, 4 views were obtained (lateromedial [LM], dorsopalmar/dorsoplantar [D12Pr-PaD/D12Pr-PlD], dorsopalmar/dorsoplantar/dorsolateral-plantaromedial [DL-PaMO/DL-PlMO] and dorsomedial-palmarolateral [DM-PaLO], or dorsomedial-plantarolateral [DM-PlLO]).
Under general anesthesia, helical CT was performed in 35 affected limbs with a 40-slice scanner (Somatom Sensation Open; Siemens Medical Solutions). Settings included 120 KV, 100 mAs, 1-s tube rotation, a pitch of 0.65, 2-mm slice collimation with an increment of 2-mm reconstructed to 0.75-mm images applying a medium-frequency image reconstruction algorithm for soft tissue, and a high-frequency image reconstruction algorithm for bone, respectively.
Dedicated software was used for reviewing the radiographic and CT images (OsiriX Open Source 5.0.2; OsiriX Foundation). For evaluation of the CT images, multiplanar imaging (dorsal, transverse, sagittal planes) and a bone window (window width, 3,000 Hounsfield units; window level, 500 Hounsfield units) were applied. Because of the retrospective study design, markers were not used on radiographs and radiographic measurements could not be corrected for magnification. All diagnostic images were reviewed by the same radiologist.
The following criteria were evaluated in each SCL on radiographic and CT images: location (3 subgroups: proximal PP, group A, or distal PP, group B; medial, lateral, or mid sagittal; and dorsal, central, palmar/plantar), shape (3 subgroups: well-delineated, circular single-chambered cysts; multichambered well-delineated cysts; SCLs with blurred and undefined borders), maximum cross-sectional area (DP view or dorsal plane, respectively, in mm2), continuity of the subchondral bone (continuous, discontinuous), peripheral sclerosis (none, mild, moderate, severe), presence of a fracture (yes, no), as well as osteoarthritis (OA; yes, no) and periostitis (none, mild (< 1 mm), moderate (1 to 2 mm) and severe (> 2 mm). A fracture was defined as a short, thin radiolucent line (crack) extending from the subchondral bone into, but not through the bone. The presence of vascular channels (yes, no) was assessed. Circular, hypoattenuating tracts leading to or from the SCL towards the margin of PP were addressed as vascular channels.35
Data analyses
Data were coded in Excel and analyzed with the SPSS statistical program (IBM SPSS Statistics; Version 23.0). Descriptive statistics such as mean and standard deviation as well as absolute and relative frequencies were computed. Data were visualized by scattergrams and boxplots. The nonparametric Mann-Whitney test was applied to disclose differences in medians of a continuous outcome between two groups. Association between two discrete variables was assessed by a chi-squared test. Paired associations between two discrete variables were evaluated by the MacNemar test. The Bland-Altmann analysis was provided disclosing the bias of two methods (CT and radiographic methods) and 95% limits of agreement. To assess the bias, the 1-sample t test for differences was computed. In the data set clustering is present, as it is possible that a patient has more than 1 subchondral cystic lesion. Consequently, linear mixed models were applied to adjust for clustering. Results of statistical analyses with a P value < 5% were interpreted as statistically significant.
Results
Forty-six horses met the inclusion criteria, which amounted to 62 SCLs to be evaluated. Thirty-nine (84.8%) of these horses were Warmbloods, 3 (6.5%) were Freiberger, and the remaining 4 horses consisted of 2 (2.2%) Icelandic horses, 2 (2.2%) Quarter horses, 2 (2.2%) Thoroughbred, and 1 (2.2%) pony. There were 25 mares (54.3% females) and 18 geldings and 3 stallions (45.7% males). The mean age was 9.9 years with the youngest foal being 3 months of age and the oldest gelding being 22 years old.
Forty-three (70.5%) SCLs were found in the proximal PP (group A) and 18 (29.5%) were found in the distal PP (group B). The mean age of horses in group A was 11.47 years, and the mean age of horses in group B was 6.72 years (Figure 1). This proved to be significant with a P value of .002. Even including the clustering of data (1 horse could have multiple SCLs in this study), the data show a strong trend. No association between distribution and sex or race of the horses was found.
Proximal versus distal location of SCLs in relation to age. Note that the mean age of horses of group A (left bar) was higher than the mean age of horses of group B (right bar).
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
Most horses (93.5%) were initially presented for an orthopedic evaluation; in 3 cases (6.5%) however, the subchondral cystic lesions were discovered in a prepurchase inspection. Every lameness was localized through flexion tests and diagnostic anesthesia. Sixteen horses (34.7%) presented with a lameness, which had lasted 1 to 8 weeks; 15 horses (32.6%) had shown a lameness of 2 to 12 months previous to arriving at the referral center; and in 12 cases (26%), the information concerning exact lameness duration was missing in the records. The median degree of lameness was 2/5 (range, 0 to 4/5).34 Of the 4 nonlame horses (8.7%), 3 were evaluated for a prepurchase inspection and 1 horse had been lame for 3 months but showed no lameness at the time of presentation.
Thirty-four (73.9%) horses had a unilateral SCL, 8 (17.4%) horses showed bilateral SCLs, and 4 (8.6%) horses showed SCLs in 3 limbs. No patient had lesions in all 4 limbs. All patients with 3 affected limbs belong to group A. The patients with bilateral SCLs proved to have both distal and proximal SCLs. However, 7 of 8 showed either proximal or distal SCLs in both respective limbs. Only 1 of the horses had a proximal SCL in 1 front leg and a distal SCL in the other.
Of all 62 SCLs, 61 (98.4%) were assessed radiographically, and in 35 cases (56.5%), a CT examination was performed. For 1 (1.6%) proximolateral lesion, only CT was used as a means of evaluation as it was detected while assessing a second SCL. As there is a higher number of SCLs being described on radiographic images, the following numbers and percentages show the distribution of those 61 SCLs. The subchondral cystic lesions were mainly localized in the forelimbs (58%), while a slightly smaller percentage were situated in the hindlimbs (42%). Forty-three (70.5%) SCLs of the sample group were found in the proximal PP (group A) and 18 (29.5%) were found in the distal PP (group B), near the proximal interphalangeal joint. The ratio of percentages of proximal versus distal PP SCLs in the front- versus the hindlimbs was equal. The described radiographic distribution was consistent with the evaluation in the gold standard CT.28,29,36 The distinction between medial, mid sagittal, or lateral located lesions proved slightly less exact comparing radiography and CT images. Two (5.9%) out of 34 SCLs evaluated in both radiographic images and CT were not categorized the same in the 2 different imaging techniques. This was mainly because, in CT, the evaluation of the midline of the PP in relation to the SCL could be measured more exactly.
On radiographic assessment, 36 of 60 (60.0%) SCLs were situated mid sagittal, 17 (28.3%) SCLs medial, and 7 (11.7%) SCLs lateral. One SCL was only evaluated through CT and therefore was not counted in this statistic, and 1 SCL could not be classified in the dorsoplantar radiographic view in retrospect. This medial to lateral distribution of lesions in the dorsopalmar/-plantar plane occurred only in group A. The medial to lateral distribution of SCLs in group B was even (Figure 2).
Dorsopalmar (A) and lateromedial (B) radiographs of a left front fetlock. Note the even distribution of SCLs of group B (A) and the distinct majority of mid sagittal SCLs in group A.
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
In agreement with earlier studies,29 only 28 (45.2%) of 62 SCLs could be diagnosed in the lateromedial radiographic view. As a consequence, the case numbers in the CT-evaluated cysts are higher and the evaluation is more exact. Of the CT analysis of the available 35 proximal and distal SCLs, 30 (85.7%) were situated centrally, 3 (8.5%) were located palmar or plantar, respectively, and 2 (5.7%) were found dorsal. A distinct distribution between proximal and distal SCLs can be observed in this plane as well. In group A, 23 (92%) of 25 SCLs were in the center of PP, while the remaining 2 (8%) were located dorsally. In group B, on the other hand, 7 of 10 SCLs (70%) were located centrally, and 3 (30%) palmarly or plantarly, respectively. None of the SCLs of group B were located dorsally.
For the 3 different shapes that were differentiated radiographically, 17 (27.9%) SCLs were circular, single chambered, and well delineated, 13 (21.3%) showed a circular shape as well but were multichambered. The remaining 31 (50.8%) were blurred, with an irregular outline and hard to differentiate (Figure 3). The 34 SCLs evaluated through both radiography and CT showed a 100% agreement on form assessment. No association between form and duration of lameness could be found.
Dorsopalmar radiographic view of a sagittal SCL (A), a sagittal CT view of a central SCL (B), and view of a medial SCL (C) of group A. The obvious difference of the circular shape (C, thick arrow) between abaxial positioning versus the irregularly delineated SCL with a long, central shape, which is found sagittal (A, thin arrow, and B), has proven to be typical.
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
Since for the first and the second shape all the main criteria of morphology overlapped, they were put into the same category in the following statistics (49.2% circular and/or chambered SCLs).
With a P value of .004, the difference in the shapes of cysts from proximal to distal proved significant. While in group A, 27 (62.8%) of 43 SCLs showed a blurred shape, in group B, a total of 14 of 18 (77.8%) SCLs were circular and easily distinguishable.
The mean size in radiographic images was 29.66 mm2, while in CT analysis, the mean size turned out to be 33.48 mm2. The observed differences in measurements of radiographic images and CT images proved to be nonsignificant (P = .236), which places radiography as a suitable and satisfactory modality to evaluate the size of SCLs in the PP in the horse. However, as this was a retrospective study, there is a magnification artifact on these measurements.
SCLs of group A showed a mean radiologic size of 20.19 mm2, while SCLs of group B proved to be distinctly larger with a mean size of 52.3 mm2 (P < .001) (Figure 4). The same observation was made in CT, where SCLs of group A were on average 23.38 mm2 and SCLs of group B were 60.24 mm2 (P = .009).
Dorsopalmar radiographic view of a medial (A) and a lateral, chambered SCL (B) of group B, with a narrow (A) or wide cloaca (B). The wide cloaca is also visible in the dorsal CT view (C). Note the larger and circular shape opposed to the proximal SCLs (see Figure 3). Marked periostal reaction (thin arrows) and vascular channels (thick arrows) can also be seen.
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
Neither radiologic size nor CT size is directly associated with the age of the horse. The images could retrospectively not be corrected for magnification, so these numbers can only show a trend.
In 46 (76.7%) cases, there was a discontinuity of the subchondral bone to be seen in the radiographic images. In the CT analysis, however, all 35 (100%) out of 35 analyzed SCLs showed a connection to the adjacent joint.
There were 9 short, incomplete fractures observed in the radiographic images. Four of them were recognized in CT as well, 4 were not evaluated in CT, and 1 hypodense line was characterized as a fracture in radiographs but did not exist in CT. All observed fractures in the radiographic images occurred in group A in the proximal, sagittal PP (Figure 5). Through CT, a total of 14 (40%) short, incomplete fractures in 35 SCLs were found. Only four of these had been recognized in radiographs, meaning 71% of fractures went undetected through radiographic evaluation. Since CT is the gold standard in recognizing short, incomplete fractures,21,24,36 the lack of power in evaluating fractures on radiographs has to be acknowledged. Eleven out of 14 (78.6%) CT-detected fractures occurred in group A. and only 3 (21.4%) were detected in group B. Eleven out of 25 (44%) proximal SCLs were accompanied by a fracture.
Dorsopalmar radiographic view of a proximosagittal SCL (A) with a short, incomplete fracture and the transverse CT view onto PP (B), showing the same fracture.
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
Existence and thickness of sclerosis were measured as a feature of adaption of the subchondral bone to chronic stress factors. Various stages of sclerosis could be seen, as stated before by Rechenberg et al.1 Four SCLs (6.6%) showed low-grade (< 1 mm thickness), 19 (31.1%) were surrounded by moderate (1 to 2 mm), and a total of 38 (62.3%) SCLs showed high-grade sclerosis (> 2 mm) in radiographic images (Figure 6). In CT, 1 (2.9%) SCL showed no sclerosis, 2 (5.7%) low-grade, 6 (17.1%) moderate, and 26 (74.3%) high-grade sclerosis.
Dorsopalmar view of a distal SCL with high-grade sclerosis and a narrow cloaca. The thickness of sclerosis is marked by a green line: length = 3.686 mm.
Citation: American Journal of Veterinary Research 83, 12; 10.2460/ajvr.22.04.0071
Periosteal reactions were evaluated as a marker of possible fracture pathology37 and occurred on the lateral and the medial sides of the PP in 25 (41%) cases (Figure 4). They could be diagnosed in radiographic images as well as in CT, where there were 14 (41.2%) SCLs affiliated to periosteal reactions. In radiographic evaluation, 20 (80%) of the periosteal reactions were found proximally on the PP, 5 (20%) of them distally, while in CT, 12 (85.7%) periosteal reactions were found proximally and 2 (14.3%) of them distally on the PP. This distribution mirrors the proportion of proximal versus distal SCLs and a significant connection between proximal SCLs and increased periosteal reaction formation could be proven in neither analysis (P = .142 and P = .149). Also, no association between periosteal reaction and fracture presence was found. Eight of 14 (57%) fracture cases showed periosteal reaction, while 6 (43%) did not.
Vascular channels were evaluated as a feature of increased perfusion to abnormal bone35. They occurred in radiographic images in 12 (19.7%) cases (Figure 4). In CT analysis, 21 (60.0%) SCLs showed channels. The accuracy between the two modalities was unsatisfactory though significant (P = .004). Sixteen (47.1%) SCLs out of 34 SCLs did not show any signs of channels in radiographic images, even though in CT, they existed.
There were 18 (29.5%) SCLs that occurred with simultaneous signs of osteoarthrosis in the affected joint. There was no significant difference between its existence in proximal versus distal joints (P = .314). Fourteen of 43 SCLs of group A (32.5%) showed osteoarthrosis in the metacarpo-/metatarsophalangeal joint.
Only four (6.5%) horses were observed having an accident or putting excessive stress on the discussed joints. None of them had a fracture in the diagnostic images. Three (75%) of said horses belonged to group A and 1 (25%) to group B.
Discussion
SCLs of the first phalanx showed a distinct distribution and different morphological attributes depending on their location. Almost two-thirds of SCLs of PP were situated proximally (group A) and almost 70% of these were situated mid sagittally. This pattern mirrors the distribution of short, incomplete fractures of the proximal PP24,37 as well as subchondral bone trauma.19,23,38 A common origin of chronic, repetitive stress on the articular cartilage and/or the subchondral bone is possible for these proximal lesions. The majority of SCLs of group B (77.8%), on the other side, showed a circular or oval, well-defined shape. They were evenly distributed from lateral to medial and mainly found central to palmar/plantar of the distal PP. As further discussed below, the distribution and morphology of these lesions show high accordance with developmental bone cysts originating from a local failure of enchondral ossification of a growing individual.3
SCLs of group A proved to be significantly smaller than the large, circular distal lesions (P = .001). All the described proximal, mid sagittal lesions showed a blurred shape in radiographic images, which was due to a more scattered demarcation and many of those lesions showed the typical long and wide shape with only shallow depth in CT, which does not occur in the distal PP. The remaining medial and lateral proximal SCLs either showed a circular shape like the distal SCLs or the same typical blurred, long, wide, and shallow shape. The morphological attributes of proximal PP SCLs as well as their relation to fractures, subchondral bone lesions, and periosteal reactions indicate lesions developed due to chronic, repetitive microtrauma to the articular cartilage and subchondral bone.
Proximal incomplete PP stress fractures occur often and have been well-documented in racehorses and sports horses.21,23,24,39 About 80% of them occur mid sagittal,27,39 which is explained by the fact that here maximal force is transmitted.40,41 Not only a similar distribution but also a coexistence of both SCLs and fractures, as well as SCLs and bone marrow lesions (BMLs) of the PP, has been described several times.23,24 Kümmerle et al24 demonstrated in a cross-sectional study that short, incomplete proximal PP fractures are highly associated with SCLs in the same subregion. However, no chronological relationship between these two features could be assessed. Brünisholz et al37 described stress-related short, incomplete PP fractures with concurring subchondral defects, osteolysis, and a distinct chromosome-like fracture pattern, which appear on radiographs as irregular SCL. In CT images, those lesions showed the same typical long and wide shape as many of the proximal SCLs in this study. Their described fractures were accompanied by adaptive processes such as subchondral sclerosis, periosteal new bone formation, and osteoarthritic changes, so a stress-related, chronic origin was suspected. Brünisholz et al37 concluded that the occurrence of such a fracture with the emergence of clinical signs can be considered the acute manifestation of a more chronic pathological process.
A chronological association between primary osseous trauma of the PP without a fracture and a formed SCL in the same location has been observed through scintigraphy and MRI.19,23,42 It is interesting to note that the mentioned bone trauma was not only situated mainly in the same mid sagittal location as the mentioned short, incomplete fractures and most proximal SCLs but also fit the additional proximal locations we observed in our study. The remaining 28.6% of SCLs of group A occur mainly medial and rarely lateral. Even though CT provides the highest specificity of location and morphologic markers like discontinuity of the bone and additional data like the presence of fractures and degenerative joint disease, it does not recognize bone contusions and cartilage lesions sensitively.29,35,36 This places scintigraphy and especially MRI as a valuable additional tool in the diagnosis of a pastern lameness if no radiographic or CT abnormalities were found. These modalities are a more sensitive means to recognize cartilage or bone marrow lesions, which can later progress to SCLs.19,23,38 The BMLs, however, can resolve with rest and time, without developing any other pathologies.42 As the medial and lateral proximal SCLs in our study sometimes showed a circular shape like the distal ones, the possibility of bone contusions at that same site in younger, growing individuals, which might lead to the described vascular failure in the epiphyseal growth cartilage3 and cyst formation, should be recognized. In these locations, it might be a question of at which point of the maturation process a disruption of the articular surface or the subchondral bone occurs, deciding how the SCL develops and which shape it will take.
The smaller shape of SCLs of group A opposed to the larger SCLs of group B is symptomatic of cystic enlargement over time.4,28,30 When lesions are exposed to high loads or stress, microfractures and subsequently osteoclastic resorption will occur.3 Additionally, fibrous tissue from equine bone cysts has been shown to produce enzymes and cytokines that are associated with bone resorption.43,44 Both processes will result in progressive enlargement of the lesion. Trauma-induced SCLs, even though sometimes taking a couple of weeks to get diagnosed,19,24 still are discovered early in their development due to the trauma causing lameness as well. In comparison, the distal developmental bone cysts will only be present when the large lesion can no longer support the overlying cartilage and gives way to infolding and cloaca formation. The sudden onset of lameness in horses with such long-lasting pathologies is explained by the event of cloaca3 or pathological fracture formation if the bone is unable to withstand the physical forces put on it.36,45 In our study, all SCLs of group B analyzed through CT imaging showed a cloaca, and the presence of a distal fracture was detected twice.
The majority of SCLs of group B (77.8%) showed a circular or oval, well-defined shape. They were evenly distributed from lateral to medial and mainly found central to palmar/plantar of the distal PP. The morphology of the lesion as well as their location was remarkably similar to a lesion found in a horse less than 5 years old and mentioned in a paper by Olstad et al.3 They call SCLs derived from an etiology of osteochondrosis developmental bone cysts.3 Blood supply to the epiphyseal growth cartilage runs within cartilage canals, which are only temporarily present during the early phases of growth. Microlesions of these transient blood vessels lead to a focal failure of blood supply in the epiphyseal growth cartilage, which leads to necrosis of chondrocytes and, in connection, to dilation of blood vessels in the surrounding fibrous granulation tissue. The dilated blood vessels with loss of function progress to cysts in the epiphyseal bone.3
Comparing the described lesions of Olstad et al3 and the proposed thesis for the distal SCLs in our study, many observed properties overlap. As in our study, since histological evaluation was not possible, there can be no statement about markers like epithelial lining, fibrous granulation tissue, or a possible cartilage fold of the SCLs. However, the evaluated cysts were generally larger than the proximal SCLs and well delineated as well as of a circular or oval shape. All of them showed a connection to the proximal interphalangeal joint, which underlines the importance of cloaca formation as all cases presented due to lameness. There were some multichambered cysts observed. In 80% of distal SCLs, vascular channels3,35 to the cortex were diagnosed, while the same occurred in only 52% of proximal SCLs. As Olstad et al3 mentioned, dilated blood vessels were found in and adjacent to developmental bone cyst; this finding supports an origin of osteochondrosis.
While Olstad et al3 detected a mean patient age of 5 years when presenting with lameness and multiple other osteochondrosis papers12,46 described similar and even younger symptomatic horses, in this study, the mean age of horses of group B was 6.7 years. Even though our patients were older, the mean age was still significantly lower in distal SCLs than in proximal SCLs at 11.5 years, adding to the probability of different etiopathogenesis of proximal and distal SCLs. Even though the significance of age could not be repeated, when considering that one horse could have several SCLs, a strong trend can be assumed.
A possible explanation for the higher age of our horses of group B, in comparison to typical osteochondrosis patients, is that the patients only presented after developing a lameness. In the prevalent population of Warmblood horses, the training starts later and the intensity of training at a young age is generally lower than in the often-analyzed racehorses.32,47 Also, SCLs originating from osteochondrosis would have had a lot of time to develop and only present with lameness once a cloaca develops. The 100% of distal SCLs found with a cloaca as well as the most severe degree of sclerosis support this theory. However, no significant correlation between the 13 horses in this study that reportedly suffered from osteochondrosis in any other joint and the patients showing distal SCLs in the PP could be found.
The distribution of the distal SCLs of the PP in our study is very similar to SCLs in the distal interphalangeal joint.47,48 Fairburn et al48 only recently showed that affected DIP joints are more likely to have incongruence of the joint surfaces than joints without defects. Joint incongruity is a feature of joint dysplasia, which supports the theory that SCL formation of the DIP joint may be associated with osteochondrosis of the joint.48 Denoix et al46 described juvenile subchondral bone cystic-like lesions found at focally highly loaded convex articular surfaces like the distal aspect of PP46 matching our findings. As those mentioned authors, we connected our found SCLs on the distal aspect of PP to osteochondrosis. Through the selective high load at a growing age, a focal failure of blood supply occurs in the epiphyseal cartilage and, as described by Olstad et al,3 dilated blood vessels progress to cysts in the epiphyseal bone.
The vast majority of cases in this study consisted of Warmbloods (84.8%) with a mean age of 9.9 years. It reinforces the statement of Trotter et al9,49 about phalangeal SCLs being prevalent in Warmbloods. The frequent presence of stallions and geldings in other studies1,14,16,17 could not be repeated. In fact, in the present study, 54.3% of cases were mares.
As all data were collected retrospectively. A limitation of this study is the lack of explicit information on anamnesis and the lack of a standardized lameness examination. The horses were examined by different clinicians and, in some cases, the referring veterinarian. The grading of lameness degree and flexion tests is therefore subjective. Also, the obtained radiographic images could not be corrected for magnification. In this study, therefore, radiographic measurements can only show a trend.
In conclusion, the results of this study reveal that SCLs of the proximal phalanx occur at consistent sites and in a very predictable morphology, depending on their respective location. Proximal and mid sagittal, sometimes proximomedial, SCLs show a longitudinal, irregular shape often occur with short, incomplete fractures, and are generally small. They are found in older horses, about 11.5 years old. An origin of chronic microtrauma to the articular cartilage and subchondral bone is likely. Distal SCLs are located central or palmar/plantar, are evenly distributed from medial to lateral, and are circular as well as very large in comparison to the proximal ones. They occur in younger horses and about 6.7 years of age and often show vascular channels. These findings support the theory of osteochondrosis as an etiology. The proximal SCLs should especially be evaluated through CT, as in many cases, present fissures are not recognized in radiographic images and are sometimes even misdiagnosed.37 With this diagnosis, a chronic weakening of the sagittal subchondral bone and articular cartilage should be expected and addressed.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
Dr. Ohlert, DECVDI, reviewed all diagnostic images.
References
- 1.↑
Von Rechenberg B, McIlwraith CW, Auer JA. Cystic bone lesions in horses and humans: a comparative review. Vet Comp Orthop Traumatol. 1998;11(1):8–18. doi:10.1055/s-0038-1632602
- 2.↑
Garcia-Lopez JM, Kirker-Head CA. Occult subchondral osseous cyst-like lesions of the equine tarsocrural joint. Vet Surg. 2004;33(5):557–564. doi:10.1111/j.1532-950x.2004.04078.x
- 3.↑
Olstad K, Ostevik L, Carlson CS, Ekman S. Osteochondrosis can lead to formation of pseudocysts and true cysts in the subchondral bone of horses. Vet Pathol. 2015;52(5):862–872. doi:10.1177/0300985814559399
- 4.↑
Ray CS, Baxter GM, McIlwraith CW, Trotter GW, Powers BE, Park RD, Steyn PF. Development of subchondral cystic lesions after articular cartilage and subchondral bone damage in young horses. Equine Vet J. 1996;28(3):225–232. doi:10.1111/j.2042-3306.1996.tb03777.x
- 5.↑
Bramlage LR. Osteochondrosis-related bone cysts. In: Proceedings of the Annual Meeting of the American Association of Equine Practitioners. AAEP; 1993:83–85.
- 6.↑
Olstad K, Hendrickson EHS, Carlson CS, et al. Transection of vessels in epiphyseal cartilage canals leads to osteochondrosis and osteochondrosis dissecans in the femoro-patellar joint of foals; a potential model of juvenile osteochondritis dissecans. Osteoarthritis Cartilage. 2013;21(5):730–738. doi:10.1016/j.joca.2013.02.005
- 7.↑
Crema MD, Roemer FW, Zhu Y, et al. Subchondral cystlike lesions develop longitudinally in areas of bone marrow edema-like lesions in patients with or at risk for knee osteoarthritis: detection with MR imaging–the MOST study. Radiology. 2010;256(3):855–862. doi:10.1148/radiol.10091467
- 8.↑
Rhaney K, Lamb DW. The cysts of osteoarthritis of the hip; a radiological and pathological study. J Bone Joint Surg Br. 1955;37-B(4):663–675. doi:10.1302/0301-620X.37B4.663
- 9.↑
Howard RD, McIlwraith CW, Trotter GW. Arthroscopic surgery for subchondral cystic lesions of the medial femoral condyle in horses: 41 cases (1988–1991). J Am Vet Med Assoc. 1995;206(6):842–850.
- 10.↑
McIlwraith CW. Subchondral cystic lesions (osteochondrosis) in the horse. Compend Cont Educ Pract Vet. 1982;4:394–404.
- 11.
McIlwraith CW. of subchondral cystic lesions of medial femoral condyle–an evolution based on research and clinical evidence. Pferdeheilkunde. 2010;26(4):591–597. doi:10.21836/PEM20100415
- 12.↑
Stromberg B. A review of the salient features of osteochondrosis in the horse. Equine Vet J. 1979;11:211–214. doi:10.1111/j.2042-3306.1979.tb01346.x
- 13.↑
Textor JA, Nixon AJ, Lumsden J, Ducharme NG. Subchondral cystic lesions of the proximal extremity of the tibia in horses: 12 cases (1983–2000). J Am Vet Med Assoc. 2001;218(4):408–413. doi:10.2460/javma.2001.218.408
- 14.↑
Story MR, Bramlage LR. Arthroscopic debridement of subchondral bone cysts in the distal phalanx of 11 horses (1994-2000). Equine Vet J. 2004;36(4):356–360. doi:10.2746/0425164044890643
- 15.↑
Jeffcott LB, Kold SE. Clinical and radiological aspects of stifle bone cysts in the horse. Equine Vet J. 1982;14(1):40–46. doi:10.1111/j.2042-3306.1982.tb02333.x
- 16.↑
White NA, McIlwraith CW, Allen D. Curettage of subchondral bone cysts in medial femoral condyles of the horse. Equine Vet J. 1988;20:120–124. doi:10.1111/j.2042-3306.1988.tb04658.x
- 17.↑
Hogan PM, McIlwraith CW, Honnas CM, Watkins JP, Bramlage LR. Surgical treatment of subchondral cystic lesions of the third metacarpal bone: results in 15 horses. Equine Vet J. 1997;29(6):477–482. doi:10.1111/j.2042-3306.1997.tb03162.x
- 18.↑
Verschooten F, De Moor A. Subchondral cystic and related lesions affecting the equine pedal bone and stifle. Equine Vet J. 1982;14(1):47–54. doi:10.1111/j.2042-3306.1982.tb02334.x
- 19.↑
Dyson S, Nagy A, Murray R. Clinical and diagnostic imaging findings in horses with subchondral bone trauma of the sagittal groove of the proximal phalanx. Vet Radiol Ultrasound. 2011;52(6):596–604. doi:10.1111/j.1740-8261.2011.01852.x
- 20.↑
Yovich JV, Stashak TS. Subchondral osseous cyst formation after an intra-articular fracture in a filly. Equine Vet J. 1989;21(1):72–74. doi:10.1111/j.2042-3306.1989.tb02094.x
- 21.↑
Hanson JA, Seeherman HJ, Kirker-Head CA, O’Callaghan MW. The role of computed tomography in evaluation of subchondral osseous lesions in seven horses with chronic synovitis. Equine Vet J. 1996;28(6):480–488. doi:10.1111/j.2042-3306.1996.tb01621.x
- 22.↑
Kold SE, Hickman J. An experimental study of the healing process of equine chondral and osteochondral defects. Equine Vet J. 1986;18(1):18–24. doi:10.1111/j.2042-3306.1986.tb03529.x
- 23.↑
Dyson SJ, Murray R. Osseous trauma in the fetlock region of mature sports horses. In: Proceedings of the Annual Meeting of the American Association of Equine Practitioners. AAEP; 2006:443–456.
- 24.↑
Kümmerle JM, Auer JA, Rademacher N, Lischer CJ, Bettschart-Wolfensberger R, Fürst AE. Short incomplete sagittal fractures of the proximal phalanx in ten horses not used for racing. Vet Surg. 2008;37(2):193–200. doi:10.1111/j.1532-950X.2007.00359.x
- 25.↑
Markel MDJ. Noncomminuted fractures of the proximal phalanx in 69 horses. J Am Vet Med Assoc. 1985;186(6):573–579.
- 26.↑
Nixon A. Phalanges and the metacarpophalangeal and metatarsophalangeal joints. In: Auer J, Stick J, Kümmerle J, Prange T, eds. Equine Surgery. Saunders Elsevier; 2019:1587–1618.
- 27.↑
Jackson MA, Fürst AE. Subchondral cystic lesions. In: Auer J, Stick J, Kümmerle J, Prange T, eds. Equine Surgery. Saunders Elsevier; 2019:1528–1542.
- 28.↑
Walker WT, Silverberg JL, Kawcak CE, Nelson BB, Fortier LA. Morphological characteristics of subchondral bone cysts in medial femoral condyles of adult horses as determined by computed tomography. Am J Vet Res. 2016;77(3):265–274. doi:10.2460/ajvr.77.3.265
- 29.↑
Schön S, Fürst AE, Ohlert S, Kircher PR, Roos M, Jackson MA. Computed tomographic versus radiographic assessment of the visibility and features of subchondral cystic lesions in equine limbs. Pferdeheilkunde. 2017; 33(3):256–262. doi:10.21836/PEM20170306
- 30.↑
Sherlock C, Mair T. Osseous cyst-like lesions/subchondral bone cysts of the phalanges. Equine Vet Educ. 2011;23:191–204. doi:10.1111/j.2042-3292.2010.00222.x
- 31.↑
Smith MA, Walsmley JP, Phillips TJ, et al. Effect of age at presentation on outcome following arthroscopic debridement of subchondral cystic lesions of the medial femoral condyle: 85 horses (1993-2003). Equine Vet J. 2005;37(2):175–180. doi:10.2746/0425164054223741
- 32.↑
Sandler EA, Bramlage LR, Embertson RM, Ruggles AJ, Frisbie DD. Correlation of lesion size with racing performance in thoroughbreds after arthroscopic surgical treatment of subchondral cystic lesions of the medial femoral condyle: 150 cases (1989–2000). In: Proceedings of the Annual Meeting of the American Association of Equine Practitioners. AAEP; 2002:255–256.
- 33.↑
Wallis TW, Goodrich LR, McIlwraith CW, et al. Arthroscopic injection of corticosteroids into the fibrous tissue of subchondral cystic lesions of the medial femoral condyle in horses: a retrospective study of 52 cases (2001–2006). Equine Vet J. 2008;40(5):461–467. doi:10.2746/042516408X258843
- 34.↑
Ross M W, Dyson SJ. Diagnosis and Management of Lameness in the Horse. 2nd ed. W.B. Saunders;2011:72.
- 35.↑
Valdes-Martinez A. Computed tomographic arthrography of the equine stifle joint. Vet Clin North Am Equine Pract. 2012;28(3):583–598. doi:10.1016/j.cveq.2012.09.002
- 36.↑
Del Chicca F, Kümmerle JM, Ossent P, Nitzl D, Fürst A, Ohlert S. Use of computed tomography to evaluate a fracture associated with a subchondral pedal bone cyst in a horse. Equine Vet Educ. 2008;20:515–519. doi:10.2746/095777308X356983
- 37.↑
Brünisholz HP, Hagen R, Fürst A, Kümmerle JM. Radiographic and computed tomographic configuration of incomplete proximal fractures of the proximal phalanx in horses not used for racing. Vet Surg. 2015;44(7):809–815. doi:10.1111/vsu.12364
- 38.↑
Gold SJ, Werpy NM. Injuries of the sagittal groove of the proximal phalanx in warmblood horses detected with low-field magnetic resonance imaging: 19 cases. Vet Radiol Ultrasound. 2017;58(3):344–353. doi:10.1111/vru.12488
- 39.↑
Ellis DR, Simpson DJ, Greenwood RES, Crowhurst JS. Observations and management of fractures of the proximal phalanx in young Thoroughbreds. Equine Vet J. 1987;19(1):43–49. doi:10.1111/j.2042-3306.1987.tb02579.x
- 40.↑
Weekes JS, Murray RC, Dyson SJ. Scintigraphic evaluation of metacarpophalangeal and metatarsophalangeal joints in clinically sound horses. Vet Radiol Ultrasound. 2004;45(1):85–90. doi:10.1111/j.1740-8261.2004.04014.x
- 41.↑
O’Hare LMS, Cox PG, Jeffery N, Singer ER. Finite element analysis of stress in the equine proximal phalanx. Equine Vet J. 2013;45(3):273–277. doi:10.1111/j.2042-3306.2012.00635.x
- 42.↑
Olive J, Mair, T, Charles B. Use of standing low-field magnetic resonance imaging to diagnose middle phalanx bone marrow lesions in horses. Equine Vet Educ. 2009;21:116–123. doi:10.2746/095777309X383612
- 43.↑
Von Rechenberg B, Guenther H, McIlwraith CW, et al. Fibrous tissue of subchondral cystic lesions in horses produce local mediators and neutral metalloproteinases and cause bone resorption in vitro. Vet Surg. 2000;29(5):420–429. doi:10.1053/jvet.2000.7538
- 44.↑
Von Rechenberg B, Leutenegger C, Zlinsky K, McIlwraith CW, Akens MK, Auer JA. Upregulation of mRNA of interleukin-1 and-6 in subchondral cystic lesions of four horses. Equine Vet J. 2001;33(2):143–149. doi:10.1111/j.2042-3306.2001.tb00592.x
- 45.↑
Scott, E.A., Snyder, S.P., Schmotzer, W.B. Pool, R. Subchondral bone cysts with fractures of the extensor processes in a horse. J Am Vet Med Assoc. 1991;199(5):595–597.
- 46.↑
Denoix JM, Jeffcott LB, McIlWraith CW, van Weeren PR. A review of terminology of equine juvenile osteochondral conditions (JOCC) based on anatomical and functional considerations. Vet J. 2013;197(1):29–35. doi:10.1016/j.tvjl.2013.03.038
- 47.↑
Peter VG, O’Keeffe TA, Smith LCR, Schweizer-Gorgas D. Radiographic identification of osseous cyst-like lesions in the distal phalanx in 22 lame thoroughbred horses managed conservatively and their racing performance. Front Vet Sci. 2018;22(5):286.
- 48.↑
Fairburn AJ, Sherlock CE, Partridge SM, Mair TS. A case-control study of the morphological measurements of equine distal interphalangeal joints affected by osseous cyst-like lesions. Equine Vet Educ. 2022;34:473–479. doi:10.1111/eve.13449.
- 49.↑
Trotter GW, McIlwraith CW, Norrdin RW, Turner AS. Degenerative joint disease with osteochondrosis of the proximal interphalangeal joint in young horses. J Am Vet Med Assoc. 1982;180(11):1312–1318.
