Skip to main content

Advertisement

Log in

Update on the imaging features of the enchondromatosis syndromes

  • Review Article
  • Published:
Skeletal Radiology Aims and scope Submit manuscript

Abstract

Ollier disease and Maffucci syndrome are the commonest enchondromatosis subtypes, arising from non-hereditary mutations in the IDH1 and IDH2 genes, presenting in childhood and being characterised by multiple enchondromas. Maffucci syndrome also includes multiple soft tissue haemangiomas. Aside from developing bony masses, osseous deformity and pathological fracture, ~ 40% of these patients develop secondary central chondrosarcoma, and there is increased risk of non-skeletal malignancies such as gliomas and mesenchymal ovarian tumours. In this review, we outline the molecular genetics, pathology and multimodality imaging features of solitary enchondroma, Ollier disease and Maffucci syndrome, along with their associated skeletal complications, in particular secondary chondrosarcoma. Given the lifelong risk of malignancy, imaging follow-up will also be explored. Metachondromatosis, a rare enchondromatosis subtype characterised by enchondromas and exostoses, will also be briefly outlined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  1. Pansuriya TC, Kroon HM, Bovée JVMG. Enchondromatosis: insights on the different subtypes. Int J Clin Exp Pathol. 2010;3(6):557–69.

    PubMed  PubMed Central  Google Scholar 

  2. Flemming DJ, Murphey MD. Enchondroma and chondrosarcoma. Semin Musculoskelet Radiol. 2000;4(1):59–71.

    Article  CAS  PubMed  Google Scholar 

  3. Mulder JD, editor. Radiologic atlas of bone tumors. Amsterdam: Elsevier; 1993. 749 p

  4. Mirra JM, Picci P, Gold RH. Bone tumors: clinical, radiologic, and pathologic correlations. Philadelphia: Lea & Febiger; 1989. p. 2.

    Google Scholar 

  5. Dahlin DC, Unni KK, Inwards CY. Bone tumors: general aspects and data on 10,165 cases. Philadelphia: Wollters Kluwer / Lippincott Williams & Wilkins; 2010.

    Google Scholar 

  6. Herget GW, Strohm P, Rottenburger C, Kontny U, Krauß T, Bohm J, et al. Insights into enchondroma, enchondromatosis and the risk of secondary chondrosarcoma. Review of the literature with an emphasis on the clinical behaviour, radiology, malignant transformation and the follow up. Neoplasma. 2014;61(4):365–78.

    Article  CAS  PubMed  Google Scholar 

  7. Altay M, Bayrakci K, Yildiz Y, Erekul S, Saglik Y. Secondary chondrosarcoma in cartilage bone tumors: report of 32 patients. J Orthop Sci. 2007;12(5):415–23.

    Article  PubMed  Google Scholar 

  8. Herget GW, Uhl M, Opitz OG, Adler CP, Südkamp NP, Knöller S. The many faces of chondrosarcoma of bone, own cases and review of the literature with an emphasis on radiology, pathology and treatment. Acta Chir Orthop Traumatol Cech. 2011;78(6):501–9.

    CAS  PubMed  Google Scholar 

  9. Superti-Furga A, Spranger J, Nishimura G. Enchondromatosis revisited: new classification with molecular basis. Am J Med Genet C Semin Med Genet. 2012;160C(3):154–64.

  10. Pansuriya TC, van Eijk R, d’Adamo P, van Ruler MAJH, Kuijjer ML, Oosting J, et al. Somatic mosaic IDH1 and IDH2 mutations are associated with enchondroma and spindle cell hemangioma in Ollier disease and Maffucci syndrome. Nat Genet. 2011;43(12):1256–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Amary MF, Damato S, Halai D, Eskandarpour M, Berisha F, Bonar F, et al. Ollier disease and Maffucci syndrome are caused by somatic mosaic mutations of IDH1 and IDH2. Nat Genet. 2011;43(12):1262–5.

    Article  CAS  PubMed  Google Scholar 

  12. Amary MF, Bacsi K, Maggiani F, Damato S, Halai D, Berisha F, et al. IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and central and periosteal chondromas but not in other mesenchymal tumours. J Pathol. 2011;224(3):334–43.

  13. Tarpey PS, Behjati S, Cooke SL, Van Loo P, Wedge DC, Pillay N, et al. Frequent mutation of the major cartilage collagen gene COL2A1 in chondrosarcoma. Nat Genet. 2013;45(8):923–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bowen ME, Boyden ED, Holm IA, Campos-Xavier B, Bonafé L, Superti-Furga A, et al. Loss-of-function mutations in PTPN11 cause metachondromatosis, but not Ollier disease or Maffucci syndrome. Wilkie AOM, editor. PLoS Genet. 2011;14;7(4):e1002050.

    Article  Google Scholar 

  15. Choi JH, Ro JY. The 2020 WHO classification of tumors of bone: an updated review. Adv Anat Pathol. 2021;28(3):119–38.

    Article  CAS  PubMed  Google Scholar 

  16. Kurek KC, Pansuriya TC, van Ruler MAJH, van den Akker B, Luks VL, Verbeke SLJ, et al. R132C IDH1 mutations are found in spindle cell hemangiomas and not in other vascular tumors or malformations. Am J Pathol. 2013;182(5):1494–500.

    Article  CAS  PubMed  Google Scholar 

  17. The WHO Classification of Tumours Editorial Board. WHO classification of tumours soft tissue and bone tumours. 5th ed. Lyon: IARC Press; 2020.

    Google Scholar 

  18. Silve C, Jüppner H. Ollier disease. Orphanet J Rare Dis. 2006;1(1):37.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Goto T, Motoi T, Komiya K, Motoi N, Okuma T, Okazaki H, et al. Chondrosarcoma of the hand secondary to multiple enchondromatosis; report of two cases. Arch Orthop Trauma Surg. 2003;123(1):42–7.

    Article  PubMed  Google Scholar 

  20. Verdegaal SHM, Bovée JVMG, Pansuriya TC, Grimer RJ, Ozger H, Jutte PC, et al. Incidence, predictive factors, and prognosis of chondrosarcoma in patients with Ollier disease and Maffucci syndrome: an international multicenter study of 161 patients. Oncologist. 2011;16(12):1771–9.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Candas F, Yildizhan A, Gorur R. Different appearance of Ollier disease: enchondromatosis of the ribs. ANZ J Surg. 2017;87(12):E305–6.

    Article  PubMed  Google Scholar 

  22. Jurik AG. Multiple hereditary exostoses and enchondromatosis. Best Pract Res Clin Rheumatol. 2020 Jun;34(3):101505.

  23. Ghatan A, Scharschmidt T, Conrad E. Extreme enchondromatosis: a report of two cases and review of the literature. J Bone Joint Surg Am. 2010;92(13):2336–43.

    Article  PubMed  Google Scholar 

  24. Kadar A, Kleinstern G, Morsy M, Soreide E, Moran SL. Multiple enchondromas of the hand in children: long-term follow-up of mean 15.4 years. J Pediatr Orthop. 2018;38(10):543–8.

    Article  PubMed  Google Scholar 

  25. Kumar A, Jain VK, Bharadwaj M, Arya RK. Ollier disease: pathogenesis, diagnosis, and management. Orthopedics. 2015;38(6):e497-506.

    Article  PubMed  Google Scholar 

  26. Prokopchuk O, Andres S, Becker K, Holzapfel K, Hartmann D, Friess H. Maffucci syndrome and neoplasms: a case report and review of the literature. BMC Res Notes. 2016;27(9):126.

    Article  Google Scholar 

  27. Foreman KL, Kransdorf MJ, O’Connor MI, Krishna M. AIRP best cases in radiologic-pathologic correlation: Maffucci syndrome. Radiographics. 2013;33(3):861–8.

    Article  PubMed  Google Scholar 

  28. Fukunaga M, Suzuki K, Saegusa N, Folpe AL. Composite hemangioendothelioma: report of 5 cases including one with associated Maffucci syndrome. Am J Surg Pathol. 2007;31(10):1567–72.

    Article  PubMed  Google Scholar 

  29. Lissa FCT, Argente JS, Antunes GN, Basso F de O, Furtado J. Maffucci syndrome and soft tissue sarcoma: a case report. Int Semin Surg Oncol. 2009 Dec;6(1):2.

  30. El Abiad JM, Robbins SM, Cohen B, Levin AS, Valle DL, Morris CD, et al. Natural history of Ollier disease and Maffucci syndrome: patient survey and review of clinical literature. Am J Med Genet A. 2020;182(5):1093–103.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Casal D, Mavioso C, Mendes M-M, Mouzinho M-M. Hand involvement in Ollier disease and Maffucci syndrome: a case series. Acta Reumatol Port. 2010;35(3):375–8.

    PubMed  Google Scholar 

  32. Lee SM, Lee JJ, Kim YK, Lee JW, Chung J-H, Kim SE. Bone scintigraphy findings of a case with Maffucci’s syndrome. Nucl Med Mol Imaging. 2010;44(2):150–3.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sharif B, Rajakulasingam R, Sharifi S, O’Donnell P, Saifuddin A. MRI features of low-grade and high-grade chondrosarcoma in enchondromatosis. Skeletal Radiol. 2021;50:1637–1646

  34. Zwenneke Flach H, Ginai AZ, Wolter OJ. Best cases from the AFIP: Maffucci syndrome: radiologic and pathologic findings. Radiographics. 2001;21(5):1311–6.

    Article  CAS  PubMed  Google Scholar 

  35. Ranger A, Szymczak A. Do intracranial neoplasms differ in ollier disease and maffucci syndrome? An in-depth analysis of the literature. Neurosurgery. 2009;65(6):1106–15.

    Article  PubMed  Google Scholar 

  36. Mandonnet E, Anract P, Martin E, Roujeau T, Spena G, Cormier-Daire V, et al. Brain and skull base MRI findings in patients with Ollier-Maffucci disease: a series of 12 patient-cases. Clin Neurol Neurosurg. 2017;160:147–51.

    Article  PubMed  Google Scholar 

  37. Ahmed SK, Lee WC, Irving RM, Walsh AR. Is Ollier’s disease an understaging of Maffucci’s syndrome? J Laryngol Otol. 1999;113(9):861–4.

    Article  CAS  PubMed  Google Scholar 

  38. Biondi NL, Varacallo M. Enchondroma. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020 [cited 2021 Feb 7]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK536938/. Accessed 7 Feb 2021.

  39. Murphey MD, Flemming DJ, Boyea SR, Bojescul JA, Sweet DE, Temple HT. Enchondroma versus chondrosarcoma in the appendicular skeleton: differentiating features. Radiographics. 1998;18(5):1213–37.

    Article  CAS  PubMed  Google Scholar 

  40. Mulligan ME. How to diagnose enchondroma, bone infarct, and chondrosarcoma. Curr Probl Diagn Radiol. 2019;48(3):262–73.

    Article  PubMed  Google Scholar 

  41. Buirski G, Ratliff AHC, Watt I. Cartilage-cell-containing tumours of the pelvis: a radiological review of 40 patients. Br J Radiol. 1986;59(699):197–204.

    Article  CAS  PubMed  Google Scholar 

  42. Onuoha KM, Idowu BS, Orimolade EA, Makinde ON. Pelvic enchondroma: a rare location and cause of dyspareunia and infertility. IOSR J Dent Med Sci. 2016;15(10):91–3.

    Article  Google Scholar 

  43. Alfaro PA, Ciani G, Herrera CA, Donati DM, Errani C. Differential diagnosis and treatment of enchondromas and atypical cartilaginous tumours of the pelvis: analysis of 21 patients. Eur J Orthop Surg Traumatol. 2020;30(1):25–30.

    Article  PubMed  Google Scholar 

  44. Sharif B, Lindsay D, Saifuddin A. The role of imaging in differentiating low-grade and high-grade central chondral tumours. Eur J Radiol. 2021;137:109579.

    Article  PubMed  Google Scholar 

  45. Yang KY, Sung MS, Lee HJ, Park IJ, Lee JY, Yu WJ, et al. MR features of multiple enchondromas with associated chondrosarcoma in the lower extremities. J Korean Soc Radiol. 2016;74(2):137.

    Article  Google Scholar 

  46. Fallahi B, Bostani M, Gilani KA, Beiki D, Gholamrezanezhad A. Manifestations of Ollier’s disease in a 21-year-old man: a case report. J Med Case Reports. 2009;28(3):7759.

    Article  Google Scholar 

  47. Suster D, Hung YP, Nielsen GP. Differential diagnosis of cartilaginous lesions of bone. Arch Pathol Lab Med. 2020;144(1):71–82.

    Article  CAS  PubMed  Google Scholar 

  48. Park Y-K. Multiple Enchondromatosis (Ollier’s Disease). In: Santini-Araujo E, Kalil RK, Bertoni F, Park Y-K, editors. Tumors and tumor-like lesions of bone [Internet]. London: Springer London; 2015 [cited 2021 Feb 9]. p. 253–8. Available from: http://link.springer.com/10.1007/978-1-4471-6578-1_17. Accessed 9 Feb 2021

  49. Muthusamy S, Conway SA, Temple HT. Five polyostotic conditions that general orthopedic surgeons should recognize (or should not miss). Orthop Clin North Am. 2014;45(3):417–29.

    Article  PubMed  Google Scholar 

  50. Vanel D, Kreshak J, Larousserie F, Alberghini M, Mirra J, De Paolis M, et al. Enchondroma vs. chondrosarcoma: a simple, easy-to-use, new magnetic resonance sign. Eur J Radiol. 2013;82(12):2154–60.

    Article  PubMed  Google Scholar 

  51. Crim J, Schmidt R, Layfield L, Hanrahan C, Manaster BJ. Can imaging criteria distinguish enchondroma from grade 1 chondrosarcoma? Eur J Radiol. 2015;84(11):2222–30.

    Article  PubMed  Google Scholar 

  52. Douis H, Parry M, Vaiyapuri S, Davies AM. What are the differentiating clinical and MRI-features of enchondromas from low-grade chondrosarcomas? Eur Radiol. 2018;28(1):398–409.

    Article  PubMed  Google Scholar 

  53. Ferrer-Santacreu EM, Ortiz-Cruz EJ, Díaz-Almirón M, Pozo Kreilinger JJ. Enchondroma versus chondrosarcoma in long bones of appendicular skeleton: clinical and radiological criteria—a follow-up. J Oncol. 2016;2016:1–10.

    Article  Google Scholar 

  54. Fayad LM, Ahlawat S, Khan MS, McCarthy E. Chondrosarcomas of the hands and feet: a case series and systematic review of the literature. Eur J Radiol. 2015;84(10):2004–12.

    Article  PubMed  Google Scholar 

  55. De Coninck T, Jans L, Sys G, Huysse W, Verstraeten T, Forsyth R, et al. Dynamic contrast-enhanced MR imaging for differentiation between enchondroma and chondrosarcoma. Eur Radiol. 2013;23(11):3140–52.

    Article  PubMed  Google Scholar 

  56. Geirnaerdt MJ, Hermans J, Bloem JL, Kroon HM, Pope TL, Taminiau AH, et al. Usefulness of radiography in differentiating enchondroma from central grade 1 chondrosarcoma. Am J Roentgenol. 1997;169(4):1097–104.

    Article  CAS  Google Scholar 

  57. Choi B-B, Jee W-H, Sunwoo H-J, Cho J-H, Kim J-Y, Chun K-A, et al. MR differentiation of low-grade chondrosarcoma from enchondroma. Clin Imaging. 2013;37(3):542–7.

    Article  PubMed  Google Scholar 

  58. Murphey MD, Walker EA, Wilson AJ, Kransdorf MJ, Temple HT, Gannon FH. From the archives of the AFIP: imaging of primary chondrosarcoma: radiologic-pathologic correlation. Radiographics. 2003;23(5):1245–78.

    Article  PubMed  Google Scholar 

  59. Yoo HJ, Hong SH, Choi J-Y, Moon KC, Kim H-S, Choi J-A, et al. Differentiating high-grade from low-grade chondrosarcoma with MR imaging. Eur Radiol. 2009;19(12):3008–14.

    Article  PubMed  Google Scholar 

  60. Deckers C, Steyvers MJ, Hannink G, Schreuder HWB, de Rooy JWJ, Van Der Geest ICM. Can MRI differentiate between atypical cartilaginous tumors and high-grade chondrosarcoma? A systematic review Acta Orthop. 2020;91(4):471–8.

    Article  PubMed  Google Scholar 

  61. Douis H, Singh L, Saifuddin A. MRI differentiation of low-grade from high-grade appendicular chondrosarcoma. Eur Radiol. 2014;24(1):232–40.

    Article  PubMed  Google Scholar 

  62. Littrell LA, Wenger DE, Wold LE, Bertoni F, Unni KK, White LM, et al. Radiographic, CT, and MR imaging features of dedifferentiated chondrosarcomas: a retrospective review of 174 de novo cases. Radiographics. 2004;24(5):1397–409.

    Article  PubMed  Google Scholar 

  63. Saifuddin A, Mann BS, Mahroof S, Pringle JAS, Briggs TWR, Cannon SR. Dedifferentiated chondrosarcoma: use of MRI to guide needle biopsy. Clin Radiol. 2004;59(3):268–72.

    Article  CAS  PubMed  Google Scholar 

  64. Liu J, Hudkins PG, Swee RG, Unni KK. Bone sarcomas associated with Ollier’s disease. Cancer. 1987;59(7):1376–85.

    Article  CAS  PubMed  Google Scholar 

  65. Tsuchiya H, Tomita K, Yasutake H, Takagi Y, Ueda Y, Kadoya M. Maffucci’s syndrome combined with dedifferentiated chondrosarcoma. Arch Orthop Trauma Surg. 1991;110(5):269–72.

    Article  CAS  PubMed  Google Scholar 

  66. Subhawong TK, Jacobs MA, Fayad LM. Insights into quantitative diffusion-weighted MRI for musculoskeletal tumor imaging. Am J Roentgenol. 2014;203(3):560–72.

    Article  Google Scholar 

  67. Makis W, Hickeson M, Lisbona R. Maffucci syndrome with extraosseous chondrosarcoma imaged with F-18 FDG PET-CT. Clin Nucl Med. 2010;35(1):29–31.

    Article  PubMed  Google Scholar 

  68. Jo I, Gould D, Schlicht S, Taubman K, Choong P. Diagnostic accuracy of functional imaging modalities for chondrosarcoma: a systematic review and meta-analysis. J Bone Oncol. 2019;19:100262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Johnson JD, Rainer WG, Rose PS, Houdek MT. Utility of bone scintigraphy and PET-CT in the surgical staging of skeletal chondrosarcoma. Anticancer Res. 2020;40(10):5735–8.

    Article  PubMed  Google Scholar 

  70. Fisher TJ, Williams N, Morris L, Cundy PJ. Metachondromatosis: more than just multiple osteochondromas. J Child Orthop. 2013;7(6):455–64.

    Article  PubMed  PubMed Central  Google Scholar 

  71. McFarlane J, Knight T, Sinha A, Cole T, Kiely N, Freeman R. Exostoses, enchondromatosis and metachondromatosis; diagnosis and management. Acta Orthop Belg. 2016;82(1):102–5.

    PubMed  Google Scholar 

  72. Jamshidi K, Shooshtarizadeh T, Bahrabadi M. Chondrosarcoma in metachondromatosis: a rare case report. Acta Med Iran. 2017;55(12):793–9.

    PubMed  Google Scholar 

  73. Bovée JV. Multiple osteochondromas. Orphanet J Rare Dis. 2008;3(1):3.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Kanaya K, Ishikawa A, Yaoita M, Niihori T, Aoki Y, Iba K, et al. Metachondromatosis without enchondromas: a case report and review of the literature. JBJS Case Connect. 2016;6(2):e30.

    Article  PubMed  Google Scholar 

  75. Mavrogenis AF, Skarpidi E, Papakonstantinou O, Papagelopoulos PJ. Chondrosarcoma in metachondromatosis: a case report. J Bone Jt Surg-Am. 2010;92(6):1507–13.

    Article  Google Scholar 

  76. Banks RJ. Pathological fractures; a consideration with metachondromatosis and differential diagnoses. Osteochondromatosis and Gauchers disease. Australas Chiropr Osteopat J Chiropr Osteopath Coll Australas. 2002;10(2):105–10.

    Google Scholar 

  77. Herman TE, Chines A, McAlister WH, Gottesman GS, Eddy MC, Whyte MP. Metachondromatosis: report of a family with facial features mildly resembling trichorhinophalangeal syndrome. Pediatr Radiol. 1997;27(5):436–41.

    Article  CAS  PubMed  Google Scholar 

  78. Pannier S, Legeai-Mallet L. Hereditary multiple exostoses and enchondromatosis. Best Pract Res Clin Rheumatol. 2008;22(1):45–54.

    Article  CAS  PubMed  Google Scholar 

  79. Mansor N, Saisu T, Kakizaki J, Oikawa Y, Kamegaya M. Arthroscopic resection of femoral neck osteochondroma: report of a pediatric case of metachondromatosis. J Orthop Sci. 2019;Sep:S0949265819302593.

    Google Scholar 

  80. Mavrogenis AF, Papaparaskeva KT, Galanakos S, Papagelopoulos PJ. Pigmented villonodular synovitis of the distal tibiofibular joint: a case report. Clin Podiatr Med Surg. 2011;28(3):589–97.

    Article  PubMed  Google Scholar 

  81. Wenger DR, Birch J, Rathjen K, Tobin R, Billman G. Metachondromatosis and avascular necrosis of the femoral head: a radiographic and histologic correlation. J Pediatr Orthop. 1991;11(3):294–300.

    Article  CAS  PubMed  Google Scholar 

  82. Lin PP, Moussallem CD, Deavers MT. Secondary chondrosarcoma: Am Acad. Orthop Surg. 2010;18(10):608–15.

    Google Scholar 

  83. McGarry ME. Long term oncologic surveillance in Maffucci syndrome: a case report. J Oncol Sci. 2017;3(3):140–4.

    Article  Google Scholar 

  84. Jurik AG, Jørgensen PH, Mortensen MM. Whole-body MRI in assessing malignant transformation in multiple hereditary exostoses and enchondromatosis: audit results and literature review. Skeletal Radiol. 2020;49(1):115–24.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ban Sharif.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharif, B., Lindsay, D. & Saifuddin, A. Update on the imaging features of the enchondromatosis syndromes. Skeletal Radiol 51, 747–762 (2022). https://doi.org/10.1007/s00256-021-03870-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00256-021-03870-0

Keywords

Navigation