Skip to main content
Log in

Evaluation of low-level laser therapy on skeletal muscle ischemia–reperfusion in streptozotocin-induced diabetic rats by assaying biochemical markers and histological changes

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

Abstract

The purpose of the present study was to assess the effects of low-level laser therapy (LLLT) on skeletal muscle ischemia–reperfusion (IR) injuries in streptozotocin-induced diabetic rats. Twenty male Wistar rats were randomly assigned into two experimental groups, as follows: the diabetic IR group (G1, n = 10) and the diabetic IR + LLLT group (G2, n = 10). Ischemia was induced in anesthetized rats from the right femoral artery clipping for 2 h, followed by a reperfusion for 24 h. Then, the laser irradiation (K30 handheld probe, AZOR, Technica, Russia, 650 nm, 30 mW, surface area = 1 cm2, energy density = 1.8 J/cm2) was carried out by irradiating the rats over a unique point on the skin over the middle region of the right gastrocnemius muscle belly three times (every 8 h), starting after initiating the reperfusion for 3 min. At the end of the reperfusion period, rats were anaesthetized and blood samples were collected and used for the estimation of pO2, pCO2, pH, HCO3, serum creatine phosphokinase (CPK), and lactate dehydrogenase (LDH). Subsequently, the right gastrocnemius muscle samples were taken for wet/dry weight ratio assessment and histological/biochemical examination. The pO2, pCO2, HCO3, and pH levels were similar for both groups (P > 0.05). The serum LDH and CPK levels were significantly lower (P < 0.05) for G2 compared to G1. In comparison to G1, tissue malondialdehyde level in G2 was significantly decreased (P < 0.05). In G2, superoxide dismutase activity was significantly increased compared to G1 (P < 0.05). Unlike G2, a significant decrease in the activity of catalase was observed in G1 (P < 0.05). The wet/dry ratio in G1 was significantly higher than that of G2 (P < 0.05). Histological examination confirmed that the extent of muscle changes in G1 was higher than G2 (P < 0.05). Finally, according to this study, LLLT has a beneficial effect on the IR muscle injury treatment in the diabetic rats. Therefore, we suggest that further research needs to be conducted using different laser parameters and examining response over a longer period of tissue recovery.

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

Access this article

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
Fig. 4

Similar content being viewed by others

References

  1. Aydın ME, Erbatur ME, Çomu FM, Arslan M (2015) Effect of sevoflurane and desflurane on erythrocyte deformability during ischaemia-reperfusion injury of lower extremity in diabetic rats. Int J Anesth Anesthesiol 2:026

    Google Scholar 

  2. Vaghasiya JD, Sheth NR, Bhalodia YS, Jivani NP (2010) Exaggerated liver injury induced by renal ischemia reperfusion in diabetes: effect of exenatide. Saudi J Gastroenterol 16:174–80

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shinohara K, Shoji T, Kimoto E, Yokoyama H, Fujiwara S, Hatsuda S et al (2005) Effect of atorvastatin on regional arterial stiffness in patients with type 2 diabetes mellitus. J Atheroscler Thromb 12:205–10

    Article  CAS  PubMed  Google Scholar 

  4. Abbott RD, Brand FN, Kannel WB (1990) Epidemiology of some peripheral arterial findings in diabetic men and women: experiences from the Framingham Study. Am J Med 88:376–81

    Article  CAS  PubMed  Google Scholar 

  5. Centers for Disease Control and Prevention (CDC) (1998) Diabetes related amputations of lower extremities in the Medicare population–Minnesota, 1993–1995. Morb Mortal Wkly Rep 47:649–52

    Google Scholar 

  6. Hackam DG (2005) Cardiovascular risk prevention in peripheral artery disease. J Vasc Surg 41:1070–3

    Article  PubMed  Google Scholar 

  7. UK Prospective Diabetes Study (UKPDS) Group (1998) Intensive blood glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–53

    Article  Google Scholar 

  8. Mishra N, Singh N (2013) Blood viscosity, lipid profile, and lipid peroxidation in type-1 diabetic patients with good and poor glycemic control. N Am J Med Sci 5:562–6

    Article  PubMed  PubMed Central  Google Scholar 

  9. Singh R, Bhardwaj P, Sharma P (2013) Antioxidant and toxicological evaluation of Cassia sopherain streptozotocin-induced diabetic Wistar rats. Pharmacogn Res 5:225–32

    Article  Google Scholar 

  10. Lakyová L, Toporcer T, Tomečková V, Sabo J, Radoňak J (2010) Low-level laser therapy for protection against skeletal muscle damage after ischemia–reperfusion injury in rat hindlimbs. Lasers Surg Med 42(9):665–72

    Article  PubMed  Google Scholar 

  11. Takhtfooladi MA, Takhtfooladi HA, Khansari M (2014) The effects of low-intensity laser therapy on hepatic ischemia-reperfusion injury in a rat model. Lasers Med Sci 29(6):1887–93

    Article  PubMed  Google Scholar 

  12. Ashrafzadeh Takhtfooladi M, Ashrafzadeh Takhtfooladi H, Sedaghatfar H, Shabani S (2015) Effect of low-level laser therapy on lung injury induced by hindlimb ischemia/reperfusion in rats. Lasers Med Sci 30(6):1757–62

    Article  PubMed  Google Scholar 

  13. Oron U (2006) Photoengineering of tissue repair in skeletal and cardiac muscles. Photomed Laser Surg 242:111–20

    Article  Google Scholar 

  14. Vasilenko T, Sleza’k M, Kova’cˇ I, Bottkova’ Z, Jakubcˇo J, Kostelnı’kova’ M, Tomori Z, Ga’l P (2010) The effect of equal daily dose achieved by different power densities of low-level laser therapy at 635 and 670nm on wound tensile strength in rats: a short report. Photomed Laser Surg 28:281–3

    Article  PubMed  Google Scholar 

  15. Ferreira M, Ferrari R, Gravalos E, Martins M, Bussadori S, Gonzalez D, Fernandes K (2009) Effect of low-energy gallium–aluminum–arsenide and aluminium gallium indium phosphide laser irradiation on the viability of C2C12 myoblasts in a muscle injury model. Photomed Laser Surg 27:901–6

    Article  PubMed  Google Scholar 

  16. Bibikova A, Belkin A, Oron U (1994) Enhancement of angiogenesis in regenerating gastrocnemius muscle of the toad (Bufo viridis) by low energy laser irradiation. Anat Embryol (Berlin) 190:597–602

    Article  CAS  Google Scholar 

  17. Takhtfooladi MA, Jahanshahi A, Sotoudeh A, Jahanshahi G, Takhtfooladi HA, Aslani K (2013) Effect of tramadol on lung injury induced by skeletal muscle ischemia-reperfusion: an experimental study. J Bras Pneumol 39(4):434–9

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–8

    Article  CAS  PubMed  Google Scholar 

  19. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–75

    CAS  PubMed  Google Scholar 

  20. Fridovich I (1974) Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 41:35–97

    CAS  PubMed  Google Scholar 

  21. Beutler E (1975) Catalase. In: Beutler E (ed) Red cell metabolism. Grune and Stratton Company, New York, pp 89–90

    Google Scholar 

  22. Ullrich R, Roeder G, Lorber C, Quezado ZM, Kneifel W, Gasser H, Schlag G, Redl H, Germann P (2001) Continuous venovenous hemofiltration improves arterial oxygenation in endotoxin-induced lung injury in pigs. Anesthesiology 95(2):428–36

    Article  CAS  PubMed  Google Scholar 

  23. Tong Z, Yu F, Liu Z, Liang H (2012) Influence of ShuJinHuoXue tablets on ischemia reperfusion injury of animals’ skeletal muscle. Molecules 17:8494–505

    Article  CAS  PubMed  Google Scholar 

  24. Howard AC, McNeil AK, Xiong F, Xiong WC, McNeil PL (2011) A novel cellular defect in diabetes: membrane repair failure. Diabetes 60:3034–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Al-Watban FA (2009) Laser therapy converts diabetic wound healing to normal healing. Photomed Laser Surg 27:127–35

    Article  PubMed  Google Scholar 

  26. Fulop AM, Dhimmer S, Deluca JR, Johanson DD, Lenz RV, Patel KB, Douris PC, Enwemeka CS (2009) A meta-analysis of the efficacy of phototherapy in tissue repair. Photomed Laser Surg 27:695–702

    Article  PubMed  Google Scholar 

  27. Kaviani A, Djavid GE, Ataie-Fashtami L, FatehM GM, Salami M, Zand N, Kashef N, Larijani B (2011) A randomized clinical trial on the effect of low-level laser therapy on chronic diabetic foot wound healing: a preliminary report. Photomed Laser Surg 29:109–14

    Article  PubMed  Google Scholar 

  28. de Souza TO, Mesquita DA, Ferrari RA, Dos Santos Pinto D Jr, Correa L, Bussadori SK, Fernandes KP, Martins MD (2011) Phototherapy with low-level laser affects the remodeling of types I and III collagen in skeletal muscle repair. Lasers Med Sci 26:803–14

    Article  PubMed  Google Scholar 

  29. Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP (2011) Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 26(3):335–40

    Article  PubMed  Google Scholar 

  30. Baptista J, Martins MD, Pavesi VC, Bussadori SK, Fernandes KP, Pinto Júnior D dos S, Ferrari RA (2011) Influence of laser photobiomodulation on collagen IV during skeletal muscle tissue remodeling after injury in rats. Photomed Laser Surg 29:11–7

    Article  CAS  PubMed  Google Scholar 

  31. Ihsan FR (2005) Low level laser therapy accelerates collateral circulation and enhances microcirculation. Photomed Laser Surg 23:289–94

    Article  CAS  PubMed  Google Scholar 

  32. Mirsky N, Krispel Y, Shoshany Y, Maltz L, Oron U (2002) Promotion of angiogenesis by low energy laser irradiation. Antioxid Redox Signal 5:785–90

    Article  Google Scholar 

  33. Avni D, Levkovitz S, Maltz L, Oron U (2005) Protection of skeletal muscles from ischemic injury: low-level laser therapy increases antioxidant activity. Photomed Laser Surg 23(3):273–7

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Ashrafzadeh Takhtfooladi.

Ethics declarations

Ethical statement

The authors declare that this manuscript was prepared according to “Ethical Responsibilities of Authors” and it is an original unpublished article that does not transgress any copyright or intellectual property rights of other people, and it is not being evaluated for publication in other journals. The article has been read, and each contribution was approved.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takhtfooladi, H.A., Asghari, A., Amirkamali, S. et al. Evaluation of low-level laser therapy on skeletal muscle ischemia–reperfusion in streptozotocin-induced diabetic rats by assaying biochemical markers and histological changes. Lasers Med Sci 31, 1211–1217 (2016). https://doi.org/10.1007/s10103-016-1969-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-016-1969-9

Keywords

Navigation