Abstract
Background: The induced membrane technique was originally described as a technique for the reconstruction of long bone defects. The authors performed a systematic review to determine whether the use of the induced membrane technique is effective in large bony defects in the upper extremity. Methods: A qualitative systematic review was conducted using PubMed, EBSCO, and Google Scholar databases to record all studies reporting on complications of the induced membrane technique in the upper extremity. Studies written after 1990 in English language journals met the inclusion criteria. Exclusion criteria were non-English language publications, animal studies, failure to identify the location of the bone defect, failure to identify whether complications were associated with the procedure, and failure to define the length of bone defect. Results: A total of 1422 studies were identified in the original search. Twelve studies satisfied the criteria for inclusion. A total of 70 patients with 83 upper extremity cases were reported: 1 proximal interphalangeal joint, 22 phalanges, 8 metacarpals, 37 forearms, 14 humeri, and 1 clavicle. The mean bone defect size was 4.0 cm (SD, 1.5). The most common complication was infection. We found that complication rates were independent of the location of the bone defect. Complication rates in the upper extremity ranged from 0% to 100%, with a total weighted mean of 10%. Conclusion: The induced membrane technique is an emerging possible treatment of large bone defects in the upper extremity. More research is needed to determine the outcomes of the induced membrane technique in the upper extremity.
Keywords: Masquelet technique, induced membrane technique, upper extremity
Introduction
The induced membrane technique otherwise known as the Masquelet technique is a useful procedure indicated for segmental bone loss, bone tumors, and septic nonunions. Traditionally, the technique has been used for bony defects of long bones of the lower extremity. The procedure involves a well-described 2-stage reconstruction for segmental bone loss.1-5
Critical-size bone defects are defined as injuries that will not heal with surgical stabilization alone and are generally bony defects larger than 2 cm. Several interventions are used for bony defects larger than 2 cm. Surgeons often need to consider soft tissue defects surrounding the bony defect and patient-specific factors when determining treatment algorithms. Bone defects of less than 5 cm may be filled with autologous bone graft in 1 stage. This procedure is limited in defects greater than 5 cm due to difficulties in obtaining significant graft and resorption of the graft. Acute limb shortening is also an option when the segment is less than 5 cm and is well tolerated in the upper extremity, which is not dependent on equality of length.6-8
Distraction osteogenesis is a viable option for defects larger than 5 cm, but is associated with high cost, pin-site infections, and nonunion. Free vascularized bone flaps (FVBFs) such as a free fibula, free iliac crest, scapula, or distal radius are alternatives. Free vascularized bone flaps require a microvascular trained team and have been associated with early uncontrolled bleeding, thrombosis of the anastomosis, concerns for donor site morbidity, and flap failure.9-15
The induced membrane technique has been shown to be effective in deficits as large as 25 cm. Karger et al 5 in the largest case series to date demonstrated union in 90.4% of patients who underwent this procedure. This study also found no correlation between time to union and size of bony defect or location. A recent systematic review of this procedure found this technique to achieve union in 383 of 427 patients with segmental bone loss. In this review, the vast majority of operations were performed for injuries to the lower limb. Variable complication rates have been shown with the induced membrane technique with a mean of 49.7% (range 15%-100%).3,5,16 Limited research is available investigating the utility of the induced membrane technique in the upper limb.
The best available evidence suggests that the induced membrane technique may have utility in bone defects of the upper limb. To date, there have been few studies regarding the use of this technique in the upper limb, and what studies have been conducted mostly consist of case series and case reports.17-22
The primary goal of this systematic review was to determine the complication rate with the use of the induced membrane technique in the upper limb. Secondary goals were to (1) determine the mean size of bone defect; (2) identify complications inherent to the procedure in the hand, forearm, and arm; and (3) determine whether complications differ with the anatomical location of the bone defect.
Methods
This study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. 23 We searched PubMed, EBSCO, and Google Scholar databases to record all studies reporting on the complications of the induced membrane technique in the upper extremity published from January 1, 1990, to January 1, 2019. The following MeSH (Medical Subject Headings) terms were used: induced membrane technique OR Masquelet technique OR bone defect OR segmental bone loss AND upper extremity OR hand OR forearm OR humerus. Articles were preliminarily screened using titles and abstracts to identify publications that met the inclusion criteria. Full manuscripts that fulfilled the inclusion criteria were further reviewed (Figure 1).
Figure 1.
Flowchart of the screening used during literature review.
Inclusion and Exclusion Criteria
We included full peer-reviewed publications in English that addressed complications of the induced membrane technique in the upper limb. Publications needed to include length of the bone defect(s), a detailed description of protocol used for treatment, outcomes/complications in each case (if any), and the anatomical location of the defect. We excluded all studies that did not meet the above inclusion criteria.
Data Extraction
We recorded the title, author, year, methodological index for nonrandomized studies (MINORS) score, country, study design, level of evidence, total number of patients, number of patients with upper limb defects, mechanism of segmental bone loss, anatomical site, defect size, time between stages, time to union, and complications.
Outcomes
The primary outcome measure was the complication rate with the use of the induced membrane technique in the upper limb. Secondary outcomes were defect size and time to union. The MINORS score was calculated for each study included. The MINORS score is a validated instrument designed to assess the methodological quality of nonrandomized studies, and the global ideal score for noncomparative studies is 16 and 24 for comparative studies. 29
Study Characteristics
The characteristics for the studies included (1) 1 study reporting on the induced membrane technique on the clavicle, (2) 6 studies reporting on 14 cases of the technique on humeral defects, (3) 8 studies reporting on 37 cases of the technique in the forearm, and (4) 2 studies reporting on 31 cases in the hand, including its use in the metacarpals and phalanges, and 1 case of a proximal interphalangeal joint fusion.
Statistical Analysis
The number of upper extremity cases, anatomical location, mean defect size (cm), mean time to union, and complication rate were extracted from each study. Mean, median, and range values were calculated for the size of the defect, time to union, and complication rate. A weighted mean complication rate was calculated for all upper extremity defects treated.
Complication rates were grouped based on their anatomical location. A t test was performed with 95% confidence interval to compare weighted mean complication rates among clavicle defects, humeral defects, forearm defects, and hand defects.
Results
The initial literature search identified 1422 studies. After initial analysis, 37 studies were identified for full manuscript review. Of the 37 studies reviewed, 12 studies were included. The 12 studies included 9 case series studies and 3 case reports (Table 1).
Table 1.
Characteristics of Studies on the Induced Membrane Technique in the Upper Limb.
| Author | Year | Country | Study design | Methodological quality (MINORS score) |
|---|---|---|---|---|
| Walker et al 17 | 2018 | United States | Case series | 10 |
| Kombate et al 24 | 2017 | Africa | Case series | 10 |
| Anoumou et al 25 | 2017 | Ivory Coast | Case series | 9 |
| Moris et al 21 | 2016 | France | Case series | 10 |
| Scholz et al 26 | 2015 | Germany | Case series | 9 |
| Kawakami et al 27 | 2015 | Japan | Case series | 9 |
| Giannoudis et al 22 | 2016 | United Kingdom | Case series | 12 |
| Wong et al 28 | 2014 | China | Case series | 9 |
Note. MINORS = methodological index for nonrandomized studies.
A total of 70 patients with 83 upper extremity cases were reported. The mean bone defect size was 4.0 cm (SD, 1.5). The mean time to union was 6.7 months (SD, 5.6). The most common complication was infection. There were a total of 3 persistent nonunions of a total of 116 cases, representing an overall failure rate of 2.6% for upper extremity bone defects treated with the induced membrane technique. Complication rates in the upper extremity ranged from 0% to 100% with a total weighted mean of 10% (Table 2).
Table 2.
Anatomical Region, Bone Defect Length, Time to Union and Complications of the Induced Membrane Technique in the Upper Limb.
| Author | No. of UE | Anatomical location | Mean defect size, cm | Mean time to union, mo | Complication rate, % | Complications |
|---|---|---|---|---|---|---|
| Walker et al 17 | 9 | 9 forearms | 4.7 | 4.6 | 11 | 1 reoperation for a plate fracture before union |
| Kombate et al 24 | 2 | 3 humeri | 2.8 | — | 0 | None |
| Anoumou et al 25 | 6 | 4 forearms | 5.2 | 4.6 | 50 | 1 stiffness/CPRS, 1 suppurative nonunion |
| 2 humeri | 4.0 | 4.5 | 50 | 1 superficial infection | ||
| Moris et al 21 | 18 | 8 metacarpals, 22 phalanges | 2.0 | 4.0 | 40 | 2 nonunions, 2 cases of sepsis requiring additional surgery, 4 cases of persistent dysesthesia at the reconstructed site, 4 cases of clinodactyly |
| Scholz et al 26 | 1 | 1 forearms | 7.0 | 12 | 100 | Loss of range of motion of the wrist secondary to loss of radial length |
| Kawakami et al 27 | 4 | 3 forearms | 4.5 | 4.0 | 100 | 2 cases with adhesion of extensor tendons, 1 case of infection requiring revision surgery and free vascularized fibular grafting |
| 1 humerus | 3.5 | 3.0 | 0 | None | ||
| Giannoudis et al 22 | 15 | 14 forearms | 2.9 | 3.6 | 0 | None |
| 1 humerus | 6.5 | — | 100 | Infected nonunion in previous background of bone radiation that required free vascularized fibular grafting | ||
| Wong et al 28 | 3 | 1 humerus | 2.0 | — | 0 | None |
| 2 forearms | 3.0 | — | 0 | None | ||
| Calori et al | 1 | 1 clavicle | 4.0 | 9.0 | 0 | None |
| Micev et al 19 | 1 | 1 forearm | 4.5 | 22 | 100 | Atrophic nonunion of the radius requiring revision autogenous bone grafting |
| Hara et al | 1 | 1 PIP joint | 2.0 | 2.0 | 100 | Known complication of arthrodesis of the PIP joint |
| Zappaterra et al 20 | 9 | 6 humeri | 5.1 | — | 33 | 1 case of plate fracture requiring reosteosynthesis, 1 case of radial nerve palsy on the nonoperated on extremity |
| 3 forearms | 4.3 | — | 33 | 1 case of plate fracture requiring wrist arthrodesis | ||
| Total | 70 | No. of UE cases: 83 | Mean bone defect: 4.0 (SD, 1.5) | Mean time to union: 6.7 (SD, 5.6) | Weighted mean complication rate: 10% |
Note. UE = upper extremity; PIP = proximal interphalangeal; CPRS = complex regional pain syndrome.
Weighted mean complication rates were 0.0% for clavicle defects, 25% for humeral defects, 23% for forearm defects, and 41% for hand defects. A t test performed with 95% confidence interval demonstrated no significant difference between complication rates among the various anatomical regions (P = .59).
All the studies included were assessed using the MINORS scoring system for assessment of their methodological quality. The mean MINORS score was 8.9 (SD, 1.9; range, 5-12; Table 1).
Discussion
This study investigated the use of the induced membrane technique in the upper limb. Most upper limb cases in our study were those who underwent treatment of segmental bone defects for infected nonunions. The most common complication shown was infection. There was no difference seen in complication rates between the different anatomical regions of the upper limb treated with the induced membrane technique.
The results of this study need to be interpreted in light of its limitations. There are currently limited data on the treatment of segmental bone defects in the upper limb. The data from this study were from level IV and level V studies. These data may be a result of poorly collected data, and further prospective trials comparing outcomes of the induced membrane technique in the upper limb are needed.
The data from our study demonstrate that the induced membrane technique may serve as a viable option for the reconstruction of segmental bone defects in the upper limb. When compared with data from oncological reconstruction of upper extremities, the induced membrane technique compares favorably. The average time to union was shorter for free bone flaps by 1.7 months compared with the induced membrane technique; however, this difference may not be clinically significant. 25 Furthermore, this technique allows limb salvage in patients who are not able to undergo microvascular bone flaps. Patients who are unable to tolerate prolonged anesthesia, have peripheral vascular disease, no microsurgical expertise available, or available donor sites that are expendable are not candidates for FVBGs9,11,13-15 and should be offered the induced membrane technique to treat their bone defects.
The induced membrane technique has a role in managing large osseous defects in the upper limb in patients who are not candidates for microvascular reconstruction, in an austere environment without access to microsurgical reconstruction, or desire limited donor site morbidity. The alternative to the induced membrane technique is a microvascular bone flap. Both options have similar complication profiles and generally require revision operations, and have significant complication burden, including fracture, nerve injury, infection, and reoperation.1,7,9-16 The reoperation rate for FVBFs has been shown to be around 34% and the nonunion rate to be 17.5%. 30
Future research should further investigate the complications associated with the use of the induced membrane technique. Larger randomized controlled trials would be ideal for comparing the use of the induced membrane technique with the FVBG in the upper limb. Studies of this magnitude will be difficult to envision as the number of segmental bone defect cases is limited at this time.
Footnotes
Authors’ Note: This work was performed at the Albany Medical Center, Albany, NY.
Ethical Approval: The study has been performed in accordance with the ethical standards in the 1964 Declaration of Helsinki and has been carried out in accordance with relevant regulations of the US Health Insurance Portability and Accountability Act.
Statement of Human and Animal Rights: This article does not contain any studies with human or animal subjects.
Statement of Informed Consent: Informed consent was not required for this study as it did not study human subjects.
Declaration of Conflicting Interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iD: Casey M. O’Connor 
https://orcid.org/0000-0001-9376-9801
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