Tibial Cortex Transverse Transport Facilitates Severe Diabetic Foot Wound Healing via HIF-1α-Induced Angiogenesis

References

• Sun H, Saeedi P, Karuranga S, et al. IDF Diabetes Atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabet Res Clin Pract. 2022;183:109119. doi:10.1016/j.diabres.2021.109119
   PubMed Web of Science ®Google Scholar
• Senneville É, Albalawi Z, van Asten SA, et al. IWGDF/IDSA guidelines on the diagnosis and treatment of diabetes-related foot infections (IWGDF/IDSA 2023). Clin Infect Dis off Publ Infect Dis Soc Am. 2023:ciad527. doi:10.1093/cid/ciad527
   Google Scholar
• Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet Lond Engl. 2005;366:9498. doi:10.1016/S0140-6736(05)67698-2
   Web of Science ®Google Scholar
• M K, F M, Ajm B, S E. Etiology, epidemiology, and disparities in the burden of diabetic foot ulcers. Diabetes Care. 2023;46(1). doi:10.2337/dci22-0043
   PubMed Web of Science ®Google Scholar
• van Netten JJ, Bus SA, Apelqvist J, et al. Definitions and criteria for diabetes-related foot disease (IWGDF 2023 update). Diabetes Metab Res Rev. 2023:e3654. doi:10.1002/dmrr.3654
   PubMed Web of Science ®Google Scholar
• Chen Y, Kuang X, Zhou J, et al. Proximal tibial cortex transverse distraction facilitating healing and limb salvage in severe and recalcitrant diabetic foot ulcers. Clin Orthop. 2020;478(4):836–851.
   PubMed Web of Science ®Google Scholar
• Oda T, Niikura T, Fukui T, et al. Transcutaneous CO2 application accelerates fracture repair in streptozotocin-induced type I diabetic rats. BMJ Open Diabetes Res Care. 2020;8(2):e001129. doi:10.1136/bmjdrc-2019-001129
   PubMed Web of Science ®Google Scholar
• Edmonds M, Manu C, Vas P. The current burden of diabetic foot disease. J Clin Orthop Trauma. 2021;17. doi:10.1016/j.jcot.2021.01.017
   Google Scholar
• Ilizarov GA. 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. 1989;238:249–281.
   PubMed Web of Science ®Google Scholar
• 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. 1989;239:263–285. doi:10.1097/00003086-198902000-00029
   PubMedGoogle Scholar
• Ilizarov GA, Ledyaev VI. The replacement of long tubular bone defects by lengthening distraction osteotomy of one of the fragments. Clin Orthop. 1992;280:7–10.
   Google Scholar
• Ilizarov GA. Clinical application of the tension-stress effect for limb lengthening. Clin Orthop. 1990;250:8–26.
   PubMed Web of Science ®Google Scholar
• Minematsu K, Tsuchiya H, Taki J, Tomita K. Blood flow measurement during distraction osteogenesis. Clin Orthop. 1998;347:229–235.
   Google Scholar
• Gubin AV, Borzunov DY, Marchenkova LO, Malkova TA, Smirnova IL. Contribution of G.A. Ilizarov to bone reconstruction: historical achievements and state of the art. Strateg Trauma Limb Reconstr. 2016;11(3):145–152. doi:10.1007/s11751-016-0261-7
   PubMedGoogle Scholar
• Kuo KN, Qureshi A, Bush-Joseph CA, Templeton A. Ilizarov distraction histogenesis to reconstruct massive posttraumatic osteoarticular defects: a case report. J Bone Joint Surg Am. 2003;85(6):1125–1128. doi:10.2106/00004623-200306000-00025
   PubMedGoogle Scholar
• Aston JW, Williams SA, Allard RN, Sawamura S, Carollo JJ. A new canine cruciate ligament formed through distraction histogenesis. Report of a pilot study. Clin Orthop. 1992;280:30–36.
   Google Scholar
• Matsuyama J, Ohnishi I, Kageyama T, Oshida H, Suwabe T, Nakamura K. Osteogenesis and angiogenesis in regenerating bone during transverse distraction: quantitative evaluation using a canine model. Clin Orthop. 2005;433(243–250). doi:10.1097/01.blo.0000150562.24256.a4
   Google Scholar
• Ohashi S, Ohnishi I, Kageyama T, Imai K, Nakamura K. Distraction osteogenesis promotes angiogenesis in the surrounding muscles. Clin Orthop. 2007;454:223–229. doi:10.1097/01.blo.0000238795.82466.74
   PubMedGoogle Scholar
• Yang Y, Li Y, Pan Q, et al. Tibial cortex transverse transport accelerates wound healing via enhanced angiogenesis and immunomodulation. Bone Jt Res. 2022;11(4):189–199. doi:10.1302/2046-3758.114.BJR-2021-0364.R1
   PubMed Web of Science ®Google Scholar
• Ou S, Wu X, Yang Y, et al. Tibial cortex transverse transport potentiates diabetic wound healing via activation of SDF-1/CXCR4 signaling. PeerJ. 2023:11:e15894. doi:10.7717/peerj.15894
   Web of Science ®Google Scholar
• Chen Y, Ding X, Zhu Y, et al. Effect of tibial cortex transverse transport in patients with recalcitrant diabetic foot ulcers: a prospective multicenter cohort study. J Orthop Transl. 2022;36:194–204.
   PubMed Web of Science ®Google Scholar
• Liu G, Li S, Kuang X, et al. The emerging role of tibial cortex transverse transport in the treatment of chronic limb ischemic diseases. J Orthop Transl. 2020;25:17–24.
   Web of Science ®Google Scholar
• Botusan IR, Sunkari VG, Savu O, et al. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci U S A. 2008;105(49):19426–19431. doi:10.1073/pnas.0805230105
   PubMed Web of Science ®Google Scholar
• Chen Z, Fu S, Wu Z, et al. Relationship between plasma angiogenic growth factors and diabetic foot ulcers. Clin Chim Acta Int J Clin Chem. 2018;482:95–100. doi:10.1016/j.cca.2018.03.035
   PubMed Web of Science ®Google Scholar
• M S, H Q, J Y, et al. Effect of negative-pressure wound therapy on the circulating number of peripheral endothelial progenitor cells in diabetic patients with mild to moderate degrees of ischaemic foot ulcer. Vascular. 2019;27(4). doi:10.1177/1708538119836360
   Web of Science ®Google Scholar
• Wieman TJ, Smiell JM, Su Y. Efficacy and safety of a topical gel formulation of recombinant human platelet-derived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers. A Phase III randomized placebo-controlled double-blind study. Diabetes Care. 1998;21(5):822–827. doi:10.2337/diacare.21.5.822
   PubMed Web of Science ®Google Scholar
• Li G, Ko CN, Li D, et al. A small molecule HIF-1α stabilizer that accelerates diabetic wound healing. Nat Commun. 2021;12(1):3363. doi:10.1038/s41467-021-23448-7
   PubMed Web of Science ®Google Scholar
• Zubair M, Ahmad J. Role of growth factors and cytokines in diabetic foot ulcer healing: a detailed review. Rev Endocr Metab Disord. 2019;20(2):207–217. doi:10.1007/s11154-019-09492-1
   PubMed Web of Science ®Google Scholar
• Saaristo A, Tammela T, Farkkilā A, et al. Vascular endothelial growth factor-C accelerates diabetic wound healing. Am J Pathol. 2006;169(3):1080–1087. doi:10.2353/ajpath.2006.051251
   PubMed Web of Science ®Google Scholar
• Patel S, Srivastava S, Singh MR, Singh D. Mechanistic insight into diabetic wounds: pathogenesis, molecular targets and treatment strategies to pace wound healing. Biomed Pharmacother Biomedecine Pharmacother. 2019;112:108615. doi:10.1016/j.biopha.2019.108615
   PubMed Web of Science ®Google Scholar
• Okonkwo UA, DiPietro LA. Diabetes and wound angiogenesis. Int J Mol Sci. 2017;18(7):1419. doi:10.3390/ijms18071419
   PubMed Web of Science ®Google Scholar
• Mori S, Akagi M, Kikuyama A, Yasuda Y, Hamanishi C. Axial shortening during distraction osteogenesis leads to enhanced bone formation in a rabbit model through the HIF-1alpha/vascular endothelial growth factor system. J Orthop Res off Publ Orthop Res Soc. 2006;24(4):653–663. doi:10.1002/jor.20076
   PubMed Web of Science ®Google Scholar
• Xu J, Sun Y, Wu T, et al. Enhancement of bone regeneration with the accordion technique via HIF-1α/VEGF activation in a rat distraction osteogenesis model. J Tissue Eng Regen Med. 2018;12(2):e1268–e1276. doi:10.1002/term.2534
   PubMed Web of Science ®Google Scholar
• Cao J, Wang L. A comparison of stromal cell-derived factor-1 expression during distraction osteogenesis and bone fracture in the mandible. J Craniofac Surg. 2013;24(3):805–808. doi:10.1097/SCS.0b013e31828f1ca7
   PubMed Web of Science ®Google Scholar
• Fujio M, Yamamoto A, Ando Y, et al. Stromal cell-derived factor-1 enhances distraction osteogenesis-mediated skeletal tissue regeneration through the recruitment of endothelial precursors. Bone. 2011;49(4):693–700. doi:10.1016/j.bone.2011.06.024
   PubMed Web of Science ®Google Scholar
• Weiss S, Zimmermann G, Baumgart R, Kasten P, Bidlingmaier M, Henle P. Systemic regulation of angiogenesis and matrix degradation in bone regeneration--distraction osteogenesis compared to rigid fracture healing. Bone. 2005;37(6):781–790. doi:10.1016/j.bone.2005.06.014
   PubMed Web of Science ®Google Scholar
• Shen Z, Chen Z, Li Z, et al. Total Flavonoids of rhizoma drynariae enhances angiogenic-osteogenic coupling during distraction osteogenesis by promoting type H vessel formation through PDGF-BB/PDGFR-β Instead of HIF-1α/ VEGF axis. Front Pharmacol. 2020;11:503524. doi:10.3389/fphar.2020.503524
   PubMed Web of Science ®Google Scholar
• Xu J, Chen Y, Liu Y, et al. Effect of SDF-1/Cxcr4 signaling antagonist AMD3100 on bone mineralization in distraction osteogenesis. Calcif Tissue Int. 2017;100(6):641–652. doi:10.1007/s00223-017-0249-4
   PubMed Web of Science ®Google Scholar
• Sanapalli BKR, Yele V, Singh MK, Thaggikuppe Krishnamurthy P, Karri VVSR. Preclinical models of diabetic wound healing: a critical review. Biomed Pharmacother Biomed Pharmacother. 2021;142:111946. doi:10.1016/j.biopha.2021.111946
   PubMed Web of Science ®Google Scholar
• Cheng KY, Lin ZH, Cheng YP, et al. Wound healing in streptozotocin-induced diabetic rats using atmospheric-pressure argon plasma jet. Sci Rep. 2018;8(1):12214. doi:10.1038/s41598-018-30597-1
   PubMedGoogle Scholar
• Guo SC, Tao SC, Yin WJ, Qi X, Yuan T, Zhang CQ. Exosomes derived from platelet-rich plasma promote the re-epithelization of chronic cutaneous wounds via activation of YAP in a diabetic rat model. Theranostics. 2017;7(1):81–96. doi:10.7150/thno.16803
   PubMed Web of Science ®Google Scholar
• Całkosiński I, Gostomska-Pampuch K, Majda J, et al. The influence of α-tocopherol on serum biochemical markers during experimentally induced pleuritis in rats exposed to dioxin. Inflammation. 2017;40(3):913–926. doi:10.1007/s10753-017-0536-2
   PubMed Web of Science ®Google Scholar
• Sun F, Lei Y, You J, et al. Adiponectin modulates ventral tegmental area dopamine neuron activity and anxiety-related behavior through AdipoR1. Mol Psychiatry. 2019;24(1):126–144. doi:10.1038/s41380-018-0102-9
   PubMed Web of Science ®Google Scholar
• Ricles LM, Hsieh PL, Dana N, et al. Therapeutic assessment of mesenchymal stem cells delivered within a PEGylated fibrin gel following an ischemic injury. Biomaterials. 2016;102:9–19. doi:10.1016/j.biomaterials.2016.06.011
   PubMed Web of Science ®Google Scholar
• Monteforte AJ, Lam B, Das S, et al. Glypican-1 nanoliposomes for potentiating growth factor activity in therapeutic angiogenesis. Biomaterials. 2016;94:45–56. doi:10.1016/j.biomaterials.2016.03.048
   PubMed Web of Science ®Google Scholar
• Nie X, Kuang X, Liu G, et al. Tibial cortex transverse transport facilitating healing in patients with recalcitrant non-diabetic leg ulcers. J Orthop Transl. 2021;27:1–7.
   PubMed Web of Science ®Google Scholar
• Chen Y, Huang YC, Yan CH, et al. Abnormal subchondral bone remodeling and its association with articular cartilage degradation in knees of type 2 diabetes patients. Bone Res. 2017;5:17034. doi:10.1038/boneres.2017.34
   PubMed Web of Science ®Google Scholar
• Chen Y, Hu Y, Yu YE, et al. Subchondral trabecular rod loss and plate thickening in the development of osteoarthritis. J Bone Miner Res off J Am Soc Bone Miner Res. 2018;33(2):316–327. doi:10.1002/jbmr.3313
   PubMed Web of Science ®Google Scholar
• Yuan Y, Ding X, Jing Z, et al. Modified tibial transverse transport technique for the treatment of ischemic diabetic foot ulcer in patients with type 2 diabetes. J Orthop Transl. 2021;29:100–105. doi:10.1016/j.jot.2021.04.006
   PubMed Web of Science ®Google Scholar
• Hua Q, Zhang Y, Wan C, et al. Chinese Association of Orthopaedic Surgeons (CAOS) clinical guideline for the treatment of diabetic foot ulcers using tibial cortex transverse transport technique (version 2020). J Orthop Transl. 2020;25:11–16. doi:10.1016/j.jot.2020.05.003
   Web of Science ®Google Scholar
• Shiha AE, Khalifa ARH, Assaghir YM, Kenawey MO. Medial transport of the fibula using the Ilizarov device for reconstruction of a massive defect of the tibia in two children. J Bone Joint Surg Br. 2008;90(12):1627–1630. doi:10.1302/0301-620X.90B12.21378
   PubMedGoogle Scholar
• Qu L, Wang A, Tang F. The therapy of transverse tibial bone transport and vessel regeneration operation on thromboangitis obliterans. Zhonghua Yi Xue Za Zhi. 2001;81(10):622–624.
   PubMedGoogle Scholar
• Li G, Simpson AH, Kenwright J, Triffitt JT. Effect of lengthening rate on angiogenesis during distraction osteogenesis. J Orthop Res off Publ Orthop Res Soc. 1999;17(3):362–367. doi:10.1002/jor.1100170310
   PubMed Web of Science ®Google Scholar
• Simpson AHRW, Keenan G, Nayagam S, Atkins RM, Marsh D, Clement ND. Low-intensity pulsed ultrasound does not influence bone healing by distraction osteogenesis: a multicentre double-blind randomised control trial. Bone Jt J. 2017;99(4):494–502. doi:10.1302/0301-620X.99B4.BJJ-2016-0559.R1
   PubMedGoogle Scholar
• Shen J, Sun Y, Liu X, et al. EGFL6 regulates angiogenesis and osteogenesis in distraction osteogenesis via Wnt/β-catenin signaling. Stem Cell Res Ther. 2021;12(1):415. doi:10.1186/s13287-021-02487-3
   PubMed Web of Science ®Google Scholar
• Yang Y, Andersson P, Hosaka K, et al. The PDGF-BB-SOX7 axis-modulated IL-33 in pericytes and stromal cells promotes metastasis through tumour-associated macrophages. Nat Commun. 2016;7:11385. doi:10.1038/ncomms11385
   PubMed Web of Science ®Google Scholar
• Kellerová E, Delius W, Olerud S, Ström G. Changes in the muscle and skin blood flow following lower leg fracture in man. Acta Orthop Scand. 1970;41(3):249–260. doi:10.3109/17453677008991512
   PubMed Web of Science ®Google Scholar
• Zimna A, Kurpisz M. Hypoxia-inducible factor-1 in physiological and pathophysiological angiogenesis: applications and therapies. BioMed Res Int. 2015;2015:549412. doi:10.1155/2015/549412
   PubMed Web of Science ®Google Scholar
• Fang J, Ji Q, Gao S, et al. PDGF-BB is involved in HIF-1α/CXCR4/CXCR7 axis promoting capillarization of hepatic sinusoidal endothelial cells. Heliyon. 2023;9(1):e12715. doi:10.1016/j.heliyon.2022.e12715
   PubMed Web of Science ®Google Scholar