- Research
- Open Access
- Published:
A comparative study of bone union and nonunion during distraction osteogenesis
BMC Musculoskeletal Disorders volume 23, Article number: 1053 (2022)
Abstract
Background
The clinical characteristics of bone nonunion during distraction osteogenesis (DO) were rarely discussed. This study was employed to specify the difference between bone union and nonunion during DO.
Methods
The patients with bone lengthening were recruited in our study. The bone union cases indicated the ones that remove the external fixator successfully, whereas the bone nonunion represented the bridging callus did not appear even after 9 months (an absence of bridging callus for at least three out of four cortices on plain radiographs) that needs autogenous bone transplantation. The differences in the pixel value ratio (PVR) growth of regenerated callus, lengthening index (LI), healing index (HI), external fixation index (EFI) and blood biochemical indexes between bone union and nonunion were analyzed.
Results
A total of 8 bone nonunion and 27 bone union subjects were included in this study. The PVR growth in bone nonunion was significantly lower than that in bone union (0.19 ± 0.06 vs. 0.32 ± 0.16, P = 0.048). Interestingly, the HI and EFI in bone nonunion was significantly higher than that in bone union (62.0 ± 31.4 vs. 37.0 ± 27.4, P = 0.036; 75.0 ± 30.9 vs. 49.9 ± 16.1, P = 0.006). However, no significant difference with regard to LI was identified (0.76 ± 0.52 vs. 0.77 ± 0.32, P = 0.976). Moreover, the circulating level of urea and lymphocyte count in bone union was significantly lower than that in bone nonunion (4.31 ± 1.05 vs. 5.17 ± 1.06, P = 0.049; 2.08 ± 0.67 vs. 2.73 ± 0.54, P = 0.018). On the contrary, the circulating level of magnesium in bone union was significantly higher than that in bone nonunion (0.87 ± 0.07 vs. 0.80 ± 0.07, P = 0.014).
Conclusion
Compared to the bone union, the PVR growth was significantly lower, whereas the HI and EFI was significantly higher in the bone nonunion. Moreover, the circulating level of urea, magnesium and lymphocyte count was also different between these two. Therefore, the PVR, HI and EFI seems to be reliable and sensitive indicators to reflect the bone nonunion during DO, which might be considered in bone lengthening. Further prospective studies are still needed to elaborate the concerned issues.
Introduction
Distraction osteogenesis (DO) is a surgical technique that widely used to treat a variety of pathological conditions in children and adults, such as limbs length discrepancy, bone deformity or resection secondary to trauma, infection or malignant tumor [1]. The tension-stress rule of DO exerts continuous, stable and slow distraction force to living tissue, stimulates/activates tissue cell regeneration and growth, and promotes bone regeneration [2]. It has become an integral part of the arsenal in the orthopedics community worldwide, and the evolutionary development of the method has considerably improved the quality of life for millions around the world [3].
Meanwhile, the complications caused by DO may also need to be considered. Generally speaking, the DO-related complications include bone nonunion, new bone fracture, nail infection and relaxation, muscle contracture and joint stiffness, force line deviation, etc. [4,5,6,7]. Among them, the bone nonunion is a serious clinical issue that prolong the treatment period and increase the burden in bone lengthening [8]. However, the current evidence on bone nonunion is rather limited. Paley et al. [9] demonstrated that both technical (traumatic corticotomy, initial diastasis, instability, rapid distraction) and patient factors (infection, malnutrition, and metabolic) might lead to DO-related bone nonunion. Moreover, McKee et al. [10] found that the cigarette smoking was also associated with DO-related bone nonunion in limb lengthening. In addition, Liantis et al. [11] indicated that age, treatment days and fixator time were significantly correlated with a variety of DO-related complications, including bone nonunion. Papakostidis et al. [12] further suggested that the bone fracture risk will increase when the lengthening was larger than 8Â cm. However, a comprehensive and systematic comparative study between bone union and nonunion during DO is still needed.
Several indicators were employed to assess the outcome in DO. Pixel value ratio (PVR) is mainly utilized to assess the maturity of late callus and the timing to remove the external fixator [13,14,15,16,17]. In addition, the lengthening index (LI), healing index (HI) and external fixator index (EFI) is served as general indicator to analysis bone healing during DO [18]. However, these above indicators were only considered in bone union cases. It was unclear if they could reflect the characteristics of bone nonunion. Moreover, some biochemical indexes are also reported to be associated with osteogenesis [19, 20]. Therefore, we aimed to investigate the difference in the following indexes between bone union and nonunion during DO: (1) the PVR growth pattern of regenerated callus; (2) the HI, LI and EFI; and (3) the comprehensive biochemical index, and identify some novel and sensitive indicators for bone nonunion during DO.
Materials and methods
Study design
This study was approved by the ethics committee of Xiangya Hospital of Central South University. The clinical and imaging data of patients who completed bone lengthening in Xiangya Hospital of Central South University were reviewed retrospectively. All surgical procedures were performed by the senior surgeons. The inclusion criteria were: (1) Lower limb lengthening by using Ilizarov technique; (2) Patients with bone union and nonunion during DO. Bone union indicated the ones that remove the external fixator successfully, whereas bone nonunion represented the bridging callus did not appear even after 9 months (an absence of bridging callus for at least three out of four cortices on plain radiographs) that needs autogenous bone transplantation[21,22,23].; (3) Primary surgery. The exclusion criteria were: (1) Amputation patients who are unable to complete bone lengthening therapy; (2) Patients with skeletal disorder affecting healing (e.g., congenital pseudarthrosis of tibia); (3) Patients with missing follow-up data. The Ilizarov technique was used for bone lengthening in femur and tibia. The distraction was initiated one week after the osteotomy (1.0Â cm/day in juvenile and 0.75Â cm/day in adult), and the patients were examined by X-ray monthly. The conditions to remove the external fixator were listed as follow: (1) bridging callus appears on three of the four cortices; (2) the fixation time is generally in line with the average extension index; (3) no abnormal feeling of weight-bearing after loosening the nut [24].
The general characteristics of patients
A total of 27 bone union and 8 bone nonunion patients were recruited in our study. The general characteristics of patients including sex, age, BMI, lengthening length, cigarette smoking, alcohol drinking, external fixator type (unilateral or ring external fixator), reason for DO and site of osteotomy were collected, respectively.
The difference in the PVR growth of regenerated callus
The PV of regenerated and adjacent bone after osteotomy were measured and recorded by using the image measurement tool of picture archiving the communication system (PACS) system (Fig. 1). All radiographs were taken by the same technician using the same equipment and were independently assessed by two senior orthopedists who were blinded to the subjects’ clinical symptoms. Subjects with inconsistent opinions were recalled after the survey and resolved by discussion. In order to improve the accuracy of PVR, the part of the metal bar was rigorously avoided. Then, the ratio of the regenerated callus PV to the adjacent bone PV was calculated. The higher PVR indicated that the regenerated callus was closer to the reference bone, whereas the lower PVR reflected a lower immaturity of the callus [17, 25]. The formula for the calculations of PVR were as follows:
The PVR growth indicates the PVR difference between external fixator install and removal for bone union (Fig. 2A), or final autogenous bone transplantation for bone nonunion (Fig. 2B), respectively. The PVR growth was compared in bone union and nonunion. Moreover, the monthly PVR growth of regenerated callus in bone union and nonunion was also analyzed.
The difference in healing index, lengthening index and external fixator index
The HI was calculated as the duration of complete consolidation (three cortices in distraction callus) in days divided by the length gained in centimeter, whereas the LI was the number of months required to achieve 1Â cm lengthening [26, 27]. In addition, the EFI was calculated as dividing the using period of frames (days) by the distracted length of the bone (cm) [18]. All these three were decent and reliable indicators to reflect the bone healing potential, as well as the clinical outcome in DO. The HI, LI and EFI of the bone union and nonunion was therefore analyzed and compared.
The difference in biochemical index
The comprehensive biochemical indexes before the surgery/osteotomy (CRP, total bilirubin, mean hemoglobin content, ESR, uric acid, urea, white blood cell count, lymphocyte count, basophil count, eosinophil count, fibrinogen, monocyte count, magnesium, calcium, phosphorus and total protein) in the bone union and nonunion was analyzed and compared.
Statistical analysis
All the analyses were done by using the SPSS 26.0. The difference was analyzed by variance analysis. P < 0.05 was regarded as statistically significant.
Results
The general characteristics of patients
The general characteristics of patients were showed in Table 1. There was no significant statistical difference for sex, age, BMI, lengthening length, cigarette smoking, alcohol drinking, external fixator type, reason and site of osteotomy for DO between bone union and nonunion.
The PVR growth in bone nonunion was significantly lower
The PVR growth in bone nonunion was significantly lower than that in bone union during DO (0.19 ± 0.06 vs. 0.32 ± 0.16, P = 0.048) (Table 2; Fig. 2C). Obviously, the PVR grew more quickly in bone union (Supplementary Tables 1, Fig. 2D).
The healing index and external fixator index in bone nonunion was significantly higher
The HI and EFI in bone nonunion was significantly higher than that in bone union (62.0 ± 31.4 vs. 37.0 ± 27.4, P = 0.036; 75.0 ± 30.9 vs. 49.9 ± 16.1, P = 0.006) (Table 3; Fig. 3A, C). However, no significant difference with regard to LI was identified (0.76 ± 0.52 vs. 0.77 ± 0.32, P = 0.976) (Table 3; Fig. 3B).
The circulating level of urea, magnesium and lymphocyte count was different
The circulating level of urea and lymphocyte count in bone union was significantly lower (4.31 ± 1.05 vs. 5.17 ± 1.06, P = 0.049; 2.08 ± 0.67 vs. 2.73 ± 0.54, P = 0.018), whereas the circulating level of magnesium was significantly higher (0.87 ± 0.07 vs. 0.80 ± 0.07, P = 0.014) than that in bone nonunion (Table 4). With regard to other biochemical index, no significant difference was obtained (Supplementary Table 2).
Discussions
Compared to bone union, the PVR growth was significantly lower, whereas the HI and EFI was significantly higher in bone nonunion. The PVR, HI and EFI seems to be reliable and sensitive indicators to reflect the bone nonunion during DO. Moreover, the circulating level of urea, magnesium and lymphocyte count was also different between bone union and nonunion (Fig. 4).
To our best knowledge, the PVR has only been considered in bone union. Zhao et al. [17] suggested that the PVR could be severed as an objective measurement to guide the timing of external fixator removal (carry weight partially when the PVR of two cortices reached to 1, and carry weight fully when the PVR of three cortices reached to 1). Moreover, Bafor et al. [13] demonstrated that full weight-bearing could be initiated when the cortical PVR of 3/4 was at least 0.93 in bone lengthening. In addition, Vulcano et al. [16] indicated that a PVR value of 0.90 could be considered as bone healing. Zak et al. [28] further proved that the combination of PVR and subjective evaluation parameters (continuity, signal intensity and homogeneity of regenerated tissue) was conducive to monitoring the bone healing in DO. Futhermore, we previously found that the early PVR was gradually increasing in the first 3months after osteotomy, which might be significantly influenced by chronological age, sex, and lengthening site. Moreover, the early PVR seemed to be moderately inversely associated with HI and LI, respectively. In another word, the early PVR of callus may partly reflect the potential clinical outcome for DO [25]. On the basis of these above, our study further figured out the PVR growth pattern in bone nonunion during DO.
Interestingly, the HI and EFI in bone nonunion was significantly higher than that in bone union, whereas no significant difference with regard to LI was identified in our study. Although these three were reliable indicators for the outcome in DO [26, 27, 29,30,31], their difference should be identified and emphasized. Basically, LI refers to the average time to lengthen 1Â cm. Therefore, the lengthening speed is similar between bone union and nonunion group, which ensures the homogeneity and comparability of the bone union and nonunion group (consistent average distraction speed). However, HI and EFI refers to the average time per 1Â cm of bone healing or external fixator period, respectively. Indeed, the bone consolidation and healing in bone nonunion are exactly inferior to bone union. As a consequence, the HI and EFI is suggested to be routinely considered in bone lengthening.
Several biochemical indexes have been reported to be associated with bone disorder/osteogenesis before. Adunsky et al. [32] found that the urea might be served as a reliable indicator to predict the functional outcomes in hip fractures. In addition, Zhang et al. [33] found that magnesium could promote new bone formation in vivo, and Liu et al. [34] further demonstrated that magnesium could improve the osteogenic differentiation and angiogenesis in vitro. On the other hand, immune cells were considered to be important to bone dynamic balance [35]. Xu and Hong et al. [36, 37] indicated that the increased lymphocytes could lead to systemic bone loss by reducing the osteogenesis of bone marrow mesenchymal stem cells. Consistently, our results showed that the circulating level of urea, magnesium and lymphocyte count was different between bone union and nonunion. However, the circulating levels of magnesium and urea fall well within the normal ranges, and the differences could be related to the patients themselves. Therefore, more studies were still needed to address the issue.
The strengths of our study can be listed as follow: (1) this is the first comprehensive and systematic comparative study for bone union and nonunion during DO; (2) our results may be beneficial to the clinical management of bone lengthening. The limitations of the present study should also be acknowledged. First, several issues cannot be addressed due to the nature of retrospective study design. For example, the functional assessment during follow-up, the timing (midterm and final follow up) and variety (osteogenic index: osteocalcin, bone-specific alkaline phosphatase, etc.) of biochemical index cannot be considered in our study. Second, we cannot fully make sure that all the comparisons were on the same baseline. Third, the number of bone nonunion is relatively small, which may inevitability influence our results.
Conclusion
Compared to bone union, the PVR growth was significantly lower, whereas the HI and EFI was significantly higher in bone nonunion. Moreover, the circulating level of urea, magnesium and lymphocyte count was also different between bone union and nonunion. Therefore, the PVR, HI and EFI seems to be reliable and sensitive indicators to reflect the bone nonunion during DO, which might be considered in bone lengthening. Further prospective studies are still needed to elaborate the concerned issues.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Malkova TA, Borzunov DY. International recognition of the Ilizarov bone reconstruction techniques: current practice and research (dedicated to 100(th) birthday of G. A. Ilizarov). World J Orthop. 2021;12(8):515–33.
Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: part II. The influence of the rate and frequency of distraction. Clin Orthop Relat Res. 1989;239:263–85.
Gubin AV, Borzunov DY, Malkova TA. The Ilizarov paradigm: thirty years with the Ilizarov method, current concerns and future research. Int Orthop. 2013;37(8):1533–9.
Liu Y, Yushan M, Liu Z, Liu J, Ma C, Yusufu A. Complications of bone transport technique using the Ilizarov method in the lower extremity: a retrospective analysis of 282 consecutive cases over 10 years. BMC Musculoskelet Disord. 2020;21(1):354.
Borzunov DY, Kolchin SN, Malkova TA. Role of the Ilizarov non-free bone plasty in the management of long bone defects and nonunion: problems solved and unsolved. World J Orthop. 2020;11(6):304–18.
Liu Q, Liu Z, Guo H, Liang J, Zhang Y. The progress in quantitative evaluation of callus during distraction osteogenesis. BMC Musculoskelet Disord. 2022;23(1):490.
Liu Z, Liu Q, Guo H, Liang J, Zhang Y. Overview of physical and pharmacological therapy in enhancing bone regeneration formation during distraction osteogenesis. Front Cell Dev Biol. 2022;10:837430.
Berner A, Reichert JC, Muller MB, Zellner J, Pfeifer C, Dienstknecht T, Nerlich M, Sommerville S, Dickinson IC, Schutz MA, et al. Treatment of long bone defects and non-unions: from research to clinical practice. Cell Tissue Res. 2012;347(3):501–19.
Paley D. Problems, obstacles, and complications of limb lengthening by the Ilizarov technique. Clin Orthop Relat Res. 1990;(250):81–104.
McKee MD, DiPasquale DJ, Wild LM, Stephen DJ, Kreder HJ, Schemitsch EH. The effect of smoking on clinical outcome and complication rates following Ilizarov reconstruction. J Orthop Trauma. 2003;17(10):663–7.
Liantis P, Mavrogenis AF, Stavropoulos NA, Kanellopoulos AD, Papagelopoulos PJ, Soucacos PN, Babis GC. Risk factors for and complications of distraction osteogenesis. Eur J Orthop Surg Traumatol. 2014;24(5):693–8.
Papakostidis C, Bhandari M, Giannoudis PV. Distraction osteogenesis in the treatment of long bone defects of the lower limbs: effectiveness, complications and clinical results; a systematic review and meta-analysis. Bone Joint J. 2013;95-B(12):1673–80.
Bafor A, Duncan ME, Iobst CA. Evaluating the utility of the pixel value ratio in the determination of time to full weight-bearing in patients undergoing Intramedullary Limb Lengthening. Strategies Trauma Limb Reconstr. 2020;15(2):74–8.
Hazra S, Song H, Biswal S, Lee S, Lee S, Jang K, Modi H. Quantitative assessment of mineralization in distraction osteogenesis. Skeletal Radiol. 2008;37(9):843–7.
Song SH, Agashe M, Kim TY, Sinha S, Park YE, Kim SJ, Hong JH, Song SY, Song HR. Serial bone mineral density ratio measurement for fixator removal in tibia distraction osteogenesis and need of a supportive method using the pixel value ratio. J Pediatr Orthop B. 2012;21(2):137–45.
Vulcano E, Markowitz JS, Ali S, Nguyen J, Fragomen AT, Rozbruch SR. Assessment of Bone Healing during Antegrade Intramedullary Rod Femur Lengthening using Radiographic Pixel density. J Am Acad Orthop Surg. 2018;26(18):e388–94.
Zhao L, Fan Q, Venkatesh KP, Park MS, Song HR. Objective guidelines for removing an external fixator after tibial lengthening using pixel value ratio: a pilot study. Clin Orthop Relat Res. 2009;467(12):3321–6.
Abulaiti A, Liu Y, Cai F, Liu K, Abula A, Maimaiti X, Ren P, Yusufu A. Bone defects in Tibia managed by the bifocal vs. trifocal bone transport technique: a retrospective comparative study. Front Surg. 2022;9:858240.
Sabbaghzadeh A, Bonakdar S, Gorji M, Gholipour M. Evaluation of the effect of preoperative hemoglobin level and proinflammatory factors on intertrochanteric fracture union. Wien Klin Wochenschr. 2022;134(11–12):458–62.
Choi IH, Kim JK, Chung CY, Cho TJ, Lee SH, Suh SW, Whang KS, Park HW, Song KS. Deformity correction of knee and leg lengthening by Ilizarov method in hypophosphatemic rickets: outcomes and significance of serum phosphate level. J Pediatr Orthop. 2002;22(5):626–31.
Jiang Y, Wang X, Huang W, Zhu Y, Zhang K, Feng D. A novel bone graft technique combined with plating for aseptic recalcitrant long bone nonunion. BMC Musculoskelet Disord. 2022;23(1):873.
Wu S, Quan K, Mei J, Dai M, Song S. Cortical allograft strut augmented with platelet-rich plasma for the treatment of long bone non-union in lower limb- a pilot study. BMC Musculoskelet Disord. 2022;23(1):512.
Zhang J, Yin P, Han B, Zhao J, Yin B. The treatment of the atrophic clavicular nonunion by double-plate fixation with autogenous cancellous bone graft: a prospective study. J Orthop Surg Res. 2021;16(1):22.
Iobst CA, Mohammed W, Colley R. Determining when it is safe to remove the external fixator: results from a survey of the Limb Lengthening and Reconstruction Society. Orthopedics. 2017;40(5):e876–9.
Liu Q, Mei H, Zhu G, Liu Z, Guo H, Wang M, Liang J, Zhang Y. Early Pixel Value Ratios to Assess Bone Healing during Distraction Osteogenesis. Front Bioeng Biotechnol. 2022;10:929699.
Wright SE, Goodier WD, Calder P. Regenerate deformity with the precice tibial nail. Strategies Trauma Limb Reconstr. 2020;15(2):98–105.
Koczewski P, Shadi M. Factors influencing bone regenerate healing in distraction osteogenesis. Ortop Traumatol Rehabil. 2013;15(6):591–9.
Zak L, Tiefenboeck TM, Wozasek GE. Bone reconstruction: subjective evaluation and objective analysis based on conventional digital X-rays - a retrospective evaluation. Orthop Traumatol Surg Res. 2021;107:103081.
Sangkaew C. Distraction osteogenesis of the femur using conventional monolateral external fixator. Arch Orthop Trauma Surg. 2008;128(9):889–99.
Bozan ME, Altinel L, Kuru I, Maralcan G, Acar M, Durmaz H. Factors that affect the healing index of metacarpal lengthening: a retrospective study. J Orthop Surg (Hong Kong). 2006;14(2):167–71.
Li Y, Han B, Tang J, Chen M, Wang Z. Identification of risk factors affecting bone formation in gradual ulnar lengthening in children with hereditary multiple exostoses: a retrospective study. Med (Baltim). 2019;98(5):e14280.
Adunsky A, Mizrahi EH, Kaplan A, Purits E, Waitzman A, Arad M. Elevated blood urea, independent of glomerular filtration rate (GFR), confers increased risk of adverse functional outcome in elderly hip fracture patients. Arch Gerontol Geriatr. 2011;53(2):e174–8.
Zhang Y, Xu J, Ruan YC, Yu MK, O’Laughlin M, Wise H, Chen D, Tian L, Shi D, Wang J, et al. Implant-derived magnesium induces local neuronal production of CGRP to improve bone-fracture healing in rats. Nat Med. 2016;22(10):1160–9.
Liu W, Guo S, Tang Z, Wei X, Gao P, Wang N, Li X, Guo Z. Magnesium promotes bone formation and angiogenesis by enhancing MC3T3-E1 secretion of PDGF-BB. Biochem Biophys Res Commun. 2020;528(4):664–70.
Konnecke I, Serra A, El Khassawna T, Schlundt C, Schell H, Hauser A, Ellinghaus A, Volk HD, Radbruch A, Duda GN, et al. T and B cells participate in bone repair by infiltrating the fracture callus in a two-wave fashion. Bone. 2014;64:155–65.
Xu X, Li R, Zhou Y, Zou Q, Ding Q, Wang J, Jin W, Hua G, Gao J. Dysregulated systemic lymphocytes affect the balance of osteogenic/adipogenic differentiation of bone mesenchymal stem cells after local irradiation. Stem Cell Res Ther. 2017;8(1):71.
Hong W, Tang L, Ge R, Li W, Shen X, Hong L, Xu X. Persistent abnormal Immunocytes Induced systemic bone loss in locally irradiated rats. Calcif Tissue Int. 2021;109(6):706–18.
Acknowledgements
Not applicable.
Funding
This study was supported by National Natural Science Foundation of China (82102581, 82270930), National Postdoctoral Science Foundation of China (2021M693562), Provincial Natural Science Foundation of Hunan (2019JJ40517, 2022JJ40843), Provincial Outstanding Postdoctoral Innovative Talents Program of Hunan (2021RC2020), Young Investigator Grant of Xiangya Hospital, Central South University (2020Q14), FuQing Postdoc Program of Xiangya Hospital, Central South University (176) and Fund of Reform and Practice of Ideological and Political in Xiangya Hospital, Central South University (36, 40).
Author information
Authors and Affiliations
Contributions
YZ decided and conceptualized this article, and revised the draft. QL and YZ wrote the manuscript. HBG, MW and ZL collected and analyzed the data, prepared the figures and tables. YZ and JYL were the guarantors of the overall content. All authors approved the final version of the manuscript and agreed to be accountable for all specs of the work.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Ethical approval was obtained by the ethics committee of Xiangya Hospital of Central South University. The informed consent was obtained from all subjects and/or their legal guardian(s). All methods were carried out in accordance with relevant guidelines and regulations.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Additional file 1: Supplementary Table 1.
The different PVR growth pattern between bone union and nonunion. Supplementary Table 2. The difference in biochemical index between bone union and nonunion.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
About this article
Cite this article
Liu, Q., Liu, Z., Guo, H. et al. A comparative study of bone union and nonunion during distraction osteogenesis. BMC Musculoskelet Disord 23, 1053 (2022). https://doi.org/10.1186/s12891-022-06034-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s12891-022-06034-w
Keywords
- Bone union and nonunion
- Distraction osteogenesis
- External fixator
- Pixel value ratio
- Healing index
- Lengthening index
- External fixator index
- Biochemical index