Hyperbaric oxygen enhances collagen III formation in wound of ZDF rat
Jazyk angličtina Země Česko Médium print-electronic
Typ dokumentu hodnotící studie, časopisecké články
PubMed
34505531
PubMed Central
PMC8820531
DOI
10.33549/physiolres.934684
PII: 934684
Knihovny.cz E-zdroje
- MeSH
- diabetická noha metabolismus terapie MeSH
- hojení ran * MeSH
- hyperbarická oxygenace * MeSH
- kolagen typ III metabolismus MeSH
- krysa rodu Rattus MeSH
- náhodné rozdělení MeSH
- potkani Zucker MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- hodnotící studie MeSH
- Názvy látek
- kolagen typ III MeSH
Diabetic foot ulcer (DFU) is a serious complication of diabetes and hyperbaric oxygen therapy (HBOT) is also considered in comprehensive treatment. The evidence supporting the use of HBOT in DFU treatment is controversial. The aim of this work was to introduce a DFU model in ZDF rat by creating a wound on the back of an animal and to investigate the effect of HBOT on the defect by macroscopic evaluation, quantitative histological evaluation of collagen (types I and III), evaluation of angiogenesis and determination of interleukin 6 (IL6) levels in the plasma. The study included 10 rats in the control group (CONT) and 10 in the HBOT group, who underwent HBOT in standard clinical regimen. Histological evaluation was performed on the 18th day after induction of defect. The results show that HBOT did not affect the macroscopic size of the defect nor IL6 plasma levels. A volume fraction of type I collagen was slightly increased by HBOT without reaching statistical significance (1.35+/-0.49 and 1.94+/-0.67 %, CONT and HBOT, respectively). In contrast, the collagen type III volume fraction was ~120 % higher in HBOT wounds (1.41+/-0.81 %) than in CONT ones (0.63+/-0.37 %; p=0.046). In addition, the ratio of the volume fraction of both collagens in the wound ((I+III)w) to the volume fraction of both collagens in the adjacent healthy skin ((I+III)h) was ~65 % higher in rats subjected to HBOT (8.9+/-3.07 vs. 5.38+/-1.86 %, HBOT and CONT, respectively; p=0.028). Vessels density (number per 1 mm2) was found to be higher in CONT vs. HBOT (206.5+/-41.8 and 124+/-28.2, respectively, p<0.001). Our study suggests that HBOT promotes collagen III formation and decreases the number of newly formed vessels at the early phases of healing.
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ANDRÉ-LÉVIGNE D, MODARRESSI A, PIGNEL R, BOCHATON-PIALLAT ML, PITTET-CUÉNOD B. Hyperbaric oxygen therapy promotes wound repair in ischemic and hyperglycemic conditions, increasing tissue perfusion and collagen deposition. Wound Repair Regen. 2016;24:954–965. doi: 10.1111/wrr.12480. PubMed DOI
APELQVIST J. The foot in perspective. Diabetes Metab Res Rev. 2008;24(Suppl 1):110–115. doi: 10.1002/dmrr.834. PubMed DOI
AYDIN F, KAYA A, KARAPINAR L, KUMBARACI M, IMERCI A, KARAPINAR H, KARAKUZU C, INCESU M. IGF-1 increases with hyperbaric oxygen therapy and promotes wound healing in diabetic foot ulcers. J Diabetes Res. 2013;2013:567834. doi: 10.1155/2013/567834. PubMed DOI PMC
BROUWER RJ, LALIEU RC, HOENCAMP R, Van HULST RA, UBBINK DT. A systematic review and meta-analysis of hyperbaric oxygen therapy for diabetic foot ulcers with arterial insufficiency. J Vasc Surg. 2020;71:682–692. doi: 10.1016/j.jvs.2019.07.082. PubMed DOI
BUCKLEY CJ, COOPER JS. StatPearls [Internet] Treasure Island (FL): StatPearls Publishing; 2021. Hyperbaric affects on angiogenesis. https://www.ncbi.nlm.nih.gov/books/NBK482485/ PubMed
BURNHAM KP, ANDERSON DR. Model Selection and Inference. Springer; New York: 1998. p. 355. DOI
BUZGO M, PLENCNER M, RAMPICHOVA M, LITVINEC A, PROSECKA E, STAFFA A, KRALOVIC M, FILOVA E, DOUPNIK M, LUKASOVA V, VOCETKOVA K, ANDEROVA J, KUBIKOVA T, ZAJICEK R, LOPOT F, JELEN K, TONAR Z, AMLER E, DIVIN R, FIORI F. Poly-e-caprolactone and polyvinyl alcohol electrospun wound dressings: adhesion properties and wound management of skin defects in rabbits. Regen Med. 2019;14:423–445. doi: 10.2217/rme-2018-0072. PubMed DOI
CAMPELO MBD, SANTOS JAF, FILHO ALM, FERREIRA DCL, SANT’ANNA LB, OLIVEIRA RA, MAIA LF, ARISAWA EÂL. Effects of the application of the amniotic membrane in the healing process of skin wounds in rats. Acta Cir Bras. 2018;33:144–155. doi: 10.1590/s0102-865020180020000006. PubMed DOI
CHENG C, SINGH V, KRISHNAN A, KAN M, MARTINEZ JA, ZOCHODNE DW. Loss of innervation and axon plasticity accompanies impaired diabetic wound healing. PLoS One. 2013;8:e75877. doi: 10.1371/journal.pone.0075877. PubMed DOI PMC
CLORE JN, COHEN IK, DIEGELMANN RF. Quantitation of collagen types I and III during wound healing in rat skin. Proc Soc Exp Biol Med. 1979;161:337–340. doi: 10.3181/00379727-161-40548. PubMed DOI
DALE PD, SHERRATT JA, MAINI PK. A mathematical model for collagen fibre formation during foetal and adult dermal wound healing. Proc Biol Sci. 1996;263:653–660. doi: 10.1098/rspb.1996.0098. PubMed DOI
DIPIETRO LA. Angiogenesis and wound repair: when enough is enough. J Leukoc Biol. 2016;100:979–984. doi: 10.1189/jlb.4MR0316-102R. PubMed DOI PMC
DREIFKE MB, JAYASURIYA AA, JAYASURIYA AC. Current wound healing procedures and potential care. Mater Sci Eng C Materl Biol Appl. 2015;48:651–662. doi: 10.1016/j.msec.2014.12.068. PubMed DOI PMC
EAST B, PLENCNER M, KRALOVIC M, RAMPICHOVA M, SOVKOVA V, VOCETKOVA K, OTAHAL M, TONAR Z, KOLINKO Y, AMLER E, HOCH J. A polypropylene mesh modified with poly-ε-caprolactone nanofibers in hernia repair: large animal experiment. Int J Nanomedicine. 2018;13:3129–3143. doi: 10.2147/IJN.S159480. PubMed DOI PMC
ELRAIYAH T, TSAPAS A, PRUTSKY G, DOMECQ JP, HASAN R, FIRWANA B, NABHAN M, PROKOP L, HINGORANI A, CLAUS PL, STEINKRAUS LW, MURAD MH. A systematic review and meta-analysis of adjunctive therapies in diabetic foot ulcers. J Vasc Surg. 2016;63:46S–58S.e1–2. doi: 10.1016/j.jvs.2015.10.007. PubMed DOI
FLEISCHMAJER R, PERLISH JS, BURGESON RE, SHAIKH-BAHAI F, TIMPL R. Type I and type III collagen interactions during fibrillogenesis. Ann N Y Acad Sci. 1990;580:161–175. doi: 10.1111/j.1749-6632.1990.tb17927.x. PubMed DOI
GOOD PI. Permutation, Parametric and Bootstrap Tests of Hypotheses. Springer; New York: 2005. p. 316. DOI
GUNDERSEN HJG. Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc. 1977;111:219–223. doi: 10.1111/j.1365-2818.1977.tb00062.x. DOI
GUO S, DIPIETRO LA. Factors affecting wound healing. J Dent Res. 2010;89:219–229. doi: 10.1177/0022034509359125. PubMed DOI PMC
HOBIZAL KB, WUKICH DK. Diabetic foot infections: current concept review. Diabetic Foot Ankle. 2012;3:18409. doi: 10.3402/dfa.v3i0.18409. PubMed DOI PMC
HORAKOVA J, MIKES P, LUKAS D, SAMAN A, JENCOVA V, KLAPSTOVA A, SVARCOVA T, ACKERMANN M, NOVOTNY V, KALAB M, LONSKY V, BARTOS M, RAMPICHOVA M, LITVINEC A, KUBIKOVA T, TOMASEK P, TONAR Z. Electrospun vascular grafts fabricated from poly(L-lactide-co-ε-caprolactone) used as a bypass for the rabbit carotid artery. Biomed Mater. 2018;13:065009. doi: 10.1088/1748-605X/aade9d. PubMed DOI
HUANG X, LIANG P, JIANG B, ZHANG P, YU W, DUAN M, GUO L, CUI X, HUANG M, HUANG X. Hyperbaric oxygen potentiates diabetic wound healing by promoting fibroblast cell proliferation and endothelial cell angiogenesis. Life Sci. 2020;259:118246. doi: 10.1016/j.lfs.2020.118246. PubMed DOI
HUANG X, LIANG P, JIANG B, ZHANG P, YU W, DUAN M, GUO L, CUI X, HUANG M, HUANG X. Hyperbaric oxygen potentiates diabetic wound healing by promoting fibroblast cell proliferation and endothelial cell angiogenesis. Life Sci. 2020;259:118246. doi: 10.1016/j.lfs.2020.118246. PubMed DOI
JIRKOVSKÁ A. Adherence to the international guidelines on the treatment of diabetic leg syndrome. Vnitr Lek. 2011;57:908–912. PubMed
JUNQUEIRA LCU, BIGNOLAS G, BRENTANI RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J. 1979;11:447–455. doi: 10.1007/BF01002772. PubMed DOI
JUNQUEIRA LCU, MONTES GS, SANCHEZ EM. The influence of tissue section thickness on the study of collagen by the Picrosirius-polarization method. Histochemistry. 1982;74:153–156. doi: 10.1007/BF00495061. PubMed DOI
KATSUDA Y, OHTA T, MIYAJIMA K, KEMMOCHI Y, SASASE T, TONG B, SHINOHARA M, YAMADA T. Diabetic complications in obese type 2 diabetic rat models. Exp Anim. 2014;63:121–132. doi: 10.1538/expanim.63.121. PubMed DOI PMC
KLINGE U, SI Z, ZHENG H, SCHUMPELICK V, BHARDWAJ S, KLOSTERHALFEN B. Abnormal collagen I to III distribution in the skin of patients with incisional hernia. Eur Surg Res. 2000;32:43–48. doi: 10.1159/000008740. PubMed DOI
KRANKE P, BENNETT MH, MARTYN-ST JAMES M, SCHNABEL A, DEBUS SE, WEIBEL S. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev. 2015;2015:CD004123. doi: 10.1002/14651858.CD004123.pub4. PubMed DOI PMC
KUMAR A, SHUKLA U, PRABHAKAR T, SRIVASTAVA D. Hyperbaric oxygen therapy as an adjuvant to standard therapy in the treatment of diabetic foot ulcers. J Anaesthesiol Clin Pharmacol. 2020;36:213–218. doi: 10.4103/joacp.JOACP_94_19. PubMed DOI PMC
LIPSKY BA, SENNEVILLE É, ABBAS ZG, ARAGÓN-SÁNCHEZ J, DIGGLE M, EMBIL JM, KONO S, LAVERY LA, MALONE M, Van ASTEN SA, URBANČIČ-ROVAN V, PETERS EJG International Working Group on the Diabetic Foot (IWGDF) Guidelines on the diagnosis and treatment of foot infection in persons with diabetes (IWGDF 2019 update) Diabetes Metab Res Rev. 2020;36(Suppl 1):e3280. doi: 10.1002/dmrr.3280. PubMed DOI
MARGOLIS DJ, GUPTA J, HOFFSTAD O, PAPDOPOULOS M, GLICK HA, THOM SR, MITRA N. Lack of effectiveness of hyperbaric oxygen therapy for the treatment of diabetic foot ulcer and the prevention of amputation: a cohort study. Diabetes Care. 2013;36:1961–1966. doi: 10.2337/dc12-2160. PubMed DOI PMC
MOHAMMADZADEH E, NIKRAVESH MR, JALALI M, FAZEL A, EBRAHIMI V, EBRAHIMZADEH-BIDESKAN AR. Immunohistochemical study of type III collagen expression during pre and post-natal rat skin morphogenesis. Iran J Basic Med Sci. 2014;17:196–200. PubMed PMC
OTTO KJ, WYSE BD, CABOT PJ, SMITH MT. Longitudinal study of painful diabetic neuropathy in the Zucker diabetic fatty rat model of type 2 diabetes: impaired basal G-protein activity appears to underpin marked morphine hyposensitivity at 6 months. Pain Med. 2011;12:437–450. doi: 10.1111/j.1526-4637.2011.01067.x. PubMed DOI
PACKER CF, ALI SA, MANNA B. Diabetic ulcer. StatPearls, Treasure Island (FL): StatPearls Publishing; 2021. PubMed
PEÑA-VILLALOBOS I, CASANOVA-MALDONADO I, LOIS P, PRIETO C, PIZARRO C, LATTUS J, OSORIO G, PALMA V. Hyperbaric oxygen increases stem cell proliferation, angiogenesis and wound-healing ability of WJ-MSCs in diabetic mice. Front Physiol. 2018;9:995. doi: 10.3389/fphys.2018.00995. PubMed DOI PMC
PINHEIRO J, BATES D, DEBROY S, SARKAR D R CORE TEAM. nlme: Linear and nonlinear mixed effects models. 2018. [Accessed September 24, 2018]. https://cran.r-project.org/web/packages/nlme/citation.html .
R Development Core Team. R: A Language and Environment for Statistical Computing. 2020. https://www.r-project.org/
RAYMAN G, VAS P, DHATARIYA K, DRIVER V, HARTEMANN A, LONDAHL M, PIAGGESI A, APELQVIST J, ATTINGER C, GAME F International Working Group on the Diabetic Foot (IWGDF) Guidelines on use of interventions to enhance healing of chronic foot ulcers in diabetes (IWGDF 2019 update) Diabetes Metab Res Rev. 2020;36:e3283. doi: 10.1002/dmrr.3283. PubMed DOI
RICH L, WHITTAKER P. Collagen and picrosirius red staining: A polarized light assessment of fibrillar hue and spatial distribution. J Morphol Sci. 2005;22:97–104.
SCHNEIDER CA, RASBAND WS, ELICEIRI KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC
SIWY J, ZOJA C, KLEIN J, BENIGNI A, MULLEN W, MAYER B, MISCHAK H, JANKOWSKI J, STEVENS R, VLAHOU A, KOSSIDA S, PERCO P, BAHLMANN FH. Evaluation of the Zucker diabetic fatty (ZDF) rat as a model for human disease based on urinary peptidomic profiles. PLoS One. 2012;7:e51334. doi: 10.1371/journal.pone.0051334. PubMed DOI PMC
SLAVKOVSKY R, KOHLEROVA R, TKACOVA V, JIROUTOVA A, TAHMAZOGLU B, VELEBNY V, REZAČOVÁ M, SOBOTKA L, KANTA J. Zucker diabetic fatty rat: a new model of impaired cutaneous wound repair with type II diabetes mellitus and obesity. Wound Repair Regen. 2011;19:515–525. doi: 10.1111/j.1524-475X.2011.00703.x. PubMed DOI
TEGUH DN, BOL RAAP R, KOOLE A, KNIPPENBERG B, SMIT C, OOMEN J, Van HULST RA. Hyperbaric oxygen therapy for nonhealing wounds: Treatment results of a single center. Wound Repair Regen. 2020;2020:1–7. doi: 10.1111/wrr.12884. PubMed DOI PMC
THIRUVOTH FM, MOHAPATRA DP, KUMAR D, CHITTORIA RK, NANDHAGOPAL V. Current concepts in the physiology of adult wound healing. Plast Aesthet Res. 2015;2015:250–256. doi: 10.4103/2347-9264.158851. DOI
TONAR Z, KUBÍKOVÁ T, PRIOR C, DEMJÉN E, LIŠKA V, KRÁLÍČKOVÁ M, WITTER K. Segmental and age differences in the elastin network, collagen, and smooth muscle phenotype in the tunica media of the porcine aorta. Ann Anat. 2015;201:79–90. doi: 10.1016/j.aanat.2015.05.005. PubMed DOI
TONAR Z, EGGER GF, WITTER K, WOLFESBERGER B. Quantification of microvessels in canine lymph nodes. Microsc Res Tech. 2008;71:760–772. doi: 10.1002/jemt.20619. PubMed DOI
TUK B, TONG M, FIJNEMAN EMG, Van NECK JW. Hyperbaric oxygen therapy to treat diabetes impaired wound healing in rats. PLoS One. 2014;9:e108533. doi: 10.1371/journal.pone.0108533. PubMed DOI PMC
Van NECK JW, TUK B, FIJNEMAN EMG, REDEKER JJ, TALAHATU EM, TONG M. Hyperbaric oxygen therapy for wound healing in diabetic rats: Varying efficacy after a clinically-based protocol. PLoS One. 2017;12:e0177766. doi: 10.1371/journal.pone.0177766. PubMed DOI PMC
VELNAR T, BAILEY T, SMRKOLJ V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res. 2009;37:1528–1542. doi: 10.1177/147323000903700531. PubMed DOI
VINIK AI, MASER RE, MITCHELL BD, FREEMAN R. Diabetic autonomic neuropathy. Diabetes Care. 2003;26:1553–1579. doi: 10.2337/diacare.26.5.1553. PubMed DOI
WANG T, GU Q, ZHAO J, MEI J, SHAO M, PAN Y, ZHANG J, WU H, ZHANG Z, LIU F. Calcium alginate enhances wound healing by up-regulating the ratio of collagen types I/III in diabetic rats. Int J Clin Exp Pathol. 2015;8:6636–6645. PubMed PMC
WANG Z, WANG Q, WANG L, XU W, HE Y, LI Y, HE S, MA H. Improvement of skin condition by oral administration of collagen hydrolysates in chronologically aged mice. J Sci Food Agric. 2017;97:2721–2726. doi: 10.1002/jsfa.8098. PubMed DOI
WANICZEK D, KOZOWICZ A, MUC-WIERZGOŃ M, KOKOT T, SWIĘTOCHOWSKA E, NOWAKOWSKA-ZAJDEL E. Adjunct methods of the standard diabetic foot ulceration therapy. Evid Based Complement. doi: 10.1155/2013/243568. PubMed DOI PMC
WITTER K, TONAR Z, MATEJKA VM, MARTINCA T, JONÁK M, ROKOSNÝ S, PIRK J. Tissue reaction to three different types of tissue glues in an experimental aorta dissection model: a quantitative approach. Histochem Cell Biol. 2010;133:241–259. doi: 10.1007/s00418-009-0656-3. PubMed DOI
WOOD SN. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Royal Stat Soc Stat Methodol. 2011;73:3–36. doi: 10.1111/j.1467-9868.2010.00749.x. DOI
WU Q. Hyperbaric oxygen for treatment of diabetic foot ulcers: love you more than I can say. Ann Transl Med. 2018;6:228. doi: 10.21037/atm.2018.04.33. PubMed DOI PMC
WYNN TA. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008;214:199–210. doi: 10.1002/path.2277. PubMed DOI PMC
YAMAMOTO N, OYAIZU T, ENOMOTO M, HORIE M, YUASA M, OKAWA A, YAGISHITA K. VEGF and bFGF induction by nitric oxide is associated with hyperbaric oxygen-induced angiogenesis and muscle regeneration. Sci Rep. 2020;10:2744. doi: 10.1038/s41598-020-59615-x. PubMed DOI PMC
YOUNG A, McNAUGHT CE. The physiology of wound healing. Surgery. 2011;29:475–479. doi: 10.1016/j.mpsur.2011.06.011. DOI
YU M, YUAN HS, LI Q, LI Q, TENG YF. Combination of cells-based therapy with apelin-13 and hyperbaric oxygen efficiently promote neovascularization in ischemic animal model. Eur Rev Med Pharmacol Sci. 2019;23:2630–2639. doi: 10.26355/eurrev_201903_17413. PubMed DOI