Skip to main content
SpringerLink
Log in

Effects of photobiomodulation on oxidative stress in rats with type 2 diabetes mellitus

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

The present study aimed to evaluate photobiomodulation effects on oxidative stress in type 2 diabetes mellitus (DM2). Thirty-one male Wistar rats were used and divided into 4 groups: group 1 – animals without diabetes mellitus 2 without laser 21 J/cm2 (C-SHAM), group 2 – animals with diabetes mellitus 2 without laser 21 J/cm2 (C-DM2), group 3 – animals without diabetes mellitus 2 with laser 21 J/cm2 (L-SHAM), group 4 – animals with diabetes mellitus 2 with laser 21 J/cm2 (L-DM2). The protocol was performed 5 days/week, for 6 weeks. The animals that received photobiomodulation had one dose irradiated at two spots in the right gastrocnemius muscle. Twenty-four hours after the last intervention, the animals were euthanized. Heart, diaphragm, liver, right gastrocnemius, plasma, kidneys, weighed, and stored for further analysis. In rats with DM2, photobiomodulation promoted a decrease in thiobarbituric acid reactive substance assay (TBARS) in plasma levels. On the other hand, photobiomodulation demonstrated an increase in non-protein thiol levels (NPSH) in the heart, diaphragm and gastrocnemius. Moreover, photobiomodulation produced in the heart, diaphragm and plasma levels led to an increase in superoxide dismutase (SOD). Interestingly, photobiomodulation was able to increase superoxide dismutase in rats without DM2 in the heart, diaphragm, gastrocnemius and kidneys. These findings suggested that 6 weeks of photobiomodulation in rats with DM2 promoted beneficial adaptations in oxidative stress, with a decrease in parameters of oxidant activity and an increase in antioxidant activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

Materials availability

Not applicable.

Code availability

Not applicable.

References

  1. Saeedi P, Petersohn I, Salpea P et al (2019) Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9th edn. Diabetes Res Clin Pract 157:107843. https://doi.org/10.1016/j.diabres.2019.107843

  2. American Diabetes Association (2019) Diagnosis and classification of diabetes mellitus. Diabetes Care 42(1):S13–S28. https://doi.org/10.2337/dc19-S002

    Article  Google Scholar 

  3. Eizirik DL, Pasquali L, Cnop M (2020) Pancreatic β-cells in type 1 and type 2 diabetes mellitus: different pathways to failure. Nat Rev Endocrinol 16(7):349–362. https://doi.org/10.1038/s41574-020-0355-7

    Article  CAS  PubMed  Google Scholar 

  4. Denadai AS, Aydos RD, Silva IS et al (2017) Acute effects of low-level laser therapy (660 nm) on oxidative stress levels in diabetic rats with skin wounds. J Exp Ther Oncol 11(2):85–89

    PubMed  Google Scholar 

  5. Daryabor G, Atashzar MR, Kabelitz D, Meri S, Kalantar K (2020) The effects of type 2 diabetes mellitus on organ metabolism and the immune system. Front Immunol 11:1582. https://doi.org/10.3389/fimmu.2020.01582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Di Meo S, Venditti P (2020) Evolution of the Knowledge of Free Radicals and Other Oxidants. Oxid Med Cell Longev 2020:9829176. https://doi.org/10.1155/2020/9829176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. De Leon JAD, Borges CR (2020) Evaluation of oxidative stress in biological samples using the thiobarbituric acid reactive substances assay. J Vis Exp 159:e61122. https://doi.org/10.3791/61122.10.3791/61122

    Article  Google Scholar 

  8. Su LJ, Zhang JH, Gomez H et al (2019) Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev 2019(2019):5080843. https://doi.org/10.1155/2019/5080843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Liguori I, Russo G, Curcio F et al (2018) Oxidative stress, aging, and diseases. Clin Interv Aging 13:757–772. https://doi.org/10.2147/CIA.S158513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Luc K, Schramm-Luc A, Guzik TJ, Mikolajczyk TP (2019) Oxidative stress and inflammatory markers in prediabetes and diabetes. J Physiol Pharmacol 70(6):809–24. https://doi.org/10.26402/jpp.2019.6.01

    Article  CAS  Google Scholar 

  11. Ighodaro OM (2018) Molecular pathways associated with oxidative stress in diabetes mellitus. Biomed Pharmacother 108:656–662. https://doi.org/10.1016/j.biopha.2018.09.058

    Article  CAS  PubMed  Google Scholar 

  12. Ahmed OM, Mohamed T, Moustafa H, Hamdy H, Ahmed RR, Aboud E (2018) Quercetin and low-level laser therapy promote wound healing process in diabetic rats via structural reorganization and modulatory effects on inflammation and oxidative stress. Biomed Pharmacother 101:58–73. https://doi.org/10.1016/j.biopha.2018.02.040

    Article  CAS  PubMed  Google Scholar 

  13. Firat ET, Dağ A, Günay A et al (2013) The effects of low-level laser therapy on palatal mucoperiosteal wound healing and oxidative stress status in experimental diabetic rats. Photomed Laser Surg 31(7):315–321. https://doi.org/10.1089/pho.2012.3406

    Article  CAS  PubMed  Google Scholar 

  14. Reinehr T (2019) Inflammatory markers in children and adolescents with type 2 diabetes mellitus. Clin Chim Acta. 496:100–107. https://doi.org/10.1016/j.cca.2019.07.006

    Article  CAS  PubMed  Google Scholar 

  15. Mostafavinia A, Ahmadi H, Amini A et al (2021) The effect of photobiomodulation therapy on antioxidants and oxidative stress profiles of adipose derived mesenchymal stem cells in diabetic rats. Spectrochim Acta A Mol Biomol Spectrosc 262:120157. https://doi.org/10.1016/j.saa.2021.120157

    Article  CAS  PubMed  Google Scholar 

  16. Abdel-Wahhab KG, Daoud EM, El Gendy A et al (2018) Efficiencies of low-level laser therapy (LLLT) and gabapentin in the management of peripheral neuropathy: diabetic neuropathy. Appl Biochem Biotechnol 186(1):161–173. https://doi.org/10.1007/s12010-018-2729-z

    Article  CAS  PubMed  Google Scholar 

  17. Feitosa MC, Carvalho AF, Feitosa VC, Coelho IM, Oliveira RA, Arisawa EÂ (2015) Effects of the low-level laser therapy (LLLT) in the process of healing diabetic foot ulcers. Acta Cir Bras 30(12):852–857. https://doi.org/10.1590/S0102-865020150120000010

    Article  PubMed  Google Scholar 

  18. Mathur RK, Sahu K, Saraf S, Patheja P, Khan F, Gupta PK (2017) Low-level laser therapy as an adjunct to conventional therapy in the treatment of diabetic foot ulcers. Lasers Med Sci 32(2):275–282. https://doi.org/10.1007/s10103-016-2109-2

    Article  CAS  PubMed  Google Scholar 

  19. Chen H, Tu M, Shi J, Wang Y, Hou Z, Wang J (2021) Effect of photobiomodulation on CCC-ESF reactive oxygen species steady-state in high glucose mediums. Lasers Med Sci 36(3):555–562. https://doi.org/10.1007/s10103-020-03057-4

    Article  CAS  PubMed  Google Scholar 

  20. Frigero M, Dos Santos SA, Serra AJ et al (2018) Effect of photobiomodulation therapy on oxidative stress markers of gastrocnemius muscle of diabetic rats subjected to high-intensity exercise. Lasers Med Sci 33(8):1781–1790. https://doi.org/10.1007/s10103-018-2540-7

    Article  PubMed  Google Scholar 

  21. Karkada G, Maiya GA, Arany P, Rao M, Adiga S, Kamath SU (2022) Effect of photobiomodulation therapy on oxidative stress markers in healing dynamics of diabetic neuropathic wounds in Wistar rats. Cell Biochem Biophys 80(1):151–160. https://doi.org/10.1007/s12013-021-01021-9

    Article  CAS  PubMed  Google Scholar 

  22. Anju M, Ummer VS, Maiya AG, Hande M (2019) Low level laser therapy for the patients with painful diabetic peripheral neuropathy - a systematic review. Diabetes Metab Syndr 13(4):2667–2670. https://doi.org/10.1016/j.dsx.2019.07.035

    Article  Google Scholar 

  23. Kumar B, Gupta SK, Nag TC et al (2014) Retinal neuroprotective effects of quercetin in streptozotocin-induced diabetic rats. Exp Eye Res 125:193–202. https://doi.org/10.1016/j.exer.2014.06.009

    Article  CAS  PubMed  Google Scholar 

  24. Guex CG, Reginato FZ, de Jesus PR, Brondani JC, Lopes GHH, Bauermann LF (2019) Antidiabetic effects of Olea europaea L. leaves in diabetic rats induced by high-fat diet and low-dose streptozotocin. J Ethnopharmacol 235:1–7. https://doi.org/10.1016/j.jep.2019.02.001

    Article  CAS  PubMed  Google Scholar 

  25. Srinivasan K, Viswanad B, Asrat L, Kaul CL, Ramarao P (2005) Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res 52(4):313–320. https://doi.org/10.1016/j.phrs.2005.05.004

    Article  CAS  PubMed  Google Scholar 

  26. Vatandoust N, Rami F, Salehi AR et al (2018) Novel high-fat diet formulation and streptozotocin treatment for induction of prediabetes and type 2 diabetes in rats. Adv Biomed Res 7:107. https://doi.org/10.4103/abr.abr_8_17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hentschke VS, Jaenisch RB, Schmeing LA, Cavinato PR, Xavier LL, Dal Lago P (2012) Low-level laser therapy improves the inflammatory profile of rats with heart failure. Lasers Med Sci 28(3):1007–1016. https://doi.org/10.1007/s10103-012-1190-4

    Article  PubMed  Google Scholar 

  28. Aquino AE Jr, Sene-Fiorese M, Castro CA et al (2015) Can low-level laser therapy when associated to exercise decrease adipocyte area? J Photochem Photobiol B 149:21–26. https://doi.org/10.1016/j.jphotobiol.2015.04.033

    Article  CAS  PubMed  Google Scholar 

  29. Oyenihi AB, Langa SOP, Mukaratirwa S, Masola B (2019) Effects of Centella asiatica on skeletal muscle structure and key enzymes of glucose and glycogen metabolism in type 2 diabetic rats. Biomed Pharmacother. 112:108715. https://doi.org/10.1016/j.biopha.2019.108715

    Article  CAS  PubMed  Google Scholar 

  30. Martins RP, Hartmann DD, de Moraes JP, Soares FA, Puntel GO (2016) Platelet-rich plasma reduces the oxidative damage determined by a skeletal muscle contusion in rats. Platelets 27(8):784–790. https://doi.org/10.1080/09537104.2016.1184752

    Article  CAS  PubMed  Google Scholar 

  31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    Article  CAS  PubMed  Google Scholar 

  32. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358. https://doi.org/10.1016/0003-2697(79)90738-3

    Article  CAS  PubMed  Google Scholar 

  33. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6

    Article  CAS  PubMed  Google Scholar 

  34. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175

    Article  CAS  PubMed  Google Scholar 

  35. Elimam H, Abdulla AM, Taha IM (2019) Inflammatory markers and control of type 2 diabetes mellitus. Diabetes Metab Syndr 13(1):800–804. https://doi.org/10.1016/j.dsx.2018.11.061

    Article  PubMed  Google Scholar 

  36. Gong L, Zou Z, Liu L, Guo S, Xing D (2021) Photobiomodulation therapy ameliorates hyperglycemia and insulin resistance by activating cytochrome c oxidase-mediated protein kinase B in muscle. Aging 13(7):10015–10033. https://doi.org/10.18632/aging.202760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bhawal UK, Yoshida K, Kurita T et al (2019) Effects of 830 nm low-power laser irradiation on body weight gain and inflammatory cytokines in experimental diabetes in different animal models. Laser Ther 28(4):257–265. https://doi.org/10.5978/islsm.19-OR-17

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gonçalves AB, Bovo JL, Gomes BS et al (2021) Photobiomodulation (λ=808nm) and platelet-rich plasma (PRP) for the treatment of acute rheumatoid arthritis in Wistar rats. J Lasers Med Sci 12:e60. Published 2021 Oct 18. https://doi.org/10.34172/jlms.2021.60

  39. Tatmatsu-Rocha JC, Ferraresi C, Hamblin MR et al (2016) Low-level laser therapy (904nm) can increase collagen and reduce oxidative and nitrosative stress in diabetic wounded mouse skin. J Photochem Photobiol B 164:96–102. https://doi.org/10.1016/j.jphotobiol.2016.09.017

    Article  CAS  PubMed  Google Scholar 

  40. Yaribeygi H, Atkin SL, Sahebkar A (2019) A review of the molecular mechanisms of hyperglycemia-induced free radical generation leading to oxidative stress. J Cell Physiol. 234(2):1300–1312. https://doi.org/10.1002/jcp.27164

    Article  CAS  PubMed  Google Scholar 

  41. Tomé RFF, Silva DFB, Dos Santos CAO, de Vasconcelos NG, Rolim AKA, de Castro Gomes DQ (2020) ILIB (intravascular laser irradiation of blood) as an adjuvant therapy in the treatment of patients with chronic systemic diseases-an integrative literature review. Lasers Med Sci 35(9):1899–1907. https://doi.org/10.1007/s10103-020-03100-4

    Article  PubMed  Google Scholar 

  42. Zhang P, Li T, Wu X, Nice EC, Huang C, Zhang Y (2020) Oxidative stress and diabetes: antioxidative strategies. Front Med 14(5):583–600. https://doi.org/10.1007/s11684-019-0729-1

    Article  PubMed  Google Scholar 

  43. Asghari A, Takhtfooladi MA, Hoseinzadeh HA (2016) Effect of photobiomodulation on ischemia/reperfusion-induced renal damage in diabetic rats. Lasers Med Sci 31(9):1943–1948. https://doi.org/10.1007/s10103-016-2073-x

    Article  PubMed  Google Scholar 

  44. de Oliveira HA, Antonio EL, Arsa G et al (2018) Photobiomodulation leads to reduced oxidative stress in rats submitted to high-intensity resistive exercise. Oxid Med Cell Longev 2018:5763256. https://doi.org/10.1155/2018/5763256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sunemi SM, Teixeira ILA, Mansano BSDM et al (2021) Post-resistance exercise photobiomodulation therapy has a more effective antioxidant effect than pre-application on muscle oxidative stress. Photochem Photobiol Sci 20(4):585–595. https://doi.org/10.1007/s43630-021-00042-w

    Article  CAS  PubMed  Google Scholar 

  46. da Silva Leal MV, Lima MO, Nicolau RA et al (2020) Effect of modified laser transcutaneous irradiation on pain and quality of life in patients with diabetic neuropathy. Photobiomodul Photomed Laser Surg 38(3):138–144. https://doi.org/10.1089/photob.2019.4714

    Article  CAS  PubMed  Google Scholar 

  47. Poblete-Aro C, Russell-Guzmán J, Parra P et al (2018) Exercise and oxidative stress in type 2 diabetes mellitus. Rev Med Chil 146(3):362–372. https://doi.org/10.4067/s0034-98872018000300362

    Article  PubMed  Google Scholar 

Download references

Funding

This study was funded in part by the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES) and by the Foundation for Research Support of the State of Rio Grande do Sul (FAPERGS)—EDITAL FAPERGS/CAPES 05/2017—Master’s Degree.

Author information

Authors and Affiliations

  1. Department of Physiotherapy and Rehabilitation, Postgraduate Program in Movement and Rehabilitation Sciences, Federal University of Santa Maria, Santa Maria, Brazil

    Larissa da Silva Tonetto, Carlos Cassiano Figueiró da Silva, Nubia Gonzatti, Maria Elaine Trevisan & Rodrigo Boemo Jaenisch

  2. Department of Physiology and Pharmacology, Federal University of Santa Maria, Santa Maria, RS, Brazil

    Camille Gaube Guex & Liliane de Freitas Bauermann

  3. Department of Biochemical Sciences, Postgraduate Program in Toxicological Biochemistry, Federal University of Santa Maria, Santa Maria, RS, Brazil

    Diane Duarte Hartmann

  4. Department of Physiotherapy, Pontifical Catholic University of Rio Grande Do Sul, Porto Alegre, RS, Brazil

    Emerson Soldateli Boschi

  5. Department of Physiotherapy, Federal University of Health Sciences, Porto Alegre, RS, Brazil

    Pedro Dal Lago

Authors
  1. Larissa da Silva Tonetto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos Cassiano Figueiró da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nubia Gonzatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Camille Gaube Guex
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Diane Duarte Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emerson Soldateli Boschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pedro Dal Lago
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Elaine Trevisan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Liliane de Freitas Bauermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Rodrigo Boemo Jaenisch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Not applicable.

Corresponding author

Correspondence to Rodrigo Boemo Jaenisch.

Ethics declarations

Research involving human and/or animal participants

Study approved by the Ethics Committee in the Use of Animals (CEUA) of the Federal University of Santa Maria (UFSM) under number 6622101118.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethical approval

The approval was obtained from the CEUA of the UFSM of Santa Maria. The procedures used in this study are in accordance with the Animal Use Ethics Commission.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva Tonetto, L., da Silva, C.C.F., Gonzatti, N. et al. Effects of photobiomodulation on oxidative stress in rats with type 2 diabetes mellitus. Lasers Med Sci 38, 90 (2023). https://doi.org/10.1007/s10103-023-03745-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10103-023-03745-x

Keywords

Search

Navigation