Introduction
A 3-year-old 27-kg female spayed American Bulldog was evaluated at a veterinary medical teaching hospital on an emergency basis because of severe burns sustained after a gasoline can exploded and ignited the dog’s caudal half (day 1). On days 1 to 4 after sustaining the burn injuries, the dog was medically managed by a primary care veterinarian. Due to the severity of injuries noted, the dog was referred for ongoing medical and surgical management on day 5 and was hospitalized at a veterinary teaching hospital from day 5 to day 82 (hospital duration, 78 days). On presentation, partial- and full-thickness burns with large eschars had affected nearly the entire dorsum, tail, pelvic limbs, and perineal region of the dog; it was estimated that 50% of the dog’s total body surface area (TBSA) was affected (Figure 1; Supplementary Figure 1). Additional burns affected the margins of the pinnae and periocular regions with severe corneal involvement bilaterally. The dog was cardiovascularly stable but had signs of extreme pain. Multimodal analgesia consisting of IV continuous rate infusions (CRIs) of fentanyl citrate (3 to 5 μg/kg/h), ketamine hydrochloride (5 to 10 μg/kg/min), and lidocaine hydrochloride (20 μg/kg/min) was initiated. The initial treatment plan consisted of administration of 480 mL of fresh frozen plasma, crystalloid fluid therapy, gabapentin (Neurontin; 30 mg/kg, PO, q 8 h), metoclopramide CRI (2 mg/kg/d, IV), and potassium supplementation as directed by point-of-care blood work. Additional treatment included ampicillin-sulbactam (Unasy; 30 mg/kg, IV, q 6 h), cisapride (1 mg/kg, PO, q 8 h), sucralfate (1 g, PO, q 8 h), and maropitant (Cerenia; 1 mg/kg, IV, q 24 h) and applications of silver sulfadiazine cream around the dog’s eyes and facial burns every 6 hours, neomycin-polymyxin-bacitracin ophthalmic ointment in the eyes every 6 hours, and antimicrobial wound gel (Silvasorb) around its perineum every 6 hours. After induction of general anesthesia, the dog had a catheter placed in a jugular vein. The initial wound evaluation and debridement were performed while the dog was anesthetized, and an esophagostomy tube was placed for nutritional support. Wound care was divided into 2 phases, namely debridement and reconstruction, although overlap of procedure days occurred. Initially, debridement procedures included evaluation of tissue viability and removal of eschars during anesthesia. The decision regarding the primary layer was made in accordance with the gross wound appearance. Alginate wound dressing (Teva Pharmaceutical Industries Ltd) was used over areas of necrotic tissue, while amorphous hydrogel wound dressing (Kendall; Covidien), nonadhering dressing (Adaptic; Systagenix Wound Management Ltd), and hydrogel-impregnated gauze (Kendall; Covidien) were used as a primary layer over healthy granulation tissue, depending on hospital availability. Seven days after the explosion, the dog was anesthetized for the debridement of large areas of necrotic eschar from the thighs, perineal area, and caudal portion of the dorsum. Due to foul-smelling mucopurulent debris under the eschars and the extent of the wounds, antimicrobial treatment was empirically broadened with enrofloxacin (Baytril; 15 mg/kg, IV, q 24 h). In an attempt to divert feces away from the wounds, a 12F cuffed endotracheal tube was inserted in the dog’s rectum and attached to an empty fluid bag that was changed regularly for 28 days. Fecal diversion was assisted by feeding a blenderized high–water content diet and 1 tablespoon of oral psyllium (Equate; Walmart Inc) every 8 hours. Due to the extent of inguinal and perineal burns, an indwelling urinary catheter (Surgivet; Smiths Medical) was placed for 31 days to assist in urine diversion away from the wounds. Ten days after the dog sustained the burn injuries, large islands of necrotic eschar were noted near its anus and vulva. Due to concerns regarding the degree of sharp debridement necessary for the perineal burns, use of medical grade maggots was elected for continued debridement. Approximately 750 to 1,500 maggots (Medical Maggots; Monarch Labs) were applied to the wounds, with greatest focus in the perineal region. The maggots were maintained in place for 2 days by a semipermeable dressing (nylon tights) covered with a light soft padded bandage. After the maggots were placed, it was perceived that the dog was markedly more uncomfortable and it began to bite at the areas of maggot application. As a result, meloxicam (0.1 mg/kg, PO, q 24 h) and a CRI of dexmedetomidine (Dexdomitior; 1 μg/kg/h, IV) were added to the analgesic regimen, resulting in resolution of these behaviors. On day 13, the dog was anesthetized for maggot removal and sharp debridement was continued (Figure 2). To facilitate maggot removal, the dog was also given a single oral dose of nitenpyram (Capstar; 57 mg). Small foci of necrotic tissue remained on the right caudolateral region of the dorsum, but no areas of necrosis were present in the perineal area. While it was anesthetized, the dog was given 480 mL of fresh frozen plasma and 4 g of canine albumin transfusion solution (Animal Blood Resources) due to anesthesia-related hypotension. After the procedure, the dog became persistently tachycardic and its PCV and total solids concentration decreased from 21% and 3.8 g/dL, respectively, at the beginning of the day to 17% and 3.0 g/dL, respectively, after the procedure. After receiving 250 mL of canine packed RBCs (Animal Blood Resources), the dog’s tachycardia resolved and the PCV increased to 21% at 1 hour after the transfusion. The PCV was 25%, and total solids concentration was 5.4 g/dL the following day.
Beginning on day 17, the reconstruction phase began by preconditioning a right caudal superficial epigastric flap during debridement and skin stretching devices were employed. Using a sterile marking pen and ruler, the outline of the right caudal superficial epigastric flap was made to include the right 3 to 5 mammae. The skin of the entire flap was incised with a scalpel blade, and approximately 45% of the flap was elevated. The subcutaneous tissue was apposed in a simple continuous pattern, and the skin was apposed in an interrupted cruciate pattern. Skin stretching was performed by use of the technique previously described for management of a severe burn injury (SBI) in a dog1 to stretch the skin on the ventral aspect of the thorax; the hook-and-loop material was advanced at each subsequent bandage change. Prior to flap preconditioning, viability of the caudal superficial epigastric vessels was confirmed with color flow Doppler ultrasonography on day 15. Initial surgical plans included prioritizing reconstruction of the perineal area due to increased risk of infection from fecal and urinary contamination. On day 26, the dog was anesthetized for right caudal superficial epigastric flap elevation and rotation to the left perineal region (180° rotation) and split-thickness skin graft collection (donor site was the right lateral region of the thorax, and the defect was closed primarily) by use of a dermatome. The flap was sutured to subcutaneous tissue and deep granulation tissue in the inguinal region and along the left side of the vulva and perianal skin. When skin was present, 3-0 nonabsorbable nylon suture material (Ethilon; Ethicon) was used. On the dorsum where skin was not available for apposition, the subcutaneous tissue and skin of the flap were tacked to the granulation bed with deep suture bites of 3-0 monocryl 25 suture material (Monocryl; Ethicon). Meshed split-thickness skin grafts were placed between the anus and vulva and throughout the right perineal area. To the extent possible given the location of the free graft, a bandage was placed by use of nonadherent dressing (Adaptic; Systagenix Wound Management Ltd) with triple antimicrobial ointment (Perrigo) over the grafts, as well as on the donor sites. Four days after surgery, it was noted that the rotational flap had developed marked edema and distal tip necrosis was present with partial dehiscence along the anus. Epithelialization was present along the margins of the granulation tissue of the dorsum and right medial thigh region. Thirty-four days after the dog sustained the burn injuries, the patient was persistently tachycardic that was nonresponsive to escalated analgesia or volume resuscitation. Results of point-of-care blood analyses revealed that the dog’s PCV had decreased from 24% to 21%; therefore, a 302-mL transfusion of canine packed RBCs (Animal Blood Resources) was given at that time. On day 36, the bandage was changed, 1 to 2 inches of epithelialization was present along the dorsal wound margins, and the necrotic tip of the axial pattern flap (approx 15%) was resected. By day 38, the flap edema completely subsided and epithelial tissue covered nearly the entire lateral aspect of the left pelvic limb at the level of the stifle joint.
In preparation for an acellular fish skin graft, the edges of the entire wound bed were sharply debrided. The granulation tissue was gently cleaned with dilute 2% chlorhexidine (ChlorHexQ scrub) and lavaged with saline (0.9% NaCl) solution. The acellular fish (cod) skin grafts (Omega3; Kerecis) were prepared by soaking the grafts in saline solution followed by meshing with both a mesher and by hand. The acellular fish skin graft was secured at the skin margin including the dog’s entire dorsum, and the acellular fish skin graft sections were secured to each other as well as tacked to the granulation bed with 4-0 nylon suture material (Ethilon; Ethicon) in an interrupted pattern on day 47. Once the acellular fish skin graft sections were secured, foam was placed over the graft and secured in place with adhesive dressing (Figure 3). To maximize healing of the grafts, negative pressure wound therapy (NPWT; VAC Freedom therapy system; 3M) was placed for adequate suction.2 The NPWT was set to provide 75 mm Hg (negative pressure) of continuous suction. A soft padded bandage was placed to further secure the NPWT.1 The NPWT was applied for 5 days and then removed.
On day 61, the dog’s last surgical procedure was performed. A split-thickness graft (donor site was the left thoracic region, which was allowed to heal by second intention) was placed on the left lateral and medial tarsal regions and proximal portion of the thigh. The body was bandaged, and a nonadherent dressing (Adaptic; Systagenix Wound Management Ltd) with triple antimicrobial ointment (Perrigo) was used to cover the grafts. A small portion (6 cm2) of the split-thickness graft harvested from the left side of the thorax was used to prepare an autologous skin cell suspension (Recell; Avita Medical). Once prepared, the autologous skin cell suspension was sprayed over the split-thickness grafts, acellular fish skin grafts, left thoracic donor site, and all remaining granulation tissue along the dorsum. A bandage was placed over all autologous skin cell suspension application sites with the primary layer being a nonadherent dressing (Adaptic; Systagenix Wound Management Ltd). By days 65 to 68, the left pelvic limb and tail were completely epithelialized and approximately 30% of the dorsum and right hip had epithelialized. Once the dog’s pelvic limb and perineal burns were healed, the dog was transitioned to outpatient wound management. At the time of discharge from the hospital on day 82, the dog’s right pelvic limb, tail, left pelvic limb, inguinal area, and perineal area were fully epithelialized, and approximately 50% of the dorsum and right hip region was epithelialized. The dog had been hospitalized for 78 days. Initially, the dog was returned to the veterinary medical teaching hospital or primary care veterinarian every 3 to 5 days for bandage changes for 60 days and every 10 to 14 days thereafter until the wounds were healed. Over the subsequent 6 months, the dog’s wound healing dramatically slowed as a result of overactivity and prednisone administration as a result of non–wound-related dermatologic issues. Additionally, routine visits for bandage changes were not always possible due to COVID-19 pandemic–related constraints, which may have contributed to prolonged wound healing. Despite the delayed wound healing due to motion in the final stages, no major bandage complications developed. At almost 2 years after the dog sustained the burn injuries, the last area of granulation tissue on the dorsum had healed, aside from some small crusts (Figure 4). Overall, the small crusts may have been associated with local skin fragility; however, there were no major burn-associated complications such as contracture of the left pelvic limb, widespread tearing of thin epithelium, or solar burns. Contracture of the limb with 360° burns was prevented by diligent passive range of motion during hospitalization and regular exercise when appropriate.
Discussion
The presentation of small animals with burn injuries, particularly SBIs involving accelerants, to emergency rooms is infrequent, and case reports of dogs with > 20% to 30% TBSA affected are exceedingly rare.1,3 In human burn patients, burns secondary to accelerants (gasoline or lighter fluid) result in a greater TBSA affected, longer hospitalization, and increased cost of care in comparison to burn patients with non–accelerant-related burns.4,5 In veterinary medicine, there are only 2 case reports of successful treatment of SBIs in dogs,1,3 to our knowledge. One case with 50% TBSA affected used NPWT as a mainstay of burn management; however, given the extent and location of the wounds, sole treatment with NPWT was not considered possible.3 A second case report1 describes the usage of skin stretching devices and bilateral caudal superficial epigastric axial pattern flaps as the sole wound management technique. The dog in the present report sustained both deep partial- and full-thickness burns affecting the entire caudal half of its body, and on the basis of the rule of nines, it was estimated that the dog sustained SBIs to 50% of its body.6,7 This case presented a unique combination of challenges due to the large TBSA affected and the anatomic locations of the burns. No single traditional reconstruction technique could be used due to the location of the dog’s wounds and lack of healthy donor skin and flaps available. The dog’s wound management was divided into 2 phases: debridement and reconstruction. Major surgical debridements occurred on days 5, 8, and 13 after the dog had sustained its burn injuries, although the wounds and granulation tissue were constantly assessed for viability. On day 11, a considerable area of perineal necrosis remained, and due to concerns regarding excessive sharp debridement around the vulva and anus, maggot treatment (Medical Maggots; Monarch Labs) was used for debridement. Maggot debridement has been reported to have 3 distinct benefits when applied to wounds: disinfection, debridement, and promotion of wound healing.8,9 Maggots provide disinfection through antimicrobial activities including alteration of tissue pH, ingestion of bacteria, and direct killing of bacteria through the secretion of proteolytic enzymes.8,9 Maggot movement within wound beds physically contributes to debridement by spreading proteolytic enzymes and physical scraping along the tissue bed in addition to disrupting biofilm formation.8,9 These proteolytic enzymes result in liquification of necrotic debris that is eventually digested, allowing a single maggot to digest 25 mg of necrotic tissue in 24 hours.8,9 Maggots promote wound healing by means of stimulation of fibroblasts and increased angiogenesis.8,9 There are many successful case reports of maggot treatment in humans with nonhealing wounds; however, there are only reports of maggot treatment for 2 dogs and 4 cats in the veterinary medical literature.10,11,12 In those dogs and cats, necrotic wounds occurred secondary to trauma, neoplasia, or bandage-related pressure, and good debridement with maggot treatment was achieved in all cases. However, that case information was limited and overall case outcome varied with a high mortality rate.10 For the dog of the present report, the provider’s recommendation of 5 to 8 maggots/cm2 was followed, and 750 to 1,500 maggots (Medical Maggots; Monarch Labs; 3 vials) were applied to the dog’s right hip region and perineal area. Also, as recommended, a semipermeable primary layer (nylon tights) was applied along with a soft padded bandage. The soft padded bandage was changed the next day, and maggots were removed after 48 hours. Mild to moderate pain is a commonly reported complication of maggot treatment in humans and is theorized to be associated with the movement of the larva exiting the wounds.11,13 This complication was noted in the dog of the present report and ameliorated with administration of meloxicam (0.1 mg/kg, PO, q 24 h) and a CRI of dexmedetomidine (Dexdomitor; 1 μg/kg/h, IV), which provided additional analgesia and sedation to the patient. Maggot treatment was extremely successful in tissue debridement of the perineal region, revealing healthy granulation tissue around the anus and vulva following maggot removal. Alternative methods of nonsurgical debridement in human burn patients include chemical or enzymatic debridement and hydrosurgery.14 In humans, a newly popular method of chemical debridement includes enzymatic debridement with a bromelain-based debriding enzyme that is derived from the pineapple plant stem.14 Like maggot debridement, this form of specific enzymatic debridement only removes necrotic tissue and is typically only mildly painful after application14; however, use of this method in dogs has not been described to our knowledge. The major disadvantages of more traditional enzymatic debridement agents such as trypsin or collagenase in veterinary medicine are their nonselective nature and cost.15 Although these enzymatic debridement products are effective, they tend to be extremely costly.16 Hydrosurgery involves tissue debridement with high-velocity, high-pressure application of saline solution directed at necrotic tissues and requires specialized instruments.14,15 In the case described in the present report, maggot treatment was chosen due to its availability, lack of required specialized equipment, and potential application to extensive, contaminated wounds. Although judicious and staged debridement of newly burned tissue is imperative to ensure minimal healthy tissue is removed, the dog underwent more aggressive surgical debridement of a large dorsal eschar as soon as it was identified. In humans, early eschar removal is pivotal in reducing proinflammatory mediators, as well as reducing the risk of infection and sepsis.17,18,19 The dog’s second phase of burn wound management could be characterized as a reconstructive phase. Early reconstruction reduces the risk of sepsis in SBIs because host defenses are severely diminished.17,18,19 Techniques employed in the present case included a caudal superficial epigastric axial pattern flap, several free split-thickness grafts, and, most notably, novel applications of acellular cod skin grafts (Omega3; Kerecis) and autologous skin spray (Recell; Avita Medical). The initial goal in reconstruction was to first address the perineal area because the risks of contamination with feces and infection were considered highest. A right caudal superficial epigastric axial pattern flap was rotated ventrally through the inguinal area extending to the left of the anus. A caudal superficial epigastric axial pattern flap and split-thickness free grafts were chosen initially because of the robust viability of this island of tissue as a vascularized flap and the best chance of covering the perianal area, which was expected to be difficult to keep clean and bandaged, even with urinary and fecal diversion. Due to the superficial burn to the dermis in the inguinal region, the viability of the caudal superficial epigastric vessels was confirmed with color flow Doppler ultrasonography, which has previously been shown to be a viable method for planning axial pattern flaps.20 Prior to flap rotation and free graft collection, both skin stretching devices and flap preconditioning were performed at separate bandage changes in attempts to minimize graft failure and decrease tension. The estimated 15% distal flap necrosis that the dog developed has been previously described for longer rotational flaps, and the extent of that necrosis was likely favored, despite preconditioning, because of maximizing the length of the flap along with rotation of 180°.21 This likely contributed to increased edema and venous congestion that resulted in flap tip necrosis and partial dehiscence and may have been minimized with use of hirudotherapy.22 Split-thickness free grafts were harvested from the dog’s left and right lateral regions of the thorax and placed along the left lateral and medial aspects of the tarsus and right perianal area, respectively, in staged procedures. Split-thickness free grafts were chosen rather than full-thickness grafts due to the extent of TBSA affected in this dog, insufficient donor skin, and the ability to achieve further expansion and wound coverage with meshing.23,24 Free grafts require a vascular wound bed for successful engraftment, and due to the location and size of the dog’s wounds, neither axial pattern flaps nor free grafts could be used as the sole means for reconstruction considering the lack of healthy skin available.25 One day after perianal graft placement, feces leaked into the dog’s bandage and it is estimated that approximately 50% of the first perianal free graft was lost. Diversion of feces from wound beds was another integral aspect of the dog’s supportive care, and a temporary rectal stent attached to a fecal collection system was designed.26 Additionally, the usage of a stool softener and a blenderized high–water content diet also ensured feces were the correct consistency to be properly diverted.
Due to the significant TBSA affected in the dog of the present report, additional techniques were explored to facilitate reconstruction and epithelialization, the first of which was the use of acellular fish skin xenografts (Omega3; Kerecis). Acellular dermal matrices act as scaffolding, thereby promoting fibroblast cellular migration and endogenous matrix formation.27 Currently, there are many mammalian acellular dermal matrix products; however, the use of piscine acellular dermal matrix products is associated with less zoonotic risk.27,28 There have been various successful reports of acellular cod skin xenograft use in humans with chronic, nonhealing wounds and during oncologic reconstruction.29,30 Acellular cod skin graft, approved by the FDA for human use in 2013, has the reported added benefit of containing omega-3 fatty acids, which have an anti-inflammatory role and provide superior engraftment.28,31 In addition to omega-3 fatty acids, cod skin contains collagen, fibrin, proteoglycans, and glycosaminoglycan, which provide scaffolding for the patient’s own fibroblasts.28,31 Only 1 other case report32 exists where acellular cod skin was used to treat burn wounds in a canine patient, and in that case, only a small surface area was covered by the cod skin graft. In the dog of the present report, donated human-grade cod skin product was prepared and applied according to the manufacturer’s recommendation, although a veterinary-specific product is now available. The product was meshed to expand surface area for wound coverage, and NWPT (VAC Freedom therapy system; 3M) was applied to assist in engraftment.2
In combination with acellular cod skin grafts, autologous skin cell suspensions (Recell; Avita Medical) have been used in chronic wound management in humans. Cellular spray devices allow thin split-thickness skin to be harvested from the patient and transformed into an autologous spray. As the manufacturer recommends, an at least 6-cm2 split-thickness graft should collected with a dermatome. By use of a proprietary enzymatic solution and bedside device, the graft is turned into a sprayable solution that contains the patient’s own cellular populations of keratinocytes, melanocytes, Langerhans cells, and fibroblasts for immediate delivery.33 Spray application of autologous skin cell suspensions allows for better epithelialization of large-surface burn injuries by providing more widespread coverage than a traditional meshed graft.24,33 In humans, it is reported that use of autologous skin cell suspensions in conjunction with mesh grafts increases the donor area-to-graft area ratio from 1:3 up to 1:100,33,34 making the use of an autologous skin cell suspension highly desirable in the case described in the present report. Autologous skin suspension derived from a small portion of the left lateral thorax split-thickness graft was also sprayed on the dog on day 61. Use of autologous skin cell suspensions has not been described in veterinary medicine previously, to our knowledge. For the dog of the present report, applications of both the acellular cod skin graft and autologous skin suspension allowed us to expedite healing of this dog’s wounds, something that was not possible with traditional reconstruction techniques, such as free grafts or flaps, alone. In comparison to pure second intention healing, these techniques may have led to more rapid healing and transition of the dog to outpatient wound management. These techniques aided in a successful outcome for this dog; however, further controlled studies are indicated to demonstrate the usefulness of these techniques in the treatment of wounds in small animals. No complications occurred following use of either the acellular cod skin or autologous skin suspension, although additional studies are needed to investigate the safety of both treatments in veterinary medicine.
Although the case described in the present report had an overall positive outcome, there were several limitations in the care provided, including timing of surgical debridement, antimicrobial choice, and nutritional support. Multiple debridement techniques were successfully used in this case, but the debridement phase was prolonged, which may have resulted in delayed wound healing and systemic consequences due to ongoing inflammatory stimulation. Additionally, several antimicrobial choices were made empirically, and the first wound culture was performed in preparation for skin flap advancement. To limit antimicrobial resistance, cultures were performed on the basis of the appearance of the wound at subsequent bandage changes with a focus on topical wound management rather than systemic treatment if indicated. Finally, more aggressive nutrition support with partial parenteral nutrition provided more frequently on surgery days could be considered. In addition to the challenges of SBI wound management, burns cause persistent inflammatory stimulation, resulting in a hyperdynamic, hypermetabolic state for months to years following the initial injury.17,18,35 It is estimated that metabolic rate can be elevated as much as 3 times the normal rate.17,18 Patients with SBIs can also develop severe cachexia because skeletal muscle serves as a major amino acid source for wound healing.17,35 The dog of the present report lost approximately 7 kg during hospitalization, and it is possible that being in a persistent negative energy balance also contributed to delayed wound healing. Due to multiple procedures requiring sedation and anesthesia, the dog was consistently fed less than its daily caloric requirements. This case has highlighted the need for a concise surgical plan, judicious use of antimicrobials, and a tailored nutritional plan for patients with SBIs. The financial burden of lengthy hospitalization and long-term treatment could not be assumed by all dog owners.
Regardless of species, SBIs cause profound inflammatory stimulation and disruption of the normal epithelial barrier, initiating numerous systemic derangements and resulting in a high risk of sepsis and death. The combination of systemic treatment, pain control, and wound management represents unique challenges. Treatment should be focused on managing and preventing systemic complications of burn injuries, providing aggressive multimodal analgesia, and performing staged debridement and reconstruction of the wounds. The case described in the present report involved a dog that had extensive partial- and full-thickness burns with 50% of its TBSA affected; the burn injuries were successfully managed with a combination of innovative techniques including maggot debridement near the delicate perianal area and vulva, the use of acellular cod skin grafts, and application of an autologous skin cell suspension along with traditional surgical flaps and grafts.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
Acknowledgments
Kerecis Omega3 and Recell products were donated by Kerecis and Avita Medica, respectively.
References
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