Treatment of postoperative tibial chronic osteomyelitis using bone transport techniques; an observational study

Published:October 22, 2021DOI:https://doi.org/10.1016/j.jcot.2021.101652

      Abstract

      Purpose

      Postoperative Tibial chronic osteomyelitis is one of the most challenging orthopaedic conditions especially when extensive, the anatomy of subcutaneous anteromedial part of the tibia with less soft tissue coverage complicates the situation. The extent of infected tibial part varies in size and duration from one patient to another. We report our experience using Bifocal and Monofocal bone transport techniques with regard to clinical outcome, recurrence of infection and re-fracture rate.

      Methods

      This is a retrospective observational review of 49 patients with postoperative Tibial chronic osteomyelitis which were treated using either Bifocal distraction compression BFDCO technique group I (31 patients) or Monofocal compression osteosynthesis MFCO technique Group II (18 patients). The average age of the patients was (41.6 ± 13.1 years), (range: 17–67 years). Leg length discrepancy was measured in 33 (58.9%) patients with an average of (1.4 ± 1.7 cm). Contracture of the ankle joint and equinus deformity were detected in 36 (64.3%) patients. Pre and Post-operative radiography together with Modified Irzhansky A.A et al. leg functional assessment system were used to assess the functional outcome.

      Results

      The time spent in the Ilizarov fixator (External Fixation Index) in the first group was (142 ± 72 days) and in the second group was (75 ± 54 days). The infection recurred in 2 patients (6%) in group I and in 5 patients (28%) in group II. Lack of consolidation or re-fracture within 6 months after the dismantling of the apparatus was detected in 6 patients (19.5%) in group I and in 5 patients (27.8%) in group II. Lack of consolidation or re-fracture within 6 months after dismantling of the apparatus in group I was detected in 6 patients (19.5%) in group I and in 5 patients (27.8%) in Group II. The average functional state score (AFSS) in the first group was (12.45 ± 2.41) on admission and increased to (16.16 ± 2.99) on the final follow-up which corresponded to a “good” result. In the second group II the AFSS was (12.11 ± 2.22) on admission and increased to (15.06 ± 2.88) at the final follow-up which corresponded to a “satisfactory” result.

      Conclusion

      Treatment of Tibial chronic osteomyelitis using either Bifocal or Monofocal bone transport is an effective method. However our results have demonstrated better functional outcome and less infection recurrence and re-fracture rates when using the Bifocal distraction compression technique (BFDCO).

      Keywords

      1. Introduction

      Chronic osteomyelitis of the tibia is one of the most serious complications after intra or extramedullary osteosynthesis of leg fractures which occurs in (15–41.2%) of all extremity fractures, It represents physical, socioeconomic and psychological impact on patients.
      • Poultsides 1 Lazaros A.
      • Liaropoulos Lycurgus L.
      • Malizos Konstantinos N.
      The socioeconomic impact of musculoskeletal infections.
      • Anandasivam
      • Nidharshan S.
      • et al.
      Tibial shaft fracture: a large-scale study defining the injured population and associated injuries.
      • Jorge L.S.
      • Chueire A.G.
      • Fucuta P.S.
      • et al.
      Predisposing factors for recurrence of chronic posttraumatic osteomyelitis: a retrospective observational cohort study from a tertiary referral center in Brazil.
      It is estimated that half of the osteomyelitis cases in adults are due to trauma.
      • Lima A.L.
      • Oliveira P.R.
      • Carvalho V.C.
      • Cimerman S.
      • Savio E.
      Diretrizes Panamericanas para el Tratamiento de las Osteomielitis e Infecciones de Tejidos Blandos Group. Recommendations for the treatment of osteomyelitis.
      Moreover, a multicenteric study have shown that people of the working age 20–50 years old are the most often affected which represent a major impact on patients quality of life and also a financial burden to both individuals and health care systems. Established osteomyelitis present a challenging complication to the treating surgeon which could reach up to (22.4%) in some series. A recent increase of the condition is reported due to different reasons which includes using inappropriate metal work, contaminated surgical environment, open fractures, foreign bodies and hematogenous spread.
      • Lazzarini L.
      • Mader J.T.
      • Calhoun J.H.
      Osteomyelitis in long bones.
      • Calhoun J.H.
      • Manring M.M.
      • Shirtliff M.
      Osteomyelitis of the long bones.
      • Kremers H.M.
      • Nwojo M.E.
      • Ransom J.E.
      • Wood-Wentz C.M.
      • Melton 3rd, L.J.
      • Huddleston 3rd, P.M.
      Trends in the epidemiology of osteomyelitis: a population-based study, 1969 to 2009.
      The condition is usually recalcitrant to conventional methods like Sequestrectomy plus antibiotics as the only strategy of treatment especially when the infection is extensive and long standing. Ilizarov technique is a well-known technique for bone transport.
      • Spiegelberg B.
      • Parratt T.
      • Dheerendra S.K.
      • Khan W.S.
      • Jennings R.
      • Marsh D.R.
      Ilizarov principles of deformity correction.
      ,
      • Ilizarov G.A.
      • Green S.A.
      Transosseous Osteosynthesis--Theoretical and Clinical Aspects of the Regeneration and Growth of Tissue.
      To date, the Ilizarov method remains an alternative method for complex treatment of this category of patients, providing suppression of the infection process and reconstruction of the affected part whether bony defects, shortening or deformity. Moreover, limb salvage and reconstruction allows for a predictable and most effective way for treating complex chronic osteomyelitis.
      • Tetsworth Kevin D.
      • Dlaska Constantin E.
      The art of tibial bone transport using the ilizarov fixator.
      • Kliushin N.M.
      • Stepanenko P.
      • Mekki W.A.
      Treatment of forearm diaphyseal defect by distraction compression bone transport and continued distraction for radial head reduction: a case study.
      • Kliushin Nikolay Mikhailovich
      • Mekki Waleed Ahmed
      • Sudnitsyn Anatoliy Sergeyevich
      Spina bifida neuropathic foot osteomyelitis; results of using ilizarov technique in 46 cases.
      In this study we have studied and analyzed the results of using bifocal distraction-compression osteosynthesis (BFDCO) technique and the Monofocal compression osteosynthesis (MFCO) technique for treatment of this condition.

      2. Materials and methods

      This is a retrospective observational review of 49 patients with postoperative Tibial chronic osteomyelitis in the period from 2005 to 2014 which were treated using either Bifocal distraction compression BFDCO technique group I (31 patients) or Monofocal compression osteosynthesis MFCO technique Group II (18 patients). The average age of the patients was (41.6 ± 13.1 years), (range: 17–67 years). Leg length discrepancy was measured in 33 (58.9%) patients with an average of (1.4 ± 1.7 cm). Contracture of the ankle joint and equinus deformity were detected in 36 (64.3%) patients. Pre and Post-operative radiography together with Modified Irzhansky A.A et al. leg functional assessment system were used to assess the functional outcome. The study was approved by our Institutional Review Board (IRB). Men constituted 70% of the cases. The majority of patients had a high-energy injury during an accident, fall from a height or at work. There were 26 closed and 23 open fractures. Prior to admission to our center, all patients had metal work fixation of their fractures with plates, nails, screws and external fixators including Ilizarov Ring fixators. In the early postoperative period, 26 (53%) patients (11 of them had a closed fracture) developed locally purulent discharge from the fracture site. Upon admission, patients complained of pain during exertion on the injured limb, active wounds and fistulas with purulent discharge, and in some cases, increased body temperature, general weakness and malaise. Local examination of all patients showed wound defects with exposed parts of bone at the bottom (12 cases 24.5%) and/or fistulous passages (37 cases 75.5%) with purulent discharge. In 34 cases (69.4%) the skin of the lower leg in the infected area was represented by scar tissue fused to the underlying bone. In 40 (81.6%) patients leg and foot edema was present and in 8 cases (16.3%) post-thrombotic syndrome was detected. Leg length discrepancy was revealed in 33 (58.9%) patients on average of (1.4 ± 1.7 cm). Non-union was observed clinically in 45 (91.8%) patients. Tibial fracture consolidation was achieved in only 4 patients (8.1%). Contracture of the ankle joint and equinus deformity were detected in 36 (64.3%) patients.
      Radiography in all patients was characterized by destruction of the tibia, the presence in some cases of foreign bodies and bony defects of the tibia ranging from 1 to 10 cm (averaged 2.3 ± 1.8 cm) with regard to fixation modality two patients arrived with an intramedullary nail, 13 patients with a bone plate, three patients had fragments of screws in the tibia and 6 patients had Ilizarov apparatus. The results of the microbial swab for culture and sensitivity was represented by gram-positive flora (St. Aureus). The gram-negative flora was represented by pseudomonas aeruginosa and Corynebacterium spp. Microbial associations were detected in 59% of patients with closed fracture and in 29% of patients with an open fracture. Statistical analysis used categorical variables presented as number and percentage and continuous variables were presented as mean ± standard deviation (SD). The data were analyzed using Microsoft Excel office 2013.

      3. Surgical technique

      The treatment of patients is carried out at the infection department which is represented by a separate building. The protocol consisted of debridement and fixation by Ilizarov apparatus, with regard to the technique we either used the bifocal distraction-compression osteosynthesis (BFDCO) technique or the monofocal compression osteosynthesis (MFCO) technique depending on the size of the bone defect the patients were divided into two groups: group I consisted of (31 patients) treated by the BFDCO technique with resultant defects ≥2 cm and Group II (18 patients) treated by the Monofocal compression osteosynthesis MFCO technique with resultant defects ≤2 cm. Intra-operative swabs are taken from the discharge fluid, superficial and deep tissues and bone, we review x-rays, CT scans and when there is sinus we inject a brilliant green dye to determine the extent of the infection (Fig. 1. D), skin and soft tissue incisions are made layer by layer to access bone segments, removal of infected tissues is done until healthy bleeding margins could be noticed on the osseous bed (paprika sign) when sequestrectomy is performed the wound is washed thoroughly with antiseptic solution and with ultra-sonic wash system, a drain is inserted inside the wound and with skin undermining a primary closure of the wound is done (Fig. 1). Corticotomy is performed when there is a need to compensate for bony defects with the BFDCO technique, when the bone transport is about to complete 2–3 mm before docking we open the wound and perform debridement of the remaining non-viable and fibrous tissue associated with process of bone transport, we also perform refreshment of the bony ends and close the wound surgically and instruct the patient to continue the distraction 1–5 mm beyond docking to make sure that bone ends are engaged and in some cases when the proximal tibia provide a tapering end we continue distraction until it descend inside the distal fragment (Fig. 1. I).
      Fig. 1
      Fig. 139 years Male with Chronic post-traumatic osteomyelitis of the right tibia, treatment of the patient according to the BFDKO technique (A) infected plate fixation of the Right Tibia, (B) skin ulceration over the plate with discharging sinus, (C) Plate removal but with infected nonunion and unstable leg,(D) brilliant green dye to determine the extent of the infection, (E) Resection of 10 cm of sequestrum, (F,G) Proximal Tibail osteotomy and start of bone transport, (H) Clinical appearance after one year follow up with healed ulceration and sinuses with good function at both knee and Ankle joints (20 points), (I) Radiographic appearance one year postoperative showing consolidated regenerate and healed docking site.

      4. Results

      Assessment of the results of treatment in patients with post-traumatic tibial osteomyelitis was carried out within two years after treatment according to the main clinical criteria: suppression of the pyogenic infection, achievement of consolidation of bone fragments and the functional state of the limb. The time spent in Ilizarov fixator in patients in the first group was (142 ± 72 days) and in the second group was (75 ± 54 days) since the first group have larger defects. The results for both groups have shown consolidation of bone fragments in (81.5%) of patients in the first group and (72.2%) in the second group. Infection recurrence was observed in 14.3%, and complete fusion was achieved in 81.5% and hence Lack of consolidation or re-fracture within 6 months after dismantling of the apparatus was detected in 6 (19.5%) patients in group I and in 5 patients (27.8%) in group II· In addition 2 (6%) patients developed recurrence of infection in group I and in 5 (28%) patients in group II. We used the validation and cross-cultural adaptation of rating systems WOMAC and FJ-12 for evaluating the functional results of treatment.
      • Irzhansky A.A.
      • Kulyaba T.A.
      • Kornilov N.N.
      Validation and cross-cultural adaptation OF rating systems WOMAC, KSS and FJS-12 IN patients with knee disorders and injuries.
      To simplify the use of the scale we identified four main criteria: the presence of pain, impaired function of the ankle joint, shortening of the limb and the use of additional means of support. Each of these criteria included 5 parameters characterizing the degree of the functional state of the limb. The maximum score was 20 points (Table 1). Excellent = 19–20 points, good = 16–18, satisfactory = 13–15 and less than 13 is unsatisfactory. The calculation of the average functional state score (AFSS) made it possible to study the results of treatment in each group.
      Table 1Modified Irzhansky A.A et al. leg functional assessment system.
      • Irzhansky A.A.
      • Kulyaba T.A.
      • Kornilov N.N.
      Validation and cross-cultural adaptation OF rating systems WOMAC, KSS and FJS-12 IN patients with knee disorders and injuries.
      GradeAssessment Indicators
      PainAnkle movementShorteningAdditional support
      1 pointStanding aloneAnkylosis in abduction>5 cmWheelchair
      2 pointsIntermittent at restEquinus contractureUp to 5 cmCrutches
      3 pointsConstant walkingFunctional ankylosisUp to 3 cmCane
      4 pointsIntermittent walking90–100°Up to 2 cmOrthotics
      5 pointsNo painFull ROMNo shorteningNot required
      ROM; Range of Motion.
      In all 49 patients the preoperative score of the AFSS was (12.33 ± 2.32) and at final follow-up increased to (15.75 ± 2.97) which corresponded to an overall good result.
      In the first group I the preoperative AFSS score was (12.45 ± 2.41) and increased to (16.16 ± 2.99) at final follow-up which corresponded to good result. In the second group II the preoperative AFSS score was (12.11 ± 2.22) and increased to (15.06 ± 2.88) which corresponded to satisfactory result.

      5. Discussion

      Postoperative chronic osteomyelitis provides a difficult and challenging condition for the treating surgeon, the traditional methods consist of removal of dead bone and tissues or sequestrectomy and administering oral or IV antibiotics and repeated fixation by metalwork or linear external fixators which proved to be futile and ineffective in the majority of cases
      • Henke P.K.
      • Blackburn S.A.
      • Wainess R.W.
      • et al.
      Osteomyelitis of the foot and toe in adults is a surgical disease : conservative management worsens lower extremity salvage.
      ,
      • Heitzmann Lourenço Galizia
      • Battisti Raphael
      • Rodrigues
      • et al.
      Postoperative chronic osteomyelitis in the long bones - current knowledge and management of the problem.
      fixation by metalwork usually result in recurrence of infection and reappearance of the sinuses, with this regard it is very important to establish an extra focal fixation in the healthy part to avoid any further dissemination of infection, another element which is mostly needed is the stability of the fixation which is provided by Ilizarov fixators.
      • Plakseychuk A.
      • Plakseychuk Y.
      • Gruen G.S.
      • Ziran B.H.
      Treatment of osteomyelitis with Ilizarov frame.
      ,
      • McNally M.
      • Ferguson J.
      • Kugan R.
      • Stubbs D.
      Ilizarov treatment protocols in the management of infected nonunion of the tibia.
      Moreover the use of tension and compression forces create regenerative environment and increased bactericidal activity by increasing angiogentic reparative activities.
      • Ilizarov G.A.
      The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation.
      ,
      • Pacicca D.M.
      • Patel N.
      • Lee C.
      • et al.
      Expression of angiogenic factors during distraction osteogenesis.
      That's why Ilizarov believed that infection burns in the flame of regeneration, in this aspect, the BFDCO has an advantage over the MFCO by having osteotomy and distraction histogensis to transport bone fragment to the docking site and creating new tissues, our results showed that the number of infection relapse in group I was detected in 2 patients (6%) which is less than group II which was detected in 5 patients (28%). Lack of consolidation or re-fracture within 6 months after the dismantling of the apparatus in group I was detected in 6 patients (19.5%), in group II in 5 patients (27.8%) similar results were obtained by McNally M et al.
      • McNally M.
      • Ferguson J.
      • Kugan R.
      • Stubbs D.
      Ilizarov treatment protocols in the management of infected nonunion of the tibia.
      which reported 79 cases of infected tibial nonunion which were treated by Ilizarov technique, they found that consolidation of bone fragments was achieved in 81% of patients in the first group, and 72% in the second group. Purulent infection recurrence was observed in 14.3%, and complete fusion was achieved in 77.5%, they concluded that Monofocal compression achieved the lowest union rate (73.7%) and a re-fracture rate of (31.6%) where in the bifocal distraction compression group union was achieved in (77.8%). However, infection-free union was achieved 100% after further treatment which is a merit accredited to the use of Ilizarov technique.
      • McNally M.
      • Ferguson J.
      • Kugan R.
      • Stubbs D.
      Ilizarov treatment protocols in the management of infected nonunion of the tibia.
      Other similar results were obtained by different authors
      • Jain A.K.
      • Sinha S.
      Infected nonunion of the long bones.
      • Saleh M.
      • Royston S.
      Management of nonunion of fractures by distraction with correction of angulation and shortening.
      • Kocaoglu M.
      • Eralp L.
      • Sen C.
      • et al.
      Management of stiff hypertrophic nonunions by distraction osteogenesis: a report of 16 cases.
      • Magadum M.P.
      • Yadav C.M.B.
      • Phaneesha M.S.
      • et al.
      Acute compressionand lengthening by the ilizarov technique for infected nonunion of the tibia with large bone defects.
      • Shahid M.
      • Hussain A.
      • Bridgeman P.
      • Bose D.
      Clinical outcomes of the Ilizarov method after an infected tibial non union.
      • Yin P.
      • Zhang L.
      • Li T.
      • et al.
      Infected nonunion of tibia and femur treated by bone transport.
      The use of distraction histogenesis was also effective in treating septic coxitis.
      • Teplenky M.
      • Mekki W.
      • Parfenov E.
      • Oleinikov E.
      Reconstruction by ilizarov technique for sequelae of pediatric hip septic coxitis: a case study of a new technique with 14 years follow-up.
      We opt to the Monofocal compression technique in cases with small defects ≤2 cm and with shorter duration of infection, most of infection recurrence and re-fracture were in this group. In cases with larger defects ≥2.5 cm, Intercalary resection of the necrotic bone is performed to eradicate the infection and bifocal compression distraction technique BFDCO is carried out to compensate for the defect.
      • Jain A.K.
      • Sinha S.
      Infected nonunion of the long bones.
      • Saleh M.
      • Royston S.
      Management of nonunion of fractures by distraction with correction of angulation and shortening.
      • Kocaoglu M.
      • Eralp L.
      • Sen C.
      • et al.
      Management of stiff hypertrophic nonunions by distraction osteogenesis: a report of 16 cases.
      In our series, infection was eradicated in most cases with the distraction compression technique, but this may be due to the meticulous debridement of the infected tissue with a larger resection gap compared with the Monofocal compression group. The BFDCO has the advantage of concomitant accurate correction of deformity, leg length correction and bony union with poor soft tissue conditions. Magadum et al.
      • Magadum M.P.
      • Yadav C.M.B.
      • Phaneesha M.S.
      • et al.
      Acute compressionand lengthening by the ilizarov technique for infected nonunion of the tibia with large bone defects.
      presented 27 cases treated with bifocal compression distraction. They performed acute shortening with no reported complications in defects averaging 10 cm, with the largest defect measuring 17 cm. In our cases, we could not acutely compress such large defects, because of scarred and indurated soft tissues. In cases in which the overall limb alignment was satisfactory with an intact fibula, we prefer to retain the intact fibula for stability and continue with the bone transport. One of the main advantages of the Ilizarov technique is that it allows for early weight bearing in comparison to other techniques like the Masquelet technique which does not allow for early weight bearing Karger et al.
      • Karger C.
      • Kishi T.
      • Schneider L.
      • et al.
      Treatment of posttraumatic bone defects by the induced membrane technique.
      Our patients are mostly able to weight bear at the first postoperative day which may prevent other complications as osteoporosis, muscle atrophy and gait disturbances associated with other techniques.
      • McNally M.
      • Ferguson J.
      • Kugan R.
      • Stubbs D.
      Ilizarov treatment protocols in the management of infected nonunion of the tibia.
      • Ilizarov G.A.
      The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation.
      • Pacicca D.M.
      • Patel N.
      • Lee C.
      • et al.
      Expression of angiogenic factors during distraction osteogenesis.
      • Jain A.K.
      • Sinha S.
      Infected nonunion of the long bones.
      • Saleh M.
      • Royston S.
      Management of nonunion of fractures by distraction with correction of angulation and shortening.
      • Kocaoglu M.
      • Eralp L.
      • Sen C.
      • et al.
      Management of stiff hypertrophic nonunions by distraction osteogenesis: a report of 16 cases.
      • Magadum M.P.
      • Yadav C.M.B.
      • Phaneesha M.S.
      • et al.
      Acute compressionand lengthening by the ilizarov technique for infected nonunion of the tibia with large bone defects.
      • Shahid M.
      • Hussain A.
      • Bridgeman P.
      • Bose D.
      Clinical outcomes of the Ilizarov method after an infected tibial non union.
      • Yin P.
      • Zhang L.
      • Li T.
      • et al.
      Infected nonunion of tibia and femur treated by bone transport.

      6. Conclusion

      Treatment of Tibial chronic osteomyelitis using either Bifocal or Monofocal bone transport is an effective method. However our results have demonstrated better functional outcome and less infection recurrence and re-fracture rates when using the Bifocal distraction compression technique (BFDCO).

      7. Summary and highlights

      • 1.
        Postoperative Tibial chronic osteomyelitis is on rise.
      • 2.
        Meticulous debridement, IV Antibiotics according to C/S and ring external fixators (Ilizarov) to guard against axial deviation is an effective strategy for treatment.
      • 3.
        For small defects ≤2 cm the Monofocal Compression osteosynthesis technique (MFCO) is the preferred and more effective method.
      • 4.
        For larger defects ≥2 cm the Bifocal distraction Compression osteosynthesis bone transport technique (BFDCO) is the preferred and more effective method
      • 5.
        In our series Bifocal distraction Compression osteosynthesis bone transport technique (BFDCO) has reported less infection recurrence and re-fracture rate than the Monofocal Compression osteosynthesis technique (MFCO).
      • 6.
        In general, surgeons are advised to us the Bifocal distraction Compression osteosynthesis bone transport technique (BFDCO) in patients with larger bony defects and more complicated cases where deformity correction and lengthening might be required.

      Ethical approval

      The procedures performed in this study were in accordance with our institutional standards and approved by the Ethical Committee of our Center. The study was carried out as per the 1964 Helsinki declaration and its later amendments or comparable ethical standardshttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4763146/

      Informed consent

      Informed consent was obtained from all individual participants included in the study.

      Declaration of competing interest

      All Authors declare that they have no conflict of Interest with regard to the study.

      References

        • Poultsides 1 Lazaros A.
        • Liaropoulos Lycurgus L.
        • Malizos Konstantinos N.
        The socioeconomic impact of musculoskeletal infections.
        J Bone Joint Surg Am. 2010 Sep 1; 92: e13
        • Anandasivam
        • Nidharshan S.
        • et al.
        Tibial shaft fracture: a large-scale study defining the injured population and associated injuries.
        J Clin Orthopaed Trauma. 2017; 8: 225-231https://doi.org/10.1016/j.jcot.2017.07.012
        • Jorge L.S.
        • Chueire A.G.
        • Fucuta P.S.
        • et al.
        Predisposing factors for recurrence of chronic posttraumatic osteomyelitis: a retrospective observational cohort study from a tertiary referral center in Brazil.
        Patient Saf Surg. 2017; 11: 17
        • Lima A.L.
        • Oliveira P.R.
        • Carvalho V.C.
        • Cimerman S.
        • Savio E.
        Diretrizes Panamericanas para el Tratamiento de las Osteomielitis e Infecciones de Tejidos Blandos Group. Recommendations for the treatment of osteomyelitis.
        Braz J Infect Dis. 2014 Sep-Oct; 18: 526-534
        • Lazzarini L.
        • Mader J.T.
        • Calhoun J.H.
        Osteomyelitis in long bones.
        J Bone Joint Surg Am. 2004 Oct; 86: 2305-2318
        • Calhoun J.H.
        • Manring M.M.
        • Shirtliff M.
        Osteomyelitis of the long bones.
        Semin Plast Surg. 2009; 23: 59-72
        • Kremers H.M.
        • Nwojo M.E.
        • Ransom J.E.
        • Wood-Wentz C.M.
        • Melton 3rd, L.J.
        • Huddleston 3rd, P.M.
        Trends in the epidemiology of osteomyelitis: a population-based study, 1969 to 2009.
        J Bone Joint Surg Am. 2015; 97: 837-845
        • Spiegelberg B.
        • Parratt T.
        • Dheerendra S.K.
        • Khan W.S.
        • Jennings R.
        • Marsh D.R.
        Ilizarov principles of deformity correction.
        Ann R Coll Surg Engl. 2010; 92: 101-105
      1. (Springer-Verlag; Berlin)
        • Ilizarov G.A.
        • Green S.A.
        Transosseous Osteosynthesis--Theoretical and Clinical Aspects of the Regeneration and Growth of Tissue.
        1992
        • Tetsworth Kevin D.
        • Dlaska Constantin E.
        The art of tibial bone transport using the ilizarov fixator.
        Tech Orthop. Sept. 2015; 30: 142-155
        • Kliushin N.M.
        • Stepanenko P.
        • Mekki W.A.
        Treatment of forearm diaphyseal defect by distraction compression bone transport and continued distraction for radial head reduction: a case study.
        Chin J Traumatol. 2019 Oct; 22 (Epub 2019 Jun 15): 304-307https://doi.org/10.1016/j.cjtee.2019.04.005
        • Kliushin Nikolay Mikhailovich
        • Mekki Waleed Ahmed
        • Sudnitsyn Anatoliy Sergeyevich
        Spina bifida neuropathic foot osteomyelitis; results of using ilizarov technique in 46 cases.
        Acta Orthop Belg. 2020; 86
        • Irzhansky A.A.
        • Kulyaba T.A.
        • Kornilov N.N.
        Validation and cross-cultural adaptation OF rating systems WOMAC, KSS and FJS-12 IN patients with knee disorders and injuries.
        Traumatol Orthoped Russia. 2018; 24: 70-79https://doi.org/10.21823/2311-2905-2018-24-2-70-79
        • Henke P.K.
        • Blackburn S.A.
        • Wainess R.W.
        • et al.
        Osteomyelitis of the foot and toe in adults is a surgical disease : conservative management worsens lower extremity salvage.
        Ann Surg. 2005; 241: 885-894
        • Heitzmann Lourenço Galizia
        • Battisti Raphael
        • Rodrigues
        • et al.
        Postoperative chronic osteomyelitis in the long bones - current knowledge and management of the problem.
        Revista Brasileira de Ortopedia. 2019; 54 (Epub . 2019): 627-635
        • Plakseychuk A.
        • Plakseychuk Y.
        • Gruen G.S.
        • Ziran B.H.
        Treatment of osteomyelitis with Ilizarov frame.
        Operat Tech Orthop. 2002; 12: 273-281
        • McNally M.
        • Ferguson J.
        • Kugan R.
        • Stubbs D.
        Ilizarov treatment protocols in the management of infected nonunion of the tibia.
        J Orthop Trauma. 2017; 31: S47-S54
        • Ilizarov G.A.
        The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation.
        Clin Orthop Relat Res. 1989; 238: 249-281
        • Pacicca D.M.
        • Patel N.
        • Lee C.
        • et al.
        Expression of angiogenic factors during distraction osteogenesis.
        Bone. 2003; 33: 889-898
        • Jain A.K.
        • Sinha S.
        Infected nonunion of the long bones.
        Clin Orthop Relat Res. 2005; 431: 57-65
        • Saleh M.
        • Royston S.
        Management of nonunion of fractures by distraction with correction of angulation and shortening.
        J Bone Joint Surg Br. 1996 Jan; 78: 105-109
        • Kocaoglu M.
        • Eralp L.
        • Sen C.
        • et al.
        Management of stiff hypertrophic nonunions by distraction osteogenesis: a report of 16 cases.
        J Orthop Trauma. 2003; 17: 543-554
        • Magadum M.P.
        • Yadav C.M.B.
        • Phaneesha M.S.
        • et al.
        Acute compressionand lengthening by the ilizarov technique for infected nonunion of the tibia with large bone defects.
        J Orthop Surg. 2006; 14: 273-279
        • Shahid M.
        • Hussain A.
        • Bridgeman P.
        • Bose D.
        Clinical outcomes of the Ilizarov method after an infected tibial non union.
        Arch Trauma Res. 2013 Aug; 2 (Epub 2013 Aug 1): 71-75https://doi.org/10.5812/atr.11300
        • Yin P.
        • Zhang L.
        • Li T.
        • et al.
        Infected nonunion of tibia and femur treated by bone transport.
        J Orthop Surg Res. 2015; 10: 1-9
        • Teplenky M.
        • Mekki W.
        • Parfenov E.
        • Oleinikov E.
        Reconstruction by ilizarov technique for sequelae of pediatric hip septic coxitis: a case study of a new technique with 14 years follow-up.
        J clin Orthopaed Trauma. 2020 Oct; 11: S812-S816
        • Karger C.
        • Kishi T.
        • Schneider L.
        • et al.
        Treatment of posttraumatic bone defects by the induced membrane technique.
        Orthop Traumatol Surg Res. 2012; 98: 97-102