Effect of Polymeric Nanoparticles with Entrapped Fish Oil or Mupirocin on Skin Wound Healing Using a Porcine Model

. 2022 Jul 11 ; 23 (14) : . [epub] 20220711

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35887016

The utilization of poly(lactic-co-glycolic) acid (PLGA) nanoparticles (NPs) with entrapped fish oil (FO) loaded in collagen-based scaffolds for cutaneous wound healing using a porcine model is unique for the present study. Full-depth cutaneous excisions (5 × 5 cm) on the pig dorsa were treated with pure collagen scaffold (control, C), empty PLGA NPs (NP), FO, mupirocin (MUP), PLGA NPs with entrapped FO (NP/FO) and PLGA NPs with entrapped MUP (NP/MUP). The following markers were evaluated on days 0, 3, 7, 14 and 21 post-excision: collagen, hydroxyproline (HP), angiogenesis and expressions of the COX2, EGF, COL1A1, COL1A3, TGFB1, VEGFA, CCL5 and CCR5 genes. The hypothesis that NP/FO treatment is superior to FO alone and that it is comparable to NP/MUP was tested. NP/FO treatment increased HP in comparison with both FO alone and NP/MUP (day 14) but decreased (p < 0.05) angiogenesis in comparison with FO alone (day 3). NP/FO increased (p < 0.05) the expression of the CCR5 gene (day 3) and tended (p > 0.05) to increase the expressions of the EGF (day 7, day 14), TGFB1 (day 21) and CCL5 (day 7, day 21) genes as compared with NP/MUP. NP/FO can be suggested as a suitable alternative to NP/MUP in cutaneous wound treatment.

Zobrazit více v PubMed

Gercek A., Yildirim O., Konya D., Bozkurt S., Ozgen S., Kilic T. Effects of parenteral fish-oil emulsion (Omegaven) on cutaneous wound healing in rats treated with dexamethasone. J. Parenter. Enter. Nutr. 2007;31:161–166. doi: 10.1177/0148607107031003161. PubMed DOI

Caetano G.F., Fronza M., Leite M.N., Gomes A., Cipriani Frade M.A. Comparison of collagen content in skin wounds evaluated by biochemical assay and by computer-aided histomorphometric analysis. Pharm. Biol. 2016;54:2555–2559. doi: 10.3109/13880209.2016.1170861. PubMed DOI

Nascimento A.P., Costa A.M. Overweight induced by high-fat diet delays rat cutaneous wound healing. Br. J. Nutr. 2006;96:1069–1077. doi: 10.1017/BJN20061955. PubMed DOI

Zhou J., Zhao Y., Simonenko V., Xu J.J., Liu K., Wang D., Shi J., Zhong T., Zhang L., Zeng J., et al. Simultaneous silencing of TGF-ß1 and COX-2 reduces human skin hypertrophic scar through activation of fibroblast apoptosis. Oncotarget. 2017;8:80651–80665. doi: 10.18632/oncotarget.20869. PubMed DOI PMC

Ramanathan G., Muthukumar T., Sivagnanan U.T. In vivo efficiency of the collagen nanofibrous scaffold and their effect on growth factors and pro-inflammatory cytokines in wound healing. Eur. J. Pharmacol. 2017;814:44–45. doi: 10.1016/j.ejphar.2017.08.003. PubMed DOI

Pastor-Clerigues A., Marti-Bonmati E., Milara J., Almudever P., Cortijo J. Anti-inflammatory and anti-fibrotic profile of fish oil emulsions used in parenteral nutrition-associated liver disease. PLoS ONE. 2014;9:e115404. doi: 10.1371/journal.pone.0115404. PubMed DOI PMC

Ridiandries A., Bursill C., Tan J. Broad-spectrum inhibition of the CC-chemokine class improves wound healing and wound angiogenesis. Int. J. Mol. Sci. 2017;18:155. doi: 10.3390/ijms18010155. PubMed DOI PMC

Ishida Y., Kimura A., Kuninaka Y., Inui M., Matsushima K., Mukaida N., Kondo T. Pivotal role of the CCL5/CCR5 interaction for recruitment of endothelial progenitor cells in mouse wound healing. J. Clin. Investig. 2012;122:711–721. doi: 10.1172/JCI43027. PubMed DOI PMC

Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature. 2008;453:314–321. doi: 10.1038/nature07039. PubMed DOI

Vojtová L., Pavliňáková V., Muchová J., Kacvinská K., Brtníková J., Knoz M., Lipový B., Faldyna M., Göpfert E., Holoubek J., et al. Healing and Angiogenic Properties of Collagen/Chitosan Scaffolds Enriched with Hyperstable FGF2-STAB® Protein: In Vitro, Ex Ovo and In Vivo Comprehensive Evaluation. Biomedicines. 2021;9:590. doi: 10.3390/biomedicines9060590. PubMed DOI PMC

Pensalfini M., Haertel E., Hopf R., Wietecha M., Werner S., Mazza E. The mechanical fingerprint of murine excisional wounds. Acta Biomater. 2018;65:226–236. doi: 10.1016/j.actbio.2017.10.021. PubMed DOI

Seaton M., Hocking A., Gibran N.S. Porcine models of cutaneous wound healing. ILAR J. 2015;56:127–138. doi: 10.1093/ilar/ilv016. PubMed DOI

Chereddy K.K., Vandermeulen G., Préat V. PLGA based drug delivery systems: Promising carriers for wound healing activity. Wound Repair Regen. 2016;24:223–236. doi: 10.1111/wrr.12404. PubMed DOI

Berthet M., Gauthier Y., Lacroix C., Verrier B., Monge C. Nanoparticle-based dressing: The future of wound treatment? Trends Biotechnol. 2017;35:770–784. doi: 10.1016/j.tibtech.2017.05.005. PubMed DOI

Kemme M., Heinzel-Wieland R. Quantitative assessment of antimicrobial activity of PLGA films loaded with 4-hexylresorcinol. J. Funct. Biomater. 2018;9:4. doi: 10.3390/jfb9010004. PubMed DOI PMC

Sritharadol R., Nakpheng T., Heng P.W.S., Srichana T. Development of a topical mupirocin spray for antibacterial and wound-healing applications. Drug Dev. Ind. Pharm. 2017;43:1715–1728. doi: 10.1080/03639045.2017.1339077. PubMed DOI

Budhiraja M., Zafar S., Akhter S., Alrobaian M., Rashid M.A., Barkat M.A., Beg S., Ahmad F.J. Mupirocin-loaded chitosan microspheres embedded in Piper betle extract containing collagen scaffold accelerate wound healing activity. AAPS Pharm. Sci. Tech. 2022;23:77. doi: 10.1208/s12249-022-02233-9. PubMed DOI

Solak E.K., Kaya S., Asman G. Preparation, characterization, and antibacterial properties of biocompatible material for wound healing. J. Macromol. Sci. A Pure Appl. Chem. 2021;58:709–716. doi: 10.1080/10601325.2021.1929315. DOI

Giustina A.D., de Souza Goldim M.P., Gainski Danielski L., Garbossa L., Oliveira Junior A.N., Cidreira T., Denico T., Bonfante S., da Rosa N., Fortunato J.J., et al. Lipoic acid and fish oil combination potentiates neuroinflammation and oxidative stress regulation and prevents cognitive decline of rats after sepsis. Mol. Neurobiol. 2020;57:4451–4466. doi: 10.1007/s12035-020-02032-y. PubMed DOI

Rakotoarisoa M., Angelov B., Garamus V.M., Angelova A. Curcumin- and fish oil-loaded spongosome and cubosome nanoparticles with neuroprotective potential against H2O2-induced oxidative stress in differentiated human SH-SY5Y cells. ACS Omega. 2019;4:3061–3073. doi: 10.1021/acsomega.8b03101. DOI

Komprda T. Effect of n-3 long-chain polyunsaturated fatty acids on wound healing using animal models—A review. Acta Vet. Brno. 2018;87:309–320. doi: 10.2754/avb201887040309. DOI

Schmitz G., Ecker J. The opposing effects of n-3 and n-6 fatty acids. Prog. Lipid Res. 2008;47:147–155. doi: 10.1016/j.plipres.2007.12.004. PubMed DOI

Komprda T. Eicosapentaenoic and docosahexaenoic acids as inflammation-modulating and lipid homeostasis influencing nutraceuticals: A review. J. Funct. Foods. 2012;4:25–38. doi: 10.1016/j.jff.2011.10.008. DOI

Chereddy K.K., Coco R., Memvanga P.B., Ucakar B., Rieux A., Vandermeulen G., Préat V. Combined effect of PLGA and curcumin on wound healing activity. J. Control. Release. 2013;171:208–215. doi: 10.1016/j.jconrel.2013.07.015. PubMed DOI

Liu S.-J., Kau Y.-C., Chou C.-Y., Chen J.-K., Wu R.-C., Yeh W.-L. Electrospun PLGA/collagen nanofibrous membrane as early-stage wound dressing. J. Membr. Sci. 2010;355:53–59. doi: 10.1016/j.memsci.2010.03.012. DOI

Candreva T., Kühl C.M.C., Burger B., dos Anjos M.B.P., Torsoni M.A., Consonni S.R., Crisma A.R., Fisk H.L., Calder P.C., de Mato F.C.P., et al. Docosahexaenoic acid slows inflammation resolution and impairs the quality of healed skin tissue. Clin. Sci. 2019;133:2345–2360. doi: 10.1042/CS20190753. PubMed DOI

Cardoso C.R., Favoreto S., Oliveira L.L., Vancim J.O., Barban G.B., Ferraz D.B., Silva J.S. Oleic acid modulation of the immune response in wound healing: A new approach for skin repair. Immunobiology. 2011;216:409–415. doi: 10.1016/j.imbio.2010.06.007. PubMed DOI

Bradberry J.C., Hilleman D.E. Overview of omega-3 fatty acid therapies. Pharm. Ther. 2013;38:681–691. PubMed PMC

Turk H.F., Monk J.M., Fan Y.Y., Callaway E.S., Weeks B., Chapkin R.S. Inhibitory effects of omega-3 fatty acids on injury-induced epidermal growth factor receptor transactivation contribute to delayed wound healing. Am. J. Physiol. Cell Physiol. 2013;304:C905–C917. doi: 10.1152/ajpcell.00379.2012. PubMed DOI PMC

McDaniel J.C., Belury M., Ahijevych K., Blakely W. Omega-3 fatty acids effects on wound healing. Wound Repair Regen. 2008;16:337–345. doi: 10.1111/j.1524-475X.2008.00388.x. PubMed DOI PMC

Arantes E.L., Dragano N., Ramalho A., Vitorino D., de Souza G.F., Lima M.H.M., Velloso L.A., Araúcho E.P. Topical docosahexaenoic acid accelerates skin wound healing in rats and activates GPR120. Biol. Res. Nurs. 2016;18:411–419. doi: 10.1177/1099800415621617. PubMed DOI

Kadler K.E., Holmes D.F., Trotter J.A., Chapman J.A. Collagen fibril formation. Biochem. J. 1996;316:1–11. doi: 10.1042/bj3160001. PubMed DOI PMC

Wolfram D., Tzankov A., Pülzl P., Piza-Katzer H. Hypertrophic scars and keloids a review of their pathophysiology, risk factors, and therapeutic management. Dermatol. Surg. 2009;35:171–181. doi: 10.1111/j.1524-4725.2008.34406.x. PubMed DOI

Hayakawa T., Hashimoto Y., Myokei Y., Aoyama H., Izawa Y. Changes in type of collagen during the development of human post-burn hypertrophic scars. Clin. Chim. Acta. 1979;93:119–125. doi: 10.1016/0009-8981(79)90252-3. PubMed DOI

Wang J.F., Olson M.E., Reno C.R., Kulyk W., Wright J.B., Hart D.A. Molecular and cell biology of skin wound healing in a pig model. Connect. Tissue Res. 2000;41:195–211. doi: 10.3109/03008200009005290. PubMed DOI

Kawai K., Larson B.J., Ishise H., Carre A.L., Nishimoto S., Longaker M., Lorenz H.P. Calcium-Based Nanoparticles Accelerate Skin Wound Healing. PLoS ONE. 2021;6:e27106. doi: 10.1371/journal.pone.0027106. PubMed DOI PMC

Kwan K.H.L., Liu X., To M.K.T., Yeung K.W.K., Ho C.H., Wong K.K.Y. Modulation of collagen alignment by silver nanoparticles results in better mechanical properties in wound healing. Nanomedicine. 2011;7:497–504. doi: 10.1016/j.nano.2011.01.003. PubMed DOI

Tanideh N., Abdordide E., Yousefabad S.L.A., Daneshi S., Hosseinabadi O.K., Samani S.M. A comparison of the effects of honey, fish oil and their combination on wound healing in rat. J. Coast. Life Med. 2016;4:683–688.

Rittié L. Cellular mechanisms of skin repair in humans and other mammals. J. Cell Commun. Signal. 2016;10:103–120. doi: 10.1007/s12079-016-0330-1. PubMed DOI PMC

Turgeon J., Dussault S., Maingrette F., Groleau J., Haddad P., Perez G., Rivard A. Fish oil-enriched diet protects against ischemia by improving angiogenesis, endothelial progenitor cell function and postnatal neovascularization. Atherosclerosis. 2013;229:295–303. doi: 10.1016/j.atherosclerosis.2013.05.020. PubMed DOI

Ali M., Radad K. Cod liver oil/honey mixture: An effective treatment of equine complicated lower leg wounds. Vet. World. 2011;4:304–310.

Shingel K.I., Faure M.P., Azoulay L., Roberge C., Deckelbaum R.J. Solid emulsion gel as a vehicle for delivery ofpolyunsaturated fatty acids: Implications for tissuerepair, dermal angiogenesis and wound healing. J. Tissue Eng. Regen. Med. 2008;2:383–393. doi: 10.1002/term.101. PubMed DOI

Okur N.Ü., Hökenek N., Okur M.H., Ayla S., Yoltaş A., Siafaka P.I., Cevherg E. An alternative approach to wound healing field; new composite films from natural polymers for mupirocin dermal delivery. Saudi Pharm. J. 2019;27:738–752. doi: 10.1016/j.jsps.2019.04.010. PubMed DOI PMC

Farahpoura M.R., Pirkhezrb E., Ashrafianc A., Sonboli A. Accelerated healing by topical administration of Salvia officinalis essentialoil on Pseudomonas aeruginosa and Staphylococcus aureus infected wound model. Biomed. Pharmacother. 2020;128:110–120. PubMed

Khezri K., Farahpour M.R., Rad S.M. Accelerated infected wound healing by topical application of encapsulated Rosemary essential oil into nanostructured lipid carriers. Artif. Cells Nanomed. Biotechnol. 2019;47:980–988. doi: 10.1080/21691401.2019.1582539. PubMed DOI

Golmohammadi R., Najar-Peerayeh S., Moghadam T.T., Hosseini S.M.J. Synergistic antibacterial activity and wound healing properties of selenium-chitosan-mupirocin nanohybrid System: An in vivo study on rat diabetic Staphylococcus aureus wound infection model. Sci. Rep. 2020;10:2854. doi: 10.1038/s41598-020-59510-5. PubMed DOI PMC

Porporato P., Payen V., Saedeleer C., Préat V., -Thissen P.J., Feron O. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012;15:581–592. doi: 10.1007/s10456-012-9282-0. PubMed DOI

Barui A.K., Nethi S.K., Haque S., Basuthakur P., Patra C.H.R. Recent Development of metal nanoparticles for angiogenesis study and their therapeutic applications. ACS Appl. Bio Mater. 2019;2:5492–5511. doi: 10.1021/acsabm.9b00587. PubMed DOI

Kargozar S., Baino F., Hamzehlou S., Hamblin M.R., Mozafari M. Nanotechnology for angiogenesis: Opportunities and challenges. Chem. Soc. Rev. 2020;49:5008–5057. doi: 10.1039/C8CS01021H. PubMed DOI PMC

Bluff J.E., O'Ceallaigh S., O'Kane S., Ferguson M.W., Ireland G. The microcirculation in acute murine cutaneous incisional wounds shows a spatial and temporal variation in the functionality of vessels. Wound Repair Regen. 2006;14:434–442. doi: 10.1111/j.1743-6109.2006.00142.x. PubMed DOI

Pan S.-C., Li C.-Y., Kuo C.-Y., Kuo Y.-Z., Fang W.-Y., Huang Y.-H., Hsieh T.-C., Kao H.-Y., Kuo Y., Kang Y.-R., et al. The p53-S100A2 positive feedback loop negatively regulates epithelialization in cutaneous wound healing. Sci. Rep. 2018;8:5458. doi: 10.1038/s41598-018-23697-5. PubMed DOI PMC

Hardwicke J., Schmaljohann D., Boyce D., Thomas D. Epidermal growth factor therapy and wound healing–past, present and future perspectives. Surgeon. 2008;6:172–177. doi: 10.1016/S1479-666X(08)80114-X. PubMed DOI

Cheng W., Xu R., Li D., Bortolini C., He J., Dong M., Besenbacher F., Huang Y., Chen M. Artificial extracellular matrix delivers TGFb1 regulating myofibroblast differentiation. RSC Adv. 2016;6:21922–21928. doi: 10.1039/C5RA26164C. DOI

Khalaf A.A., Hassanen E.I., Zaki A.R., Tohamy A.F., Ibrahim M.A. Histopathological, immunohistochemical, and molecular studies for determination of wound age and vitality in rats. Int. Wound J. 2019;19:1416–1425. doi: 10.1111/iwj.13206. PubMed DOI PMC

Behm B., Babilas P., Landthaler M., Schreml C. Cytokines, chemokines and growth factors in wound healing. J. Eur. Acad. Dermatol. Venereol. 2012;26:812–820. doi: 10.1111/j.1468-3083.2011.04415.x. PubMed DOI

Rezaii M., Oryan S., Javeri A. Curcumin nanoparticles incorporated collagen-chitosan csaffold promotes cutaneous wound healing through regulation of TGF-ß1/Smad7 gene expression. Mater. Sci. Eng. C. 2019;98:347–357. doi: 10.1016/j.msec.2018.12.143. PubMed DOI

Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 2003;83:835–870. doi: 10.1152/physrev.2003.83.3.835. PubMed DOI

Chanda W., Joseph T.P., Guo X.F., Wang W.D., Liu M., Vuai M.S., Zhong M.T. Effectiveness of omega-3 polyunsaturated fatty acids against microbial pathogens. J. Zhejiang Univ.-SCIENCE B. 2018;19:253–262. doi: 10.1631/jzus.B1700063. PubMed DOI PMC

Casillas-Vargas G., Ocasio-Malavé C., Medina S., Morales-Guzmán C., Del Valle R.G., Carballeira N.M., Sanabria-Ríos D.J. Antibacterial fatty acids: An update of possible mechanisms of action and implications in the development of the next-generation of antibacterial agents. Prog. Lipid Res. 2021;82:101093. doi: 10.1016/j.plipres.2021.101093. PubMed DOI PMC

Azzazy H.M.E.-S., Fahmy S.A., Mahdi N.K., Meselhy M.R., Bakowsky U. Chitosan-coated PLGA nanoparticles loaded with Peganum harmala alkaloids with promising antibacterial and wound healing activities. Nanomaterials. 2021;11:2438. doi: 10.3390/nano11092438. PubMed DOI PMC

Hasan N., Cao J., Lee J., Hlaing S.P., Oshi M.A., Naeem M., Ki M.-H., Lee B.L., Jung Y., Yoo J.-W. Bacteria-targeted clindamycin loaded polymeric nanoparticles: Effect of surface charge on nanoparticle adhesion to MRS, antibacterial activity, and wound healing. Pharmaceutics. 2019;11:236. doi: 10.3390/pharmaceutics11050236. PubMed DOI PMC

Komprda T., Popelková V., Košarišťanová L., Šmídová V. Poly(lactic-co-glycolic) Acid Nanoparticles as Delivery System of Fish Oil for Wound Healing. Acta Vet. Brno. 2022;91 in print .

Popelková V., Košarišťanová L., Komprda T., Vymazalová P., Fialová T., Švec P., Šmídová V., Bytešníková Z., Astete C.E., Sabliov C., et al. Poly(lactic-co-glycolic) Acid Nanoparticles as Feasible Delivery System of Antimicrobial Mupirocin for Possible Wound Healing. RSC Adv. 2022 submitted .

Dorazilová J., Muchová J., Šmerková K., Kočiová S., Diviš P., Kopel P., Veselý R., Pavliňáková V., Adam V., Vojtová L. Synergistic effect of chitosan and selenium nanoparticles on biodegradation and antibacterial properties of collagenous scaffolds designed for infected burn wounds. Nanomaterials. 2020;10:1971. doi: 10.3390/nano10101971. PubMed DOI PMC

Suresh K.P. An overview of randomization techniques: An unbiased assessment of outcome in clinical research. J. Hum. Reprod. Sci. 2011;4:8–11. doi: 10.4103/0974-1208.82352. PubMed DOI PMC

Maia-Figueiró T.L., Odashiro A.N., De Menezes G.P., Coelho L.R., Breda I., De Souza B.A., Figueiró-Filho E.A. Semi-Quantitative Histological Analysis of the Effect of Intense Pulsed Light (IPL) and Carbon Dioxide (CO2) Intradermic injection on fibroblast and collagen proliferation in the skin of Wistar rats. J. Cosmet. Dermatol. Sci. Appl. 2012;2:164–173.

Andersen C.L., Jensen J.L., Ørntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64:5245–5250. doi: 10.1158/0008-5472.CAN-04-0496. PubMed DOI

Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009;55:611–622. doi: 10.1373/clinchem.2008.112797. PubMed DOI

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

von der Hardt K., Kandler M.A., Fink L., Schoof E., Dötsch J., Brandenstein O., Bohle R.M., Rascher W. High frequency oscillatory ventilation suppresses inflammatory response in lung tissue and microdissected alveolar macrophages in surfactant depleted piglets. Pediatr. Res. 2004;55:339–346. doi: 10.1203/01.PDR.0000106802.55721.8A. PubMed DOI

Ondrackova P., Leva L., Kucerova Z., Vicenova M., Mensikova M., Faldyna M. Distribution of porcine monocytes in different lymphoid tissues and the lungs during experimental Actinobacillus pleuropneumoniae infection and the role of chemokines. Vet. Res. 2013;44:98. doi: 10.1186/1297-9716-44-98. PubMed DOI PMC

Nygard A.B., Jørgensen C.B., Cirera S., Fredholm M. Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol. Biol. 2007;8:67. doi: 10.1186/1471-2199-8-67. PubMed DOI PMC

Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012;13:134–145. doi: 10.1186/1471-2105-13-134. PubMed DOI PMC

Brakstad O.G., Aasbakk K., Maeland J.A. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol. 1992;30:1654–1660. doi: 10.1128/jcm.30.7.1654-1660.1992. PubMed DOI PMC

Candrian U., Furrer B., Höfelein C., Meyer R., Jermini M., Lüthy J. Detection of Escherichia coli and identification of enterotoxigenic strains by primer-directed enzymatic amplification of specific DNA sequences. Int. J. Food Microbiol. 1991;12:339–351. doi: 10.1016/0168-1605(91)90148-I. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...