Similar to the skin of higher vertebrates, reptile skin consists of an epidermis and dermis and acts as a physical barrier against pathogens and to prevent the loss of electrolytes and fluids. Integumentary injury is characterized initially by an inflammatory and vascular response. The inflammatory response in lizards may be minimal, compared with that in snakes.1,2 This is followed by a fibroblast response that is from the adjacent dermis, as opposed to the response in mammals that is from the underlying subcutaneous tissues.1,2 Restoration of the epidermis and maturation of the epithelium follow restoration of dermal integrity. The amount of scab formation can differ, with lizards generally forming little epithelial scab and snakes forming substantial scab. Mitotic activity of epidermal cells occurs only during times of ecdysis, which occurs simultaneously over the body in squamates (lizards and snakes).1,2
Although wound healing in reptiles occurs in the same general phases as that of mammals, it is at a slower rate, differs among reptilian species, and is affected by a variety of factors.2–4 The relatively slow rate of healing creates additional potential for contamination and bacterial colonization, which can delay wound healing.5 Wound healing in common garter snakes (Thamnophis sirtalis) is more rapid when animals are housed at the upper end of their preferred optimum temperature range,6 whereas restraint-associated stress in tree lizards (Urosauras ornatus) decreases healing of experimentally created cutaneous wounds.7 Other factors, such as the direction of an incision as well as the instrumentation used to create incisions, also affect wound healing in reptiles.1,5,8,9
Basic wound management of reptiles, including primary closure, healing by secondary intention, or delayed primary closure, parallels that of mammals, with irrigation, debridement, daily treatments, and bandaging considered standard practices.1,6,10 The type of wound management in both reptiles and other vertebrates can have important effects on wound healing.1 Because of the propensity for reptile skin to invert during the healing process, it is recommended that primary closure (if performed) be accomplished by the use of everting suture patterns, and recommendations for the most appropriate suture type for reptile skin have been reported.1,11 Healing by secondary intention may be more appropriate for certain wounds, such as those that are contaminated or are chronic in nature, although sequelae may include skin contracture, delayed wound healing, and incomplete epithelial coverage.1,2
A variety of modalities, including the use of topical treatments, wound dressings, and adjunct treatments, have been used in attempts to improve wound healing in reptiles. Use of topical antimicrobials and antiseptics have been documented in the human and veterinary literature and are typically aimed at a specific stage of the healing process. Assessment of the effects of various topical products as well as the use of various suture materials on wound healing in reptiles has revealed substantial variability, and some products have been found to delay wound healing.10 The variability in wound healing for products that are routinely used in nonreptilian patients supports the need for development of additional modalities for the treatment of wounds in reptiles. This is particularly true for wounds that heal by secondary intention.
Photobiomodulation has been used in both human and veterinary medicine because of its anti-inflammatory, analgesic, and wound-healing effects. Photobiomodulation improves the rate of healing in patients with epithelial trauma, musculoskeletal injuries, and chronic pain in multiple species, including rats,12 pigs,13 rabbits,14 and humans.15 By inducing a photochemical reaction at the cellular level, laser light stimulates a biochemical response that results in both local and systemic wound-healing effects. Absorption of photons by mitochondria of photo-responsive cells stimulates an increase in ATP,16,17 which makes energy available for a variety of cellular processes, including angiogenesis, fibroblast proliferation, transition of fibroblasts to myofibroblasts, collagen synthesis, and anti-inflammatory processes.18,19 Evidence for additional effects, such as analgesia and a reduction in edema, has been found in canine patients,20 and an increase in epithelialization in both primary- and secondary-intention healing has been reported for a variety of animals, including rabbits,21 rats,12 calves,22 humans,23 and pigs.13
Increased fibroblast proliferation and migration with a consequent increase in collagen production have also been attributed to laser treatment. Secondary effects of increased fibroblast production, including an increased rate of contraction of granulation tissue and increased tensile strength, have been reported in multiple studies24–26 on wound healing of rats. Despite the growing body of literature to support the clinical effects of photobiomodulation, studies27,28 of dogs revealed a lack of response to laser treatment when compared with control treatments. Additionally, there is evidence to support a decrease in wound healing with higher doses for laser treatments.29
Effects of photobiomodulation differ greatly depending on the wavelength, energy, energy density, duration, and delivery system.30 Discrepancies in results of wound-healing studies may be related to these variables, and it is difficult to make comparisons among studies because of the variability in treatment protocols. There is little information available on efficacy and safety of protocols for use of lasers in terms of wavelength, power, energy, and duration of treatment, particularly for exotic species. A recent study31 on the effects of photobiomodulation on primary-intention wound healing in ball pythons (Python reguis) revealed a significant improvement in collagen maturity at day 14, but there were no other significant improvements in wound healing during the 30-day study. Use of a laser for the treatment of skin and shell ulceration in a soft-shelled turtle (Pelodiscus sinensis)32 and for skin wounds in 2 species of chelonians (Testudo hermanni and Trachemys scripta)33 resulted in subjective improvements, but results were not verified by histologic examination.
The purpose of the study reported here was to investigate the effects of photobiomodulation on secondary-intention wound healing in green iguanas (Iguana iguana) and to compare effects with those for traditional topical treatments. We hypothesized that there would be no significant difference in healing among wounds regardless of treatment method.
Supported by The Pamela de Journo Endowment Fund at the University of Georgia and by LiteCure.
Presented in abstract form at the Exoticscon Conference, Portland, Ore, August-September 2016.
The authors thank Nia Chau for technical assistance.
Strictly Reptile Inc, Hollywood, Fla.
Silvion, Molecular Therapeutics LLC, Athens, Ga.
CTX therapy laser, provided by LiteCure, Newark, Del.
SAS, version 9.3, SAS Institute Inc, Cary, NC.
1. Mader DR, Bennett RA, Funk RS, et al. Surgery. In: Mader DR, ed. Reptile medicine and surgery. 2nd ed. St Louis: Saunders Elsevier, 2006;581–630.
3. Alibardi L. Ultrastructural features of the process of wound healing after tail and limb amputation in lizard. Acta Zoologica 2009;91:306–318.
4. Peacock HM, Gilbert EAB, Vickaryous MK. Scar-free cutaneous wound healing in the leopard gecko, Eublepharis macularius. J Anat 2015;227:596–610.
5. Smith DA, Barker IK. Healing of cutaneous wounds in the common garter snake (Thamnophis sirtalis). Can J Vet Res 1988;52:111–119.
6. Smith DA, Barker IK, Allen OB. The effect of ambient temperature and type of wound on healing of cutaneous wounds in the common garter snake (Thamnophis sirtalis). Can J Vet Res 1988;52:120–128.
7. French SS, Matt KS, Moore MC. The effects of stress on wound healing in male tree lizards (Urosaurus ornatus). Gen Comp Endocrinol 2006;145:128–132.
8. Hernández-Divers SJ, Stahl SJ, Rakich PM, et al. Comparison of CO(2) laser and 4.0 MHz radiosurgery for making incisions in the skin and muscles of green iguanas (Iguana iguana). Vet Rec 2009;164:13–16.
9. Hodshon RT, Sura PA, Schumacher JP, et al. Comparison of first-intention healing of carbon dioxide laser, 4.0-MHz radiosurgery, and scalpel incisions in ball pythons (Python regius). Am J Vet Res 2013;74:499–508.
10. Smith DA, Barker IK, Allen OB. The effect of certain topical medications on healing of cutaneous wounds in the common garter snake (Thamnophis sirtalis). Can J Vet Res 1988;52:129–133.
11. McFadden MS, Bennett RA, Kinsel MJ, et al. Evaluation of the histologic reactions to commonly used suture materials in the skin and musculature of ball pythons (Python regius). Am J Vet Res 2011;72:1397–1406.
12. Calisto FC, Calisto SL, Souza AP, et al. Use of low-power laser to assist the healing of traumatic wounds in rats. Acta Cir Bras 2015;30:204–208.
13. Figurová M, Valent L, Karasová M, et al. Histological assessment of a combined low-level laser/light-emitting diode therapy (685 nm/470 nm) for sutured skin incisions in a porcine model: a short report. Photomed Laser Surg 2016;34:53–55.
14. Hussein AJ, Alfars AA, Falih MA, et al. Effects of a low level laser on the acceleration of wound healing in rabbits. N Am J Med Sci 2011;3:193–197.
15. Ahmed Omar MT, Ebid A, El Morsy A. Treatment of post-mastectomy lymphedema with laser therapy: double blind placebo control randomized study. J Surg Res 2011;165:82–90.
17. Karu T. Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 1999;49:1–17.
18. Carvalho KC, Nicolau RA, Maia Filho AL, et al. Study of the strength of healing skin of rats treated with phototherapy in laser. Con Scientiae Saude 2010;9:179–186.
19. Gonçalves RV, Novaes RD, do Carmo Cupertino M, et al. Time-dependent effects of low-level laser therapy on the morphology and oxidative response in the skin wound healing in rats. Lasers Med Sci 2013;28:383–390.
20. Millis DM, Saunders DG. Laser therapy in canine rehabilitation. In: Millis DM, Levine D, eds. Canine rehabilitation and physical therapy. 2nd ed. St Louis: Saunders Elsevier, 2013;359–380.
21. Takhtfooladi MA, Sharifi D. A comparative study of red and blue light-emitting diodes and low-level laser in regeneration of the transected sciatic nerve after an end to end neurorrhaphy in rabbits. Lasers Med Sci 2015;30:2319–2324.
22. Bhowmick D, Bhargava MK. Cold laser irradiation for biostimulation of wounds—a histological and histochemical study in bovine calves. Intas Polivet 2015;16:26–31.
23. Chow RT, Johnson MI, Lopes-Martins RA, et al. Efficacy of low-level laser therapy in the management of neck pain: a systematic review and meta-analysis of randomised placebo or active-treatment controlled trials. Lancet 2009;374:1897–1908.
24. Dancáková L, Poláková M, Kovác I, et al. Low-level laser therapy at 808 nm increases tensile strength of healing skin wounds in rats. Folia Vet 2012;5:35–39.
25. Reddy GK, Stehno-Bittel L, Enwemeka CS. Laser photostimulation accelerates wound healing in diabetic rats. Wound Repair Regen 2001;9:248–255.
26. Rezende SB, Ribeiro MS, Núñez SC, et al. Effects of a single near-infrared laser treatment on cutaneous wound healing: biometrical and histological study in rats. J Photochem Photobiol B 2007;87:145–153.
27. Kurach LM, Stanley BJ, Gazzola KM, et al. The effect of low-level laser therapy on the healing of open wounds in dogs. Vet Surg 2015;44:988–996.
28. Stich AN, Rosenkrantz WS, Griffin CE. Clinical efficacy of low-level laser therapy on localized canine atopic dermatitis severity score and localized pruritic visual analog score in pedal pruritus due to canine atopic dermatitis. Vet Dermatol 2014;25:464–e74.
29. Mendez TM, Pinheiro AL, Pacheco MT, et al. Dose and wavelength of laser light have influence on the repair of cutaneous wounds. J Clin Laser Med Surg 2004;22:19–25.
30. Hirata K, Kawabuchi M. Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc Res Tech 2002;57:541–547.
31. Cole GL, Lux CN, Schumacher JP, et al. Effect of laser treatment on first-intention incisional wound healing in ball pythons (Python regius). Am J Vet Res 2015;76:904–912.
32. Kraut S, Fischer D, Heuser W, et al. Laser therapy in a soft-shelled turtle (Pelodiscus sinensis) for the treatment of skin and shell ulceration. A case report. Tierarztl Prax Ausg K Kleintiere Heimtiere 2013;41:261–266.
34. Enwemeka CS, Parker JC, Dowdy DS, et al. The efficacy of low-power lasers in tissue repair and pain control: a meta-analysis study. Photomed Laser Surg 2004;22:323–329.
36. Ghamsari SM, Taguchi K, Abe N, et al. Evaluation of low level laser therapy on primary healing of experimentally induced full thickness teat wounds in dairy cattle. Vet Surg 1997;26:114–120.
37. Vasilenko T, Slezak M, Kovác I, et al. The effect of equal daily dose achieved by different power densities of low-level laser therapy at 635 and 670 nm on wound tensile strength in rats: a short report. Photomed Laser Surg 2010;28:281–283.
38. Cho Lee AR, Leem H, Lee J, et al. Reversal of silver sulfadiazine-impaired wound healing by epidermal growth factor. Biomaterials 2005;26:4670–4676.
39. Leitch IO, Kucukcelebi A, Robson MC. Inhibition of wound contraction by topical antimicrobials. Aust N Z J Surg 1993;63:289–293.
40. Muller MJ, Hollyoak MA, Moaveni Z, et al. Retardation of wound healing by silver sulfadiazine is reversed by Aloe vera and nystatin. Burns 2003;29:834–836.
41. Park MV, Neigh AM, Vermeulen JP, et al. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 2011;32:9810–9817.
42. Yaman I, Durmus AS, Ceribasi SM, et al. Effects of Nigella sativa and silver sulfadiazine on burn wound healing in rats. Vet Med 2010;55:619–624.
43. Rodrigo SM, Cunha A, Pozza DH, et al. Analysis of the systemic effect of red and infrared laser therapy on wound repair. Photomed Laser Surg 2009;27:929–935.
44. Schindl A, Heinze G, Schindl M, et al. Systemic effects of low-intensity laser irradiation on skin microcirculation in patients with diabetic microangiopathy. Microvasc Res 2002;64:240–246.
45. Smith J. 8 Whys, whens, and hows for deep tissue applicator (on contact) laser therapy. Available at: www.litecure.com/companion/laser-therapy. Accessed Feb 23, 2016.
Histologic assessment of epithelial wounds in green iguanas (Iguana iguana).
|Epidermis||Ulceration||Absent or present|
|Bacteria*||Absent or present|
|Reepithelialization||0 = Absent, 1 = mild (regular, thin epithelial migration with no rete ridges), 2 = partial (irregular, thickened epithelial projections with rete ridges), or 3 = complete (complete epithelial migration)|
|Dermis||Necrosis||Absent or present|
|Inflammation||0 = Absent, 1 = mild (scattered perivascular accumulations of inflammatory cells), 2 = moderate (perivascular and interstitial accumulations of inflammatory cells), or 3 = severe (coalescing areas of perivascular and interstitial accumulations of inflammatory cells)|
|Fibrosis†||0 = Absent, 1 = mild (scattered fibers), 2 = moderate (collagen fibers accumulated in the dermis), or 3 = severe (accumulated collagen fibers and distorted adjacent tissues)|
|Collagen maturity†||1 = Immature (thin, wispy, light blue-stained collagen), 2 = moderately mature (scattered, blue-stained collagen bundles), or 3 = mature (thick blue-stained collagen bundles similar to adjacent normal dermis)|
Visual detection of large aggregates of bacteria on the epidermis or ulcer surface.
Assessed by use of Masson trichrome stain.