Experimental study on the causes of spontaneous osteogenesis of Masquelet technique induced membrane_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

YIN Qudong ¹ , MAO Dong ² ,  RUI Yongjun ¹

1. Department of Orthopaedics, Wuxi No.9 People’s Hospital Affiliated to Soochow University, Wuxi Jiangsu, 214062, P. R. China;
2. Orthopedic Research Institute, Wuxi No.9 People’s Hospital Affiliated to Soochow University, Wuxi Jiangsu, 214062, P. R. China;

Corresponding?author：

RUI Yongjun, Email: ruiyongjun_md@163.com

Keywords：

Bone defect; Masquelet technique; induced membrane; spontaneous osteogenesis; rat

DOI：

10.7507/1002-1892.202403021

Video：

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Objective To investigate the causes of spontaneous osteogenesis of Masquelet technique induced membrane. Methods Forty-two male Sprague-Dawley rats aged 7-9 weeks were selected to establish a critical-sized bone defect of the right middle femur model. Then the rats were randomly divided into 4 groups, with 12 rats in groups A-C and 6 rats in group D. The bone defects in groups A-C were filled with vancomycin-loaded polymethyl methacrylate bone cement spacers. Then the Kirschner wires were used for intramedullary fixation in groups A and B, and the bone cement was used to connect the bone cement spacers and the bone ends in group B. The steel plate was used to fixation in group C. The bone defect in group D was only fixed with steel plate as a blank control group. The general condition was observed after operation. At 5 weeks after operation, 6 rats in groups A-C were selected for STRO-1 immunohistochemical staining to observe the content of mesenchyme stem cells (MSCs) in the induced membrane (STRO-1⁺ cells). At 12 weeks after operation, the remaining rats in groups A-D were taken for X-ray observation, gross observation, and histological observation (HE, safranin O-green staining) to observe the spontaneous osteogenesis of the membrane.Results All rats in the 4 groups survived until the completion of the experiment. At 5 weeks after operation, the immunohistochemical staining showed that group B was negative, while the contents of MSCs in the induced membrane in groups A and C were 14.20%±1.92% and 5.00%±0.71%, respectively, with a significant difference (P<0.05). At 12 weeks after operation, group A showed that the new bone formed at the osteotomy site and growth towards the center of the bone defect, with an average length of 3.1 mm on one side; and the presence of bone, cartilage lesions, fibers, and a small amount of neovascularization were observed in the induced membrane. Group C only had a small amount of new bone at the osteotomy site, and a small amount of neovascularization in the induced membrane. Groups B and D did not have any new bone, but bone resorption or atrophy at the osteotomy site. Conclusion Although the Masquelet technique induced membrane has osteogenesis, the key factor for the spontaneous osteogenesis is the bone marrow overflow from the bone marrow cavity providing MSCs. The spontaneous osteogenesis of the induced membrane belongs to endochondral ossification.

Citation： YIN Qudong, MAO Dong, RUI Yongjun. Experimental study on the causes of spontaneous osteogenesis of Masquelet technique induced membrane. Chinese Journal of Reparative and Reconstructive Surgery, 2024, 38(10): 1254-1260. doi: 10.7507/1002-1892.202403021 Copy

1.	Lu W, Zhao R, Fan X, et al. Time-varying characteristics of the induced membrane and its effects on bone defect repair. Injury, 2023, 54(2): 318-328.
2.	殷渠東, 孫振中, 顧三軍. 應用Masquelet技術修復骨缺損的研究進展. 中國修復重建外科雜志, 2013, 27(10): 1273-1276.
3.	Klein C, Monet M, Barbier V, et al. The Masquelet technique: Current concepts, animal models, and perspectives. J Tissue Eng Regen Med, 2020, 14(9): 1349-1359.
4.	Mathieu L, Murison JC, de Rousiers A, et al. The Masquelet technique: can disposable polypropylene syringes be an alternative to standard PMMA spacers? A rat bone defect model. Clin Orthop Relat Res, 2021, 479(12): 2737-2751.
5.	Luo J, Bo F, Wang J, et al. Application of the induced membrane technique of tibia using extracorporeal vs. intracorporeal formation of a cement spacer: a retrospective study. BMC Musculoskelet Disord, 2022, 23(1): 460. doi: 10.1186/s12891-022-05355-0.
6.	Wang JB, Yin QD, Gu SJ, et al. Induced membrane technique in the treatment of infectious bone defect: A clinical analysis. Orthop Traumatol Surg Res, 2019, 105(3): 535-539.
7.	Pereira R, Perry WC, Crisologo PA, et al. Membrane-induced technique for the management of combined soft tissue and osseous defects. Clin Podiatr Med Surg, 2021, 38(1): 99-110.
8.	Klaue K, Knothe U, Anton C, 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.
9.	Gruber HE, Gettys FK, Montijo HE, et al. Genomewide molecular and biologic characterization of biomembrane formation adjacent to a methacrylate spacer in the rat femoral segmental defect model. J Orthop Trauma, 2013, 27(5): 290-297.
10.	Yin Q, Chen X, Dai B, et al. Varying degrees of spontaneous osteogenesis of Masquelet’s induced membrane: experimental and clinical observations. BMC Musculoskeletal Disorders, 2023, 24(1): 384. doi: 10.1186/s12891-023-06498-4.
11.	Wang K, Gao F, Zhang Y, et al. Comparison of osteogenic activity from different parts of induced membrane in the Masquelet technique. Injury, 2023, 54(11): 111022. doi: 10.1016/j.injury.2023.111022.
12.	Henrich D, Seebach C, Nau C, et al. Establishment and characterization of the Masquelet induced membrane technique in a rat femur critical-sized defect model. J Tissue Eng Regen Med, 2016, 10(10): E382-E396.
13.	Pélissier P, Lefevre Y, Delmond S, et al. Influences of induced membranes on heterotopic bone formation within an osteo-inductive complex. Experimental study in rabbits. Ann Chir Plast Esthet, 2009, 54(1): 16-20.
14.	Caballé-Serrano J, Munar-Frau A, Ortiz-Puigpelat O, et al. On the search of the ideal barrier membrane for guided bone regeneration. J Clin Exp Dent, 2018, 10(5): e477-e483.
15.	Alford AI, Nicolaou D, Hake M, et al. Masquelet’s induced membrane technique: Review of current concepts and future directions. J Orthop Res, 2021, 39(4): 707-718.
16.	Tanner MC, Boxriker S, Haubruck P, et al. Expression of VEGF in peripheral serum is a possible prognostic factor in bone-regeneration via Masquelet-technique—A pilot study. J Clin Med, 2021, 10(4): 776. doi: 10.3390/jcm10040776.
17.	Gindraux F, Loisel F, Bourgeois M, et al. Induced membrane maintains its osteogenic properties even when the second stage of Masquelet’s technique is performed later. Eur J Trauma Emerg Surg, 2020, 46(2): 301-312.
18.	Fenelon M, Etchebarne M, Siadous R, et al. Comparison of amniotic membrane versus the induced membrane for bone regeneration in long bone segmental defects using calcium phosphate cement loaded with BMP-2. Mater Sci Eng C Mater Biol Appl, 2021, 124: 112032. doi: 10.1016/j.msec.2021.112032.
19.	薛英, 劉強. 膜引導性骨再生研究進展. 國際骨科學雜志, 2006, 27(2): 110-112.
20.	Miska M, Schmidmaier G. Diamond concept for treatment of nonunions and bone defects. Unfallchirurg, 2020, 123(9): 679-686.
21.	張浩, 盧世壁, 王繼芳. 引導性骨再生模型(GBR)成骨特點及骨髓的作用. 中華骨科雜志, 1998, 18(9): 540-543.
22.	芮菲, 卜凡玉, 張櫻嚴, 等. Masquelet技術治療骨缺損時體內制作與體外制作骨水泥間隔的療效比較. 中華創傷骨科雜志, 2021, 23(8): 674-680.

1. Lu W, Zhao R, Fan X, et al. Time-varying characteristics of the induced membrane and its effects on bone defect repair. Injury, 2023, 54(2): 318-328.
2. 殷渠東, 孫振中, 顧三軍. 應用Masquelet技術修復骨缺損的研究進展. 中國修復重建外科雜志, 2013, 27(10): 1273-1276.
3. Klein C, Monet M, Barbier V, et al. The Masquelet technique: Current concepts, animal models, and perspectives. J Tissue Eng Regen Med, 2020, 14(9): 1349-1359.
4. Mathieu L, Murison JC, de Rousiers A, et al. The Masquelet technique: can disposable polypropylene syringes be an alternative to standard PMMA spacers? A rat bone defect model. Clin Orthop Relat Res, 2021, 479(12): 2737-2751.
5. Luo J, Bo F, Wang J, et al. Application of the induced membrane technique of tibia using extracorporeal vs. intracorporeal formation of a cement spacer: a retrospective study. BMC Musculoskelet Disord, 2022, 23(1): 460. doi: 10.1186/s12891-022-05355-0.
6. Wang JB, Yin QD, Gu SJ, et al. Induced membrane technique in the treatment of infectious bone defect: A clinical analysis. Orthop Traumatol Surg Res, 2019, 105(3): 535-539.
7. Pereira R, Perry WC, Crisologo PA, et al. Membrane-induced technique for the management of combined soft tissue and osseous defects. Clin Podiatr Med Surg, 2021, 38(1): 99-110.
8. Klaue K, Knothe U, Anton C, 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.
9. Gruber HE, Gettys FK, Montijo HE, et al. Genomewide molecular and biologic characterization of biomembrane formation adjacent to a methacrylate spacer in the rat femoral segmental defect model. J Orthop Trauma, 2013, 27(5): 290-297.
10. Yin Q, Chen X, Dai B, et al. Varying degrees of spontaneous osteogenesis of Masquelet’s induced membrane: experimental and clinical observations. BMC Musculoskeletal Disorders, 2023, 24(1): 384. doi: 10.1186/s12891-023-06498-4.
11. Wang K, Gao F, Zhang Y, et al. Comparison of osteogenic activity from different parts of induced membrane in the Masquelet technique. Injury, 2023, 54(11): 111022. doi: 10.1016/j.injury.2023.111022.
12. Henrich D, Seebach C, Nau C, et al. Establishment and characterization of the Masquelet induced membrane technique in a rat femur critical-sized defect model. J Tissue Eng Regen Med, 2016, 10(10): E382-E396.
13. Pélissier P, Lefevre Y, Delmond S, et al. Influences of induced membranes on heterotopic bone formation within an osteo-inductive complex. Experimental study in rabbits. Ann Chir Plast Esthet, 2009, 54(1): 16-20.
14. Caballé-Serrano J, Munar-Frau A, Ortiz-Puigpelat O, et al. On the search of the ideal barrier membrane for guided bone regeneration. J Clin Exp Dent, 2018, 10(5): e477-e483.
15. Alford AI, Nicolaou D, Hake M, et al. Masquelet’s induced membrane technique: Review of current concepts and future directions. J Orthop Res, 2021, 39(4): 707-718.
16. Tanner MC, Boxriker S, Haubruck P, et al. Expression of VEGF in peripheral serum is a possible prognostic factor in bone-regeneration via Masquelet-technique—A pilot study. J Clin Med, 2021, 10(4): 776. doi: 10.3390/jcm10040776.
17. Gindraux F, Loisel F, Bourgeois M, et al. Induced membrane maintains its osteogenic properties even when the second stage of Masquelet’s technique is performed later. Eur J Trauma Emerg Surg, 2020, 46(2): 301-312.
18. Fenelon M, Etchebarne M, Siadous R, et al. Comparison of amniotic membrane versus the induced membrane for bone regeneration in long bone segmental defects using calcium phosphate cement loaded with BMP-2. Mater Sci Eng C Mater Biol Appl, 2021, 124: 112032. doi: 10.1016/j.msec.2021.112032.
19. 薛英, 劉強. 膜引導性骨再生研究進展. 國際骨科學雜志, 2006, 27(2): 110-112.
20. Miska M, Schmidmaier G. Diamond concept for treatment of nonunions and bone defects. Unfallchirurg, 2020, 123(9): 679-686.
21. 張浩, 盧世壁, 王繼芳. 引導性骨再生模型(GBR)成骨特點及骨髓的作用. 中華骨科雜志, 1998, 18(9): 540-543.
22. 芮菲, 卜凡玉, 張櫻嚴, 等. Masquelet技術治療骨缺損時體內制作與體外制作骨水泥間隔的療效比較. 中華創傷骨科雜志, 2021, 23(8): 674-680.

Chinese Journal of Reparative and Reconstructive Surgery

Experimental study on the causes of spontaneous osteogenesis of Masquelet technique induced membrane

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