A Novel Method to Assess Healing of Segmental Bone Defects using the Induced Membrane Technique

Abstract

Objective: Clinical concerns exist regarding the quality of bony consolidation in the context of the induced membrane technique. This study evaluates the clinical process of bone grafting in the second stage of induced membrane bone union in patients with tibial bone defects to infer the possibility of non-union and establish a reliable and effective evaluation method combined with computed tomography (CT) to assess fracture healing.

Methods: Patients with tibial bone defects who underwent the induced membrane technique at our hospital between February 2017 and February 2020 were retrospectively analyzed. The Hounsfield unit (HU) values of the patients were evaluated at different times during the second stage of bone grafting. Bone healing at the boundary value of the 120 HU output threshold (–1024 HU–3071 HU) was directionally selected, and the changes in the growth volume of union (new bone volume [selected according to HU value]/bone defect volume) were compared with analyzing individual class bone union. Method 1 involved X-rays revealing that at least three of the four cortices were continuous and at least 2 mm thick, with the patient being pain free. For Method 2, new bone volume (selected according to HU value/bone defect volume) at the stage was compared with analyzing individual class healing. Receiver operating characteristic curve analysis was used for Methods 1 and 2.

Results: A total of 42 patients with a segmental bone defect with a mean age of 40.5 years (40.5 ± 8.3 years) were included. The relationship between bone graft volume and time variation was analyzed by single factor repeated variable analysis (F = 6.477, p = 0.016). Further, curve regression analysis showed that the change in bone graft volume over time presented a logarithmic curve pattern (Y = 0.563 + 0.086 × ln(X), Ra² = 0.608, p = 0.041). ROC curve analysis showed that Method 2 is superior to Method 1 (AUC: 86.3% vs. 68.3%, p < 0.05).

Conclusion: The induced membrane technique could be used to treat traumatic long bone defects, with fewer complications and a higher healing rate. The proposed imaging grading of HU (new bone volume/bone defect volume) can be used as a reference for the quality of bony consolidation with the induced membrane technique.

Keywords

bone defect / bone union Bone reconstruction / induced membrane / open fracture

References

[1] Wiese A, Pape HC. Bone defects caused by high-energy injuries, bone loss, infected nonunions, and nonunions. Orthop Clin North Am. 2010; 41: 1–4.

[2] Schmitz JP, Hollinger JO. The critical size defect as an experimental model for craniomandibulofacialnonunions. Clin Orthop Relat Res. 1986; 205: 299–308.

[3] Ashman O, Phillips AM. Treatment of non-unions with bone defects: which option and why? Injury. 2013; 44(Suppl 1): S43–S45.

[4] Nauth A, McKee MD, Einhorn TA, et al. Managing bone defects. J Orthop Trauma. 2011; 25: 462–466.

[5] Obremskey W, Molina C, Collinge C, Tornetta P, Sagi C, Schmidt A, et al. Current practice in the management of open fractures among orthopaedic trauma surgeons. Part B: management of segmental long bone defects. A survey of orthopaedic trauma association members. J Orthop Trauma. 2014; 28: e203–e207.

[6] Haines NM, Lack WD, Seymour RB, Bosse MJ. Defining the lower limit of a “critical bone defect” in open diaphyseal tibial fractures. J Orthop Trauma. 2016; 30: e158–e163.

[7] Green SA. Skeletal defects. A comparison of bone grafting and bone transport for segmental skeletal defects. Clin Orthop Relat Res. 1994; 301: 111–117.

[8] Gubin A, Borzunov D, Malkova T. Ilizarov method for bone lengthening and defect management review of contemporary literature. Bull Hosp Jt Dis. 2013; 2016(74): 145–154.

[9] Iacobellis C, Berizzi A, Aldegheri R. Bone transport using the Ilizarov method: a review of complications in 100 consecutive cases. Strategies Trauma Limb Reconstr. 2010; 5: 17–22.

[10] Levin LS. Vascularized fibula graft for the traumatically induced long-bone defect. J Am Acad Orthop Surg. 2006; 14: S175–S176.

[11] Pederson WC, Person DW. Long bone reconstruction with vascularized bone grafts. Orthop Clin North Am. 2007; 38: 23–35.

[12] Shi S, Mercer S, Eckert GJ, Trippel SB. Growth factor transgenes interactively regulate articular chondrocytes. J Cell Biochem. 2013; 114: 908–919.

[13] Wang W, Yeung K. Bone grafts and biomaterials substitutes for bone defect repair: a review. Bioact Mater. 2017; 2: 224–247.

[14] Masquelet AC, Fitoussi F, Begue T, Muller GP. Reconstruction of the long bones by the induced membrane and spongy autograft. Ann Chir Plast Esthet. 2000; 45: 346–353.

[15] Masquelet A, Kanakaris NK, Obert L, Stafford P, Giannoudis PV. Bone repair using the Masquelet technique. J Bone Joint Surg Am. 2019; 101: 1024–1036.

[16] Cho JW, Kent WT, Oh CW, Kim BS, Cho WT, Oh JK. Bone-graft resorption reduced by the induced membrane technique and factors affecting volumetric changes: an analysis of 120 serial computed tomographic scans in 40 patients. J Bone Joint Surg Am. 2020; 102: 1269–1278.

[17] Oryan A, Alidadi S, Moshiri A, Maffulli N. Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res. 2014; 9: 18.

[18] Fischgrund J, Paley D, Suter C. Variables affecting time to bone healing during limb lengthening. Clin Orthop Relat Res. 1994; 301: 31–37.

[19] Skaggs DL, Leet AI, Money MD, Shaw BA, Hale JM, Tolo VT. Secondary fractures associated with external fixation in pediatric femur fractures. J Pediatr Orthop. 1999; 19: 582–586.

[20] Wang P, Wu Y, Rui Y, Wang J, Liu J, Ma Y. Masquelet technique for reconstructing bone defects in open lower limb fracture: analysis of the relationship between bone defect and bone graft. Injury. 2021; 52: 988–995.

[21] Anand A, Feldman DS, Patel RJ, Lehman WB, van Bosse HJP, Badra MI, et al. Interobserver and intraobserver reliability of radiographic evidence of bone healing at osteotomy sites. J Pediatr Orthop B. 2006; 15: 271–272.

[22] Liu YZ, Akhter MP, Gao X, Wang XY, Wang XB, Zhao G, et al. Glucocorticoid-induced delayed fracture healing and impaired bone biomechanical properties in mice. Clin Interv Aging. 2018; 13: 1465–1474.

[23] Gustilo RB, Mendoza RM, Williams DN. Problems in the management of type III (severe) open fractures: a new classification of type III open fractures. J Trauma. 1984; 24: 742–746.

[24] Stafford PR, Norris BL. Reamer-irrigator-aspirator bone graft and bi Masquelet technique for segmental bone defect nonunions: a review of 25 cases. Injury. 2010; 41(Suppl 2): S72–S77.

[25] Beaman FD, Bancroft LW, Peterson JJ, Kransdorf MJ, Menke DM, DeOrio JK. Imaging characteristics of bone graft materials. Radiographics. 2006; 26: 373–388.

[26] Lee SY, Kwon SS, Kim HS, Yoo JH, Kim J, Kim JY, et al. Reliability and validity of lower extremity computed tomography as a screening tool for osteo porosis. Osteoporos Int. 2015; 26: 1387–1394.

[27] Stowers JM, Black AT, Kavanagh AM, Mata KDL, Bohm A, Katchis SD, et al. Predicting nonunions in ankle fractures using quantitative tibial Hounsfield samples from preoperative computed tomography: a multicenter matched case control study. J Foot Ankle Surg. 2022; 61: 562–566.

[28] Sarkar MR, Augat P, Shefelbine SJ, Schorlemmer S, Huber-Lang M, Claes L, et al. Bone formation in a long bone defect model using a platelet-rich plasma-loaded collagen scaffold. Biomaterials. 2006; 27: 1817–1823.

[29] Klaue K, Knothe U, Anton C, Pfluger DH, Stoddart M, Masquelet AC, et al. Bone regeneration in long-bone defects: tissue compartmentalisation? In vivo study on bone defects in sheep. Injury. 2009; 40(Suppl 4): S95–S102.

[30] Pelissier P, Masquelet AC, Bareille R, Pelissier SM, Amedee J. Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res. 2004; 22: 73–79.

[31] Aho OM, Lehenkari P, Ristiniemi J, Lehtonen S, Risteli J, Leskelä HV. The mechanism of action of induced membranes in bone repair. J Bone Joint Surg Am. 2013; 95: 597–604.

[32] Gruber HE, Ode G, Hoelscher G, Ingram J, Bethea S, Bosse MJ. Osteogenic, stem cell and molecular characterisation of the human induced membrane from extremity bone defects. Bone Joint Res. 2016; 5: 106–115.

[33] Hazra S, Song HR, Biswal S, Lee SH, Lee SH, Jang KM, et al. Quantitative assessment of mineralization in distraction osteogenesis. Skeletal Radiol. 2008; 37: 843–847.

[34] Li R, Saleh M, Yang L, Coulton L. Radiographic classification of osteogenesis during bone distraction. J Orthop Res. 2006; 24: 339–347.

[35] Elsalanty ME, Genecov DG. Bone grafts in craniofacial surgery. Craniomaxillofac Trauma Reconstr. 2009; 2: 125–134.

[36] Yazar S. Onlay bone grafts in head and neck reconstruction. Semin Plast Surg. 2010; 24: 255–261.

[37] Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000; 371: 10–27.

[38] Gazdag AR, Lane JM, Glaser D, Forster RA. Alternatives to autogenous bone graft: efficacy and indications. J Am Acad Orthop Surg. 1995; 3: 1–8.

[39] Hertel R, Gerber A, Schlegel U, Cordey J, Rüegsegger P, Rahn BA. 10. Cancellous bone graft for skeletal reconstruction muscular versus periosteal bed—preliminary report. Injury. 1994; 25(Suppl 1): A59–A70.

[40] Greenwald AS, Boden SD, Goldberg VMK, et al. Bone-graft substitutes: facts, fictions, and applications. J Bone Joint Surg Am. 2001; 83-A(Suppl 2 Pt 2): 98–103.

[41] Keating JF, McQueen MM. Substitutes for autologous bone graft in orthopaedic trauma. J Bone Joint Surg Br. 2001; 83: 3–8.

[42] Taylor JC. Campbell’s Operative Orthopaedics. 1992.

[43] Firoozabadi R, Morshed S, Engelke K, Prevrhal S, Fierlinger A, Miclau T, et al. Qualitative and quantitative assessment of bone fragility and fracture healing using conventional radiography and advanced imaging technologies-focus on wrist fracture. J Orthop Trauma. 2008; 22: S83–S90.

[44] Ozcelik D, Huthut I, Kuran I, et al. Comparison of accuracy of three-dimensional spiral computed tomography, standard radiography, and direct measurements in evaluating facial fracture healing in a rat model. Ann Plast Surg. 2004; 53: 473–480.

[45] Riegger C, Kropil P, Jungbluth P, et al. Quantitative assessment of bone defect healing by multidetector CT in a pig model. Skeletal Radiol. 2012; 41: 531–537.

[46] Calhoun JH, Manring MM, Shirtliff M. Osteomyelitis of the long bones. Semin Plast Surg. 2009; 23: 59–72.

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