Effect of 630 nm Light Emitting Diode (LED) Irradiation on Wound Healing in Streptozotocin-Induced Diabetic Rats

  • JeKal, Seung-Joo (Department of Clinical Laboratory Science, Wonkwang Health Science University) ;
  • Kwon, Pil-Seung (Department of Clinical Laboratory Science, Wonkwang Health Science University) ;
  • Kim, Jin-Kyung (Vestibulocochlear Research Center & Department of Microbiology, College of Medicine, Wonkwang University, School of Medicine)
  • Received : 2010.11.19
  • Accepted : 2010.12.20
  • Published : 2010.12.31

Abstract

The purpose of this study was to clarify the effect of light emitting diode (LED) irradiation on healing of impaired wound and alteration of mast cells in experimental diabetic rats. Twenty-four male Sprague-Dawley rats were divided into four groups: excision (Ex), excision-LED irradiation (Ex-LED), diabetes + excision (DM) and diabetes + excision + LED irradiation (DM-LED). Diabetes was induced in rats by streptozotocin (STZ) injection (70 mg/kg, single dose) and 6 mm punch excision wounds were created on the back after shaving hair. The LED-irradiated rats were treated to a daily dose of $5\;J/cm^2$ LED (630 nm) light for 11 days after surgery, and were killed at day 1, 3, 7 and 11. The lesion and adjacent skin tissues were excised, fixed with 10% buffered formalin and embedded with paraffin. For evaluation of wound healing, hematoxylin-eosin (HE) and Masson trichrome staining were performed. Mast cells (MCs) were stained with toluidine blue (pH 0.5) and quantified using a computerized image analysis system. The proliferation activity of keratinocyte in skin tissues was analyzed on sections immunostained with proliferative cell nuclear antigen (PCNA). The results showed that wound healing rate, collagen density and neo-epidermis length, number of PCNA-positive cells, fibroblasts and mast cells were significantly higher in the LED-irradiated rats than in the DM and Ex rats throughout the periods of experiment. Exceptionally, the number of MCs was significantly lower at day 11 compared with day 7 after surgery in the all groups. These findings suggest that the LED irradiation may promote the tissue repair process by accelerating keratinocyte and fibroblast proliferation and collagen production in normal rats as well as in diabetic rats, and MCs may play an important role at an early stage of skin wound healing in normal and diabetic rats.

Keywords

References

  1. Allendorf JD, Bessler M, Huang J, Kayton ML, Laird D, Nowygrod R, Treat MR. Helium-neon laser irradiation at fluences of 1, 2, and 4 J/$cm^2$ failed to accelerate wound healing as assessed by both wound contracture rate and tensile strength. Lasers Surg Med. 1997.20: 340-345. https://doi.org/10.1002/(SICI)1096-9101(1997)20:3<340::AID-LSM13>3.0.CO;2-H
  2. Blakytny R, Jude E. The molecular biology of chronic wounds and delayed healing in diabetes. Diabet Med. 2006. 23: 594-608. https://doi.org/10.1111/j.1464-5491.2006.01773.x
  3. Barolet D. Light-Emitting Diodes (LEDs) in Dermatology. Semin Cutan Med Surg. 2008. 27: 227-238. https://doi.org/10.1016/j.sder.2008.08.003
  4. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest. 2007. 117: 1219-1222. https://doi.org/10.1172/JCI32169
  5. Connelly K, Kelly D, Gilbert R. Clinically relevant models of diabetic cardiac complications. Circ Res. 2007. 101: 78-80. https://doi.org/10.1161/CIRCRESAHA.106.147264
  6. Dall Agnol MA, Nicolau RA, de Lima CJ, Munin E. Comparative analysis of coherent light action (laser) versus non-coherent light (light-emitting diode) for tissue repair in diabetic rats. Lasers Med Sci. 2009. 24: 909-916. https://doi.org/10.1007/s10103-009-0648-5
  7. Enerback L. Mast cells in rat gastrointestinal tract: Effect of fIxation. Acta Pathol Microbiol Scand. 1966.66: 289-302.
  8. Fahey TJ 3rd, Sadaty A, Jones WG 2nd, Barber A, Smoller B, Shries GT. Diabetes impairs the late inflammatory response to wound healing. J Surg Res. 1991. 50: 308-313. https://doi.org/10.1016/0022-4804(91)90196-S
  9. Goodson WH 3rd, Hung TK. Studies of wound healing in experimental diabetes mellitus. J Surg Res. 1977. 22: 221-227. https://doi.org/10.1016/0022-4804(77)90137-8
  10. Hamblin MR, Demidova TN. Mechanisms for Low-Light Therapy. Proc SPIE. 2006. 6140: 1-12.
  11. Iba Y, Shibata A, Kato M, Masukawa T. Possible involvement of mast cells in collagen remodeling in the late phase of cutaneous wound healing in mice. Int Immunopharmacol. 2004. 4: 1873-1880. https://doi.org/10.1016/j.intimp.2004.08.009
  12. Jekal SJ, Lee KS, Chung OB, Lee JH. Effects of Electrical Stimulation on Wound Healing and Skin Mast Cells in Streptozotocin-Induced Diabetic Rats. Korean J Clin Lab Sci. 2008.40: 118-128.
  13. Kalka K, Merk H, Mukhtar H. Photodynamic Therapy in Dermatology. J Am Acad Dermatol. 2000. 42: 389-413. https://doi.org/10.1016/S0190-9622(00)90209-3
  14. Karu T. Primary and secondary mechanisms of action of visible to near-lR radiation on cells. J Photochem Photobiol B. 1999. 49: 1-17. https://doi.org/10.1016/S1011-1344(98)00219-X
  15. Katayama I, Yokozeki H, Nishioka K. Mast-cell-derived mediators induce epidermal cell proliferation: clue for lichenifIed skin lesion formation in atopic dermatitis. Int Arch Allergy Immunol. 1992.98: 410-414. https://doi.org/10.1159/000236218
  16. Khan AA, Banwell PE, Bakker MC, Gillespie PG, McGrouther DA, Roberts AH. Topical radiant heating in wound healing: an experimental study in a donor site wound model. Int Wound J. 2004. 1: 233-240. https://doi.org/10.1111/j.1742-4801.2004.00065.x
  17. Klebanov GI, Shuraeva NIu, Chichuk TV, Osipov AN, Vladimirov luA. Comparison of the effects of laser and light-emitting diodes on lipid peroxidation in rat wound exudate. BiofIzika. 2006.51: 332-339.
  18. Lee SY, Park KH, Choi JW, Kwon JK, Lee DR, Shin MS, Lee JS, You CE, Park MY. A Prospective, Randomized, Place-bocontrolled, Double-blinded, and Split-face Clinical Study on LED Phototherapy tor Skin Rejuvenation: Clinical, Profilometric, Histologic, Ultrastructural, and Biochemical Evaluations and Comparison of Three Different Treatment Settings. J Photochem Photobiol. B. 2007. 27: 51-67.
  19. Leibovich J, Martin P. Inflammatory cells during wound repair: The good, the bad and the ugly. Trends Cell Biol. 2005. 15: 599-607. https://doi.org/10.1016/j.tcb.2005.09.002
  20. Lim W, Lee S, Kim I, Chung M, Kim M, Lim H, Park J, Kim O, Choi H. The Anti-inflammatory Mechanism of 635nm light-emitting diode irradiation compared with existing COX Inhibitors. Lasers Surg Med. 2007. 39: 614-621. https://doi.org/10.1002/lsm.20533
  21. Maurer M, Opitz M, Hens BM, Paus R. The mast cell products histamine and serotonin stimulate and TNF-alpha inhibits the proliferation of murine epidermal keratinocytes in situ. J Dermatol Sci. 1997. 16: 79-84. https://doi.org/10.1016/S0923-1811(97)00043-1
  22. Miller EJ. Biochemical characteristics and biologieal significance of the genetically-distinct collagens. Mol Cell Biochem. 1976. 13: 165-192. https://doi.org/10.1007/BF01731779
  23. Nienartowicz A, Sobaniec-Lotowsk ME, Jarocka-Cytra E, Lemancewicz D. Mast cells in neoangiogenesis. Med Sci Monit. 2006. 12: 53-56.
  24. Nishikor Y, Kakizoo E, Kobayashi Y, Shimoura K, Okunishi H, Dekio S. Skin mast cell promotion of matrix remodeling in bum wound healing in mice: Relevance of chymase. Arch Dermatol Res. 1998. 290: 553-560. https://doi.org/10.1007/s004030050351
  25. Passarella S, Casamassima E, Molinari S, Pastore D, Quagliariello E, Catalano IM, Cingolani A. Increase of proton electrochemical potential and ATP synthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett. 1984. 175: 95-99. https://doi.org/10.1016/0014-5793(84)80577-3
  26. Pessoa ES, Melhado RM, Theodoro LH, Garcia VG. A histologic assessment of the influence of low-intensity laser therapy on wound healing in steroid-treated animals. Photomed Laser Surg. 2004. 22: 199-204. https://doi.org/10.1089/1549541041438533
  27. Petersen SL, Botes C, Olivier A, Guthrie AJ. The effect of low level laser therapy (LLLT) on wound healing in horses. Equine Vet J. 1999.31: 228-231. https://doi.org/10.1111/j.2042-3306.1999.tb03177.x
  28. Posten W, Wrone DA, Dover JS, Arndt KA, Silapunt S, Alam M. Low-level laser therapy for wound healing: mechanism and efficacy. Dermatol Surg. 2005. 31: 334-340.
  29. Rabelo SB, Villaverde AB, Nieolau R, Salgado MC, Melo Mda S, Pacheco M1: Comparison between wound healing in induced diabetic and nondiabetic rats after low-level laser therapy. Photomed Laser Surg. 2006. 24: 474-479. https://doi.org/10.1089/pho.2006.24.474
  30. Schlager A, Kronberger P, Petschke F, Ulmer H. Low-power laser light in the healing of bums: a comparison between two different wavelengths (635 nm and 690 nm) and a placebo group. Lasers Surg Med. 2000. 27: 39-42. https://doi.org/10.1002/1096-9101(2000)27:1<39::AID-LSM5>3.0.CO;2-4
  31. Simpson CR, Kohl M, Essenpreis M, Cope M. Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique. Phys Med Biol. 1998.43: 2465-2478. https://doi.org/10.1088/0031-9155/43/9/003
  32. Singer AJ, Clark- RA. Cutaneous wound healing. N Engl J Med. 1999. 341: 738-746. https://doi.org/10.1056/NEJM199909023411006
  33. Souil E, Capon A, Mordon S, Dinh-Xuan AT, Polla BS, Bachelet M. Treatment with 815-nm diode laser induces long-lasting expression of 72-kDa heat shock protein in normal rat skin. Br J Dermatol. 2001. 144: 260-266. https://doi.org/10.1046/j.1365-2133.2001.04010.x
  34. Stallmeyer B, Kampfer H, Kolb N, Pfeilschifter J, Frank S. The function of nitric oxide in wound repair: inhibition of inducible nitric oxide-synthase severely impairs wound reepithelialization. J Invest Dermatol. 1999. 113: 1090-1093. https://doi.org/10.1046/j.1523-1747.1999.00784.x
  35. Tada K, Ikeda K, Tomita K Effect of polarized light emitting diode irradiation on wound healing. J Trauma. 2009. 67: 1073-1079. https://doi.org/10.1097/TA.0b013e318187ad02
  36. Trautmann A, Toksoy A, Engelhardt E, Brocker EG. Mast cell involvement in normal human skin wound healing: Expression of monocyte chemoattractant protein-l is corrected with recruitment of mast cells which synthesize interleukin-4 in vivo. J Pathol. 2000. 190: 100-106. https://doi.org/10.1002/(SICI)1096-9896(200001)190:1<100::AID-PATH496>3.0.CO;2-Q
  37. Tsuboi R, Shi CM, Rifkin DB, Ogawa H. A wound healing model using healing-impaired diabetic mice. J Dermatol. 1992. 19: 673-675.
  38. Vasheghani MM, Bayat M, Rezaei F, Bayat A, Karimipour M. Effect of low-level laser therapy on mast cells in second-degree bums in rats. Photomed Laser Surg. 2008. 26: 1-5. https://doi.org/10.1089/pho.2007.2103
  39. Walker MD, Rumpf S, Baxter GD, Hirst DG, Lowe AS. Effect of low-intensity laser irradiation (660 nm) on a radiation-impaired wound-healing model in murine skin. Lasers Surg Med. 2000.26:41-47. https://doi.org/10.1002/(SICI)1096-9101(2000)26:1<41::AID-LSM7>3.0.CO;2-M
  40. Wong-Riley MT, Liang HL, Eells JT, Chance B, Henry MM, Buchmann E, Kane M, Whelan HT. Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J Biol Chem. 2005. 280: 4761-4771.
  41. Xia Z, Sato A, Hughes MA, Cherry GW. Stimulation of fibroblast growth in vitro by intermittent radiant warming. Wound Repair Regen. Int Wound J. 2004. 1: 233-240.