Combined Use of Photobiomodulation and CurcuminLoaded Iron Oxide Nanoparticles Significantly Improved Wound Healing in Diabetic Rats Compared to Either Treatment Alone Photobiomodulation and curcumin nanoparticles for diabetic wounds
Journal of Lasers in Medical Sciences,
Vol. 14 (2023),
29 January 2023
,
Page e18
Abstract
Introduction: Here, we assess the therapeutic effects of photobiomodulation (PBM) and curcumin (CUR)-loaded superparamagnetic iron oxide nanoparticles (SPIONs), alone or together, on the maturation step of a type 1 diabetes (DM1) rat wound model.
Methods: Full-thickness wounds were inflicted in 36 rats with diabetes mellitus (DM) induced by the administration of streptozotocin (STZ). The rats were randomly allocated to four groups. Group one was untreated (control); group two received CUR; group 3 received PBM (890 nm, 80 Hz, 0.2 J/cm2 ); group 4 received a combination of PBM plus CUR. On days 0, 4, 7, and 15, we measured microbial flora, wound closure fraction, tensile strength, and stereological analysis.
Results: All treatment groups showed a substantial escalation in the wound closure rate, a substantial reduction in the count of methicillin-resistant Staphylococcus aureus (MRSA), a substantial improvement in wound strength, a substantial improvement in stereological parameters compared to the control group, however, the PBM+CUR group was superior to the other treatment groups (all, P≤0.05).
Conclusion: All treatment groups showed significantly improved wound healing in the DM1 rat model. However, the PBM+CUR group was superior to the other treatment groups and the control group in terms of wound strength and stereological parameters.
Keywords:
- Wound healing; Diabetes mellitus; Photobiomodulation; Low level laser therapy; Magnetic iron oxide nanoparticles
How to Cite
Hekmat, M., Ahmadi, H., Baniasadi, F., Ashtari, B., Naserzadeh, P. ., Mirzaei, M. ., Omidi, H., Mostafavinia, A., Amini, A. ., Hamblin, M. R. ., Chien, S. ., & Bayat, M. (2023). Combined Use of Photobiomodulation and CurcuminLoaded Iron Oxide Nanoparticles Significantly Improved Wound Healing in Diabetic Rats Compared to Either Treatment Alone: Photobiomodulation and curcumin nanoparticles for diabetic wounds. Journal of Lasers in Medical Sciences, 14, e18. Retrieved from https://journals.sbmu.ac.ir/jlms/article/view/40484
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[28] G. Silva, C. Ferraresi, R.T. de Almeida, M.L. Motta, T. Paixao, V.O. Ottone, I.A. Fonseca, M.X. Oliveira, E. Rocha‐Vieira, M.F. Dias‐Peixoto, Insulin resistance is improved in high‐fat fed mice by photobiomodulation therapy at 630 nm, Journal of biophotonics, 13 (2020) e201960140.
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[30] L. Prompers, M. Huijberts, J. Apelqvist, E. Jude, A. Piaggesi, K. Bakker, M. Edmonds, P. Holstein, A. Jirkovska, D. Mauricio, High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study, Diabetologia, 50 (2007) 18-25.
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[35] X. Dai, J. Liu, H. Zheng, J. Wichmann, U. Hopfner, S. Sudhop, C. Prein, Y. Shen, H.-G. Machens, A.F. Schilling, Nano-formulated curcumin accelerates acute wound healing through Dkk-1-mediated fibroblast mobilization and MCP-1-mediated anti-inflammation, NPG Asia Materials, 9 (2017) e368-e368.
[36] P. Anand, A.B. Kunnumakkara, R.A. Newman, B.B. Aggarwal, Bioavailability of curcumin: problems and promises, Molecular pharmaceutics, 4 (2007) 807-818.
[37] H. Soleimani, A. Amini, S. Taheri, E. Sajadi, S. Shafikhani, L.A. Schuger, V.B. Reddy, S.K. Ghoreishi, R. Pouriran, S. Chien, M. Bayat, The effect of combined photobiomodulation and curcumin on skin wound healing in type I diabetes in rats, J Photochem Photobiol B, 181 (2018) 23-30.
[38] A. Amini, H. Soleimani, M.A. Abdollhifar, A. Moradi, S.K. Ghoreishi, S. Chien, M. Bayat, Stereological and gene expression examinations on the combined effects of photobiomodulation and curcumin on wound healing in type one diabetic rats, J Cell Biochem, 120 (2019) 17994-18004.
[39] M. Martínez-Ballesta, Á. Gil-Izquierdo, C. García-Viguera, R. Domínguez-Perles, Nanoparticles and controlled delivery for bioactive compounds: Outlining challenges for new “smart-foods” for health, Foods, 7 (2018) 72.
[40] H. Ezhilarasu, D. Vishalli, S.T. Dheen, B.-H. Bay, D.K. Srinivasan, Nanoparticle-based therapeutic approach for diabetic wound healing, Nanomaterials, 10 (2020) 1234.
[41] M.E.d.A. Chaves, A.R.d. Araújo, A.C.C. Piancastelli, M. Pinotti, Effects of low-power light therapy on wound healing: LASER x LED, Anais brasileiros de dermatologia, 89 (2014) 616-623.
[42] S.C. Gupta, S. Patchva, W. Koh, B.B. Aggarwal, Discovery of curcumin, a component of golden spice, and its miraculous biological activities, Clinical and experimental pharmacology and physiology, 39 (2012) 283-299.
[43] D. Akbik, M. Ghadiri, W. Chrzanowski, R. Rohanizadeh, Curcumin as a wound healing agent, Life sciences, 116 (2014) 1-7.
[44] B. Mordorski, J. Rosen, A. Friedman, Nanotechnology as an innovative approach for accelerating wound healing in diabetes, Diabetes Management, 5 (2015) 329-332.
[45] P. Lau, N. Bidin, S. Islam, W. Shukri, N. Zakaria, N. Musa, G. Krishnan, Influence of gold nanoparticles on wound healing treatment in rat model: Photobiomodulation therapy, Lasers Surg Med, 49 (2017) 380-386.
[46] T. Fujimura, A. Mitani, M. Fukuda, M. Mogi, K. Osawa, S. Takahashi, M. Aino, Y. Iwamura, S. Miyajima, H. Yamamoto, T. Noguchi, Irradiation with a low-level diode laser induces the developmental endothelial locus-1 gene and reduces proinflammatory cytokines in epithelial cells, Lasers Med Sci, 29 (2014) 987-994.
[47] S.S. Dhilip Kumar, N.N. Houreld, H. Abrahamse, Selective Laser Efficiency of Green-Synthesized Silver Nanoparticles by Aloe arborescens and Its Wound Healing Activities in Normal Wounded and Diabetic Wounded Fibroblast Cells: In vitro Studies, Int J Nanomedicine, 15 (2020) 6855-6870.
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[5] D. Baltzis, I. Eleftheriadou, A. Veves, Pathogenesis and treatment of impaired wound healing in diabetes mellitus: new insights, Adv Ther, 31 (2014) 817-836.
[6] W.J. Jeffcoate, L. Vileikyte, E.J. Boyko, D.G. Armstrong, A.J. Boulton, Current challenges and opportunities in the prevention and management of diabetic foot ulcers, Diabetes care, 41 (2018) 645-652.
[7] S. Morbach, H. Furchert, U. Gröblinghoff, H. Hoffmeier, K. Kersten, G.-T. Klauke, U. Klemp, T. Roden, A. Icks, B. Haastert, Long-term prognosis of diabetic foot patients and their limbs: amputation and death over the course of a decade, Diabetes care, 35 (2012) 2021-2027.
[8] C. Bommer, E. Heesemann, V. Sagalova, J. Manne-Goehler, R. Atun, T. Bärnighausen, S. Vollmer, The global economic burden of diabetes in adults aged 20–79 years: a cost-of-illness study, The lancet Diabetes & endocrinology, 5 (2017) 423-430.
[9] G.H.J. de Smet, L.F. Kroese, A.G. Menon, J. Jeekel, A.W.J. van Pelt, G.J. Kleinrensink, J.F. Lange, Oxygen therapies and their effects on wound healing, Wound Repair Regen, 25 (2017) 591-608.
[10] L. Prompers, N. Schaper, J. Apelqvist, M. Edmonds, E. Jude, D. Mauricio, L. Uccioli, V. Urbancic, K. Bakker, P. Holstein, A. Jirkovska, A. Piaggesi, G. Ragnarson-Tennvall, H. Reike, M. Spraul, K. Van Acker, J. Van Baal, F. Van Merode, I. Ferreira, M. Huijberts, Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study, Diabetologia, 51 (2008) 747-755.
[11] A.Z. Mat Saad, T.L. Khoo, A.S. Halim, Wound bed preparation for chronic diabetic foot ulcers, International Scholarly Research Notices, 2013 (2013).
[12] E. Everett, N. Mathioudakis, Update on management of diabetic foot ulcers, Annals of the New York Academy of Sciences, 1411 (2018) 153.
[13] C.C. Naves, The Diabetic Foot: A Historical Overview and Gaps in Current Treatment, Adv Wound Care (New Rochelle), 5 (2016) 191-197.
[14] C. Mohanty, S.K. Sahoo, Curcumin and its topical formulations for wound healing applications, Drug Discovery Today, 22 (2017) 1582-1592.
[15] A. Barroso, H. Mestre, A. Ascenso, S. Simões, C. Reis, Nanomaterials in wound healing: From material sciences to wound healing applications, Nano Select, 1 (2020) 443-460.
[16] C. Justin, A.V. Samrot, C.S. Sahithya, K.S. Bhavya, C. Saipriya, Preparation, characterization and utilization of coreshell super paramagnetic iron oxide nanoparticles for curcumin delivery, PLoS One, 13 (2018) e0200440.
[17] S. Laurent, A.A. Saei, S. Behzadi, A. Panahifar, M. Mahmoudi, Superparamagnetic iron oxide nanoparticles for delivery of therapeutic agents: opportunities and challenges, Expert opinion on drug delivery, 11 (2014) 1449-1470.
[18] P. Naserzadeh, A.A. Hafez, M. Abdorahim, M.A. Abdollahifar, R. Shabani, H. Peirovi, A. Simchi, K. Ashtari, Curcumin loading potentiates the neuroprotective efficacy of Fe(3)O(4) magnetic nanoparticles in cerebellum cells of schizophrenic rats, Biomed Pharmacother, 108 (2018) 1244-1252.
[19] A. Moradi, Y. Kheirollahkhani, P. Fatahi, M.A. Abdollahifar, A. Amini, P. Naserzadeh, K. Ashtari, S.K. Ghoreishi, S. Chien, F. Rezaei, M. Fridoni, M. Bagheri, S. Taheri, M. Bayat, An improvement in acute wound healing in mice by the combined application of photobiomodulation and curcumin-loaded iron particles, Lasers Med Sci, 34 (2019) 779-791.
[20] O. Oyebode, N.N. Houreld, H. Abrahamse, Photobiomodulation in diabetic wound healing: A review of red and near‐infrared wavelength applications, Cell Biochemistry and Function, (2021).
[21] A. Moradi, F. Zare, A. Mostafavinia, S. Safaju, A. Shahbazi, M. Habibi, M.A. Abdollahifar, S.M. Hashemi, A. Amini, S.K. Ghoreishi, S. Chien, M.R. Hamblin, R. Kouhkheil, M. Bayat, Photobiomodulation plus Adipose-derived Stem Cells Improve Healing of Ischemic Infected Wounds in Type 2 Diabetic Rats, Sci Rep, 10 (2020) 1206.
[22] R. Ebrahimpour-Malekshah, A. Amini, F. Zare, A. Mostafavinia, S. Davoody, N. Deravi, M. Rahmanian, S.M. Hashemi, M. Habibi, S.K. Ghoreishi, S. Chien, S. Shafikhani, H. Ahmadi, S. Bayat, M. Bayat, Combined therapy of photobiomodulation and adipose-derived stem cells synergistically improve healing in an ischemic, infected and delayed healing wound model in rats with type 1 diabetes mellitus, BMJ Open Diabetes Res Care, 8 (2020).
[23] H. Ahmadi, A. Amini, F. Fadaei Fathabady, A. Mostafavinia, F. Zare, R. Ebrahimpour-Malekshah, M.N. Ghalibaf, M. Abrisham, F. Rezaei, R. Albright, S.K. Ghoreishi, S. Chien, M. Bayat, Transplantation of photobiomodulation-preconditioned diabetic stem cells accelerates ischemic wound healing in diabetic rats, Stem Cell Res Ther, 11 (2020) 494.
[24] J. Lodhia, G. Mandarano, N. Ferris, P. Eu, S. Cowell, Development and use of iron oxide nanoparticles (Part 1): Synthesis of iron oxide nanoparticles for MRI, Biomedical imaging and intervention journal, 6 (2010) e12.
[25] R. Pouriran, A. Piryaei, A. Mostafavinia, S. Zandpazandi, F. Hendudari, A. Amini, M. Bayat, The Effect of Combined Pulsed Wave Low-Level Laser Therapy and Human Bone Marrow Mesenchymal Stem Cell-Conditioned Medium on Open Skin Wound Healing in Diabetic Rats, Photomed Laser Surg, 34 (2016) 345-354.
[26] M. Sene‐Fiorese, F.O. Duarte, A.E. de Aquino Junior, R.M.d.S. Campos, D.C.L. Masquio, L. Tock, A.C.G. de Oliveira Duarte, A.R. Dâmaso, N.A. Parizotto, V.S. Bagnato, The potential of phototherapy to reduce body fat, insulin resistance and “metabolic inflexibility” related to obesity in women undergoing weight loss treatment, Lasers in surgery and medicine, 47 (2015) 634-642.
[27] C.O. Francisco, T. Beltrame, R.L. Hughson, J.C. Milan-Mattos, A.M. Ferroli-Fabricio, B. Galvão Benze, C. Ferraresi, N.A. Parizotto, V.S. Bagnato, A. Borghi-Silva, A. Porta, A.M. Catai, Effects of light-emitting diode therapy (LEDT) on cardiopulmonary and hemodynamic adjustments during aerobic exercise and glucose levels in patients with diabetes mellitus: A randomized, crossover, double-blind and placebo-controlled clinical trial, Complement Ther Med, 42 (2019) 178-183.
[28] G. Silva, C. Ferraresi, R.T. de Almeida, M.L. Motta, T. Paixao, V.O. Ottone, I.A. Fonseca, M.X. Oliveira, E. Rocha‐Vieira, M.F. Dias‐Peixoto, Insulin resistance is improved in high‐fat fed mice by photobiomodulation therapy at 630 nm, Journal of biophotonics, 13 (2020) e201960140.
[29] W.H. de Brito Vieira, C. Ferraresi, M.L.B. Schwantes, S.E. de Andrade Perez, V. Baldissera, M.S. Cerqueira, N.A. Parizotto, Photobiomodulation increases mitochondrial citrate synthase activity in rats submitted to aerobic training, Lasers in medical science, 33 (2018) 803-810.
[30] L. Prompers, M. Huijberts, J. Apelqvist, E. Jude, A. Piaggesi, K. Bakker, M. Edmonds, P. Holstein, A. Jirkovska, D. Mauricio, High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study, Diabetologia, 50 (2007) 18-25.
[31] F.W. Gemechu, F. Seemant, C.A. Curley, Diabetic foot infections, American family physician, 88 (2013) 177-184.
[32] S. Patel, S. Srivastava, M.R. Singh, D. Singh, Mechanistic insight into diabetic wounds: Pathogenesis, molecular targets and treatment strategies to pace wound healing, Biomedicine & Pharmacotherapy, 112 (2019) 108615.
[33] K. Alexiadou, J. Doupis, Management of diabetic foot ulcers, Diabetes Therapy, 3 (2012) 4.
[34] J.J. Salazar, W.J. Ennis, T.J. Koh, Diabetes medications: impact on inflammation and wound healing, Journal of Diabetes and its Complications, 30 (2016) 746-752.
[35] X. Dai, J. Liu, H. Zheng, J. Wichmann, U. Hopfner, S. Sudhop, C. Prein, Y. Shen, H.-G. Machens, A.F. Schilling, Nano-formulated curcumin accelerates acute wound healing through Dkk-1-mediated fibroblast mobilization and MCP-1-mediated anti-inflammation, NPG Asia Materials, 9 (2017) e368-e368.
[36] P. Anand, A.B. Kunnumakkara, R.A. Newman, B.B. Aggarwal, Bioavailability of curcumin: problems and promises, Molecular pharmaceutics, 4 (2007) 807-818.
[37] H. Soleimani, A. Amini, S. Taheri, E. Sajadi, S. Shafikhani, L.A. Schuger, V.B. Reddy, S.K. Ghoreishi, R. Pouriran, S. Chien, M. Bayat, The effect of combined photobiomodulation and curcumin on skin wound healing in type I diabetes in rats, J Photochem Photobiol B, 181 (2018) 23-30.
[38] A. Amini, H. Soleimani, M.A. Abdollhifar, A. Moradi, S.K. Ghoreishi, S. Chien, M. Bayat, Stereological and gene expression examinations on the combined effects of photobiomodulation and curcumin on wound healing in type one diabetic rats, J Cell Biochem, 120 (2019) 17994-18004.
[39] M. Martínez-Ballesta, Á. Gil-Izquierdo, C. García-Viguera, R. Domínguez-Perles, Nanoparticles and controlled delivery for bioactive compounds: Outlining challenges for new “smart-foods” for health, Foods, 7 (2018) 72.
[40] H. Ezhilarasu, D. Vishalli, S.T. Dheen, B.-H. Bay, D.K. Srinivasan, Nanoparticle-based therapeutic approach for diabetic wound healing, Nanomaterials, 10 (2020) 1234.
[41] M.E.d.A. Chaves, A.R.d. Araújo, A.C.C. Piancastelli, M. Pinotti, Effects of low-power light therapy on wound healing: LASER x LED, Anais brasileiros de dermatologia, 89 (2014) 616-623.
[42] S.C. Gupta, S. Patchva, W. Koh, B.B. Aggarwal, Discovery of curcumin, a component of golden spice, and its miraculous biological activities, Clinical and experimental pharmacology and physiology, 39 (2012) 283-299.
[43] D. Akbik, M. Ghadiri, W. Chrzanowski, R. Rohanizadeh, Curcumin as a wound healing agent, Life sciences, 116 (2014) 1-7.
[44] B. Mordorski, J. Rosen, A. Friedman, Nanotechnology as an innovative approach for accelerating wound healing in diabetes, Diabetes Management, 5 (2015) 329-332.
[45] P. Lau, N. Bidin, S. Islam, W. Shukri, N. Zakaria, N. Musa, G. Krishnan, Influence of gold nanoparticles on wound healing treatment in rat model: Photobiomodulation therapy, Lasers Surg Med, 49 (2017) 380-386.
[46] T. Fujimura, A. Mitani, M. Fukuda, M. Mogi, K. Osawa, S. Takahashi, M. Aino, Y. Iwamura, S. Miyajima, H. Yamamoto, T. Noguchi, Irradiation with a low-level diode laser induces the developmental endothelial locus-1 gene and reduces proinflammatory cytokines in epithelial cells, Lasers Med Sci, 29 (2014) 987-994.
[47] S.S. Dhilip Kumar, N.N. Houreld, H. Abrahamse, Selective Laser Efficiency of Green-Synthesized Silver Nanoparticles by Aloe arborescens and Its Wound Healing Activities in Normal Wounded and Diabetic Wounded Fibroblast Cells: In vitro Studies, Int J Nanomedicine, 15 (2020) 6855-6870.
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