The chelonian shell is a living, metabolically active structure.9,13,21 The shell is typically divided into three major regions: carapace (dorsal area), plastron (ventral area) and bridge (lateral areas). It is comprised of a bony layer covered by keratinized epithelium and reviews of shell histology for the clinician are available.8,10
The shell bone is composed of multiple bony dermal plates and modified skeletal structures and is fused to vertebral bodies (except cervical and caudal) and ribs. The limb girdles are fused to the shell in Pleurodira (side-necked turtles).17 The outer dermal layer (dermal connective tissue) has collagen fibers, melanophores, vessels and nerves.10 The inner dermal layer (dermal bone) is composed of outer and inner compact bone plates with trabecular bone between them.10 The areas where bony plates join are called sutures. The shell contains bone marrow.20
The dermis is covered with keratinized epidermal scutes formed from β-keratin in hard shelled turtles and α-keratin in soft shelled turtles.10 The areas where scutes join are called seams. The epidermis invaginates into the dermis at the seam and new keratin is produced in this area.10
The suture margins where bony plates meet do not align with the seams where scutes meet.2,17 Dermal bone and scute nomenclature has been reported.2,4,17 The number/size of bony plates varies with species as can scute pattern.2The pleuroperitoneal (coelomic) membrane separates the shell and the body cavity internal organs.
Hard shelled aquatic turtles routinely shed scutes throughout life, not just during growth.2 Retention of scutes is frequently reported anecdotally in captive aquatic turtles but normal scute shedding patterns or the impact of husbandry factors (e.g., temperature range, basking opportunity, nutritional status, light cycle) on scute shedding is poorly understood. Retained scutes may be at risk to secondary infections.
The shell can regenerate and remodel when injured. Descriptions of shell regeneration after heat damage in wild tortoises exist and wild chelonians may be found with healed shell lesions.2,3,13 Shell fracture repair is possible and various techniques have been reported.1,2,5,16,18,24 The fracture repair process in sea turtles has been described as the development of granulation tissue followed by epithelialization and invasion of pigment and then calcification.24 Healing of deep shell lesions in freshwater turtles has been described as formation of a granulation bed (yellow orange in color), scar tissue formation (white in color, not always appreciated clinically), and keratinization of the lesion.1 Overall, shell bone and keratin heal well by second intention.16 Soft tissue wound healing has been described as the wound filling with proteinaceous fluid and fibrin to form a scab under which a layer of epithelial cells migrates. This layer then divides and thickens.16
In the author's experience, various hard shelled freshwater turtles from North America, South American and Australia have shown obvious healing within weeks of debridement of deep bone abscesses. In post debridement abscesses, surgical site depth was reduced by over 50% within 4–6 weeks. As wounds neared complete regeneration of soft tissue, pigmented tissue developed. The tissue is dense (not spongy or flocculent) and contiguous with surrounding shell. Bone appeared to be deposited within the lesions over the ensuing 6–12 months based on radiographic findings. Similar healing times are noted for traumatic injuries in other species.16
Reptile immune function and inflammatory response is related to temperature and ambient temperature may be expected to impact healing rates.16,20,22 Clinically, this was appreciated by the author in a group of Australian freshwater turtles. Healing was delayed post debridement of deep shell bone abscesses until water temperatures were increased from 24°C (75°F) to 30°C (86°F) and in-water basking sites were created. In addition, at the author's facility delayed healing was associated with water changes in small systems. Water changes are completed three times a week in cases of severe shell disease and water temperature was reduced up to 12°C (10°F) for 2–4 hours after changes. Removing turtles from the water and holding them in "mandatory basking" areas at 30°C (86°F) minimum until appropriate water temperature was re-established provided for normal healing. Appropriate temperature ranges must be determined based on the species' natural history and observing the individual animal's healing response but for most chelonians a range of 26–32°C (79–90°F) may be appropriate.16
Delayed wound healing has also been associated with ongoing necrosis or infection of shell lesions and repeated debridement of impacted areas provided for normal healing. The yellow-white membrane that covers healing wounds is periodically (every 3–14 days depending on the case) removed and/or the edges examined to monitor healing. A review of factors influencing wound healing is available.16
Categorization and Etiology
Many captive turtles are noted anecdotally to have roughened, pitted keratin layers with areas of keratin loss or thinning and/or thickening. This change is usually limited to the keratin layer but may invade into deeper bone structures. An investigation of a similar condition in a group of map turtles (Graptemys ssp.) is available.8 No clear infectious agent was identified. The authors reported multiple positive anaerobic bacteria cultures (genus Clostridium) from shell biopsies in addition to more typical aerobic bacteria, though relation to pathology is not clear. The same authors propose a shell scoring system to standardize description of shell lesions within the profession.
Ulcerative and proliferative shell disease has been reported in both captive and wild freshwater turtles.1–3,6,7,12,14,19,23 Overall, ulcerative lesions are more frequently reported and are the focus of the remaining discussion. Traumatic lesions can generally be managed in a similar manner. Etiologies vary and are not always well defined. Ulcerative disease may be classified as superficial or deep. Superficial ulcerations involve the keratin layer and minimally invade bone. An infectious bacterium, Benekea chitinovora, has been described in cases of progressive superficial shell lesions leading to mortality in freshwater turtles.23 Shell or skin trauma was the proposed route of inoculation and shellfish were a possible source of contamination. Septicemic Cutaneous Ulcerative Disease (SCUD) syndrome has been described; shell lesions lead to systemic bacterial infection with Citrobacter but Serratia was implicated in initial infection.3,11 Lesions that begins superficially may progress to invade deeper regions of the bone or lead to sepsis.
Lesions deep in the bone may be the result of uncontrolled superficial lesion, but can also develop within shell bone under normal keratin.1,2 These lesions are particularly difficult to evaluate given the normal keratin layer present until the defect is advanced. In many cases, the etiological cause is unknown at the time of diagnosis. Hematogenous spread of bacteria has been proposed and it is possible that blunt trauma or other causes of improper blood flow to the shell bone may lead to sterile abscesses.1,16 The pleuroperitoneal (coelomic) membrane is generally intact but becomes thickened. Infection may tract along the membrane.
Infectious etiologies should be considered in cases of superficial or deep shell disease. Gram negative aerobic bacteria are often cited as etiological agents in reptile infections but other bacteria, including anaerobic and mycobacterial infections, in addition to fungal, viral, and parasitic infection should be considered. Husbandry factors such as poor water quality, overcrowding, inappropriate temperature, and lack of adequate basking site appear to be major predisposing factors to shell disease in aquatic turtles.3,16,23
Compared to adults and older juveniles, neonatal turtles normally have generalized soft shells. Shells become firm over the first year. Abnormal generalized shell softening can be noted with nutritional diseases or inadequate husbandry (e.g., inappropriate ultraviolet provision).3,15 Some species normally have reduced bony plates or shell kinesis which cause the shell to feel soft.3,4
Shell bone may be exposed if scutes are lost. If localized with no evidence of active lesion, treatment is not warranted and normal shell or a pseudoshell may regrow under the damaged bone.2,3 Shell scarring is also possible secondary to prior trauma or infection and may lead to noticeable malformation or change in scute quality or pattern.
Physical examination should include detailed investigation of the shell with full exploration of keratin defects. Hemorrhage under scutes or along scute seams may be indicative of sepsis but normal coloration or focal infection must be ruled out as well. Utilizing dental or similar instruments to explore lesions and lift keratin edges will assist in conducting a complete examination. In addition, a complete history and detailed review of husbandry information should be completed as part of the initial examination.
Radiographs may demonstrate focal radiolucency secondary to abscess. Gastrointestinal tract gas can mimic shell bone lesions and multiple views or repeat exams may be needed. Computed tomography imaging can be utilized to document the extent of bone lesions, particularly in relation to other skeletal structures or the body cavity. Generalized loss of bone density may support nutritional disease.
Blood work and blood culture should be considered to evaluate for evidence of systemic disease.
Lesion culture, cytology, and histology may be warranted. While Gram negative aerobic bacterial infections are typically considered in reptile infections, Gram positive, anaerobic, mycobacterial, fungal, viral, and parasitic infections should be considered. Culturing and/or molecular diagnostics may be utilized to identify possible causative or complicating infectious organisms. Samples may be collected from full thickness bone biopsy or submitted during debridement.8 Pure cultures paired with relevant cytology and/or histology are supportive of a single causative agent.
Appropriate adjustments to husbandry should be the first step in any management plan. In some cases, correcting inappropriate husbandry may allow adequate healing with minimal further management in animals with focal lesions and overall good health.
Adequate debridement is essential to managing active lesions.2,16 The level of debridement varies with the lesion. In deep bone abscesses, creation of a smooth, bowl-like surface with all necrotic material removed appears to promote healing.1 Debrided areas are typically much larger than initial lesions. The author uses sterile protocols for surgical debridement. Bone rongeurs, bone curettes, high-speed rotary power tool (e.g., Dremel®, Robert Bosch Tool Corp.) or surgical drills may be needed for deep abscesses but needles, swabs, and dental tools may be sufficient for more superficial lesions or neonates. Care should be taken to appropriately dissipate heat to prevent thermal damage when rotary tools or drills are used.
General anesthesia is necessary for debriding deep, extensive lesions. Sedation and topical analgesia may be sufficient for more superficial lesions. Continued post-operative analgesia may be warranted. Animals are typically held out of water for 12–48 hours after sedation or general anesthesia until fully recovered. A pressure bandage can be applied to reduce post operative bleeding from extensive debridements. Bandaging material can vary but the author typically utilizes a hemostatic agent (e.g., gel foam) in the defect, a layer of sterile gauze pads, a permeable barrier bandage (e.g., Tegaderm), and application of duct-tape type product around the shell to hold the bandage in place and provide additional pressure. Adhesion is adequate if the shell is dry. The following day the bandage is removed. Animals are returned to the water without any bandaging in most cases. If the pleuroperitoneal (coelomic) membrane is exposed, a duct tape barrier bandage is utilized over the site to protect it from trauma during the initial healing process. If the coelomic membrane was breached during the debridement or initial injury, the animal may be dry docked (plastron lesion) or kept in low water (carapace lesion) until soft tissue covers the defect (typically seven to ten days). Maintaining adequate hydration is important if animals are dry docked for extended periods. In some cases, temporary epoxy or methylmethacrylate barriers may be placed and the animal returned to water prior to coelomic membrane healing.
The author uses systemic antibiotics in cases where blood work indicates a systemic response, blood cultures are positive, animals are severely debilitated, and after major debridement. Antibiotic use is ideally based on culture results. In cases where empirical treatment is begun, the author typically utilizes ceftazidime 20 mg/kg I.M. or S.C. q 3d. Systemic anti-fungal medications should be utilized as appropriate based on culture and histology results.
Topical treatments fall into 3 broad categories: cleaning, anti-microbials, and barriers. The following describes generic shell wound care in the author's practice based on common clinical presentations in this population of animals. Different disease presentations and integration of other open wound management protocols may be appropriate.--The surgery site is flushed or gently cleaned with chlorhexidine 0.05% or 0.9% NaCl every one to seven days based on healing progression and husbandry needs. After flushing, a topical antimicrobial such as silver sulfadiazine cream is placed in the defect. Barriers are not typically utilized except in the immediate post operative period or if the coelomic membrane is exposed as discussed above.
Based on the authors' experience, aquatic turtles can be maintained in water during management. Extensive dry-docking is detrimental due to increased difficulty in maintaining hydration and nutritional status. Life-threatening dehydration can develop quickly in neonatal turtles kept out of water, even with fluid support. However, mandatory basking (prescribed periods of dry docking in a warm environment, generally 30 minutes to 2 hours every three to seven days) is utilized. In adult Australian freshwater turtles (Emydura and Elseya spp.), the basking area has a temperature range of 32–43°C (90–110°F).
Nutritional support is provided when animals are not eating for extended periods of time (weeks), are severely debilitated with extensive lesions, or are significantly under-weight. Nutritional support is typically administered via orogastric tube every three to seven days. A variety of feeding formulas are appropriate.
Water quality is considered important and should be maintained under standard fish parameters whenever possible. Keeping organic loads and bacterial levels low is associated with improved healing in the author's experience. In addition, salt may be added to create a low dose bath at 1–3ppt (g/L) for the duration of healing. Species appropriate water, air, and basking site temperatures are utilized.
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