Submitted in fulfillment of the Requirements for the Degree of Doctor of Philosophy in Bio-Medical and Pharmaceutical Science of the Université

Multimodality Treatment of Soft Tissue and Bone Defect:

from Tissue Transfer to Tissue Engineering

Thesis

Submitted in fulfillment of the Requirements for the Degree of Doctor of Philosophy in Bio-Medical and Pharmaceutical Science of the Université

Libre de Bruxelles - Belgium by

LÊ THUA Trung Hau, MD. MSc

November 2015

Traitement Multimodalité des Défauts de l'Os et des Tissus Mous:

de Transfert Tissulaire à l'Ingénierie Tissulaire

Thèse pour l'Obtention du Grade Académique de Docteur en Sciences Biomédicales et Pharmaceutiques à l'Université Libre de Bruxelles -

Belgique

par

LÊ THUA Trung Hâu

Composition du Jury de Thèse:

Pr. Michel TOUNGOUZ VÉNESSIGNSKY (Hôpital Erasme - ULB, Président) Pr. Frédéric SCHUIND (Hôpital Erasme - ULB, Promoteur et Secrétaire)

Pr. Albert DE MEY (CHU Brugmann - ULB, Co-promoteur) Pr. BUI Duc Phu (Hue Central Hospital, Co-promoteur) Pr. Laurent FABECK (CHU Saint Pièrre - ULB, Membre) Pr. Valérie GANGJI (Hôpital Erasme - ULB, Membre) Pr. Laurence LAGNEAUX (Hôpital Erasme - ULB, Membre)

Pr. Philipp BLONDEEL (Universitair Ziekenhuis Gent, Expert extérieur)

Pr. Jan VRANCKX (Katholieke Universiteit Leuven, Expert extérieur)

© The Author

The author and the promoter give the authorization to consult and to copy parts of this work for personal use only. Any other use is limited by the Laws of Copyright.

Permission to reproduce any material contained in this work should be obtained from the author.

To cite this work:

Lê Thua, Trung-Hau (2015). Multimodality Treatment of Soft Tissue and Bone

Defect: from Tissue Transfer to Tissue Engineering. Ph.D. Thesis, Université Libre

de Bruxelles, Belgium, 101 pages.

Belgian Promoter: Prof. Frédéric SCHUIND Chairman, Dept. of Orthopaedics & Traumatology University Clinics of Brussels, Erasme Hospital Université Libre de Bruxelles, Belgium

Vietnamese Promoter: Prof. BUI Duc Phu Chairman, Dept. of Surgery, Hue University of Medicine & Pharmacy Director, Center of Cardiac Surgery Director, Hue Central Hospital, Vietnam

Belgian Co-Promoter (Former Promoter): Prof. Albert DE MEY Chairman, Dept. of Plastic Surgery Brugmann University Hospital Université Libre de Bruxelles, Belgium

Belgian Former Co-Promoter: Professor Willy Denis BOECKX

Chef de Clinique, Dept. of Plastic Surgery

Brugmann University Hospital

Université Libre de Bruxelles, Belgium

Dedicate to my grandfather

To my mother & father

To Ngoc Nhan, Trung Thong & Trung Dung

Table  of  Contents  

         Abbreviation  ………..……….………..ii  

       Acknowledgements  ……...………..……….iii  

    Section  I:  General  Introduction  ...  1  

Background  ...  2  

  Section  II:  Tissue  Transfer    ...  8  

1.  Anatomic  Variability  of  the  Vascularized  Composite  Osteomyocutaneous  Flap  from   the  Medial  Femoral  Condyle:  An  Anatomical  Study  ...  9  

2.  Vascularized  Fibular  Transfer  in  Longstanding  and  Infected  Large  Bone  Defects  ..  19  

3.  Missed  Compartment  Syndrome  of  the  Forearm:  Limb  Salvage  &  Reconstruction  29   4.  Free  Intra-­‐osseous  Vascularized  Muscle  Transfer  for  Treatment  of  Chronic   Osteomyelitis  ...  37  

  Section  III:  Tissue  Engineering    ...  48  

5.  Tissue  Engineering  using  Mesenchymal  Stem  Cells  with  Periosteal  Wrap  for  Bone   Defect  Repair  in  Rabbits  ...  49  

6.  Mini-­‐Invasive  Treatment  for  Delayed  or  Nonunion:  The  Use  of  Percutaneous   Autologous  Bone  Marrow  Injection  ...  64  

7.  Autologous  Bone  Marrow  Stem  Cells  combined  with  Allograft  Cancellous  Bone  in   Treatment  of  Nonunion  ...  77  

  Section  IV:  General  Discussion    ...  92  

General  Discussion  ...  93  

Summary  ...  101  

       Curriculum  Vitae………...……….v  

Abbreviations  

Descending genicular artery: DGA Superomedial genicular artery: SMA Superficial femoral artery: SFA Saphenous branch: SB

Muscular branch: MB Articular branch: AB

The Disabilities of Arm, Shoulder and Hand: DASH Allograft cancellous bone: ACB

Human demineralized cancellous bone: HDCB Demineralized bone matrix: DBM

Dulbecco’s Modified Eagle Medium: DMEM Fetal bovine serum: FBS

Mesenchymal stem cells: MSCs

Bone marrow mesenchymal stem cells: BM-MSCs Bone marrow aspiration concentrate: BMAC Colony-forming unit: CFU

Fibroblast colony-forming unit: CFU-F

Acknowledgements  

Almost of experimental and clinical research in this thesis were performed in the Center of Orthopaedic and Plastic Surgery, Regional Haematology and Blood Transfusion Center, and Medical Training Center at Hue Central Hospital, Hue City, Vietnam. Undertaking this work has been a truly life-changing experience for me and it could not have been completed without the help of a large number of my collaborators and my young colleagues. I am deeply indebted all of them and I wish to express my feelings of gratitude and respect to everybody who helped me achieve my goal, as well as my apology that I could not mention personally one by one.

I am especially grateful to Prof. BUI Duc Phu, my Vietnamese promoter, for his incredible support and encouragement throughout the process of studying and work.

He also was my instructor when I was a resident doctor and when I did my Master.

His personality and longing dedication is a good example to my career development.

I would like to express my profound feelings of   gratitude to Prof. Albert DE MEY, my Belgian co-promoter. He was also my former promoter, who has been the key person in my studies. With his consent, I had the opportunity to come to Belgium to study in Université Libre de Bruxelles, and got clinical experience at his Department of Plastic Surgery, Brugmann University Hospital. Many thanks for believing in my research and for supporting me every moment I spent in Brussels.

I would like to faithfully thank to Prof. Frédéric SCHUIND, my Belgian promoter, for agreeing to continue to guide me go all the way of my studies. His wisdom and open- mind deposition has helped me a lot in supporting, planning my work, and reviewing my manuscripts.

I wish to extend my sincere gratitude to Prof. Willy Denis BOECKX, my Belgian former co-promoter, for offering his endless energies to help me give ideas in the thesis and for the pleasant atmosphere he created inside and outside Hospital. I also appreciate him for helping me to improve my microsurgical skills.

I am profoundly thankful to Doctor PHAM Dang Nhat, to whom I have been close in the daily work throughout the years. Many thanks for creating the most favorable conditions for my study and pushing me to achieve the goals.

Respectfully, I acknowledge the Chairman of Faculty Doctoral Committee, Prof.

Philippe LEBRUN and the member of my Thesis Committee (Jury de Thèse): Prof.

Michel TOUNGOUZ (President), Prof. Valérie GANGJI, Prof. Laurent FABECK,

Prof. Laurence LAGNEAUX, Prof. Philipp BLONDEEL (UZGent), and

Prof. Jan VRANCKX (KUL). All my gratitude goes to them for their critical and valuable judgment of this work.

The various advice for my studies from Prof. Lester SILVER (USA), Prof. Christian DUPUIS (Belgium), Prof. NGUYEN Duy Thang (Vietnam) and Dr. LÊ Nghi Thanh Nhan (Vietnam) was very useful to me. All my best regards to Mrs Catherine LECLERCQ (Academic Secretariat in the Faculty of Medicine) and to Mrs. Carine Faniel (Registration Service) who helped me a lot for the last four years.

Furthermore, I am grateful to the Committee of the Belgian Development Agency (BTC) for selecting me as a Ph.D. Candidate for the 2011 Award. This is a wonderful opportunity to broaden my knowledge and experience in medical field.

Thanks to Mrs. Princia BAZABIDILA, Mrs. Francoise SCYEUR, Mrs. Julie JADOT-KONINCKX, Ms. Bénédicte SPEIDEL, and Mr. Nicolas BRECHT in the BTC headquarters in Brussels, Mrs. Huong and all staffs of the BTC Hanoi office for their care of my stays in Belgium as well as support of my work in Vietnam.

I profoundly appreciate for the opportunity to contact enthusiastic persons in Brussels. The Journalist HUYNH Chieu Duong and his family, where I have lived treated me as a member of the family. I also had an interesting experience to explore the culture of my homeland through Vietnam traditional martial art - Thuy Phap with Master Huynh and Belgian friends. Thanks a lot to Doctor HOANG Anh Hao and his family for greeting me to warm dinners. They all made me to feel less homesick.

Finally, this work is dedicated to my grandfather, who passed away before the end of my academic cursus. He always encouraged me and left his footprint in every event of my life. I would like to express the biggest appreciation and gratitude to my mother and father for having sacrificed and given their kids the best education in the most difficult years of their lives. My deepest thanks to my loving wife and two adorable boys for their patience and sacrifice when I was absent or busy for the thesis. They encouraged me to go on through dark moment. I would never finish this work without the support from my brothers, sisters, relatives and my friends, special thanks to all of them and the people in my life that supported me. They have also given me the strength and motivation to make my dreams a reality.

Thank you all.

LÊ THUA Trung Hau

Brussels, November 15, 2015

Section  I   General  Introduction  

Background    

The reconstruction of soft tissue and bone defects is a big challenge in the field of the plastic and reconstructive surgery, with a particular emphasis on road accidents in Vietnam. Soft tissue and bone defects are usually the results of wound healing complications after the trauma or the results of debridement of chronic wound such as osteomyelitis, nonunion.

Assessment of wound healing complications starts with an understanding of the healing process and risk factors. These processes have been grouped into three main stages: inflammation, fibroplasia, and maturation.

Interruption in any one of these stages can lead to wound healing complications.

Additionally, the identification of patients at risk such as diabetes, smoking, immunosuppressive medications, radiation, chemotherapy, and peripheral vascular disease for aberrant wound healing allows making appropriate plans for postoperative wound management. In chronic osteomyelitis, there is an inflammatory process accompanied by bone destruction and caused by an infecting microorganism.

There are two types of procedures undertaken in reconstructive surgery: ablative surgery and restorative surgery.

Ablative surgery

The goal of ablative surgery in the first stage is to completely remove the underlying lesion. The principle of the ablative procedure depends on specific etiologies. In the case of trauma, the ablative elements include control of hemorrhage, removal of foreign materials, and infected and devitalized tissue until to well-perfused margins, to create a healthy wound bed. In established chronic wounds such as osteomyelitis and nonunion, ablation includes removal of chronic, scarred tissue, involved infected bone to create an acute wound to promote healing. In acute injury, wounds must be extended past the zone of injury to ensure complete treatment.

Restorative surgery - Tissue transfer

The aim of restoration provides an optimum possible outcome to patients with injuries that damage and destroy parts of the body. The treatment must be based on an accurate definition of the restorative problems remaining after thorough ablation.

These restorative problems include the categories of wounds, defects and deformity.

In repairing a wound, restorative surgery must be able to identify important

components and use specific surgical techniques applicable to bone, tendon, nerve,

vessels and skin. Defects require restoring lost parts, and such replacements can

consist of grafts of skin, bone, nerve and vessel. Correction of deformity requires

mobilizing the distorted parts and reassembles them in some approximation of their

normal positional and functional relationships.

Among the injuries, there are a number of extensive wounds exposing the vital structures. Early definitive soft tissue coverage and bone reconstruction of this kind of wound with well-vascularized tissue and bone using microsurgical techniques are one of the most important stages of reconstruction for salvage the extremity and restoration of function. Microsurgical reconstruction using free tissue transfer is used for complex reconstructive surgery problems when other options such as primary closure, healing by secondary intention, skin grafting, or local or regional flap transfer, are not adequate. Microsurgery can offer the reconstructive surgeon an important tool to achieve complex reconstruction by proceeding with tissue transfer from distant healthy sites.

Tissue transfer involving microvascular anastomosis is an integral part of the post- infective reconstruction process. The advances in soft tissue and bone management culminate in the creation of a wound bed that is able to withstand the metabolic demands of more complex limb reconstruction procedures.

Tissue transfer has expanded reconstructive surgery’s elements and strategies. This large tissue transfer that is not affected by the local blood flow can considerably ameliorate local soft tissue perfusion. In ablative surgery, tissue transfer can provide possibilities of intricate dissections that can preserve critical structures during debridement and resections. Additionally, the expansion of repair and replacement strategies by free tissue transfer has in turn expanded the possibilities of ablative surgery that allow more thorough radical debridement obligatory for cure, irrespectively of the resulting defect. Furthermore, tissue transfer can decrease bacterial loads in surrounding tissues, improves the local biologic environment by bringing in a blood supply important for host defense mechanisms, raise an antibiotic carrying capacity and provide adequate filling of the recipient cavity. All these beneficial effects are due to increased oxygen tension in the tissues, increased supply in leukocytes and phagocytic activity, and finally low down bacterial counts in wounds reconstructed with tissue transfer.

All these microsurgical reconstructive procedures are a "one- step" procedure. This allows gaining time and reducing the "open-wound" period.

Tissue engineering

A frequent clinical application of skeletal muscle tissue is the microsurgical transfer

of tissue flaps for the coverage of soft tissue defect. Conventional surgical treatments

including distant autologous muscle transposition yield a limited degree of success.

As one major disadvantage, the use of tissue transfer is inevitably linked to certain

donor site morbidity including the loss of functional muscle tissue.

Additionally,

absorption due to inadequate blood supply, severe defects or deformities caused by trauma and osteomyelitis.

The allotransplantation of composite tissue has been used for such situations.

Nevertheless, immunological rejection, the life-long requirement for immunosuppressive medication and lack of proper donor sites, and more importantly, psychological rejection, making transplantation difficult to be a routine treatment.

Recent developments in the fields of tissue engineering have promised to present alternative methods for the repair of soft tissue and bone defects. Langer and Vacanti first mentioned tissue engineering in 1993 as "interdisciplinary fields of research that apply the principles of engineering and the life sciences towards the development of biological substitutes that restore, maintain, or improve tissue function".

Tissue transfer is an art, but tissue engineering is a new concept. The new thinking about tissue engineering is supported by technologies that were developed during the twentieth century, including advanced cell culture, gene transfer, and materials synthesis.

The exploration of unlimited tissue engineering sources has been considered to be a promising alternative for such cases. Significant advances have been achieved in this area, especially after various adult stem cells have been found to contribute to the regeneration of various tissues in the body.

Tissue engineering is defined as the combination of living cells and biocompatible scaffolds to generate a biologic substitute capable of sustaining itself and integrating with functional native tissue. By engineering and delivering tissues and/or cells capable of replacing damaged tissue, tissue engineering offers the potential for the treatment and possibly curing of debilitating diseases. Optimized methods for improving the function and maturation of engineered cellular constructs to produce constructs with near-native tissue properties are necessary to enable translation to clinically useful therapies.

In regenerative tissue engineering, there are many issues to consider in the creation of a functional, implantable replacement tissue.

Most importantly, there must be an easily accessible, readily abundant cell source with the capacity to express the desired tissues phenotype, and a biocompatible inert scaffold to deliver the cells to the damaged region.

Tissue engineering addresses the discrepancy between the available transplantable

donor tissue and the need. There are many choices for both cells and scaffolds, and

the best combination will vary depending on the type of injury, type of repair, and

the final desired outcome. Stem cells are an ideal cell source for bone regenerative

tissue engineering applications, because they are capable of self-renewal, are

differentiated, and can give rise to specialized tissue like bone. As understanding of

these cells improves, new engineering approaches will be developed to optimize the production of functional tissues.

Studies of derived stem cells are currently in progress, for their ability to overcome these limitations and improve therapeutic efficiency.

Previously published studies have described methods of tissue engineering that have been successfully applied for soft tissue and cartilage. Due to the different interactions of the hematopoietic and mesenchymal progenitor cells in the human bone marrow, a cell therapy strategy is a potential solution to treat bone tissue defects. Especially the stages involving osteoblast differentiation and bone healing induced by human bone marrow cells are currently being investigated.

Aims of the thesis

The aim of our research is threefold:

• Study in the anatomy of the vascular system of new tissue transfers, so that it provides more options and advantages of microsurgical reconstruction

• Evaluation of clinical applications of tissue transfer for treatment of the soft tissue and bone defects

• Experimental and clinical studies in the field of tissue engineering for treatment of the bone defect .

References

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19) Amorosa LF, Lee CH, Lee FY et al. Physiologic load-bearing characteristics of autograft, allografts, and polymer-based scaffolds in a critical sized segmental defect of long bone: an experimental study.

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Section  II  

  Tissue  Transfer    

1  

Anatomic  Variability  of  the  Vascularized   Composite  Osteomyocutaneous  Flap  from  the   Medial  Femoral  Condyle:  An  Anatomical  Study  

Trung-Hau LÊ THUA

, Duc-Phu BUI

, Dang-Nhat PHAM

, Vu-Bao LÊ

, Willy D.

BOECKX

, Albert DE MEY

1

Dept. of Plastic, Reconstructive & Hand Surgery, Center of Orthopaedic & Plastic Surgery, Hue Central Hospital, Hue City, Vietnam.

2

Dept. of Surgery, Hue University of Medicine and Pharmacy, Hue City, Vietnam.

3

Dept. of Surgery, An Sinh Hospital, Ho Chi Minh City, Vietnam.  

4

Dept. of Plastic Surgery, Brugmann University Hospital, Université libre de Bruxelles, Belgium.

Journal of Plastic and Aesthetic Research 201 4, 1 (3): 85 – 89.

ABSTRACT

Aim: The anatomical study and clinical application for the vascularized corticoperiosteal flap from the medial femoral condyle have been performed and described previously. Although prior studies have described the composite osteomyocutaneous flap from the medial femoral condyle, a detailed analysis of the vascularity of this region has not yet been fully evaluated.

Methods: This anatomical study described the variability of the arteries from the medial femoral condyle in 40 cadaveric specimens.

Results: The descending genicular artery (DGA) was found in 33 of 40 cases (82.5%). The superomedial genicular artery (SMA) was present in 10 cases (25%).

All 33 cases (100%) of the DGA had articular branches to the periosteum of the medial femoral condyle. Muscular branches and saphenous branches of the DGA were present in 25 cases (62.5%) and 26 cases (70.3%), respectively.

Conclusions: The current study demonstrates that the size and length of the vessels to the medial femoral condyle are sufficient for a vascularized bone flap. A careful preoperative vascular assessment is essential prior to use of the vascularized composite osteomyocutaneous flap from the medial femoral condyle, because of the considerable anatomical variations in the different branches of the DGA.

Keywords: Medial femoral condyle, osteomyocutaneous flap, descending genicular

artery, superomedial genicular artery

Introduction

The vascularized bone graft is the gold standard for reconstruction of bony defects, especially in case of chronic nonunion.

An anatomical studies and clinical applications for the use of a vascularized corticoperiosteal flap from the medial femoral condyle have been performed and described previously.

In 1991, Sakai and Doi initially reported the use of a thin, free vascularized corticoperiosteal graft for the treatment of persistent nonunion without significant bony defects in the upper limb.

It has been demonstrated that the articular branch of the descending genicular artery (DGA) or the superomedial genicular artery (SMA) perfuse the medial femoral condyle. There are also two branches from the DGA which supply the muscle and skin at the level of the medial femoral condyle; the saphenous branch (SB) supplies the skin at the medial knee and proximal third of the leg, and the muscular branch (MB) normally runs into the vastus medialis muscle.

This may allow the use of the DGA and its branches to form a composite osteomyocutaneous flap from the medial femoral condyle in the reconstruction of soft tissue and bone defects.

Although prior studies have described the composite osteomyocutaneous flap, the detail blood vessels in this region have not yet been fully elucidated. The aim of this study was to evaluate the anatomical variability of the vessels and their branches in the medial femoral condyle.

Materials and methods

Ten fresh and ten formalin preserved adult cadavers were dissected in our study, consisting of 11 males and 9 females. Forty cadaveric specimens were harvested from both thighs. The osteomyocutaneous medial femoral condylar flap was elevated using the medial approach initially described by Sakai and Doi.

Cadavers were placed into the supine position and a 15 cm longitudinal incision was made medially along the posterior border of the vastus medialis at the level of the distal femur, extending from the adductor hiatus proximally to the medial collateral ligament distally.

The fascia of the vastus medialis was then incised, and the muscle was retracted superiorly while the adductor magnus tendon was retracted inferiorly. The descending genicular artery (DGA) was exposed on the floor of the muscle compartment proximally and on the surface of the medial femoral condyle distally.

The SMA, a medial branch of the popliteal artery, was also studied. The anatomy of

the DGA and SMA with their branches and their areas of distribution were dissected,

branches and terminations in the skin as well as in the periosteum overlying the medial femoral condylar region were determined. A dominant artery between the DGA and SMA was defined as a main artery supply to the medial femoral condyle.

The position of the artery was measured as the distance from the origin to the knee joint. The length of the artery was defined as the distance from its origin to the area of termination. The outer diameter of the artery (d) was calculated through the perimeter of the peripheral arteries (P) by the following formula: d = P / 3.14.

The perimeter (P) was calculated by flattening the artery at its origin and using a digital caliper (Anyi Instrument Co. Ltd, China) to measure its flat section, and then doubled. In the fresh cadavers, we also performed a dye injection at the origin of the articular and saphenous branches of the DGA. This allowed visualization of the areas of the corticocancellous medial femoral condylar segment and skin paddle.

All measurements were recorded in millimeters, with an accuracy of 0.02 mm.

Results

The anatomical structures differed on the two sides of the thigh in the cadavers. The DGA origin from the superficial femoral artery (SFA) was found in 33 of 40 cases (82.5%). The DGA was absent in 7 cases. In three other cases, the DGA appeared together with the SMA. The SMA was present in 10 cases (25%). The DGA was dominant over the SMA in 33 of 40 cases (82.5%). In the remaining 7 cases (17.5%), the SMA was the major blood supply to the medial femoral condyle.

The DGA usually divided into branches; there were 11 (33.3%) cases of two branches, 21 cases (63.7%) of three branches and 1 (3%) case of four branches. The branches were the articular branches (AB), the saphenous branches (SB), and the muscular branches (MB). The mean position of the DGA was 119.1 mm above the knee joint with a range of 96.2 to 148.8 mm (SD 23.6 mm). The mean outer diameter of the DGA was 2.16 mm (range, 0.94 – 3.84 mm; SD 0.69 mm). From its origin to the onset of branching, there was a mean length of 11.7 mm (range, 0 - 40.33 mm;

SD 8.61 mm) (Fig. 1).

Fig 1: The vascular distribution of the descending genicular artery and its branches at the left femur in the fresh cadaver.

All 33 cases (100%) of the DGA sent articular branches (AB) to the periosteum of

the medial femoral condyle. The AB further divided into smaller branches to the

periosteum, with 1branch in 19 cases, 2 branches in 13 cases, and 3 branches in 1

case. The mean location of its origin was 100.7 mm above the knee joint with a range

from 70.3 to 129.4 mm (SD 13.4 mm). Its average length from the origin to the bone

was 56.4 mm (range, 23.8 – 80.5 mm; SD 14.4 mm). The mean outer diameter was

1.5 mm (SD 0.4 mm). The mean area of the periosteum of the medial femoral

condyle that the AB perfused was 37.8 × 25.7 mm (Fig. 2).

In 39 (97.5%) cases the MB supplied blood to the distal aspect of the vastus medialis muscle, and in one case the MB entered the gracilis muscle. In 25 cases (62.5%) the MB was a branch from the DGA, in 14 cases (36%) it came from the SFA, and in 1 case it branched off the AB. The mean length of the MB was 16.8 mm (SD 6.5 mm).

The mean outer diameter was 1.6 mm (SD 0.9 mm).

In 37 specimens (92.5%) the SB supplied the skin at the medial part of the knee and the proximal leg. In three specimens from the fresh cadavers, the SB ran to the gracilis muscle instead of towards the skin. The SB came off the DGA in 26 (70.3%) cases and the SFA in 11 (29.7%) cases. The mean location of the origin of the SB was 103 mm (SD 18.5 mm). Its mean outer diameter was 1.3 mm (SD 0.4 mm). 10 SB had one branch, and 27 SB had two branches to the skin at the medial part of the knee and the proximal part of the leg. In 13 specimens from the fresh cadavers, methylene blue was injected. A cutaneous angiosome distribution of the saphenous branch was noted on the medial aspect of the knee and proximal leg. The average perfusion area at the level of the skin was 244 × 115 mm (Fig. 3).

Fig 3: Cutaneous angiosome distribution of the saphenous branch at the medial side of the knee and proximal leg after injected methylene blue in fresh cadavers.

The superomedial genicular artery (SMA) existed in 10 (25%) specimens, and it was

dominant over the DGA in 7 cases (17.5%). The mean outer diameter was 1.33 mm

(SD 0.4 mm). The mean location of its origin was 88.5 mm (SD 17.8 mm) above

knee joint. The mean length of the SMA to the periosteum was 37.5 mm (SD 16.9

mm).

Discussion

Either the descending genicular artery or the superomedial genicular artery perfuses the medial femoral condyle. The current study evaluated the anatomical structures and variations of the DGA and SMA as well as their branches in adult cadavers. One half of cadavers were studied in fresh condition to facilitate the evaluation of the perfusion area of skin and bone.

Prior studies have shown that the outer diameter of the artery from fresh frozen cadavers is maintained. While the diameter of arteries from cadavers preserved in formalin retracts and loses its shape, the perimeter of the artery is maintained.

We calculated the outer diameter (d) of the artery through its perimeter (P) according to the following formula: P = 2R x 3.14 = d x 3.14 (R: Radius = d/2). This measurement allowed us to determine the outer diameter in non-inflated arteries.

Our study detected the DGA in 82.5% and the SMA in 25% of the 40 specimens.

Yamamoto et al. found the DGA in 89% and the SMA in 100% of the 19 specimens.

Rahmanian-Schwarz et al. harvested the DGA in 100% of the 21 specimens and Iorio et al. also discovered the DGA in 100% of the 12 specimens.

The difference between the studies is secondary to the number of specimens.

In the current study, the dominant vessels supplying the medial femoral condyle were the DGA in 82.5% of cases and the SMA in the DGA and17.5% of cases. Van Dijck et al. showed that in 70% of cases the DGA was dominant, while in 21% of cases the SMA was the dominant vessel. In 9% of cases the DGA and SMA supplied the medial femoral condyle equally.

A comparison between the measurements of the DGA in the current study and other studies is made in Table 1.

Table 1: The comparison between our results of DGA and other authors

Studies

The mean outer diameter of DGA

(mm)

The mean length from the origin to its branching

(mm)

The mean location above the knee joint

(mm)

Present study 2.16 ± 0.69 11.7 ± 8.61 119.1 ± 23.6

Van Dijck et al.

2.43 ± 0.88 89 ± 21.8 137 ± 18.8

Rahmanian-Schwarz et

al.

2.9 (1.5 - 4.5) 25 (5 - 40) 147 (120 - 170)

addition, the AB of the DGA or the SMA always nourishes the periosteum of the medial femoral condyle. These arteries have adequate diameter and length to supply the medial femoral condylar flap. In the absence of the DGA, the SMA has sufficient size, but the vascular pedicle is shorter, and SMA is used only for a pure bone flap.

The results of previous studies of Jones, Yamamoto, Van Dijckand, and De Smet also made similar conclusions about the viability of this bone flap using the DGA or the SMA for treatment of small bony defects, especially in the treatment of non- union fractures that require a good blood supply for bone grafting.

In the specific study of Jones et al., vascular pedicles of the vascularized medial femoral condylar flap for the treatment of scaphoid non-union were the DGA in 10 cases and the SMA in 2 cases.

In many cases of chronic non-union, the soft tissue usually has a fibrous scar, infectious environment and a vascular contracture. Extensive debridement of infected and devitalized tissue and bone back to bleeding tissue is required. Vascularized bone graft associated with a well-vascularized muscle or skin paddle is necessary in these cases. In the case of small bony defects (< 6 cm), the vascularized composite osteomyocutaneous flap from medial femoral condyle can fill the dead space of bone and soft tissue. It also minimizes the risk of deep tissue infection. By increasing the vascularity and the blood supply of the composite flap, limb salvage can be obtained with a single surgical procedure. Vascularized bone grafting can be combined with muscle tissue and a skin island, and thus can be used to solve complex problems in cases with bone and soft tissue defects.

The current study showed 100% of AB, 62.5% of MB and 70.3% of SB branches come from the DGA. It allows the use of the medial femoral condylar bone flap, and this can be combined with muscle or skin in some cases. However, preoperative vascular assessment of this flap with an angiogram is very important due to the anatomical variation of the DGA as well as its muscular and saphenous branches.

This result differs from previous reports which studied fewer specimens; Iorio et al.

identified the SB in 11 of 12 specimens (92%).

Rahmanian-Schwarz et al. studied 21 specimens, and in 91.5%, the DGA split into 3 branches: AB, MB and SB.

Yamamoto et al. showed that the SB was detected in 79% of their 19 specimens, branching off a common trunk with AB.

Van Dijck et al. found that the SB was present in 14 (41%) of the 27 cases.

Conclusions

The current study demonstrates that the size and length of the vessels supplying the

medial femoral condyle are sufficient for a vascularized bone flap. This graft is very helpful in the treatment of chronic non-union and small bone gap reconstruction.

Although many studies have reported the viability of the vascularized composite osteomyocutaneous flap from the medial femoral condyle, a careful preoperative vascular assessment is essential secondary to the considerable anatomical variations in the different branches of the descending genicular artery. Further clinical studies will be required to clearly define the success of this composite osteomyocutaneous flap.

Acknowledgements

The authors would like to thank the Department of Anatomy, Ho Chi Minh University of Medicine and Pharmacy, Vietnam. We are grateful to Doctors LÊ Nghi Thanh Nhan, Paul LUU, NGUYEN Van Phung, and Peter SCOUGALL for their excellent help and support.

References

1. Rahmanian-Schwarz A, Spetzler V, Amr A, Pfau M, Schaller HE, Hirt B. A composite osteomusculocutaneous free flap from the medial femoral condyle for reconstruction of complex defects. J Reconstr Microsurg 2011; 27:251- 60.

2. Bürger HK, Windhofer CW, Gaggl AJ, Higgins JP. Vascularized medial femoral trochleaosteocartilaginous flap reconstruction of proximalpole scaphoid nonunions. J Hand Surg 2013;38:690-700.

3. Iorio ML, Masden DL, Higgins JP. The limits of medial femoral condyle corticoperiosteal flaps. J Hand Surg 2011;36:1592-6.

4. Doi K, Sakai K. Vascularized periosteal bone graft from the supracondylar region of the femur. Microsurgery 1994,15:305-15.

5. Sakai K, Doi K, Kawai S. Free vascularized thin corticoperiosteal graft.

Plastic Reconstr Surg 1991;87:290-8.

6. Van Dijck C, Mattelaer B, De Degreef I, De Smet L. Arterial anatomy of the free vascularised corticoperiosteal graft from the medial femoral condyle.

Acta Orthop Belg 2011;77:502-5.

7. Yamamoto H, Jones DB, Moran SL, Bishop AT, Shin AY. The arterial anatomy of the medial femoral condyle and its clinical implications. J Hand SurgEurVol2010; 35:569.

8. Doi K, Hattori Y. Vascularized bone graft from the supracondylar region of

9. Bakri K, Shin AY, Moran SL. The vascularized medial femoral corticoperiosteal flap for reconstruction of bony defects within the upper and lower extremities. Semin Plast Surg 2008; 22:228-33.

10. Jones DB, Burger H, Bishop AT, Shin AY. Treatment of scaphoid waist nonunion with a vascular proximal pole and carpal collapse. J Bone Joint Surge Am 2008; 90:2616-25.

11. Jones DB, Moran SL, Bishop AT, Shin AY. Free-vascularized medial femoral condyle bone transfer in the treatment of scaphoid nonunions. Plast Reconstr Surg 2010; 125:1176.

12. Kakar S, Duymaz A, Steinmann S, Shin AY, Moran SL. Vascularized medial femoral condyle corticoperiosteal flaps for the treatment of recalcitrant humeral nonunions. Microsurgery 2011; 31:85-92.

13. De Smet L. Treatment of non-unions of forearm bones with a free vascularised corticoperiosteal flap from the medial femoral condyle. Acta Orthop Belg 2009;75:611-5.

14. Del Pinal F, Garcia-Bernal FJ, Regalado J, Ayala H, Cagigal L, Studer A.

Vascularised corticoperiosteal grafts from the medial femoral condyle for difficult non-unions of the upper limb. J Hand Surg Eur Vol 2007;32:135-42.

15. Rodrıguez-Vegas JM, Delgado-Serrano PJ. Corticoperiosteal flap in the treatment of nonunions and small bone gaps: technical details and expanding possibilities. J Plast Reconstr Aesthet Surg2011;64:515-27.

16. Iorio ML, Masden DL, Higgins JP. Cutaneous angiosome territory of the

medial femoral condyle osteocutaneous flap. J Hand Surg 2012;37:1033-41.

2  

Vascularized  Fibular  Transfer  in  Longstanding    and  Infected  Large  Bone  Defects  

Trung-Hau LÊ THUA

, Dang-Nhat PHAM

, Willy D. BOECKX

, Albert DE MEY

1

Dept. of Plastic, Reconstructive & Hand Surgery, Center of Orthopaedic & Plastic Surgery, Hue Central Hospital, Hue City, Vietnam.

2

Dept. of Plastic Surgery, Brugmann University Hospital, Université libre de Bruxelles, Belgium.

Acta Orthopaedica Belgica 2014, 80 (1): 50-55.

Abstract

Background: The reconstruction of large bone defects in the infectious environment is still a big challenge for limb salvage because of disturbance in bacterial flora, bacterial resistance and limitation of blood supply at scarred tissue. This retrospective study was to evaluate long-term outcomes in patients who were performed vascularized fibular transfers for treatment of large bone defects in the infectious environment.

Patients and Methods: The review included 26 patients with an average age of 27 years old. Bone defects were located at the arm in 1 patient, the forearm in 2 patients, the thigh in 6 patients and the leg in 17 patients. The cause of the bone defects included high-energy trauma in 14 cases, chronic osteomyelitis in 7 cases, infected non-union in 5 cases. All patients had had several previous operative procedures.

Results: The average length of fibular vascularized graft was 16.6 cm (range, 10 – 22 cm), and the average size of the associated fasciocutaneous component in 16 patients was 3.6 x 8.5 cm. Three patients had partial necrosis of skin paddle. Three patients, who were stabilized by screw and external fixator, had an infection at the distal part of the fibular graft and pin tracts. 25 fibular grafts (96%) showed complete bone union.

Conclusions: This review has showed that the vascularized fibular transfer can be effective for management of large segmental bone defects in the infectious environment.

Keywords:

Vascularized fibular transfer, large bone defects, osteomyelitis and infected non-

union.

Introduction

The reconstruction of large bone defects in the infectious environment is still a challenge for limb salvage because of disturbance in bacterial flora, bacterial resistance, insufficient bone debridement and limitation of blood supply in scarred tissue (3, 10). Several reconstructive procedures have been attempted, but a biological option was to use autogenous bone. Donor autogenous bones that were used for vascularized bone graft include the fibula, ilium, scapula, and rib. But the vascularized fibular graft is a well- recognized donor of vascularized bone (2, 7, 9, 16, 17, 18).

Taylor et al. published the first successful description of vascularized fibular graft in 1975 (20). Yoshimura et al. described the first use of vascularized fibular graft with skin paddle in 1983 (22). Vascularized fibular graft has important advantages to the mechanism of bone healing by maintaining the viability of the graft and strengthening mechanical properties allows for faster union and graft hypertrophy irrespective of the avascular and infectious bed (9).

The purpose of this retrospective study was to evaluate long-term outcomes with patients in whom we performed vascularized fibular transfers for treatment of large bone defects in the infectious environment.

Patients and Methods

The review included 26 patients (18 males and 8 females) had large bone defects caused by Gustilo’s grades IIIB or IIIC open fracture, chronic osteomyelitis, or infected nonunion between 1999 and 2010. Bone defects (larger than 6 cm) were located at the arm in 1 patient, the forearm in 2 patients, the thigh in 6 patients and the leg in 17 patients. The cause of the bone defects included high-energy trauma in 14 cases, chronic osteomyelitis in 7 cases, infected nonunion in 5 cases. All patients had had several previous operative procedures: 3 patients had a bone loss associated with a very large soft tissue defect, they were previously covered soft-tissue defect before the fibular transfer: One pedicled abdominal flap at the forearm and two free latissimus dorsi flap at the leg (Table I). The delay between the accident and vascularized fibular transfer ranged from 4 months to 5 years.

Operative technique

Two teams operated simultaneously, one harvesting the fibular graft, and the other

preparing the recipient site. The vascularized fibular graft was assessed using a lateral

approach described by Gilbert (8). An angiography was carried out in case of history of

severe trauma and soft-tissue contracture.

Table I: Initial Treatment before reconstruction.

Position Initial treatment (n)

Humerus Radius &

Ulna

Femur Tibia

Internal plate (3) 1 2

Debridement + EF (13) 5 8

Serial debridement +/- VAC (7) 1 1 5

Pedicled abdominal flap (1) 1

Free latissimus dorsi flap + EF (2) 2

Total 1 2 6 17

EF: External Fixator, VAC: Vacuum Assisted Closure

At the donor site: Doppler sonography marked preoperatively the pedicle vessels and cutaneous perforators (14). If it is necessary, the graft was harvested by incorporating the skin island to provide soft-tissue coverage and to allow postoperatively monitoring of the graft (12). The length of fibular graft depends on the bone defects, which was usually the length of bone defects minimum plus 4 cm. The distal cut had to more than 8 cm above the lateral malleolus.

At the recipient site: Infected and devitalized tissue was radically debrided, all contracted scar and inflammatory tissue was thoroughly excised and both proximal and distal parts of the medullary canal were resected and reamed until good vascularized bone was found.

Samples of all tissue and bone were sent for bacterial cultures. The vessels of the recipient site were carefully dissected and exposed. Impacting both ends of the graft into the medullary cavity of the recipient bone was required. Bone fixation using screws, plate, Kirschner wires or external fixator was then achieved depending on the individual requirements of the particular defect. The peroneal vessel attached to the fibular graft was anastomosed to the recipient vessel with 9.0 interrupted nylon sutures using the microsurgical technique.

Clinical examination including color, capillary refill and bleeding were carefully be observed. Doppler sonography was used if necessary. IV antibiotics were given according to the microbiological sensitivity test. The patient was followed-up every 3 months in the first year and every 6 months from 1 year to 3 years, continuously followed up until full bone union, determined by clinical examination and radiographs.

Differences between groups of trauma, osteomyelitis and chronic non-union at the table III

were assessed using Fisher’ exact test and Anova test. A p value < 0.05 was considered

statistically significant. Statistical analyses were performed using SPSS version 18.0 (SPSS Inc., Chicago, IL).

Results

The average age of these patients was 27 years old (range, 2 – 57 years old). The average length of bone defect was 10.8 cm (range, 8 - 16 cm). The average length of the fibular vascularized graft was 16.6 cm (range, 10 – 22 cm); 16 patients with soft tissue contractures required a fibular graft reconstruction with skin paddle, and the mean size of the associated fasciocutaneous component was 3.6 x 8.5 cm. Fibular grafts were stabilized to the recipient bone by Kirschner wires, transcortical screws, bridge plates or external fixators associated with transcortical screws (Table II).

Table II: Methods of the fibular graft stabilization into the recipient bone.

Position Stabilization (n)

Humerus Radius &

Ulna

Femur Tibia

Kirschner wire (3) 1 1 1

Transcortical screws (3) 3

Bridge plate (11) 1 5 5

External fixator & screws (9) 1 8

Total 1 2 6 17

There were no intraoperative complications. Three patients had postoperatively partial skin

paddle necrosis that needed wound care and a secondary skin graft. In three patients,

stabilized by screws and external fixator, an infection was present at the distal part of the

fibular end and a pin tract infection. All of them were treated with debridement, screws

removal, pin tract transposition and antibiotics. Twice infection was controlled and the

cancellous bone autograft procedure was carried out after 3 months. But one was still a

deep infection and patient refused any further treatment and the upper third of the leg was

amputated.

Table III: Characteristics between groups of trauma, chronic osteomyelitis and infected non-union.

Group Characteristics

Trauma (n=14)

Osteomyelitis (n=7)

Infected non- union (n=5)

p value

Positive bacterial cultures 10 7 5 0.308

Previous flap coverage 2 1 0 1.000

Bony gap (cm) 8.2 11.9 6.8 0.001

Post-op infection 2 1 0 1.000

Primary bone union 12 6 5 1.000

Delay bone union 2 0 0 0.692

Failure 0 1 0 0.462

Long-term malunion 0 1 0 0.462

All remaining 25 bone grafts survived. No patient had a functional problem of the donor site. (Fig 1, 2) Only one patient, however, complained about intermittent ankle joint pain when he walked a long distance during the first six months follow-up, but this pain was relieved after one-year follow-up. Normal bone union occurred in 23 patients with a mean healing time of 3.5 months (range, 2 – 5 months). Delayed bone union in 2 patients with a mean healing time of 8 months (range, 7 – 10 months). One 9-year-old patient had an angular deformity and shortening of the leg 5 years after the fibular transfer. When he was 15 years old, he was operated for correcting the deformity and lengthening of the tibia utilizing an Ilizarov procedure (Table III).

Discussions

Our study showed that this vascularized fibular graft has been successful in reconstruction

of large bone defects in the infectious environment. The healing mechanisms of a

vascularized bone graft are distinctly different from the other procedures, restoration of the

physiologic blood flow occurs immediately at the completion of the microvascular

anastomosis. This circumstance retains osteoblastic and osteoclastic potential for primary

bone healing as in a simple fracture (1). Heitmann et al. reported that, vascularized bone

grafts remain alive, do not resorb, maintain their structural characteristics, and increase its

structural strength through hypertrophy (5). This graft allows surgeons to accomplish a

series of extensive debridement of infected and devitalized both tissue and bone back to

a b c d

Fig 1. — Radiograph of 38-year-old male patient had an atrophic and infected non-union associated with soft-tissue contracture of the left tibia. Patient had undergone four-time surgery for osteomyelitis after open fracture by a motorcycle accident 5 years ago (a).

Radiograph of vascularized fibular transfer with skin paddle and stabilization by bridged plate (b). Patient had a bone healing in radiograph (c) and restored the normal function of the leg at 2 years follow-up (d).

bleeding ones regardless how much defect will be. By immediate blood supply, this graft brings also antibiotic and immune components to the recipient site to control the infection (3, 6, 8). Furthermore, the fibular graft provides adequate length up to 26 cm, the predictable anatomy, mechanical strength and hypertrophy potential. Therefor the vascularized fibular graft is presented as the most suitable autograft for restoring the large segmental bone defects, involving high-energy trauma, chronic osteomyelitis and infected non-union in both upper and lower extremities (1, 5, 8). In addition, the fibular graft has the ability to be combined with a skin island, can be used to solve complex problems in bone and soft-tissue defects (5, 6, 15, 16, 22).

a b c d

Fig 2. — Radiograph of 28-years-old male patient had segmental bone defect at the left femur caused by open fracture and stabilized temporarily with an external fixator (a).

Postoperative radiograph showed a femoral reconstruction with vascularized fibular

The study reported no evidence of the any resorption of the vascularized fibular graft. 25 fibular grafts (96%) showed complete bone union, this compares favorably with other authors. Falder et al., success rate was 91% (29 over 32 grafts) (4), and Soucacos et al., graft healing was achieved in 92% in the upper limb (37 out of 40) (19).

One of the most important conditions for graft healing is the very strong fixation of the fibular graft. This fibular graft acts as a biological intramedullary nail, and cortical screws that fixed through the fibula and the host bone at both ends, play a role of interlocking screws (23). Kirschner wires, bridge plate or external fixator supported the fibular graft stabilization. But Kirschner wires were used only in the children. In the first period of our series, external fixators were continuously utilized for graft stabilization in the lower limb.

However, in the long-term, pin tract infections can occur. For this reason, we tried to use internal fixation for the entire femoral length. As much as possible, we used the same technique for the tibia.

Our trauma group included 14 patients who had a high risk of infection or had been extensively debrided. The fibular transfer was performed in a second stage (Figure 2). This well-vascularized composite graft permitted resection of all infected tissue and devitalized bone down to a bleeding zone. The amount of soft tissue or bone that had to be removed was not limited. Our goals of reconstruction by vascularized fibular graft were filling the dead space, minimizing the deep tissue infection and preventing the development of osteomyelitis (8, 23).

Twelve patients in the group of chronic osteomyelitis and infected non-union were failures of several previous procedures. The local situation of the recipient site showed many complications such as: bone atrophy, infectious environment and avascular soft-tissue contracture. By increasing the vascularity and the blood supply of the fibular graft, limb salvage could be obtained with a single surgical procedure (Fig 1). We had 11 bone unions and 1 failure in this group. Yajima et al. obtained bony union in 18 of 20 cases (21). The disadvantage of our study is that the fibular graft is smaller than the host bone, especially in the femur (13, 15). One of 6 patients, who had a short femoral bone defect, was treated using the double-barrel technique. But the remaining 5 patients, we could not perform that technique and needed to wait a long time before hypertrophy allowed complete weigh bearing.

Conclusions

This study has showed that the vascularized fibular transfer can be effective for

management of large bone defects in the infectious environment. Many of these patients

had been treated for many years; especially the ongoing infection, osteomyelitis,

insufficiently large debridement and nonunion were the causes for failed bony union. The

advantage is the possibility to restore the length of the bone with a single procedure and

provide a return to normal life for the patient. Therefore this fibular transfer remains our reconstructive choice for limb salvage.

Conflict of interest statement:

No benefits or funds were received in support for this study.

There was no conflict of interest.

References

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2. Belt PJ, Dickinson IC, Theile DRB. Vascularized free fibular flap in bone resection and reconstruction. Br J Plast Surg 2005; 50: 425-430.

3. Beris AE, Lykissas MG, Soucacos PN et al. Vascularized fibula transfer for lower limb reconstruction. Microsurgery 2011; 31: 205-211.

4. Gilbert A. Free vascularized bone grafts. Intern Surg 1991; 66: 27-31.

5. Heitmann C, Erdmann D, Levin LS. Treatment of segmental defects of the humerus with an osteoseptocutaneous fibular transplant. J Bone Joint Surg 2002; 84-A12: 2216- 23.

6. Jupiter J, Gerhard HJ, Levin LS et al. Treatment of segmental defects of the radius with use of the vascularized osteoseptocutaneous fibular autogenous graft. J Bone Joint Surg 1997; 79-A; 542-50.

7. Lasanianos IG, Kanakaris NK, Giannoudis PV. Current management of long bone large segmental defects. Orthopaedics and Trauma 2009; 24; 2: 149-163.

8. Korompilia AV, Paschos NK, Beris AE et al. Recent updates of surgical techniques and applications of free vascularized fibular graft in extremity and trunk reconstruction.

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10. Masquelet AC, Sales de Gauzy J, Rigal S et al. Reconstruction of post-traumatic diaphyseal bone defects: Preoperative planning, guideline, and future developments.

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11. Mojallal A, Besse JL, Breton P. Donor site morbidity after free fibula flaps. Report of 42 consecutive cases. Ann Chir Plast Esth 2004; 49: 3-10.

12. Momeni A, Stark GB. The free fibular flap: a useful flap for reconstruction following composite and injuries. J Hand Surg 2006; 31B; 3: 304–305.

13. Muramatsu K, Ihara K, Shigetomi M, Kawai S. Femoral reconstruction by single,

14. Ozalp T, Masquelet AC, Begue TC. Septocutaneous perforators of the peroneal artery relative to the fibula: Anatomical basis of the use of pedicled fasciocutaneous flap.

Surg Radio Anat 2006; 28: 54-58.

15. Pand S, Kohli JS, Arora S, Bajaj SP. The osteofasciocutaneous flap: A new method to transfer fibula along with a sufficient amount of skin. Br J Plast Surg 2000; 55: 312- 319.

16. Pliefke J, Rademacher G, Eisenschenk A et al. Postoperative monitoring of free vascularized bone grafts in reconstruction of bone defects. Microsurgery 2009; 29:

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20. Taylor GI, Miller GDH, Ham FJ. The free vascularized bone graft. A clinical extension of microvascular techniques. Plast Recon Surg 1975; 55; 5: 533- 544.

21. Yajima H, Kobata Y, Takakura Y et al. Vascularized Fibular Grafting in the Treatment of Methicillin-Resistant Staphylococcus Aureus Osteomyelitis and Infected Nonunion.

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3  

Missed  Compartment  Syndrome  of  the  Forearm:  

Limb  Salvage  and  Reconstruction  

Trung-Hau LÊ THUA

, Dang-Nhat PHAM

, Willy D. BOECKX

1

Dept. of Plastic, Reconstructive & Hand Surgery, Center of Orthopaedic & Plastic Surgery, Hue Central Hospital, Hue City, Vietnam.

2

Dept. of Plastic Surgery, Brugmann University Hospital, Université libre de Bruxelles, Belgium.

Journal of Hand and Microsurgery 2015, 7 (1): 129 - 132.