Nonunion occurred in 7% of our patients, and resulted in failure in 2%. In previous reports, none of the patients required surgery to facilitate union (Table V). Autograft use may improve union rates, but it is not suitable for reconstruction of larger defects. Also, harvesting of autografts has been associated with substantial complication rates, especially prolonged pain at the donor site31-33. On the other hand, 24% to 47% of segmental allografts demonstrate nonunion so the rate in the current study may be considered encouraging7-10. Various factors may explain these differences, including the fact that hemicortical reconstructions have a larger contact surface between allogeneic and host bone. The extent of soft-tissue dissection is generally limited in hemicortical resections; authors have hypothesized that this provides a superior environment for incorporation3,28. Moreover, the number of patients receiving adjuvant radiation or chemotherapy was limited in our study. Adjuvant therapies are known to delay bone-healing34.
Our infection rate (7%) compares unfavorably with those in previous studies in which no infections were reported (Table V). On the other hand, infection rates after segmental allograft or endoprosthetic reconstructions typically range around 10%7,9,35-37. Infection resulted in graft removal in five patients (four of whom were managed with a new biological reconstruction) in our series. The higher risk of infection following reconstructions of the tibial diaphysis may be explained by limited possibilities for soft-tissue coverage38. We did not use muscle flaps; however, muscle transfers may be useful to reduce the risk of infection in these cases39. The infection rate was associated with the extent of cortical resection; it is conceivable that extensive resections require more soft-tissue dissection and take longer, thereby increasing the infection risk40.
Most recurrences involved adamantinomas and parosteal osteosarcomas. These lesions recur frequently, especially after intralesional or marginal excision19,41-43. Until recent years, we routinely performed subperiosteal resections for these tumors. We no longer employ this technique because we assume that it results in a higher recurrence rate. The advantages of limited resection may outweigh the elevated risk of recurrence for low-grade lesions; however, 21% (three) of the fourteen high-grade lesions in our series recurred and all resulted in ablative surgery. Apparently, hemicortical resection does not provide adequate local control of high-grade lesions. We therefore recommend segmental en bloc resections for high-grade tumors (Fig. 5).
Computer-assisted navigation may prove useful for resecting tumors with minimal but adequate margins. All osseous margins obtained with computer-navigated resection were adequate. Several authors have shown that computer navigation is accurate and useful for bone tumor surgery44,45. Computer navigation may also be used to obtain precise matching of host and allograft osteotomies and thus superior fit26,46.
Nearly all reconstruction failures occurred in the first three postoperative years. This finding is in accordance with statements in previous reports that allografts offer a reliable and lasting reconstruction if they survive the first critical years9,47,48. The ten-year allograft survival rate (87%) in our series compares favorably with ten-year survival rates of 58% to 69% reported in large series on endoprosthetic reconstructions after resections of bone tumors4,49,50. In those series, however, the majority of patients had high-grade malignant tumors and thus, presumably, more extensive resections. As those patients would not have been considered eligible for hemicortical resection, the results are difficult to compare.
Our study had several limitations. As a result of its retrospective design, it was not possible for us to accurately assess time to union of allograft-host junctions. We were also unable to acquire functional outcome scores. Previous research, however, indicates that postoperative function is generally good after hemicortical reconstruction3.
In conclusion, we report excellent long-term rates of survival of hemicortical allograft reconstructions. Rates of non-oncological complications were acceptable, especially after reconstructions comprising <25% of the cortical circumference and those <8 cm in length. Hemicortical resection is not recommended for high-grade lesions. The elevated risk of residual or recurrent tumor may, however, be acceptable for low and intermediate-grade lesions, given the excellent mechanical complication rates and the fact that most failures can be managed with a second (limb-salvaging) procedure. Modern imaging techniques play a pivotal role in ensuring that clear margins are obtained. If the aforementioned requirements are met, hemicortical resection and allograft reconstruction is a safe and reliable alternative to more comprehensive segmental resections.
NOTE: The authors gratefully acknowledge Prof. A.H.M. Taminiau, emeritus professor at the Department of Orthopaedic Surgery of the Leiden University Medical Center, for operating on a substantial number of the patients included in this study.
Investigation performed at the Leiden University Medical Center, Leiden, the Netherlands
1. Bloem JL, Taminiau AH, Eulderink F, Hermans J, Pauwels EK. Radiologic staging of primary bone sarcoma: MR imaging, scintigraphy, angiography, and CT correlated with pathologic examination. Radiology. 1988 ;169(3):805–10.
2. Enneking WF. An abbreviated history of orthopaedic oncology in North America. Clin Orthop Relat Res. 2000 ;374:115–24.
3. Deijkers RL, Bloem RM, Hogendoorn PC, Verlaan JJ, Kroon HM, Taminiau AH. Hemicortical allograft reconstruction after resection of low-grade malignant bone tumours. J Bone Joint Surg Br. 2002 ;84(7):1009–14.
4. Jeys LM, Kulkarni A, Grimer RJ, Carter SR, Tillman RM, Abudu A. Endoprosthetic reconstruction for the treatment of musculoskeletal tumors of the appendicular skeleton and pelvis. J Bone Joint Surg Am. 2008 ;90(6):1265–71.
5. Gosheger G, Gebert C, Ahrens H, Streitbuerger A, Winkelmann W, Hardes J. Endoprosthetic reconstruction in 250 patients with sarcoma. Clin Orthop Relat Res. 2006 ;450:164–71.
6. Zaretski A, Amir A, Meller I, Leshem D, Kollender Y, Barnea Y, Bickels J, Shpitzer T, Ad-El D, Gur E. Free fibula long bone reconstruction in orthopedic oncology: a surgical algorithm for reconstructive options. Plast Reconstr Surg. 2004 ;113(7):1989–2000.
7. Bus MP, Dijkstra PD, van de Sande MA, Taminiau AH, Schreuder HW, Jutte PC, van der Geest IC, Schaap GR, Bramer JA. Intercalary allograft reconstructions following resection of primary bone tumors: a nationwide multicenter study. J Bone Joint Surg Am. 2014 ;96(4):e26.
8. Frisoni T, Cevolani L, Giorgini A, Dozza B, Donati DM. Factors affecting outcome of massive intercalary bone allografts in the treatment of tumours of the femur. J Bone Joint Surg Br. 2012 ;94(6):836–41.
9. Ortiz-Cruz E, Gebhardt MC, Jennings LC, Springfield DS, Mankin HJ. The results of transplantation of intercalary allografts after resection of tumors. A long-term follow-up study. J Bone Joint Surg Am. 1997 ;79(1):97–106.
10. Aponte-Tinao L, Farfalli GL, Ritacco LE, Ayerza MA, Muscolo DL. Intercalary femur allografts are an acceptable alternative after tumor resection. Clin Orthop Relat Res. 2012 ;470(3):728–34.
11. Agarwal M, Puri A, Anchan C, Shah M, Jambhekar N. Hemicortical excision for low-grade selected surface sarcomas of bone. Clin Orthop Relat Res. 2007 ;459:161–6.
12. Funovics PT, Bucher F, Toma CD, Kotz RI, Dominkus M. Treatment and outcome of parosteal osteosarcoma: biological versus endoprosthetic reconstruction. J Surg Oncol. 2011 ;103(8):782–9. Epub 2011 Jan 15.
13. Chen WM, Wu PK, Chen CF, Chung LH, Liu CL, Chen TH. High-grade osteosarcoma treated with hemicortical resection and biological reconstruction. J Surg Oncol. 2012 ;105(8):825–9. Epub 2011 Dec 27.
14. Lewis VO, Gebhardt MC, Springfield DS. Parosteal osteosarcoma of the posterior aspect of the distal part of the femur. Oncological and functional results following a new resection technique. J Bone Joint Surg Am. 2000 ;82(8):1083–8.
15. Liu T, Liu ZY, Zhang Q, Zhang XS. Hemicortical resection and reconstruction using pasteurised autograft for parosteal osteosarcoma of the distal femur. Bone Joint J. 2013 ;95-B(9):1275–9.
16. Avedian RS, Haydon RC, Peabody TD. Multiplanar osteotomy with limited wide margins: a tissue preserving surgical technique for high-grade bone sarcomas. Clin Orthop Relat Res. 2010 ;468(10):2754–64. Epub 2010 Apr 25.
17. Filippou DK, Papadopoulos V, Kiparidou E, Demertzis NT. Adamantinoma of tibia: a case of late local recurrence along with lung metastases. J Postgrad Med. 2003 ;49(1):75–7.
18. Rose PS, Dickey ID, Wenger DE, Unni KK, Sim FH. Periosteal osteosarcoma: long-term outcome and risk of late recurrence. Clin Orthop Relat Res. 2006 ;453:314–7.
19. Hazelbag HM, Taminiau AH, Fleuren GJ, Hogendoorn PC. Adamantinoma of the long bones. A clinicopathological study of thirty-two patients with emphasis on histological subtype, precursor lesion, and biological behavior. J Bone Joint Surg Am. 1994 ;76(10):1482–99.
20. Gelderblom H, Hogendoorn PC, Dijkstra SD, van Rijswijk CS, Krol AD, Taminiau AH, Bovée JV. The clinical approach towards chondrosarcoma. Oncologist. 2008 ;13(3):320–9.
21. Deijkers RL, Bloem RM, Petit PL, Brand R, Vehmeyer SB, Veen MR. Contamination of bone allografts: analysis of incidence and predisposing factors. J Bone Joint Surg Br. 1997 ;79(1):161–6.
22. Grimer RJ, Taminiau AM, Cannon SR; Surgical Subcommitte of the European Osteosarcoma Intergroup. Surgical outcomes in osteosarcoma. J Bone Joint Surg Br. 2002 ;84(3):395–400.
23. Henderson ER, Groundland JS, Pala E, Dennis JA, Wooten R, Cheong D, Windhager R, Kotz RI, Mercuri M, Funovics PT, Hornicek FJ, Temple HT, Ruggieri P, Letson GD. Failure mode classification for tumor endoprostheses: retrospective review of five institutions and a literature review. J Bone Joint Surg Am. 2011 ;93(5):418–29.
24. Lindner N, Ozaki T, Hillmann A, Blasius S, Winkelmann W. Adjuvant local treatment of parosteal osteosarcoma. Int Orthop. 1996;20(4):233–6.
25. Elias JJ, Frassica FJ, Chao EY. The open section effect in a long bone with a longitudinal defect - a theoretical modeling study. J Biomech. 2000 ;33(11):1517–22.
26. Aponte-Tinao L, Ritacco LE, Ayerza MA, Luis Muscolo D, Albergo JI, Farfall GL. Does intraoperative navigation assistance improve bone tumor resection and allograft reconstruction results? Clin Orthop Relat Res. 2015 ;473(3):796–804.
27. Ritacco LE, Farfalli GL, Milano FE, Ayerza MA, Muscolo DL, Aponte-Tinao L. Three-dimensional virtual bone bank system workflow for structural bone allograft selection: a technical report. Sarcoma. 2013;2013:524395. Epub 2013 Apr 9.
28. Cascio BM, Thomas KA, Wilson SC. A mechanical comparison and review of transverse, step-cut, and sigmoid osteotomies. Clin Orthop Relat Res. 2003 ;411:296–304.
29. Clark CR, Morgan C, Sonstegard DA, Matthews LS. The effect of biopsy-hole shape and size on bone strength. J Bone Joint Surg Am. 1977 ;59(2):213–7.
30. Stoffel K, Stachowiak G, Forster T, Gächter A, Kuster M. Oblique screws at the plate ends increase the fixation strength in synthetic bone test medium. J Orthop Trauma. 2004 ;18(9):611–6.
31. Goulet JA, Senunas LE, DeSilva GL, Greenfield ML. Autogenous iliac crest bone graft. Complications and functional assessment. Clin Orthop Relat Res. 1997 ;339:76–81.
32. Finkemeier CG. Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am. 2002 ;84(3):454–64.
33. Hernigou P, Desroches A, Queinnec S, Flouzat Lachaniette CH, Poignard A, Allain J, Chevallier N, Rouard H. Morbidity of graft harvesting versus bone marrow aspiration in cell regenerative therapy. Int Orthop. 2014 ;38(9):1855–60.
34. Hornicek FJ, Gebhardt MC, Tomford WW, Sorger JI, Zavatta M, Menzner JP, Mankin HJ. Factors affecting nonunion of the allograft-host junction. Clin Orthop Relat Res. 2001 ;382:87–98.
35. Shehadeh A, Noveau J, Malawer M, Henshaw R. Late complications and survival of endoprosthetic reconstruction after resection of bone tumors. Clin Orthop Relat Res. 2010 ;468(11):2885–95.
36. Racano A, Pazionis T, Farrokhyar F, Deheshi B, Ghert M. High infection rate outcomes in long-bone tumor surgery with endoprosthetic reconstruction in adults: a systematic review. Clin Orthop Relat Res. 2013 ;471(6):2017–27. Epub 2013 Feb 12.
37. Jeys LM, Grimer RJ, Carter SR, Tillman RM. Periprosthetic infection in patients treated for an orthopaedic oncological condition. J Bone Joint Surg Am. 2005 ;87(4):842–9.
38. Farfalli GL, Aponte-Tinao L, Lopez-Millán L, Ayerza MA, Muscolo DL. Clinical and functional outcomes of tibial intercalary allografts after tumor resection. Orthopedics. 2012 ;35(3):e391–6.
39. Myers GJ, Abudu AT, Carter SR, Tillman RM, Grimer RJ. The long-term results of endoprosthetic replacement of the proximal tibia for bone tumours. J Bone Joint Surg Br. 2007 ;89(12):1632–7.
40. Mavrogenis AF, Papagelopoulos PJ, Coll-Mesa L, Pala E, Guerra G, Ruggieri P. Infected tumor prostheses. Orthopedics. 2011 ;34(12):991–8; quiz 999-1000.
41. Han I, Oh JH, Na YG, Moon KC, Kim HS. Clinical outcome of parosteal osteosarcoma. J Surg Oncol. 2008 ;97(2):146–9.
42. Szendroi M, Antal I, Arató G. Adamantinoma of long bones: a long-term follow-up study of 11 cases. Pathol Oncol Res. 2009 ;15(2):209–16. Epub 2008 Dec 2.
43. Ritschl P, Wurnig C, Lechner G, Roessner A. Parosteal osteosarcoma. 2-23-year follow-up of 33 patients. Acta Orthop Scand. 1991 ;62(3):195–200.
44. So TY, Lam YL, Mak KL. Computer-assisted navigation in bone tumor surgery: seamless workflow model and evolution of technique. Clin Orthop Relat Res. 2010 ;468(11):2985–91.
45. Bird JE. “Advances in the surgical management of bone tumors”. Curr Oncol Rep. 2014 ;16(7):392.
46. Gerbers JG, Ooijen PM, Jutte PC. Computer-assisted surgery for allograft shaping in hemicortical resection: a technical note involving 4 cases. Acta Orthop. 2013 ;84(2):224–6. Epub 2013 Feb 15.
47. Mankin HJ, Gebhardt MC, Jennings LC, Springfield DS, Tomford WW. Long-term results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res. 1996 ;324:86–97.
48. Mankin HJ, Springfield DS, Gebhardt MC, Tomford WW. Current status of allografting for bone tumors. Orthopedics. 1992 ;15(10):1147–54.
49. Torbert JT, Fox EJ, Hosalkar HS, Ogilvie CM, Lackman RD. Endoprosthetic reconstructions: results of long-term followup of 139 patients. Clin Orthop Relat Res. 2005 ;438:51–9.
50. Ahlmann ER, Menendez LR, Kermani C, Gotha H. Survivorship and clinical outcome of modular endoprosthetic reconstruction for neoplastic disease of the lower limb. J Bone Joint Surg Br. 2006 ;88(6):790–5.