Masquelet technique combined with artificial dermis for the treatment of bone and soft tissue defects in rabbits_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

 LIU Kui ¹ , WANG Yueming ² , SUN Yichong ¹ , QI Xiaoming ³ , TIAN Lijun ¹ , ZHAO Yanbin ¹ , XU Ying ¹ , LIU Xing ¹

1. No.2 Department of Traumatic Orthopedics, the Third Hospital of Shijiazhuang City Affiliated to Hebei Medical University (Shijiazhuang Orthopaedic Hospital), Shijiazhuang Hebei, 050000, P.R.China;
2. Rheumatology and Immunology Department of Traditional Chinese Medicine, No. 256 Hospital of Chinese PLA, Shijiazhuang Hebei, 050000, P.R.China;
3. Department of Neurology, the Second Hospital of Hebei Medical University, Shijiazhuang Hebei, 050000, P.R.China;

Corresponding author：

LIU Kui, Email: liukui8153@sina.com

Keywords：

Masquelet technology; induced membrane; artificial dermis; bone defect; soft tissue defect; rabbit

DOI：

10.7507/1002-1892.201811020

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Objective To investigate the effect of Masquelet technique combined with artificial dermis on repairing bone and soft tissue defects in rabbits, and to observe the microstructure and vascularization of induced membrane, so as to guide the clinical treatment of Gustilo-Anderson type Ⅲ open fracture with large bone defect and soft tissue defect.Methods Eighty male rabbits, weighing 2.03-2.27 kg (mean, 2.11 kg), were selected. The bilateral thighs of 64 rabbits were randomly divided into experimental group and control group, the remaining 16 rabbits were sham operation group. Bone and soft tissue defect models of femur were made in all rabbits. In the experimental group, the first stage of Masquelet technique was used [polymethyl methacrylate bone cement was filled in bone defect area] combined with artificial dermis treatment; in the control group, the first stage of Masquelet technique was used only; in the sham operation group, the wound was sutured directly without any treatment. Four rabbits in sham operation group and 16 rabbits in the experimental group and control group were sacrificed at 2, 4, 6, and 8 weeks after operation, respectively. The induced membranes and conjunctive membranes were observed on both sides of the femur. The membrane structure was observed by HE staining, and the microvessel density (MVD) was counted by CD34 immunohistochemical staining.Results Gross observation showed that the spongy layer of collagen in the artificial dermis of the experimental group disappeared completely at 4 weeks after operation, and the induced membrane structure of the experimental group and the control group was complete; the membrane structure of the control group was translucent, and the membrane structure of the experimental group was thicker, light red opaque, accompanied by small vessel proliferation. The membrane structure of the experimental group and the control group increased gradually from 6 to 8 weeks after operation. In the sham operation group, only scar tissue proliferation was observed over time. HE staining showed that a large number of muscle fibers and a small amount of collagen fibers proliferation with inflammatory cell infiltration could be seen in the experimental group and the control group at 2 weeks after operation; most of the sham operation group were muscle fibers with a small amount of interfibrous vessels. At 4 weeks after operation, collagen fibers increased and some blood vessels formed in the experimental group. The nuclei of collagen fibers in the control group were round-like, while those in the experimental group were flat-round. At 6 and 8 weeks after operation, the collagen fibers in the experimental group and the control group increased. The nuclei of the collagen fibers in the control group were still round-like. The nuclei of the collagen fibers in the experimental group were fusiformis and deeply stained compared with those in the control group. The proliferation of blood vessels was observed in both groups, and the number of proliferation vessels in the experimental group was increased compared with that in the control group. In the sham operation group, a large number of fibroblasts still appeared, but no significant proliferation of blood vessels with time was observed. CD34 immunohistochemical staining showed that MVD in each group increased gradually with the prolongation of time after operation. MVD in the sham operation group was significantly higher than that in the experimental group and the control group at 2 weeks after operation, and significantly smaller than that in the experimental group and the control group at 4, 6, and 8 weeks after operation (P<0.05). MVD in the experimental group was significantly higher than that in the control group at 4 and 6 weeks after operation (P<0.05), but there was no significant difference in MVD between the two groups at 2 and 8 weeks (P>0.05).Conclusion Masquelet technique combined with artificial dermis in the treatment of femoral bone defect and soft tissue defect in rabbits can significantly promote the vascularization of membrane structure at 4-6 weeks after operation. The combination of these two methods has guiding significance for the treatment of Gustilo-Anderson type Ⅲ open fracture with bone and soft tissue defects.

Citation： LIU Kui, WANG Yueming, SUN Yichong, QI Xiaoming, TIAN Lijun, ZHAO Yanbin, XU Ying, LIU Xing. Masquelet technique combined with artificial dermis for the treatment of bone and soft tissue defects in rabbits. Chinese Journal of Reparative and Reconstructive Surgery, 2019, 33(5): 578-585. doi: 10.7507/1002-1892.201811020 Copy

1.	Masquelet AC, Fitoussi F, Begue T, et al. Reconstruction of the long bones by the induced membrane and spongy autograft. Ann Chir Plast Esthet, 2000, 45(3): 346-353.
2.	Masquelet AC, Begue T. The concept of induced membrane for reconstruction of long bone defects. Orthop Clin North Am, 2010, 41(1): 27-37.
3.	Chen X, Chen H, Zhang G. Management of wounds with exposed bone structures using an artificial dermis and skin grafting technique. Clin Plast Surg, 2012, 39(1): 69-75.
4.	Molnar JA, DeFranzo AJ, Hadaegh A, et al. Acceleration of Integra incorporation in complex tissue defects with subatmospheric pressure. Plast Reconstr Surg, 2004, 113(5): 1339-1346.
5.	Lee LF, Porch JV, Spenler W, et al. Integra in lower extremity reconstruction after burn injury. Plast Reconstr Surg, 2008, 121(4): 1256-1262.
6.	Clerici G, Caminiti M, Curci V, et al. The use of a dermal substitute to preserve maximal foot length in diabetic foot wounds with tendon and bone exposure following urgent surgical debridement for acute infection. Int Wound J, 2010, 7(3): 176-183.
7.	Yeong EK, Yu YC, Chan ZH, et al. Is artificial dermis an effective tool in the treatment of tendon-exposed wounds. J Burn Care Res, 2013, 34(1): 161-167.
8.	Murray RC, Gordin EA, Saigal K, et al. Reconstruction radial forearm free flap donor site using integra artificial dermis. Microsurgery, 2011, 31(2): 104-108.
9.	Yeong EK, Chen SH, Tang YB. The treatment of bone exposure in burns by using artificial dermis. Ann Plast Surg, 2012, 69(6): 607-610.
10.	Tarchala M, Harvey EJ, Barralet J. Biomaterial-stabilized soft tissue healing for healing of critical-sized bone defects: the Masquelet technique. Adv Healthc Mater, 2016, 5(6): 630-640.
11.	Wiese A, Pape HC. Bone defects caused by high-energy injuries, bone loss, infected nonunions, and nonunions. Orthop Clin North Am, 2010, 41(1): 1-4.
12.	Viateau V, Guillemin G, Calando Y, et al. Induction of a barrier membrane to facilitate reconstruction of massive segmental diaphyseal bone defects: an ovine model. Vet Surg, 2006, 35(5): 445-452.
13.	Precheur HV. Bone graft materials. Dent Clin North Am, 2007, 51(3): 729-746.
14.	Wang F, Wang M, She Z, et al. Collagen/chitosan based two compartment and bi-functional dermal scaffolds for skin regeneration. Mater Sci Eng C Mater Biol Appl, 2015, 52: 155-162.
15.	Giannoudis PV, Faour O, Goff T, et al. Masquelet technique for the treatment of bone defects: tips-tricks and future directions. Injury, 2011, 42(6): 591-598.
16.	Mekhail AO, Abraham E, Gruber B, et al. Bone transport in the management of posttraumatic bone defects in the lower extremity. J Trauma, 2004, 56(2): 368-378.
17.	Pelissier P, Martin D, Baudet J, et al. Behaviour of cancellous bone graft placed in induced membranes. Br J Plast Surg, 2002, 55(7): 596-598.
18.	Myeroff C, Archdeacon M. Autogenous bone graft: donor sites and techniques. J Bone Joint Surg (Am), 2011, 93(23): 2227-2236.
19.	张磊, 王新卫, 陈雨声, 等. 应用Ilizarov技术治疗骨髓炎出现复杂软组织问题的处理技巧探讨. 中国修复重建外科杂志, 2018, 32(10): 1286-1291.
20.	Motsitsi NS. Masquelet's technique for management of long bone defects: from experiment to clinical application. East Cent Afr J Surg, 2012, 17(2): 43-47.
21.	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.
22.	Koga Y, Komuro Y, Yamato M, et al. Recovery course of full-thickness skin defects with exposed bone: an evaluation by a quantitative examination of new blood vessels. J Surg Res, 2007, 137(1): 30-37.
23.	沈余明, 陈辉, 胡骁骅, 等. 组织瓣移植联合骨延长技术分期修复烧创伤后下肢严重软组织与骨缺损. 中国修复重建外科杂志, 2017, 31(2): 160-164.
24.	Dantzer E, Braye FM. Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts. Br J Plast Surg, 2001, 54(8): 659-664.
25.	Burke JF, Yannas IV, Quinby WC Jr, et al. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg, 1981, 194(4): 413-428.
26.	Suzuki S, Matsuda K, Maruguchi T, et al. Further applications of " bilayer artificial skin”. Br J Plast Surg, 1995, 48(4): 222-229.
27.	Wosgrau AC, Jeremias Tda S, Leonardi DF, et al. Comparative experimental study of wound healing in mice: pelnac versus integra. PLoS One, 2015, 10(3): e0120322.
28.	Jeremias Tad S, Machado RG, Visoni SB, et al. Dermal substitutes support the growth of human skin-derived mesenchymal stromal cells: potential tool for skin regeneration. PLoS One, 2014, 9(2): e89542.
29.	Wong TM, Lau TW, Li X, et al. Masquelet technique for treatment of posttraumatic bone defects. ScientificWorldJournal, 2014, 2014: 710302.
30.	Gouron R, Petit L, Boudot C, et al. Osteoclasts and their precursors are present in the induced-membrane during bone reconstruction using the Masquelet technique. J Tissue Eng Regen Med, 2017, 11(2): 382-389.
31.	Aho OM, Lehenkari P, Ristiniemi J, et al. The mechanism of action of induced membranes in bone repair. J Bone Joint Surg (Am), 2013, 95(7): 597-604.
32.	Woon CY, Chong KW, Wong MK. Induced membranes-a staged technique of bone-grafting for segmental bone loss: a report of two cases and a literature review. J Bone Joint Surg (Am), 2010, 92(1): 196-201.
33.	Pelissier P, Masquelet AC, Bareille R, et al. Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res, 2004, 22(1): 73-79.
34.	Masquelet AC. Muscle reconstruction in reconstructive surgery: soft tissue repair and long bone reconstruction. Langenbecks Arch Surg, 2003, 388(5): 344-346.
35.	Christou C, Oliver RA, Yu Y, et al. The Masquelet technique for membrane induction and the healing of ovine critical sized segmental defects. PLoS One, 2014, 9(12): e114122.
36.	Kenneth Ward W. A review of the foreign-body response to subcutaneously-implanted devices: the role of macrophages and cytokines in biofouling and fibrosis. J Diabetes Sci Technol, 2008, 2(5): 768-777.

1. Masquelet AC, Fitoussi F, Begue T, et al. Reconstruction of the long bones by the induced membrane and spongy autograft. Ann Chir Plast Esthet, 2000, 45(3): 346-353.
2. Masquelet AC, Begue T. The concept of induced membrane for reconstruction of long bone defects. Orthop Clin North Am, 2010, 41(1): 27-37.
3. Chen X, Chen H, Zhang G. Management of wounds with exposed bone structures using an artificial dermis and skin grafting technique. Clin Plast Surg, 2012, 39(1): 69-75.
4. Molnar JA, DeFranzo AJ, Hadaegh A, et al. Acceleration of Integra incorporation in complex tissue defects with subatmospheric pressure. Plast Reconstr Surg, 2004, 113(5): 1339-1346.
5. Lee LF, Porch JV, Spenler W, et al. Integra in lower extremity reconstruction after burn injury. Plast Reconstr Surg, 2008, 121(4): 1256-1262.
6. Clerici G, Caminiti M, Curci V, et al. The use of a dermal substitute to preserve maximal foot length in diabetic foot wounds with tendon and bone exposure following urgent surgical debridement for acute infection. Int Wound J, 2010, 7(3): 176-183.
7. Yeong EK, Yu YC, Chan ZH, et al. Is artificial dermis an effective tool in the treatment of tendon-exposed wounds. J Burn Care Res, 2013, 34(1): 161-167.
8. Murray RC, Gordin EA, Saigal K, et al. Reconstruction radial forearm free flap donor site using integra artificial dermis. Microsurgery, 2011, 31(2): 104-108.
9. Yeong EK, Chen SH, Tang YB. The treatment of bone exposure in burns by using artificial dermis. Ann Plast Surg, 2012, 69(6): 607-610.
10. Tarchala M, Harvey EJ, Barralet J. Biomaterial-stabilized soft tissue healing for healing of critical-sized bone defects: the Masquelet technique. Adv Healthc Mater, 2016, 5(6): 630-640.
11. Wiese A, Pape HC. Bone defects caused by high-energy injuries, bone loss, infected nonunions, and nonunions. Orthop Clin North Am, 2010, 41(1): 1-4.
12. Viateau V, Guillemin G, Calando Y, et al. Induction of a barrier membrane to facilitate reconstruction of massive segmental diaphyseal bone defects: an ovine model. Vet Surg, 2006, 35(5): 445-452.
13. Precheur HV. Bone graft materials. Dent Clin North Am, 2007, 51(3): 729-746.
14. Wang F, Wang M, She Z, et al. Collagen/chitosan based two compartment and bi-functional dermal scaffolds for skin regeneration. Mater Sci Eng C Mater Biol Appl, 2015, 52: 155-162.
15. Giannoudis PV, Faour O, Goff T, et al. Masquelet technique for the treatment of bone defects: tips-tricks and future directions. Injury, 2011, 42(6): 591-598.
16. Mekhail AO, Abraham E, Gruber B, et al. Bone transport in the management of posttraumatic bone defects in the lower extremity. J Trauma, 2004, 56(2): 368-378.
17. Pelissier P, Martin D, Baudet J, et al. Behaviour of cancellous bone graft placed in induced membranes. Br J Plast Surg, 2002, 55(7): 596-598.
18. Myeroff C, Archdeacon M. Autogenous bone graft: donor sites and techniques. J Bone Joint Surg (Am), 2011, 93(23): 2227-2236.
19. 张磊, 王新卫, 陈雨声, 等. 应用Ilizarov技术治疗骨髓炎出现复杂软组织问题的处理技巧探讨. 中国修复重建外科杂志, 2018, 32(10): 1286-1291.
20. Motsitsi NS. Masquelet's technique for management of long bone defects: from experiment to clinical application. East Cent Afr J Surg, 2012, 17(2): 43-47.
21. 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.
22. Koga Y, Komuro Y, Yamato M, et al. Recovery course of full-thickness skin defects with exposed bone: an evaluation by a quantitative examination of new blood vessels. J Surg Res, 2007, 137(1): 30-37.
23. 沈余明, 陈辉, 胡骁骅, 等. 组织瓣移植联合骨延长技术分期修复烧创伤后下肢严重软组织与骨缺损. 中国修复重建外科杂志, 2017, 31(2): 160-164.
24. Dantzer E, Braye FM. Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts. Br J Plast Surg, 2001, 54(8): 659-664.
25. Burke JF, Yannas IV, Quinby WC Jr, et al. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg, 1981, 194(4): 413-428.
26. Suzuki S, Matsuda K, Maruguchi T, et al. Further applications of " bilayer artificial skin”. Br J Plast Surg, 1995, 48(4): 222-229.
27. Wosgrau AC, Jeremias Tda S, Leonardi DF, et al. Comparative experimental study of wound healing in mice: pelnac versus integra. PLoS One, 2015, 10(3): e0120322.
28. Jeremias Tad S, Machado RG, Visoni SB, et al. Dermal substitutes support the growth of human skin-derived mesenchymal stromal cells: potential tool for skin regeneration. PLoS One, 2014, 9(2): e89542.
29. Wong TM, Lau TW, Li X, et al. Masquelet technique for treatment of posttraumatic bone defects. ScientificWorldJournal, 2014, 2014: 710302.
30. Gouron R, Petit L, Boudot C, et al. Osteoclasts and their precursors are present in the induced-membrane during bone reconstruction using the Masquelet technique. J Tissue Eng Regen Med, 2017, 11(2): 382-389.
31. Aho OM, Lehenkari P, Ristiniemi J, et al. The mechanism of action of induced membranes in bone repair. J Bone Joint Surg (Am), 2013, 95(7): 597-604.
32. Woon CY, Chong KW, Wong MK. Induced membranes-a staged technique of bone-grafting for segmental bone loss: a report of two cases and a literature review. J Bone Joint Surg (Am), 2010, 92(1): 196-201.
33. Pelissier P, Masquelet AC, Bareille R, et al. Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res, 2004, 22(1): 73-79.
34. Masquelet AC. Muscle reconstruction in reconstructive surgery: soft tissue repair and long bone reconstruction. Langenbecks Arch Surg, 2003, 388(5): 344-346.
35. Christou C, Oliver RA, Yu Y, et al. The Masquelet technique for membrane induction and the healing of ovine critical sized segmental defects. PLoS One, 2014, 9(12): e114122.
36. Kenneth Ward W. A review of the foreign-body response to subcutaneously-implanted devices: the role of macrophages and cytokines in biofouling and fibrosis. J Diabetes Sci Technol, 2008, 2(5): 768-777.

Chinese Journal of Reparative and Reconstructive Surgery

Masquelet technique combined with artificial dermis for the treatment of bone and soft tissue defects in rabbits

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