Abstract
Background
There are no reports on the similarities and differences between induced membrane (IM) technique and wrap bone graft(WBG) technique.
Objective
The aims of this study are to investigate the effects of IM technique and WBR technique in repairing segmental bone defects, and to analyze the similarities and differences between them.
Materials and Methods
66 patients of tibial segmental bone defects treated by IM technique and WBG technique were retrospectively analyzed. Aged 13–69 years old with an average of 35.3 years old. IM technique was divided into early IM group (bone grafting at 6–8 weeks of bone cement filling) and late IM group (bone grafting after 8 weeks of bone cement filling). WBG was divided into titanium mesh group and line suturing cortical bone blocks group. There were 11 cases, 25 cases, 10 cases and 20 cases in the early IM group, late IM group, titanium mesh group and line suturing group, respectively. Bone healing, complications and functional recovery (Paley’s method) were observed, the causes of nonunion and delayed union and factors affecting bone healing were analyzed.
Results
There were no significant differences in terms of age, sex, defect length, course, fixation method, defect location and preoperative function of adjacent joints among the 4 groups. All patients were followed up for 12–50 months, with an average of 20.1 months. The clinical healing time of early IM group, late IM group, titanium mesh group and line suturing group were (5.81 ± 0.75) months, (7.56 ± 1.66) months, (7.50 ± 0.70) months and (7.81 ± 1.81) months, respectively, showing significant differences among the 4 groups (P = 0.005). However, only early IM group had significant difference with other groups (P < 0.05), while no significance was found between late IM group and WBR group, between titanium mesh group and suture group (P > 0.05). There were no significant differences in healing ration, complications and functional recovery of adjacent joints among the 4 groups (P > 0.05). There were 4 cases of nonunion and delayed union, all of which were caused by poor quantity or quality of bone graft or unstable bone graft or internal fixation.
Conclusion
Both IM technique and WBG technique are effective method for repairing segmental bone defects. In addition to mechanical encapsulation, early IM has biological osteogenesis. However, mechanical encapsulation is a common basis for repairing bone defects, and biological osteogenesis can enhance bone healing.
Keywords: Segmental bone defect, Induced membrane technique, Wrap bone graft technique, Bone healing, Titanium mesh, Line mesh
Introduction
Segmental bone defects may result from high energy trauma, debridement of osteomyelitis, or tumor resection. Bone defects of longer than 2 cm will not heal by itself and need to be reconstructed. Autogenous bone graft remains the gold standards for repair of bone defects [1–4]. However, traditional autogenous cancellous bone graft was considered unsuitable for segmental bone defects of more than 4–6 cm due to loosening and absorption of bone graft, which resulted in a high rate of nonunion [3, 4]. In the past 3 decades, some modified free bone graft methods have been developed to be effective treatment for repairing large segmental bone defects, such as Cobb et al. [5] in 2000 first reported cancellous bone grafting wrapped using titanium mesh for large segmental bone defects. Later, Wen et al. [6], Raoxi et al. [7], Qudong et al. [8], Whately et al. [9], Hui et al. [10] adopted cancellous bone graft wrapped using line mesh or line suturing cortical bone blocks or absorbable mesh to repair large segmental bone defects. All the aforementioned methods employ mechanical encapsulation, which overcome the shortcomings of traditional method that bone graft is easy to loosen and absorb, we named “wrap bone graft (WBG) technique” [8]. In 2000, Masquelet et al. [11] first reported application of induced membrane (IM) technique in 35 cases with segmental bone defects (4–25 cm), all the patients obtained clinical healing after an average of 4 months. To our knowledge, there were no reports about the similarities and differences between IM technique and WBG technique in the literature. In this study, we retrospectively analyze the data of patients treated by IM technique and WBG technique in our hospital, to investigate the effects of IM technique and WBR technique in repairing segmental bone defects, and to analyze their similarities and differences.
Patients and Methods
Inclusion and Exclusion Criteria for Cases
The inclusive criteria were as follows: (1) tibial segmental bone defects of ≥ 4.0 cm treated with IM technique or WBG technique; (2) infectious bone defects must be effectively controlled before bone grafting; (3) complete clinical and imaging data; (3) ≥ 12 months of follow-up time.
The exclusion criteria were as follows: (1) pathological bone defects caused by malignant tumor; (2) patient with poor compliance; (3)patients associated with severe vessel and nerve injury or soft tissue defects, who were unsuitable for limb salvage.
General Data
Between January 2009 and March 2018, 66 patients (37 males and 29 females) aged 13–69 years, with an average age of 35.7 years were included. IM technique was divided into early IM group (bone grafting at 6–8 weeks of bone cement filling) and late IM group (bone grafting after 8 weeks of bone cement filling). WBG was divided into titanium mesh [5] and line suturing cortical bone blocks [8, 9]. There were 11 cases in early IM group, 25 cases in late IM group, 10 cases in titanium mesh and 20 cases in line suturing group. The bone defects were caused by severe trauma in 48 cases (15 cases associated with infection), by osteomyelitis in 13 cases and by tumor resection in 5 cases. Among the 28 cases of infective bone defects, 25 cases were in late IM group and 3 cases were in line suturing group. The number of each patient’s previous treatment including debridement, repair of flap and internal or external fixation was 0–4 times, of which, internal fixation in 38 cases and external fixation in 23 cases. The time from bone lesion to bone repair was 7–123 days (average 61 days). The length of the bone defects ranged from 4.0 to 11.5 cm with an average of 6.39 cm. The locations of the bone defects of tibia were as follows: diaphysis in 53 cases and epiphyseal in 13 cases. The final fixation method for repairing bone defects: internal fixation in 63 cases (plate in 17 cases and nail in 49 cases) and external fixation in 3 cases. The function of adjacent joints was evaluated by Paley method [12]. This study was approved by the ethics committee of our hospital and all patients provided signed informed consent.
Surgical Methods
Before WBG, the associated soft tissue defects must be repaired with skin flap, and the wound heals for at least 4 weeks; the associated infection must be controlled for 3 months. A longitudinal incision was usually made to debride the bone defects at first to ensure blood supply at the end. Second, using existing methods, such as intramedullary nails, locking plates or external fixators, to achieve reliable stability. Third, the wrap device (titanium mesh or line suturing cortical bone blocks) was placed at the bone defects wrapping the bone graft materials and the ends of the defects [8, 9, 12, 13].
In the first stage surgery of IM technique, a longitudinal incision debridement was performed, followed by internal or external fixation. Bone cement loaded with vancomycin was used for infective bone defects. In the early IM group, the second stage surgery was performed at 6–8 weeks of bone cement filling for noninfectious bone defects, while in the late IM group, the second stage surgery was performed after 8 weeks of bone cement filling for infective bone defects. The opened IM was sutured after bone grafting within the IM.
Rich autogenous cancellous bone was harvested from iliac crest and proximal tibia, cut into granular and impacted to a degree for bone graft by WBG technique or IM technique. If the amount of autogenous cancellous bone is insufficient, cortical bone or artificial bone can be used as a supplement, but no more than a quarter.
Postoperative Treatment
Antibiotics were given for 3–5 days after operation. Rehabilitation started on the 3rd day after operation. Gradual weight bearing allowed in 2–4 weeks after operation, and complete weight bearing allowed when bone connection was found by radiological examination. All patients underwent monthly X-ray examination until the bone healing. After bone healing, the follow-up interval was 2–3 months. Internal fixation can be removed in about 10 months after clinical healing. CT examination taken in cases of diagnosis of clinical healing is in doubt.
Observation Indicators
To observe the bone healing, complications and functional recovery, analyze the causes of nonunion and delayed union and the factors affecting bone healing. Clinical healing was defined as the radiographic presence of bridging bone identified on 3 of 4 cortices without gross motion or tenderness at the site of bone defects with physical examination. Nonunion was defined as when a minimum of 9 months has elapsed since fracture or bone defect with no visible progressive signs of healing for 3 months. The functional recovery of adjacent joints was evaluated by Paley method [12].
Statistical Analysis
Statistical analysis was performed using SPSS version 16.0 software (Chicago, IL, USA) to analyze the data. The categorical variables were analyzed by Fisher exact test or variance analysis, whereas the continuous variables were analyzed by one-way ANOVA. The level of statistical significance was defined as P < 0.05.
Results
General Data
There were no significant differences in terms of age, sex, defect length, course time, fixation method, defect location and preoperative function of adjacent joints among the 4 groups (all P values > 0.05, Table 1).
Table 1.
Comparison of general data of 4 groups
| Groups | Cases | Sex (M/F) | Age ( ± s, years) | Defect length (cm) | Course (D) | Fixation method (I/E) | Defect location (D/E) | Function scale (E/G/F/P) | |
|---|---|---|---|---|---|---|---|---|---|
| Early IM | 11 | 7/4 | 40.67 ± 16.11 | 6.10 ± 2.00 | 48.00 ± 30.64 | 11/0 | 9/2 | 0/0/3/8 | |
| Late IM | 25 | 15/10 | 37.02 ± 14.82 | 6.56 ± 1.45 | 6.68 ± 32.27 | 23/2 | 20/5 | 0/0/7/18 | |
| Titanium mesh | 10 | 6/4 | 38.20 ± 13.21 | 6.16 ± 1.53 | 68.30 ± 35.14 | 10/0 | 9/1 | 0/0/3/7 | |
| Line suturing | 20 | 13/7 | 41.55 ± 14.40 | 6.45 ± 0.95 | 58.50 ± 30.52 | 19/1 | 14/6 | 0/0/5/15 | |
| Statistics | 0.080 | 0.310 | 0.367 | 0.877 | 0.758 | 0.566 | 0.015 | ||
| P value | 0.971 | 0.818 | 0.777 | 0.458 | 0.522 | 0.640 | 0.998 | ||
Postoperative Results
The incision healed by first intention in 63 cases and secondary healing in 3 cases. There were no neurologic or vascular damage.
Follow-up and Complications
All patients were followed up for 12–50 months, with an average of 20.1 months. The clinical healing time of the early IM group, late IM group, titanium mesh group and line suturing group were (5.81 ± 0.75) months, (7.56 ± 1.66) months, (7.50 ± 0.70) months and (7.81 ± 1.81) months, respectively (Fig. 1), showing significant differences among the 4 groups (P = 0.005). However, only early IM group had significant difference with other groups (P < 0.05), while no significant difference found between late IM group and WBR group, between titanium mesh group and suture group (P > 0.05). See Fig. 1 and Table 2, 3. Recurrence of infection was found in 2 cases. There was no significant difference in complications among the 4 groups (P = 0.354). There was no significant difference in healing ration among the 4 groups (P = 0.805). At the last follow-up, the excellent or good rate of functional recovery of adjacent joints was 92.42%, there was no significant difference in terms of functional recovery among the 4 groups (P = 0.982). Typical cases see Figs. 2, 3 and 4. There were 2 cases of delayed union and 2 cases of nonunion (1 case of nonunion due to smaller size of the IM formed in late IM group at the junction and less amount of bone graft, the other due to instability of internal fixation in line suturing group).
Fig. 1.
The healing time of the 4 groups
Table 2.
Outcomes of 4 groups
| Groups | Cases | Heaing ratio | Healing time (M) | Complication ratio | Functional recovery (E/G/F/P) |
|---|---|---|---|---|---|
| Early IM | 11 | 11/11 | 5.81 ± 0.75* | 1/11 | 7/3/1/0 |
| Late IM | 25 | 24/25 | 7.56 ± 1.66 | 3/25 | 15/8/2/0 |
| Titanium mesh | 10 | 10/10 | 7.50 + 0.70 | 0/10 | 6/4/0/0 |
| Line suturing | 20 | 19/20 | 7.84 + 1.81 | 5/20 | 10/8/2/0 |
| Statistics | 0.985 | 4.784 | 3.254 | 0.175 | |
| P value | 0.805 | 0.005 | 0.354 | 0.982 |
*P < 0.05 as compared with late IM, titanium mesh and line suturing groups
Table 3.
Multiple comparisons
| (I) group | (J) group | Sig. | 95% confidence interval | |
|---|---|---|---|---|
| Lower bound | Upper bound | |||
| 1 | 2 | 0.002 | − 2.8242 | − 0.6595 |
| 3 | 0.013 | − 2.9889 | − 0.3748 | |
| 4 | 0.001 | − 3.1547 | − 0.9089 | |
| 2 | 1 | 0.002 | 0.6595 | 2.8242 |
| 3 | 0.915 | − 1.0593 | 1.1793 | |
| 4 | 0.521 | − 1.1874 | 0.6074 | |
| 3 | 1 | 0.013 | 0.3748 | 2.9889 |
| 2 | 0.915 | − 1.1793 | 1.0593 | |
| 4 | 0.548 | − 1.5086 | 0.8086 | |
| 4 | 1 | 0.001 | 0.9089 | 3.1547 |
| 2 | 0.521 | − 0.6074 | 1.1874 | |
| 3 | 0.548 | − 0.8086 | 1.5086 | |
1: early IM, 2: late IM, 3: titanium mesh, 4: line suturing
Fig. 2.
A 39-year old male patient with left tibia bone defects treated by IM technique. a Preoperative X-ray film showed segmental bone defects. b X-ray films after bone cement filling. c IM formed at 20 weeks of bone cement filling. d X-ray film and CT scan showed bony healing in 12 months postoperatively
Fig. 3.
A 53-year old male patient with right tibia bone defects treated by WBG technique using titanium mesh. a Preoperative X-ray films showed segmental bone defects. b Titanium mesh. c X-ray films and CT scan showed bony healing in 12 months postoperatively
Fig. 4.
A 33-year old male patient with left open comminuted fractures and bone defects treated by WBG technique using line suturing cortical bone blocks. a Preoperative appearance and X-ray. b Line suturing cortical bone blocks. c X-ray films showed bony healing in 12 months postoperatively
Discussion
The main reason for high rate of nonunion of large segmental bone defects treated with traditional cancellous bone graft is the lack of encapsulation device. When rehabilitation activities are performed, the bone graft is easily stimulated by the vibration of the surrounding tendons or muscles and limbs, resulting in loosening and absorption [6–8, 13]. For this reason, it is recommended that plaster cast or brace be used for a period of time after operation. However, immobilization can not effectively prevent bone absorption, but hampers functional recovery and bone healing.
WBG overcomes the defects of traditional cancellous bone graft and has become an effective method for repairing large segmental bone defects. The mechanism is as follows: (1) the encapsulation device provides the stability of bone graft material and avoids undesirable stimulation of surrounding tendons or muscles and limb vibration [6–10], meanwhile the encapsulation device does not interfere with vascularization and osteogenesis of the grafted bone because it has holes or good biological properties, which provides a pathway for new blood vessels and osteogenic factors. (2) The amount of grafted bone is abundant as it can be impacted within the encapsulation device [13–16]. Usually the amount of grafted bone is 1.5–2.0 times the volume of bone defects [5, 13–16]. If the amount of harvested autogenous cancellous bone is insufficient in the case of large bone defects, cortical bone or artificial bone can be used as a supplement but not more than a quarter of the total [17–19]. Recently, how to harvest large amount of autologous cancellous bone also has been reported. Studies have shown that more autologous cancellous bone can be obtained from the posterior iliac crest and proximal tibia with few complications [20–22]. The amount of granular autologous bone graft harvested from unilateral femur by reamer-irrigator-aspirator (RIA) is 2 times the amount from the posterior iliac crest by traditional method [23].Therefore, the bone graft materials obtained from bilateral femur by RIA can meet the needs of tibial defect over 10.0 cm in length [23, 24]. In conclusion, mechanical encapsulation can avoids or significantly reduces the loosening and absorption of bone graft. (3) Because of the reliable stability of bone graft, patients can carry out early rehabilitation activities, which is helpful to promote bone healing and functional recovery of adjacent joints.
Besides mechanical encapsulation, IM also has biological osteogenesis activity, because it has abundant microvessels, mesenchymal stem cells and osteogenic factors (e.g., bone morphogenetic protein-2, transforming growth factor beta 1, angiogenic growth factors, CD31 + endothelial cells, vascular endothelial growth factors and osteogenic precursor cells). However, the biological osteogenesis activity of IM is closely related to the filling time of bone cement. Experiments [25, 26] indicated that the osteogenesis activity of IM reached its peak at 4 weeks after PMMA bone cement filling, then it began to weaken at 6 weeks, at 12 weeks it became weak. Masquelet et al. [11] recommended the second stage surgery performed at 6–8 weeks after cement filling. Therefore, in the early IM cases, its healing is fast. However, for infective bone defects, the infection must be effectively controlled before bone grafting. After debridement of bone infection, antibiotics are usually given for 6 weeks, tests of ESR, blood routine and CRP are examined every 2 weeks, 3 times of normal results are needed before bone grafting [19]. Therefore, according to traditional view, some scholars [19, 27, 28] believe that bone grafting is not performed until 12 weeks after antibiotic treatment. After 8 weeks of bone cement filling, the osteogenesis activity is poor, the healing effect is worse than that of early IM, which was similar to that of the WBG group.
In literature [19, 27, 28], the healing time of IM technique repairing bone defects varied greatly, which is mainly related to the timing and location of bone graft. In general, the healing time in cases of bone grafting performed within 8 weeks of bone cement filling is faster than that after 8 weeks of bone cement filling.
Clements et al. [13], Lindsey et al. [14], Ostermann et al. [15], Attias et al. [16] reported the cases of segmental bone defects (5–12.2 cm) treated with cancellous bone graft wrapped with titanium mesh, respectively, all cases got healed in 6–10 months. Whately et al. [10] reported one case of a 10-cm-long tibial defect treated with bone graft wrapped with absorbable polymer mesh, in which clinical healing noted in 6 months postoperatively. Yaoxi et al. [7] reported 12 pediatric patients of congenital tibial pseudarthrosis and bone defects (2–11 cm) treated with cancellous bone graft wrapped with line suturing cortical bone blocks, the healing rate was 100%. Ziran et al. [29] reported a case of critical-sized bone defects of radius reconstructed using femoral fascial wrapping bone graft, demonstrating callus formation at the 8th week postoperatively.
In the present study, the healing time of early IM group was faster than that of late IM group and WBG group (P < 0.05), but there was no significant difference between the late IM group and WBG group (P > 0.05). In WBG, the titanium mesh has strong encapsulation action, in which the bone graft can be impacted, the amount of bone graft materials is large, its bone healing is fast while line suturing has relatively weak wrap action and the amount of bone graft materials is less, its bone healing is relatively slow, but there was no significant difference (P > 0.05). There were 2 cases of nonunion and 2 cases of delayed union, poor quantity or quality of bone graft, unstable bone graft or internal fixation resulted in nonunion and delayed union.
Conclusion
Both IM technique and WBG technique are effective methods for repairing segmental bone defects. IM technique is a special WBG technique, in addition to mechanical encapsulation, early IM has biological osteogenesis. However, mechanical encapsulation is a common ground and the basis for repairing bone defects, and biological osteogenesis can enhance bone healing. The stability, quality and quantity of bone graft, the surrounding blood supply or biological property of encapsulation device are the main factors affecting bone healing of segmental bone defects repaired by IM technique and WBG technique.
Limitations of the Study
This paper was a retrospective clinical study, the level of evidence was not high, the number of cases in titanium mesh and early IM groups was limited, and there was a certain bias. More clinical data from multicenter studies, large samples, and experimental research are needed to confirm the efficacy of IM technique and WBG technique.
Author contributions
YW, QY and YR put forward the concept of the study, designed the study, and prepared the manuscript. ZZ and SG contributed to the data analysis and interpretation. YR and FL reviewed the manuscript. All authors read and approved the final manuscript.
Funding
There is no funding source.
Compliance with Ethical Standards
Conflict of Interest
No conflict of interest exits in the submission of this manuscript.
Ethics Approval and Consent to Participate
For the participation in this research, written informed consent was obtained from each patient. The human beings’ study has been approved by the Ethics Committees of Wuxi Ninth People’s Hospital and Wuxi People’s Hospital.
Informed Consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Yongwei Wu, Yongjun Rui contributed equally to this work.
References
- 1.Schottle PB, Werner CM, Dumont CE. Two-stage reconstruction with free vascularized soft tissue transfer and conventional bone graft for infected nonunions of the tibia: 6 patients followed for 1.5 to 5 years. Acta Orthopaedica. 2005;76(6):878–883. doi: 10.1080/17453670510045534. [DOI] [PubMed] [Google Scholar]
- 2.El-Alfy B, El-Mowafi H, El-Moghazy N. Distraction osteogenesis in management of composite bone and soft tissue defects. International Orthopaedics. 2010;34(1):115–118. doi: 10.1007/s00264-008-0574-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.El-Alfy BS, Ali AM. Management of segmental skeletal defects by the induced membrane technique. Indian Journal of Orthopaedics. 2015;49(6):643–648. doi: 10.4103/0019-5413.168757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Borzunov DY, Balaev PI, Subramanyam KN. Reconstruction by bone transport after resection of benign tumors of tibia: A retrospective study of 38 patients. Indian Journal of Orthopaedics. 2015;49(5):516–522. doi: 10.4103/0019-5413.164042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Cobos JA, Lindsey RW, Gugala Z. The cylindrical titanium mesh cage for treatment of a long bone segmental defect: Description of a new technique and report of two cases. Journal of Orthopaedic Trauma. 2000;14(1):54–59. doi: 10.1097/00005131-200001000-00011. [DOI] [PubMed] [Google Scholar]
- 6.Wei T, Weiwei W, Fumin W, Jian H, Luyao C, Zhantu W, et al. Application of reticular bone grafting in treating distal femoral fractures complicated with massive bone defect. Orthopaedic Biomechanics and Clinical Study (Chinese) 2012;9(6):41–44. doi: 10.3969/j.issn.1672-5972.2012.06.012. [DOI] [Google Scholar]
- 7.Yaoxi L, Haibo M, Kun L, Jin T, Jiangyan W, Rongguo H, et al. Application of “4-in-1 osteosynthesis” in the combined surgical technique for the treatment of congenital pseudarthrosis of tibia in children. Chinese Journal of Orthopaedics. 2016;36(12):770–777. doi: 10.3760/cma.j.issn.0253-2352.2016.12.003. [DOI] [Google Scholar]
- 8.Qudong Y, Sanjun G, Yongjun R, Yuxin Q, Yongwei W, Xuming W, et al. Cancellous bone wrapping grafting for segmental defects of long bone. Chinese Journal of Orthopaedic Trauma. 2017;19(9):775–781. doi: 10.3760/cma.j.issn.1671-7600.2017.09.008. [DOI] [Google Scholar]
- 9.Hui Z, Yajun X, Zheng C, Xuming W, Qudong Y. Effect of cancellous bone graft with free cordical bone blocks and line bonding for tibial segmental bone defect. China Journal of Modern Medicine. 2017;27(8):109–113. doi: 10.3969/j.issn.1005-8982.2017.08.022. [DOI] [Google Scholar]
- 10.Whately C, Abdallah MA, Alwatari YA. Management of large segmental tibial defects using locking IM nail and absorbable mesh. BMJ Case Reports. 2013 doi: 10.1136/bcr-2013-010480. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Masquelet AC, Fitoussi F, Begue T, Muller GP. Reconstruction of the long bones by the induced membrane and spongy autograft. Annales de Chirurgie Plastique et Esthetique. 2000;45(3):346–353. [PubMed] [Google Scholar]
- 12.Paley D, Herzenberg JE, Paremain G, et al. Femoral lengthening over an intramedullary nail. A matched-case comparison with Ilizarov femoral lengthening. The Journal of Bone and Joint Surgery (America) 1997;79(10):1464–1480. doi: 10.2106/00004623-199710000-00003. [DOI] [PubMed] [Google Scholar]
- 13.Clements JR, Carpenter BB, Pourciau JK. Treating segmental bone defects: a new technique. Journal of Foot and Ankle Surgery. 2008;47:350–356. doi: 10.1053/j.jfas.2008.04.006. [DOI] [PubMed] [Google Scholar]
- 14.Lindsey RW, Gugala Z, Milne E, Sun M, Gannon FH, Latta LL. The efficacy of cylindrical titanium mesh cage for the reconstruction of a critical-size canine segmental femoral diaphyseal defect. Journal of Orthopaedic Research. 2006;24:1438–1453. doi: 10.1002/jor.20154. [DOI] [PubMed] [Google Scholar]
- 15.Ostermann PAW, Haase N, Rübberdt A, Wich M, Ekkernkamp Management of a long segmental defect at the proximal meta-diaphyseal junction of the tibia using a cylindrical titanium mesh cage. Journal of Orthopaedic Trauma. 2002;16(8):597–601. doi: 10.1097/00005131-200209000-00010. [DOI] [PubMed] [Google Scholar]
- 16.Attias N, Lehman RE, Bodell LS, Lindsey RW. Surgical management of a long segmental defect of the humerus using a cylindrical titanium mesh cage and plates. Journal of Orthopaedic Trauma. 2005;19(3):211–216. doi: 10.1097/01.blo.0000223982.29208.a4. [DOI] [PubMed] [Google Scholar]
- 17.Qudong Y, Zhenzhong S, Sanjun G, Yunhong M. Preliminary report of wrapped impacted bonegraft using titanium mesh for repair of large segmental bone defect. Chinese Journal of Clinical Anatomy. 2015;33(1):101–104. doi: 10.13418/j.issn.1001-165x.2015.01.024. [DOI] [Google Scholar]
- 18.Bullens PH, Bart Schreuder HW, de Waal Malefijt MC, Verdonschot N, Buma P. Is an impacted morselized graft in a cage an alternative for reconstructing segmental diaphyseal defects? Clinical Orthopaedics and Related Research. 2009;467:783–791. doi: 10.1007/s11999-008-0686-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Qudong Y, Sanjun G, Yongjun R, Zhenzhong S, Yongwei W, Youyin S. Analysis of therapeutic effect of induced membrane technique for treatment of bone defect. Chinese Journal of Orthopaedics. 2016;36(20):1284–1293. doi: 10.3760/cma.j.issn.0253-2352.2016.20.002. [DOI] [Google Scholar]
- 20.Engelstad ME, Morse T. Anterior iliac crest, posterior iliac crest, and proximal tibia donor sites:a comparison of cancellous bone volumes in fresh cadavers. J Oral and Maxillofacial Surgery. 2010;68(12):3015–3021. doi: 10.1016/j.joms.2010.07.056. [DOI] [PubMed] [Google Scholar]
- 21.Gerressen M, Prescher A, Riediger D, Van DVD, Ghassemi A. Tibial versus iliac bone grafts: A comparative examination in 15 freshly preserved adult cadavers. Clinical Oral Implants Research. 2010;19(12):1270–1275. doi: 10.1111/j.1600-0501.2008.01621.x. [DOI] [PubMed] [Google Scholar]
- 22.Lee M, Song HK, Yang KH. Clinical outcomes of autogenous cancellous bone grafts obtained through the portal for tibial nailing. Injury. 2012;43(7):1118–1123. doi: 10.1016/j.injury.2012.02.021. [DOI] [PubMed] [Google Scholar]
- 23.Cox G, Jones E, Mcgonagle D, Giannoudis PV. Reamer-irrigator-aspirator indications and clinical results: A systematic review. International Orthopaedics. 2011;35(7):951–956. doi: 10.1007/s00264-010-1189-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Mccall TA, Brokaw DS, Jelen BA. Treatment of large segmental bone defects with reamer-irrigator-aspirator bone graft: Technique and case series. Orthopedic Clinics of North America. 2010;41(1):63–73. doi: 10.1016/j.ocl.2009.08.002. [DOI] [PubMed] [Google Scholar]
- 25.Henrich D, Seebach C, Nau C, Basan S, Relja B, Wilhelm K. Establishment and characterization of the Masquelet induced membrane technique in a rat femur critical-sized defect model. Journal of Tissue Engineering and Regenerative Medicine. 2016;10(10):E382–E396. doi: 10.1002/term.1826. [DOI] [PubMed] [Google Scholar]
- 26.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. Journal of Orthopaedic Research. 2004;22(1):73–79. doi: 10.1016/s0736-0266(03)00165-7. [DOI] [PubMed] [Google Scholar]
- 27.Azi ML, Teixeira A, Cotias RB, Joeris A, Kfuri M. Membrane induced osteogenesis in the management of post-traumatic bone defects. Journal of Orthopaedic Trauma. 2016;30(10):545. doi: 10.1097/BOT.0000000000000614. [DOI] [PubMed] [Google Scholar]
- 28.Wang X, Luo F, Huang K, Xie Z. Induced membrane technique for the treatment of bone defects due to post-traumatic osteomyelitis. Bone and Joint Research. 2016;5(3):101–105. doi: 10.1302/2046-3758.53.2000487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Ziran NM, Smith WR. The ‘Ziran’ wrap: reconstruction of critical-sized long bone defects using a fascial autograft and reamer-irrigator-aspirator autograft. Patient Safety in Surgery. 2014;8(1):40. doi: 10.1186/s13037-014-0040-7. [DOI] [PMC free article] [PubMed] [Google Scholar]