Clinical Commentary Subchondral Bone Cysts - Not Always an Easy Diagnosis L

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Clinical Commentary Subchondral bone cysts - not always an easy diagnosis L. R. GOODRICH* AND C. W. MCILWRAITH† James L. Voss Veterinary Teaching Hospital; and †Gail Holmes Equine Orthopaedic Research Center, Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado 80523, USA.

Arnold et al. (2008) recently described in this journal the dome shaped, conical or spherical, with a thinner radiolucent diagnosis and surgical management of a middle aged horse tract communicating with the articular surfaces (Fig 1). with a subchondral bone cyst located in the intermediate Subchondral sclerosis surrounding the cyst may range from tubercle of the humerus. This case is unique due to the mild to intense sclerosis depending on their stage of uncommon location of the cyst. The authors performed a thorough work-up of the lameness and, through their determination and use of multiple imaging modalities, were able to diagnose the cause of pain and successfully manage it surgically. In this issue, Del Chicca et al. (2008) report on a 4-year-old gelding that presented with acute lameness of 5 weeks’ duration. A subsequent diagnosis of an intra-articular type IV fracture with an osseous cyst-like lesion and mild degenerative joint disease of the DIP joint was made based on radiological examination of the pedal bone. Computed tomographic examination was also carried out post mortem. Subchondral bone cysts (SBC) in horses are most commonly found in the medial condyle of the femur, followed by phalanges, carpal bones, metacarpal and metatarsal bones, tibia, radius, talus, sesamoid bones, humerus, patella and tarsal bones (von Rechenberg et al. 1998). To date, apart from the case described by Arnold et al. (2008), there have not been any reports of a subchondral bone cyst in the humerus or specifically, the bicipital bursa. The aetiology of SBC is considered multifactorial and various pathogenic processes have been implicated. They include genetic causes (Hoppe and Phillipson 1985), diet (Glade and Belling 1986), growth rate, hormonal and mineral imbalances (Savage et al. 1993), osteochondrosis (Pool 1993), biomechanics and trauma (Jeffcott et al. 1983). A study by Ray et al. (1996) proved that damage to the articular cartilage plus subchondral bone, but not articular cartilage alone, of the distal medial femoral condyle may lead to the development of subchondral cystic lesions. Currently, the most well accepted aetiologies for the development of SBC remain trauma or osteochondrosis (Baxter 1996; Ray et al. 1996). Regardless of the cause, grossly and histologically, SBC have characteristic features. SBC can range in size from shallow (<10 mm) to much greater than 10 mm and their shape can vary from Fig 1: A diagrammatical (left) and corresponding radiographic (right) representation of the grades of bone cysts most recently described by Wallis et al. (2008). Reprinted from Wallis et al. *Author to whom correspondence should be addressed. (2008) with permission from Equine Veterinary Journal Ltd. EVE 08-095 Goodrich 17/9/08 08:53 Page 2

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Fig 2: A gross sagittal section revealing the appearance of a subchondral cystic lesion. Sclerotic bone is present around the cyst (a), dense fibrous tissue lines the cyst (b) and the centre is often filled with gelatinous material (c). Reprinted from Wallis et al. (2008) with permission from Equine Veterinary Journal Ltd.

development (von Rechenberg et al. 1998). Various classifications of radiographic appearance have been reported (Jeffcott and Kold 1982; Howard et al. 1995). Often, SBC have c) a fibrous lining that is filled with fibrous and/or synovial gelatinous fluid and in some instances fibrocartilage (Fig 2) (von Rechenberg et al. 1998). Molecular studies of the fibrous lining revealed that the inflammatory mediators interleukin-1β and interleukin-6 are upregulated and, in combination with prostaglandin E2, nitric oxide and neutral metalloproteinases, may be responsible for pain and continuing expansion of these cystic lesions (von Rechenberg et al. 2000). SBC can be an incidental finding but often are associated with lameness. The degree of lameness can vary from mild to severe and the onset can range from an insidious presentation of lameness to fairly acute. Often, the lameness ensues at the commencement of training in young horses and in middle aged to older horses the incident of a traumatic event or correlation to ongoing intra-articular inflammation may be Fig 3: CT images from a foal with a subchondral bone cyst of associated with the onset of the SBC (von Rechenberg et al. the caudal aspect of the third carpal bone. The cyst was not 1998). Synovial effusion may be present but is not always detected on radiographic examination. The cyst can be apparent with SBC. Intra-articular anaesthesia will often detected in the dorsal plane without flexion (a), in the saggital improve the lameness, although it may not abolish it and can plane with the carpus in a flexed position (b), and in the dorsal plane image with the carpus in a flexed position (c). occasionally only minimally improve the grade. When suspected, SBC are most often confirmed radiographically (McIlwraith 1990). However, occasionally (2008), use of CT to reveal bone abnormalities was the logical cysts may not be obvious using conventional radiography and choice for further diagnostics. imaging modalities such as nuclear scintigraphy, ultrasound, Management strategies for SBC include debridement MRI or CT scan may be helpful in confirming the diagnosis of (White and McIlwraith 1985; White et al. 1988), SBC (Barrett and Zubrod 2008; Mair and Sherlock 2008). debridement with cancellous bone graft (Jackson et al. Figure 3 shows an example of a CT scan confirming a SBC in 2000), debridement with bone substitute and chondrocyte a carpus of a filly that did not have radiographic signs of SBC or progenitor cell graft in fibrin glue (Fortier and Nixon formation. In the case of the SBC of the humerus (Arnold 2005), or steroid injection into the fibrous lining by either et al. 2008), MRI and CT would have been difficult due to ultrasound guided intra-articular injection (Foerner et al. limitations of imaging the upper extremities with current 2006) or arthroscopically (Wallis et al. 2008). The goal of equipment; however, the ultrasound was a useful tool (Barrett management is to eliminate the fibrous lining or control the and Zubrod 2008). In the case report of Del Chicca et al. inflammation associated with cytokine release within this EVE 08-095 Goodrich 17/9/08 08:53 Page 3

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lining through local steroid administration (von Rechenberg also still differ in various reports with Quarter Horses and et al. 1998). Paints tending to have less success than Thoroughbreds. Case Reported prognoses for return to previous level of activity reports as well as large clinical studies reporting results with has ranged from 30–90% depending on procedure, age, current developing therapies will enhance our current breed, surface area of weightbearing cartilage affected and knowledge of appropriate management of subchondral bone the occurrence of co-inciting osteoarthritis (White and cysts in horses. McIlwraith 1985; White et al. 1988; Sandler et al. 2002; Hendrix et al. 2005; Smith et al. 2005). Early reports of References debridement ranged from a prognosis as high as 90% (White et al. 1988) to less than 50% (Howard et al. 1995). Quarter Arnold, C.E., Chaffin, M.K., Honnas, C.M., Walker, M.A. and Heite, Horses were found to have a poorer prognosis compared to W.K. (2008) Diagnosis and surgical management of a subchondral bone cyst within the intermediate tubercle of the humerus in a Thoroughbreds (Ray et al. 1996; Wallis et al. 2008). horse. Equine vet. Educ. 20, 310-315. Subchondral bone forage as part of cyst enucleation was Barrett, M.F. and Zubrod, C.J. (2008) Use of magnetic resonance associated with cyst expansion and was determined to be imaging to detect and direct therapy of an osseous cystic lesion at detrimental (Howard et al. 1995). Furthermore, packing the the solar surface of the third phalanx of a horse. Equine vet. Educ. SBC with cancellous bone graft following curettage did not 20, 19-23. improve cartilage healing (Jackson et al. 2000). More recently, Baxter, G.M. (1996) Subchondral cystic lesions in horses. In: Joint Smith et al. (2005) reported 64% of horses aged Disease in the Horse, Eds: C.W. McIlwraith and G.W. Trotter, W.B. 0–3 years with medial femoral condylar SBC returning to Saunders, Philadelphia. pp 384-397. soundness following debridement but only 35% of horses Del Chicca, F., Kuemmerle, J.M., Ossent, P., Nitzl, D., Fuerst, A. and Ohlerth, S. (2008) Use of computed tomography to evaluate a older than 3 years returning to soundness following fracture associated with a subchondral pedal bone cyst in a horse. debridement. Sandler et al. (2002) reported 70% return to Equine vet. Educ. 20, 515-519. soundness if the surface area of cartilage affected on the Glade, M.J. and Belling, T.H. (1986) A dietary etiology for medial femoral condyle was <15 mm. However, in that same osteochondrotic cartilage. J. equine vet. Sci. 6, 151-155. report, if the surface area was >15 mm only 30% of the Foerner, J.J., Rick, M.C., Juzwiak, J.S., Watt, B.C., Smalley, L.R., Keuler, horses returned to soundness (Sandler et al. 2002). Recently, N.S. and Santschi, E.M. (2006) Injection of equine subchondral Wallis et al. (2008) reported a 67% success rate (return to bone cysts with triamcinolone: 73 horses (1999-2005). Proc. Am. soundness) with injection of corticosteroids into the fibrous Ass. equine Practnrs. 52, 412-413. lining of the SBC. However, unilateral cases of SBC were Fortier, L.A. and Nixon, A.J. (2005) New surgical treatments for significantly more successful (81%) than bilateral cases (41%) osteochondritis dissecans and subchondral bone cysts. Vet. Clin. N. Am.: Equine Pract. 21, 673-690, vii. (Wallis et al. 2008). Success was not influenced by age Hendrix, S.M., Baxter, G.M., Trumble, T.N. and McIlwraith, C.W. although only 25% of the horses in the study were aged (2005) Association between medial meniscal and medial femoral >3 years. condyle subchondral lesions in horses. Vet. Surg. 34, E12. Currently, the 2 most common treatments of SBC remain Hoppe, F. and Phillipson, J.A. (1985) Genetic study of osteochodrosis debridement and corticosteroid injection into the fibrous dissecans in Swedish horses. Equine Pract. 7, 7-15. lining. Corticosteroid injections have a slightly improved Howard, R.D., McIlwraith, C.W. and Trotter, G.W. (1995) Arthroscopic success rate and a lower amount of time for return to function surgery for subchondral cystic lesions of the medial femoral condyle (2–4 months) compared to cyst debridement (6–8 months) in horses: 41 cases (1988-1991). J. Am. vet. med. Ass. 206, 842-850. (Sandler et al. 2002; Smith et al. 2005; Wallis et al. 2008). Jackson, W.A., Stick, J.A., Arnoczky, S.P. and Nickels, F.A. (2000) The Furthermore, debridement has been associated with the effect of compacted cancellous bone grafting on the healing of subchondral bone defects of the medial femoral condyle in horses. occurrence of meniscal lesions and corticosteroid injection Vet. Surg. 29, 8-16. may decrease the likelihood of this occurring (Hendrix et al. Jeffcott, L.B. and Kold, S.E. (1982) Clinical and radiological aspects of 2005). The majority of retrospective studies evaluating success stifle bone cysts in the horse. Equine vet. J. 14, 40-46. of SBC are on cystic lesions associated with weightbearing Jeffcott, L.B., Kold, S.E. and Melsen, F. (1983) Aspects of the pathology portions of the joint. The horse reported in the paper by of stifle bone cysts in the horse. Equine vet. J. 15, 304-311. Arnold et al. (2008) is interesting since the cyst was in an area Mair, T.S. and Sherlock, C.E. (2008) Osseous cyst-like lesions in the difficult to perform radiographic imaging (intermediate feet of lame horses: diagnosis by standing low-field magnetic tubercule of the humerus). The lack of weightbearing surface resonance imaging. Equine vet. Educ. 20, 47-56. lends itself to effective treatment with debridement. The McIlwraith, C.W. (1990) Subchondral cystic lesions in the horse - the aetiology of the lesion in this horse will remain unclear but indications, methods, and results of surgery. Equine vet. Educ. 2, given the age of the horse, certainly trauma to the 75-80. intertubercle eminence would seem more likely to have Pool, R.R. (1993) Difficulties in definition of equine osteochondrosis; caused the development of the SBC rather than an differentiation of developmental and acquired lesions. Equine vet. J., Suppl. 16, 5-12. osteochondrosis lesion. Ray, C.S., Baxter, G.M., McIlwraith, C.W., Trotter, G.T., Powers, B.E., The treatment of SBC remains challenging perhaps Park, R.D. and Steyn, P.F. (1996) Development of subchondral especially in horses aged >3 years with large surfaces of cystic lesions after articular cartilage and subchondral bone weightbearing cartilage affected. Results for various breeds damage in young horses. Equine vet. J. 28, 225-232. EVE 08-095 Goodrich 17/9/08 08:53 Page 4

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Sandler, E.A., Bramlage, L.R., Embertson, R.M., Ruggles, A.J. and tissue of subchondral cystic lesions of the medial femoral condyle Frisbie, D.D. (2002) Correlation of radiographic appearance, lesion in horses: A retrospective study of 52 cases (2001-2006). Equine size, and racing performance, after arthroscopic surgical treatment vet. J. 40, 461-467. of subchondral cystic lesions of the medial femoral condyle in White, N.A. and McIlwraith, C.W. (1985) Retrospective study of thoroughbreds: 150 cases. Vet. Surg. 31, 495. femoral bone cyst curettage in the horse. Vet. Surg. 14, 70. Savage, C.J., McCarthy, R.N. and Jeffcott, L.B. (1993) Effects of dietary White, N.A., McIlwraith, C.W. and Allen, D. (1988) Curettage of energy and protein on induction of dyschondroplasia in foals. subchondral bone cysts in medial femoral condyles of the horse. Equine vet. J., Suppl. 16, 74-79. Equine vet. J., Suppl. 6, 120-124. Smith, M.A., Walmsley, J.P., Phillips, T.J., Pinchbeck, G.L., Booth, T.M., Greet, T.R., Richardson, D.W., Ross, M.W., Schramme, M.C., von Rechenberg, B., McIlwraith, C.W. and Auer, J.A. (1998) Cystic Singer, E.R., Smith, R.K. and Clegg, P.D. (2005) Effect of age at bone lesions in horses and humans: a comparative review. Vet. presentation on outcome following arthroscopic debridement of Comp. orthop. Traumatol. 11, 8-18. subchondral cystic lesions of the medial femoral condyle: 85 von Rechenberg, B., Guenther, H., McIlwraith, C.W., Leutenegger, C., horses (1993–2003). Equine vet. J. 37, 175-180. Frisbie, D.D., Akens, M.K. and Auer, J.A. (2000) Fibrous tissue of Wallis, T.W., Goodrich, L.R., McIlwraith, C.W., Frisbie, D.D., subchondral cystic lesions in horses produce local mediators and Hendrickson, D.A., Trotter, G.W., Baxter, G.M. and Kawcak. C.E. neutral metalloproteinases and cause bone resorption in vitro. Vet (2008) Arthroscopic injection of corticosteroids into the fibrous Surg. 29, 420-429.