EXOTICS

Case study: successful fight wound management in a Tunisian eyed ( pater)

Extensive fight wounds are common in co-habiting . This case study describes the management of a large fight wound in a 1-year-old entire female Tunisian eyed lizard. Primary closure was initially attempted but subsequent postoperative infection and wound breakdown led to successful management by secondary intention healing. This case demonstrates the amazing capacity for healing of large integument defects in that receive appropriate medical support. https://doi.org/10.12968/coan.2019.0044

Krissy Green BVM&S BSc (Hons) MSc CertAVP (ZooMed) MRCVS, RCVS Recognised Advanced Practitioner, Ark Veterinary Clinics, 479-481 Main Street, Coatbridge, ML5 3RD. [email protected]

Key words: fight wound management | primary closure | | secondary wound healing

unisian eyed lizards (Timon pater), a member of the stratum corneum layers under the old skin. Enzymes dissolve the lacertid family, are native to North Africa. Inquisitive, connection between the new and old intermediate zones and the relatively easy to care for and tame, they make space fills with lymph, resulting in shedding of old skin. During rewarding pets. Groups of males and male-female times of growth and regeneration the resting phase time decreases Tpairs cohabit successively; however, housing females together and reptiles shed more frequently. often results in physical aggression and fight wounds. This case study looks at the management of an extensive full skin thickness Reptile wound healing fight wound covering two-thirds of the dorsolateral body wall of a Although the stages of mammalian and reptile wound healing 1-year-old entire female Tunisian eyed lizard. are similar, reptile skin has been reported to heal more slowly (Mickelson et al, 2016). Following damage there is an initial The reptile integument vascular ‘coagulation’ phase, in which vasoconstriction occurs Reptile skin comprises scales arranged in regular geometric and a fibrin clot is produced through platelet-mediated activation patterns, with a superficial keratinised epidermis and underlying of the intrinsic clotting cascade. Damaged tissue produces supporting dermis. Scales are attached to the underlying proinflammatory cytokines, which attract polymorphonuclear musculature by thin connective tissue. The epidermis comprises leukocytes, endothelial cells and fibroblasts to the wound in three layers: the stratum corneum, intermediate zone, and stratum preparation for the ‘inflammatory and debridement’ phase. germinativum. The outer stratum corneum is made from alpha This second phase is characterised by increased blood flow and and beta keratin and covered with the ‘oberhautchen’, a heavily migration of white blood cells into the wound to remove debris, keratinised, acellular serrated surface (Maas, 2013). Scales foreign material and infecting microorganisms, ready for repair, originate from the underlying stratum germinativum, a basal layer and may persist for weeks in poor wound environments. of progenitor columnar epithelium, and receives nourishment In the third, ‘proliferative’, phase there is re-epithelisation, from the dermis. granulation, angiogenesis, fibroplasia, and subsequent repair Growth and maintenance of normal healthy reptile skin is and restoration of dermal integrity. In contrast to mammals, through a cyclic physiological process called ecdysis (Mitchell fibroblastic response originates in the dermis adjacent to the and Diaz-Figueroa, 2004), commonly known as skin shedding. defect rather than from the ventral subcutaneous tissues, and This consists of renewal and resting phases. Ecdysis begins lizards do not form a significant epithelial scab (Maderson and

© 2019 MA Healthcare Ltd MA Healthcare © 2019 when the stratum germinativum forms new intermediate and Roth, 1972). The final ‘remodelling’ phase may persist for weeks to

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months; it involves restoration and maturation of epidermis and Microbiologic samples for bacterial or fungal culture should be dermis through collagen and extracellular matrix organisation, submitted as appropriate. wound contraction and scar maturation. Fight wound preparation Factors affecting wound healing Similarly to mammals, the initial goal of wound care is to prevent Reptiles are ectothermic and rely on varying their environment to further contamination and convert contaminated or dirty wounds regulate core body temperature and subsequently all physiological into clean wounds suitable for immediate or delayed surgical processes including immune system function and wound closure, or healing by secondary intention. Large open wounds healing (Mickelson et al, 2016). Reptiles not exposed to optimal should be assessed and debrided under -appropriate temperature, light and humidity gradients, nor given sufficient anaesthesia and analgesia. Initially wounds should be lavaged privacy, may experience delayed wound healing, therefore a with copious volumes of warmed, physiologically balanced fluids thorough history should be obtained. An environmental history to assist removal of foreign material and aid determination of the should include photographs of the reptile’s enclosure and records gross demarcation between viable and nonviable necrotic tissues. of environmental temperatures. Individuals receiving suboptimal Nonviable tissues should be debrided using sharp excision, while nutrition, suffering concurrent disease or suffering secondary taking care to preserve subdermal vascular supply. The wounds bacterial and fungal infections may experience extended wound should then be flushed again. healing or non-healing wounds. Aggressive debridement can facilitate regeneration of epithelium; however, in small patients with large wounds, Approach to a reptile fight wound case particular care should be taken not to remove viable tissue. The approach to wound management should consider species Nonviable tissue may appear necrotic, shrivelled and dark or behaviour, temperament, anatomy and size, and possible secondary there may be a slough of devitalised tissue, white blood cells and stress- related complications. Subsequent to obtaining the wound debris. This slough may appear soft or leathery and be patient’s history, a full clinical examination should be undertaken. yellow-white or discoloured yellow-brown (Nichols, 2015). Tissue Fractious and those in pain should be examined under of questionable viability can be left in situ and reassessed 24–48 general anaesthesia. Manipulating dermatological injuries can hours later, when the extent of tissue necrosis is more apparent, be painful, therefore appropriate species-specific multi-modal and repeat debridement performed as required. analgesia should be provided. This may include non-steroidal anti- inflammatory drugs (NSAIDs), opioids and local anaesthetics. Surgical wound closure The field of reptile analgesia is rapidly evolving (Sladky and Following irrigation and debridement, wounds can be assessed Mans, 2014; Sladky, 2019). Reptiles are adept at hiding pain, so for suitability for surgical closure, whereby appositional healing its recognition requires knowledge of the species and individual is achieved by suturing the edges of the wound together. Surgical concerned. In summary, there is currently no efficacy data for closure is generally recommended when a wound is clean, with NSAIDs in lizards, therefore dose and frequency are extrapolated minimal trauma and contamination and less than 12 hours old. from mammalian medicine. Similar deleterious side effects are However, many injury and patient specific factors need to be assumed to apply, so assessment of suitability for use should be considered before attempting primary wound closure of a reptile made for each individual patient. While opioid receptors are fight wound (Di Girolamo and Mans, 2016). expressed in reptiles, further studies are required to understand Wound specific factors include: the efficacy of commonly used opioid dugs in these species zzThe degree of contamination (Sladky and Mans, 2014). The current literature suggests that the zzThe age of the injury optimum analgesia for lizards is obtained using μ-receptor opioids. zzExtent of devitalisation of wound edges and ability to debride However, respiratory depression may occur with these; this effect zzThe location of wound is less pronounced with tramadol. Topical administration of local zzThe extent of soft tissue loss and extent of dead space anaesthetic drugs is commonly used before and after wound zzThe availability of adjacent tissue for wound closure or debridement. possibility of skin flaps or grafts Reptiles with large surface area defects can suffer loss of essential zzThe tension present on the closed wound electrolytes and fluids, therefore fluid replacement therapy should zzThe preservation of blood supply and good haemostasis. be undertaken as required. Fluids replacement may use the oral, Patients specific factors include: subcutaneous, intravenous, intraosseous or intracoelomic routes. zzIndividual health status and ability to withstand anaesthesia Oral rehydration and nutritional support with a reptile-specific zzIndividual capacity to tolerate open vs closed wounds product such as Critical Care Formula (Vetark, Winchester) or zzThe patient’s living environment and preferred optimum a species-appropriate Emeraid® Intensive Care Product (Lafeber, temperature zone (POTZ), Swindon) with the patient at optimal body temperature is ideal zzOwner compliance and ability to manage an open versus a providing a functional gastrointestinal tract. Individuals in a closed wound. catabolic state will have higher calorific requirements. Historically, monofilament suture materials that retain their Radiographs and blood samples for biochemistry and tensile strength for prolonged periods have been used in the

haematology should be taken if concurrent disease is suspected. reptile integument; however, materials considered suitable Ltd MA Healthcare © 2019

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for use in mammalian skin can be used and similar selection Adjuncts to wound healing criteria can be applied. McFadden (2011) summarised the The principles of optimising secondary intention healing in recent literature on suture material choice in reptiles. All suture lizards are similar to those for small mammals (Mitchell and materials reviewed caused a chronic inflammatory response, Diaz-Figueroa, 2004). However, optimal temperature gradients with monofilament absorbable suture material being the least for reptiles can result in desiccation of wounds and damage to reactive histologically. No suture material is absorbed by day 90, granulating tissue if inappropriately managed. Wounds should be suggesting a prolonged absorption time in reptiles compared to covered to protect against desiccation, as this may result in arrested mammals; suture extrusion often takes place before absorption wound healing and secondary infections. Infection stimulates an and this should be considered when selecting suture material. immune response characterised by invasion of inflammatory cells Reptile skin should be closed using an everting suture pattern, and release of enzymes and cytokines, which leads to indiscriminate such as horizontal mattress sutures, to counteract the tendency destruction of host tissues, and subsequently prolonged wound to invert after incision. healing. Hydrocolloids or hydrogel dressings absorb fluid from wounds and provide favourable environments for epithelisation and Secondary wound closure and adjuncts to for angiogenesis, which promotes granulation. Topical dressings healing limit opportunistic infections and prevent desiccation under If a wound is unsuitable for surgical closure then secondary environmental lighting, thus facilitate reptile wound healing. wound closure may be applied. This is appropriate for example in cases with large skin defects where the wound edges cannot Case study be opposed; contaminated wounds; or extensively devitalised A 1-year-old entire female Tunisian eyed lizard presented with wounds (Mickelson et al, 2016). This process requires formation extensive full skin thickness fight wounds covering two-thirds of granulation tissue matrix and wound contracture, which can of the left dorsolateral body wall 24 hours after fighting with a take weeks to months. Secondary intention healing may result female cage mate. To allow thorough examination, the lizard in prolonged healing times and functional deformities. Lizards was anaesthetised in a Stewarts® plastic induction chamber maybe particularly intolerant to the latter if contractures using 5% cent isoflurane (IsoFlo, Abbott, Abbott Park (IL)) in affect mobility. 100% oxygen. She was intubated using an 18-gauge intravenous

a b

c d Figure 1. Wound management in the first week following fight wound injury. The figure shows the progress of the wound in week one. (a) The degree of environmental contamination of the wound on presentation at the referring veterinary surgeon; (b) the wound after extensive lavage under anaesthetic. Some damage to underlying musculature can be seen cranially but body wall remains intact.

© 2019 MA Healthcare Ltd MA Healthcare © 2019 Primary closure was possible and seen in (c); (d) day 6, 2 days before wound breakdown.

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cannula (AniCath, Millpledge, Clarborough) attached to Ayres’ skin would act as a temporary ‘biological bandage’. Therefore, T-piece anaesthetic circuit with Jackson Rees’ modification. leaving the wound to heal by secondary intention was not chosen She was maintained on 2% isoflurane in 100% oxygen, using at this time. positive pressure ventilation throughout the procedure. A splash Surgical debridement was carried out and the wound closed block of lidocaine hydrochloride 2% (Hameln Pharmaceuticals, with horizontal mattress sutures using 5.0 polydioxanone (PDS, Gloucester) was performed before and after pressure lavage of Ethicon, USA). To minimise tension, three relief incisions were wounds. Lavage was performed for 20 minutes with warmed made dorsally in the skin, parallel to the suture line, between lactated Ringer’s solution using a 20 ml syringe with a 16-gauge scales. Surgical recovery was uneventful. The patient was hypodermic needle. Available injectable analgesics were used: hospitalised for 24 hours for assisted tube feeding with a critical 0.2 mg/kg meloxicam (Metacam, Boehringer Ingleheim, Bracknell) care nutrition product (Emeraid® Carnivore, Lafeber, Swindon) and 0.1 mg/kg buprenorphine (Vetegesic, Ceva, Amersham), given until normal eating resumed. The lizard was discharged on intramuscularly (IM) for multimodal analgesia. meloxicam (Metacam, Boehringer Ingleheim, Bracknell) (0.2 mg/ Following lavage, the extent of the wound was assessed kg PO SID), tramadol (MercuryPharma, London) (10 mg/kg PO (Figure 1). The wound ran from ventrocaudal to the left axilla BID) and ceftazidime (Ceftazidime, Frescenius Kabi, Runcorn) to the dorsal midline and along three-quarters of the body wall. 20 mg/kg every 72 hours by IM injection. The high frequency of There was some damage to the underlying musculature cranially, tramadol dosing was determined by subjectively monitoring of but the body wall was intact. Although the injury was 24 hours this individual patient for behavioural indicators of pain such as old, a decision to attempt primary closure was made because of inappetence, activity levels and ease of mobility. Relief incisions the large integument defect present and concerns that secondary were protected from desiccation using Intrasite® Gel Applipak® healing may result in excessive contracture and reduced movement (Smith and Nephew, Hull) daily. These were not covered. The under the axilla. Although the possibility of wound breakdown lizard was kept isolated from the group, on paper substrate. She was significant, the potential benefits of primary closure were remained bright and very active, so close observation for wound considered to be higher than the risks; should the wound break breakdown was undertaken. down the underlying musculature would still benefit from being After 8 days the wound broke down cranially and under the covered by the integument for the interim time period and the axilla (Figure 2a). Because of extensive tissue devitalisation and

a b

c d

Figure 2. Progress of the fight wound after the failure of primary wound closure a week after surgery. (a) Day 8: necrosis of the skin is present cranially and under the axilla. The tissue underneath appears healthy; (b) devitalised tissue can be seen sloughing in this photograph taken on day 20 and the edges of the wound are already beginning to granulate; (c) on day 27 all the devitalised skin tissue

has been sloughed and the wound is granulating; (d) epithelisation of the wound on day 40. Ltd MA Healthcare © 2019

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An amorphous hydrogel wound dressing (Intrasite, Smith and Nephew, Hull), was applied to aid autolytic debridement of necrotic tissue and promote secondary wound healing by maintaining an optimal moist environment. This hydrogel was non-adherent and did not harm viable tissue or surrounding skin. Weekly cleaning and dressing changes were performed with the lizard conscious. The wound was covered with a modified Primapore™ 10 cm×8 cm dressing (Smith and Nephew, Hull) (Figure 3). The wound progressed from necrotic to epithelised in approximately one month (Figure 2). Following wound breakdown, healthy granulation tissue was already apparent beneath devitalised tissue. Non-viable tissue was sloughing by day 20 and the fibroblastic response in the injured integument could be seen originating lateral to the adjacent dermis; this contrasts to mammals where it originates from the ventral subcutaneous Figure 3. Using a dressing to protect the fight wound from the tissues (Figure 2b). All devitalised skin tissue had sloughed and environment and to aid secondary intention healing. The optimal wound was granulating well by day 27 (Figure 2c). The wound had temperature gradients for reptiles can result in desiccation of the fully epithelised by day 40 (Figure 2d). The dressing was removed wound and damage to the granulation bed if the wound is not and all medication stopped on day 48, after which a staged appropriately managed. reintroduction to an all-male group was undertaken successfully. The aggression perpetrator, another female previously included in inability for the resulting defect to be closed, management by the group, was rehomed. secondary intention healing was opted for. Deep to the necrotic skin a healthy granulation bed was noted. Discussion A microbiological swab was taken for culture and sensitivity; This case demonstrates the amazing capacity that reptile skin has a heavy growth of Klebsiella pneumoniae was cultured and for healing and re-epithelisation. Two disadvantages of secondary found resistant to the initial antibiotic selected. The antibiotic intention wound closure reported are increased healing time and was changed to amikacin (Amikin, 100 mg/2mL, Bristol-Myers formation of a fragile epithelial scar. However, with supportive Squibb Pharmaceuticals, Uxbridge) (initially 5 mg/kg IM, then care this wound reached full epithelisation in one month. The time 2.5 mg/kg every 72 hours). required for primary oppositional wound healing in reptiles has The necrotic contaminated wound was prepared for secondary been estimated to be 8–10 weeks, therefore no increase in healing healing by flushing with warmed lactated Ringer’s solution. time occurred in this case. Figure 4 illustrates the progression

a b c

d e f

Figure 4. (a–f) The progression of wound healing following epithelisation from day 50 until day 300. (b) At day 60 shows the healing area undergoing ecdysis (shedding). Progression is then shown at day 112, 156 and 210 (c–e). In (f) return of most of the pattern,

© 2019 MA Healthcare Ltd MA Healthcare © 2019 pigmentation and scaling of the integument can be seen

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Conclusions KEY POINTS Treatment protocols for wounds in mammals can be adapted for llConsideration should be given to husbandry and social structure use in reptiles. Large wounds of the integument can heal of reptiles housed together; individuals should be separated should successfully by secondary intention without prolonged healing aggression occur. times if managed appropriately, within a POTZ, and with species- llReptile skin has an amazing regenerative capacity when managed appropriate pain relief and effective antibiosis based on culture appropriately within a Preferred Optimum Temperature Zone. and sensitivity. CA llAppropriate species-specific pain relief, and antibiosis based on culture and sensitivity should be instigated. Conflict of interest: no conflict of interest. llLarge wounds of the integument can successfully be managed for secondary intention healing in a similar time frame to wounds References undergoing primary closure in reptiles. Di Girolamo N, Mans C. Reptile soft tissue surgery. Vet Clin North Am Exot Anim Pract. 2016;19(1):97–131. https://doi.org/10.1016/j.cvex.2015.08.010 Nichols, E. Describing a wound from presentation to healing. Wound Essentials. 2015;10(1):56-61. Available at: https://www.wounds-uk.com/journal. (Accessed 2 November 2019) of wound healing following epithelisation from Day 50 until Maas AK. Vesicular, ulcerative, and necrotic dermatitis of reptiles. Vet Clin North Am Exot Anim Pract. 2013;16(3):737–755. https://doi.org/10.1016/j. Day 300. The final photograph shows return of most of the cvex.2013.05.007 pattern, pigmentation and scaling of the integument, rather than Maderson PFA, Roth SI. A histological study of early stages of cutaneous wound healing in lizards in vivo and in vitro. J Exp Zool. 1972;180(2):175–186. https:// formation of fragile scar tissue. doi.org/10.1002/jez.1401800205 In mammals, use of pain management to facilitate wound McFadden MS. Suture materials and suture selection for use in exotic pet surgical procedures. J Exot Pet Med. 2011;20(3):173–181. https://doi.org/10.1053/j. healing, reduce morbidity and mortality and contribute to rapid jepm.2011.04.003 return to normal behaviour is well documented. However, pain Mickelson MA, Mans C, Colopy SA. Principles of wound management and wound healing in exotic pets. Vet Clin North Am Exot Anim Pract. 2016;19(1):33–35. assessment and pain relief protocols are still in relative infancy https://doi.org/10.1016/j.cvex.2015.08.002 in reptiles, therefore understanding of the normal behaviour of Mitchell MA, Diaz-Figueroa O. Wound management in reptiles. Vet Clin North Am Exot Anim Pract. 2004;7(1):123–140. https://doi.org/10.1016/j.cvex.2003.08.006 a given species is particularly important. The patient remained Sladky KK. Chapter 60: Reptile and amphibian analgesia. In: Miller RE, Lamberski bright and active throughout treatment, making the timing of N, Calle PP (eds). Fowler’s Zoo and Wild Animal Medicine Current Therapy. Vol. 9. Philadelphia (PA): WB Saunders; 2019:421–431 withdrawal of pain relief an anthropomorphic decision. Once Sladky KK, Mans C. Analgesia. In: Mader DR, Divers S (eds). Current Therapy tramadol was withdrawn at day 48 the patient was even more in Reptile Medicine and Surgery. Maryland Heights (MO): Elsevier-Saunders; lively, which may suggest a sedating effect of the opioid. 2014:217–228

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