Surgical procedures in pinniped and cetacean species.

SURGICAL PROCEDURES IN PINNIPED AND CETACEAN SPECIES Author(s): Jennifer L. Higgins, B.A. and Dean A. Hendrickson, D.V.M., Dipl. A.C.V.S. Source: Journal of Zoo and Wildlife Medicine, 44(4):817-836. 2013. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2012-0286R1.1 URL: http://www.bioone.org/doi/full/10.1638/2012-0286R1.1

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Journal of Zoo and Wildlife Medicine 44(4): 817–836, 2013 Copyright 2013 by American Association of Zoo Veterinarians

SURGICAL PROCEDURES IN PINNIPED AND CETACEAN SPECIES Jennifer L. Higgins, B.A., and Dean A. Hendrickson, D.V.M., Dipl. A.C.V.S.

Abstract: Significant advances in veterinary diagnostic and surgical techniques have been made over the past several decades. Many of these advances, however, have not reached the field of marine mammal medicine. A number of limitations exist: risks of anesthesia, anatomical challenges, difficulties with wound closure, environmental constraints, equipment limitations, and perceived risks. Despite these limitations, surgical treatments have been successfully utilized in marine mammals. While surgery is performed in pinnipeds more frequently than in cetaceans, studies conducted in the 1960s and 1970s on dolphin sleep and hearing demonstrated that general anesthesia can be successfully induced in cetaceans. Since this pioneering work, a small number of successful surgeries have been performed in dolphins under both general anesthesia and heavy sedation. While these surgical procedures in pinnipeds and cetaceans have typically been limited to wound management, dentistry, ophthalmic procedures, fracture repair, and superficial biopsy, a number of abdominal surgeries have also been performed. Recently there have been pioneering successes in the application of minimally invasive surgery in marine mammals. Many of the anatomical challenges that almost prohibit traditional laparotomies in cetacean species and present challenges in pinnipeds can be overcome through the use of laparoscopic techniques. Due to the limited number of pinnipeds and cetaceans in captivity and, thus, the limited case load for veterinarians serving marine mammal species, it is vital for knowledge of surgical procedures to be shared among those in the field. This paper reviews case reports of surgical procedures, both traditional and laparoscopic, in pinnipeds and cetaceans. Limitations to performing surgical procedures in marine mammals are discussed and surgical case reports analyzed in an effort to determine challenges that must be overcome in order to make surgery a more feasible diagnostic and treatment option in the field of marine mammal medicine. Key words: Cetacean, dolphin, laparoscopy, pinniped, sea lion, surgery.

INTRODUCTION Significant advances in veterinary diagnostic and surgical techniques have been made over the past several decades. Many of these advances, however, have not reached the field of marine mammal medicine. There are numerous limitations and challenges to applying the techniques performed in domestic animals to marine mammals. These include environmental limitations, equipment limitations, anatomical challenges, difficulties with wound closure, and the challenges of restraint and anesthesia. Despite these constraints, the technology and knowledge base exists, and surgical treatments have been successfully utilized in marine mammals, especially in pinniped species. Radiography, computed tomography (CT), and nuclear medicine studies have all been performed in marine mammal species, improving the diagnostic capabilities available. While surgical procedures in pinnipeds and cetaceans are typically limited to wound manageFrom Colorado State University, Foothills Campus, 3107 W. Rampart Road, 1683 Campus Delivery, Fort Collins, Colorado 80523, USA (Higgins); and the Colorado State University, Veterinary Teaching Hospital, 300 West Drake, 1678 Campus Delivery, Fort Collins, Colorado 80523, USA (Hendrickson). Correspondence should be directed to Ms. Higgins ([email protected]).

ment, dentistry, ophthalmic procedures, fracture repair, superficial biopsy, and endoscopic procedures, a number of abdominal surgeries have been successfully performed. Recently there have been some pioneering successes in applying minimally invasive surgery (MIS) in marine mammals. MIS may expand options for abdominal surgeries in pinnipeds and cetaceans, whether for advanced diagnostics or treatment, in the future. Due to the limited number of pinnipeds and cetaceans in captivity, and thus the limited case load for veterinarians serving marine mammal species, it is vital for knowledge of surgical techniques to be shared among those in the field. Case reports of surgical procedures are rarely published in peer-reviewed journals. While some procedures are presented at conferences such as the annual meeting of the International Association for Aquatic Animal Medicine (IAAAM), many advances in surgical techniques are shared only by personal communication between practitioners. There have been no review papers published, to date, on surgical procedures in marine mammals. This paper attempts to fill this gap by reviewing case reports of surgical procedures, both traditional and MIS, in pinniped and cetacean species. The case reports included in this review come from publications in journals and IAAAM conference proceeding archives. The

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paper does not attempt to provide a comprehensive review of all procedures performed to date. Instead, the aim is to provide those in the field of marine mammal medicine with an overview of the types of surgery performed in pinniped and cetacean species. In addition, this review seeks to analyze those surgeries that have been performed, both successful and unsuccessful, so as to determine challenges that must be overcome in order to make surgery a more feasible diagnostic and treatment option in the field of marine mammal medicine.

CASE REPORTS OF SURGICAL PROCEDURES IN PINNIPEDS Successful surgical procedures require that safe, reliable chemical restraint or general anesthesia be achieved. While excellent reviews of anesthesia in pinnipeds have been published elsewhere, a brief discussion of the subject is warranted here before surgical case reports are reviewed.23,24,30,41 Regardless of the specific anesthetic agents utilized, all immobilization procedures must address the challenges associated with anesthesia in diving mammals. Bradycardia and prolonged apnea have been observed in some anesthetized pinnipeds and are frequently attributed to an inappropriate elicitation of the ‘‘dive reflex.’’ Pinnipeds, and especially the phocid seals, have developed complex physiologic adaptations to allow for conservation of oxygen for the brain and heart during breath holding. These adaptations include bradycardia, shunting of blood, and peripheral vasoconstriction. Atropine (recommended dose 0.02 mg/kg i.m.) is often used during anesthesia to decrease the reflex bradycardia associated with the dive response. Pinnipeds have also adapted a tolerance for high carbon dioxide (CO2) levels and acidosis so as to increase breath-holding ability. Normal values for end tidal CO2 levels have not been published for anesthetized pinnipeds but are believed to be higher than in domestic animals. One author suggests assisted ventilation is indicated when prolonged apnea is observed or when end tidal CO2 is above 55 mm Hg.41 Mortalities attributed to elicitation of the dive response may in some cases be caused by poor ventilation which can lead to hypoxemia, bradycardia, and cardiac arrest. Endotracheal intubation and continuous monitoring of respiratory function, with capnography for example, reduces the risk for development of hypercapnia and hypoxemia. In addition to providing the ability to ventilate the animal, endotracheal intubation is indicated in pinnipeds

due to the anatomy of their airway. The tracheal cartilage of pinnipeds is incomplete, and during anesthesia the trachea may partially collapse, leading to obstruction of the airway. Some phocid species also have a large amount of peripharyngeal tissue and a flaccid soft palate, which can further obstruct the airway during anesthesia. This abundance of peripharyngeal tissue also can make intubation of phocids difficult. Additional challenges faced during pinniped anesthesia include thermoregulation and vascular access. Although anesthesia in pinnipeds carries significant risks, a large number of safe and effective surgical procedures have been performed. The risks associated with the procedure must always be balanced against the value of the procedure. Surgical treatment of oral disease Many of the oral lesions common in domestic animals have been observed in pinniped species. Surgical treatments performed include oral mass biopsies, tooth extraction, root canal surgery, crowning, mandibular fracture repair, and excision of neoplastic oral masses.19,25,31,33,38,63 Biopsy of oral lesions in a leopard seal (Hydrurga leptonyx) is described in the literature as early as 1984.19 A stranded adult female leopard seal taken in by Atlantis Marine Park, Western Australia was found to have several raised oral mucosal lesions as well as a lesion on the hard palate. A light plane of anesthesia was induced with ketamine (2.6 mg/kg i.m.), diazepam (0.2 mg/kg i.m.), and atropine (0.006 mg/kg i.m.). These anesthetics were chosen based on past success in wild grey seals.20 Ketamine is often used as an induction agent, as it produces an increase in heart rate and blood pressure, beneficial side effects in marine mammals which may exhibit bradycardia during anesthesia due to development of the dive reflex.24 The use of atropine to reduce bradycardia and decrease respiratory secretions is common in marine mammals as in domestic animals. The recommended dose in pinnipeds and cetaceans is 0.02 mg/kg, which is more than three times the dose used in this case 3 decades ago.24 Radiographs of the skull were taken and small tissue sections cut from the oral lesions. Radiographs identified a further lesion in the nasal cavity. Histologic characteristics of the biopsied tissue were consistent with a fibromatous epulis. Surgical excision was determined to be unnecessary because fibromatous epuli are noninvasive tumors, and the lesions in this seal did not interfere with prehension or deglutition. The procedure was a success

HIGGINS AND HENDRICKSON—SURGICAL PROCEDURES IN PINNIPEDS, CETACEANS

in both surgical and anesthetic outcomes, although the authors did describe challenges with the induction of anesthesia. Ultimately anesthesia was achieved 7 min after administration of 2.6 mg/kg ketamine in the paralumbar muscle. Three previous injections in the area of the dorsal hip with 0.86 mg/kg, 0.86 mg/kg, and 1.4 mg/kg ketamine, respectively, failed to produce adequate sedation. This may have been a result of an inadequate dose or injection of the anesthetic into the thick blubber layer, a tissue which absorbs drug slowly, rather than into muscle. The repeated doses of ketamine did not lead to undesirable effects or prolonged recovery in this case. The procedure lasted only several minutes and the animal was recovered just 15 min after onset of anesthesia. Dental disease in pinnipeds is relatively common. Trauma is most frequently the cause, and tooth fracture and exposure of the pulp cavity can result. Oral surgery is often necessitated and tooth extraction, crowning, and root canal therapy have all been described in the literature, with tooth extraction most commonly employed. A case report was published by a group at Nihon University in Japan on a series of dental surgeries performed on California and South American sea lions (Zalophus californianus and Otaria flavescens).63 These animals underwent root canal surgery, crowning, or canine tooth extraction. In order to minimize stress of handling and excitement, the authors elected to avoid the use of induction drugs given by intramuscular injection. Anesthesia was induced by infusing isoflurane (5%, O2 30 L/min) into a sealed chamber with the sea lion. Once the animals were recumbent, induction was completed using a face mask. The animals were then intubated and maintained on isoflurane (1–3%) in oxygen. No apnea was reported during anesthesia and a smooth recovery from anesthesia was observed. A detailed description of the surgical procedure was not provided by the authors. In addition to trauma to the teeth themselves, oral trauma can also result in mandibular fracture. There is a case report of a 30-yr-old female harbor seal (Phoca vitulina) from the Oregon Coast Aquarium that bit down on a metal ring within a hoop net.38 Radiographs taken under general anesthesia showed a closed fracture of the left mandible between the first and second premolar teeth. There was also mild laxity of the mandibular symphysis. The first attempt of mandibular fracture repair by a group at Oregon State University’s College of Veterinary Medicine, with

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interfragmentary and interdental wiring techniques, was unsuccessful due to premature loosening of the fixation. The authors also cited difficulty in obtaining sufficient sedation to allow for intubation of the seal. This may have been due to excitement during the induction period and the pharmacokinetics associated with the intramuscular administration of premedications (0.2 mg/ kg butorphanol, 0.06 mg/kg diazepam, and 0.04 mg/kg atropine). Despite these challenges, intubation was ultimately achieved without the use of mask induction of anesthesia, which the authors chose to avoid due to concerns of eliciting the dive reflex. Recovery from anesthesia was also prolonged. The seal could not be extubated until 2 hr after termination of isoflurane administration, even with the administration of doxapram (5.0 mg/kg) and naloxone (0.2 mg/kg). The second attempt at fracture repair, with an intraoral acrylic dental splint combined with circumferential cerclage wire, was ultimately successful. This technique was chosen over the use of internal fixation so as to preserve tooth roots and neurovascular supply. Bony union was demonstrated radiographically 12 mo later at which time the fixation was removed. The authors of this case study stated that, although there is a clinical impression among marine mammal veterinarians that mandibular fractures in captive pinnipeds are relatively common, this is the first published study on fracture repair in a seal or sea lion. This case report also validated the combination of circumferential cerclage wire and an acrylic splint for long-term mandibular fracture repair. The fixation maintained its structural integrity for 12 mo, allowing for bony healing. Of final note, the anesthetic protocol used during the second procedure provided a much smoother induction and recovery. Premedications (0.14 mg/kg diazepam) were administered intravenously, which allowed improved sedation in less time. Induction with isoflurane (5%, O2 10 L/min) was in a custombuilt chamber. After induction, the seal was intubated and maintained on 2.5% isoflurane in oxygen. This technique, similar to that used by the group at Nihon University described above, minimized exposure to external stimuli and eliminated the need for mask induction of anesthesia. Periodontal disease also occurs in pinnipeds, although it is seen less frequently than trauma to the oral cavity. Extraction of affected teeth is the treatment of choice for severe periodontal disease, as antibiotic therapy is typically ineffective.33 A case of severe periodontal disease was reported

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in a California sea lion at Marine Life Oceanarium in Gulfport, Mississippi, USA.31 The 17-yr-old castrated male sea lion presented with purulent and mildly hemorrhagic nasal and auricular discharge and a swelling near his pinna. Exploratory oral surgery was performed after antibiotic therapy (doxycycline, amoxicillin, cephalexin, and Naxcelt) proved unsuccessful. The animal was premedicated with glycopyrrolate (0.007 mg/kg i.m.) 15 min prior to induction with Telazolt (1.9 mg/kg i.m.). The sea lion was then masked down with 5% isoflurane to allow for intubation. Maintenance throughout the surgery was with 2– 5% isoflurane in oxygen. Severe periodontal disease was observed around many of the incisors and premolars, leading to extraction of these teeth. The periodontal disease did not appear to be responsible for the swelling near the sea lion’s pinna. A fine needle aspirate was taken from the swelling, and analysis revealed the mass to be an abscess. Escherichia coli and Enterococcus sp. were cultured from the purulent fluid collected. An incision was made over the abscess to allow for continued drainage, and Nolvasant washes and systemic doxycycline (2.8 mg/kg) were prescribed. Recovery from anesthesia was uneventful, with extubation achieved 30 min following termination of anesthesia. A final case report on surgery of the oral cavity in pinnipeds is that of carcinoma removal from a 15-yr-old male Steller sea lion (Eumetopias jubatus) at the Vancouver Aquarium (Canada).25 This animal presented with a bullous enlargement of the hard palate, chronic dental disease, and chronic otitis. The mass was believed to be a bone cyst and medical treatment with antibiotics and carprofen (2 mg/kg p.o. once daily) was initially attempted. Oral ulceration, necrotic bony debris associated with the swelling and adjacent teeth, occasional hemorrhage, and a foul odor of increasing severity were observed despite medical treatment. A series of six surgeries followed. Anesthesia was performed with oral diazepam (0.15 mg/kg) and intramuscular injections of medetomidine (0.01 mg/kg) and midazolam (0.1 mg/kg). The animal was then masked and maintained with isoflurane in oxygen. During the first surgery, the left third incisor and canine teeth were extracted and aggressive debridement of the palatine and maxillary bones was performed. The presumptive diagnosis was osteomyelitis secondary to a tooth root abscess. Over the next 10 mo the bony defect continued to grow and a second surgical procedure was performed. Radiographs showed multiple lytic lesions in regions of the

palatine and maxillary bones that were associated with the mass. Additional teeth were extracted and biopsies taken of the bony defect. Histopathologic analysis revealed an invasive, poorly differentiated carcinoma. Over a course of three additional surgeries, surgical debridement of the mass with a CO2 laser was performed in combination with chemotherapy treatment (300 mg/m2 carboplatin i.v. and 0.2 mg/kg piroxicam p.o.). Growth of the mass was slowed; however, 6 wk following the third surgical debridement procedure severe, prolonged, frank oral hemorrhaging was observed. The sea lion was taken to surgery for emergency hemostasis and an exposed palatine artery was discovered. The artery was ligated and necrotic tissue was debrided. Recovery from anesthesia was prolonged and the sea lion died the next day. On necropsy, disseminated neoplasia was observed with lesions in the liver, lung, spleen, thyroid, kidney, and heart. Perianesthetic death can be a result of preexisting disease, surgical or procedural complications, or anesthesia itself or it can be multifactorial. It is important to distinguish between these causes of death so as to improve future anesthetic and surgical outcomes. The necropsy results from this case indicated that advanced neoplastic disease was likely the primary cause of mortality. Underlying lesions in the heart and lungs would also increase anesthetic risk, while liver and kidney lesions could interfere with elimination of anesthetic drugs. This case highlights the advanced level of surgical treatment that is possible in the oral cavity of pinnipeds. This animal was anesthetized successfully on multiple occasions, demonstrating that this major obstacle to surgical procedures in pinnipeds can be overcome. Surgical treatment of ocular disease Diseases of the cornea and lens, including corneal edema, chronic keratitis, cataracts, and lens luxations, are common in captive pinnipeds and can result in impaired vision and pain.7,8,50 Cataracts and lens luxations are estimated to affect half of the captive population of seals and sea lions, with incidence increasing to 100% in aged animals.6 Lensectomy procedures have been successfully applied to relieve pain, improve vision, and prevent secondary ocular conditions. Between 2002 and 2011, lensectomy surgeries were successfully performed in at least 47 pinnipeds.6 These cases represent a large number of successful anesthetic procedures performed on pinniped species. In the majority of these cases, an intracapsular or extracapsular approach was used.


Phacoemulsification, the most commonly used means of cataract removal in domestic species, can only be successfully applied in young pinnipeds. The round, dense lens of pinnipeds is difficult to break up and remove by phacoemulsification, making this procedure ineffective in adult animals. Of the 47 lensectomies performed by Colitz in the case report described above, only the youngest animal (7 mo of age) underwent phacoemulsification.6 The technique was also applied with some success in a 5-yr-old New Zealand fur seal (Arctocephalus forsteri).1 This animal presented with bilateral cataracts without lens luxation. The authors reported the lenses to be very hard and, while the lens of the right eye was removed by phacoemulsification, the authors were unable to break up the cataract nucleus of the left eye using this technique. Instead, the cataract nucleus was removed whole through an enlarged corneal incision. Orbital fat prolapse has also been reported in a California sea lion.34 A 23-yr-old female sea lion presented with a mass within the lateral aspect of the palpebral fissure. The animal was anesthetized with medetomidine (0.01 mg/kg i.m.), butorphanol (0.29 mg/kg i.m.), and midazolam (0.2 mg/kg i.m.). Atropine (0.02 mg/kg i.m.) was administered 10 min after induction of anesthesia. While oxygen was administered by a nasal cannula, inhalant anesthetic was not used. An incision was made through the inferior bulbar conjunctiva posterior to the nictitating membrane, allowing for exteriorization of the mass. The prolapsed material was removed and the incision closed with size 6-0 VicrylTM in a buried, subconjunctival, simple continuous pattern. Surgical time was less than 30 min and recovery was rapid after administration of the reversal agents atipamezole (0.06 mg/kg i.m.), naltrexone (0.2 mg/kg i.m.), and flumazenil (0.0057 mg/kg i.m.). No attempt was made to identify the cause of orbital fat prolapse in this sea lion. An age-related degenerative process of the orbital fasciae, however, was suspected. Surgical excision of the herniated orbital fat did not include any attempt to repair a defect in the orbital fasciae due to anesthetic time constraints and the limited surgical exposure achieved. The authors reported no reoccurrence of orbital fat prolapse in this sea lion 15 mo postoperatively. Orthopedic surgery Orthopedic surgeries are commonly performed in pinniped species, especially in stranded animals. Fractures typically are the result of trau-

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matic events such as bite wounds from other animals. Many of these fractures are open, and contamination from the aquatic environment is a significant risk. Such fractures require aggressive antibiotic therapy to prevent osteomyelitis and may require surgery. Open wounds in the hind flippers of stranded pinnipeds are of particular concern. A case report describes the treatment of osteomyelitis in six stranded grey seal pups (Halichoerus grypus) with hind flipper wounds.40 Three of these animals had osteomyelitis in the absence of any fractures, one case had a single closed fracture, and two animals had multiple open compound fractures. Diagnosis of osteomyelitis was made radiographically. Aggressive systemic antibiotic therapy, in addition to wound treatment, was essential in the management of the six cases. The authors initiated treatment with clindamycin or enrofloxacin, selected for their broad spectrum of activity. Dosing was based on recommended dosing in canines. Culture and sensitivity testing was performed when possible and antibiotic treatments were then adjusted. Carprofen (2 mg/kg) was used in cases where pain or swelling was observed. In the three cases reviewed in which fractures were absent, areas of bone rarefaction suggestive of osteomyelitis were observed radiographically in the tuber calcaneus, the proximal phalanx of digit 1, and the distal phalanx of digit 2. In two of these cases antibiotic treatment alone was successful at resolving the osteomyelitis. Repeated radiographs showed new bone growth over the area of previous lucency, and the animals were successfully released back into the wild following medical treatment. In the third case, amputation of the affected digit was necessary to treat the osteomyelitis. General anesthesia was induced with medetomidine (0.06 mg/kg i.m.) followed by ketamine (2 mg/kg i.m.) 15 min later. The animal was intubated and maintained on supplemental oxygen.2,40 The distal phalanx and a portion of the middle phalanx of digit 2 were amputated. The skin was closed in a simple interrupted pattern using PDSTM suture. Culture of the amputated bone yielded growth of Pseudomonas aeruginosa sensitive to apramycin and neomycin. The seal was maintained on carprofen and oral enrofloxacin initially. The antibiotic treatment was changed to amoxicillin-clavulanic acid and apramycin 2 wk postoperatively once the seal’s condition had stabilized and the risk of nephrotoxicity associated with aminoglycosides had decreased. The primary complications reported by the authors were associated with wound

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healing. The wound split open 12 days after surgery but ultimately healed by second intention. Wound dehiscence is a common problem in pinnipeds. Of the four hind-limb digit amputations described in this case report, only one surgical incision did not dehisce. In this case a horizontal mattress pattern was used to close the skin incision. This tension-relieving suture likely distributed the pressure created by a swelling wound better than a simple interrupted suture pattern. The other digit amputations reported in this case report included amputation of digit 1 of a single flipper, amputation of digit 1 of both hind flippers, and amputation of digits 1 and 2 of both hind flippers. In all three cases, amputation was performed at the level of the proximal phalanx. Osteomyelitis was successfully treated in all animals and they were successfully rehabilitated and released back into the wild. While fracture of the digits of the hind flipper are most common, a case report describing fracture of the tibia and fibula of a grey seal was recently published;28 this represents the first published report of long bone fracture fixation in a pinniped. A 2-wk-old stranded female seal presented with swelling and signs of pain upon manipulation of the left pelvic flipper; however, no open wounds were noted. Radiographs revealed a complete transverse fracture of the left tibial and fibular distal diaphyses. No evidence of osteomyelitis was evident on radiographs and surgical repair was attempted. This case provides proof of concept for the use of locking plates for fracture repair in pinnipeds. A successful outcome was achieved despite the surgical and anesthetic challenges present in this 2-wk-old patient. The fracture was located just 3 cm proximal to the growth plate in very soft, immature bone with a surrounding pocket of infection. Sedation for surgery was with midazolam (0.2 mg/kg i.m.), meperidine (2 mg/kg i.m.), and atropine (0.02 mg/kg i.m.). The small size of the animal allowed the use of propofol (1 mg/kg i.v.) for induction of anesthesia. The seal was maintained on isoflurane in 100% oxygen with use of intermittent positive-pressure ventilation. Butorphanol (0.1 mg/kg i.v.) was administered during surgery for additional analgesia. Upon exposure of the fracture site, evidence of abcessation was apparent although the bone seemed healthy. After necrotic tissues were thoroughly debrided, the tibial fracture was reduced and stabilized with a 5hole, locking, 2.0-mm string-of-pearls plate. Amoxicillin–clavulanic acid was administered throughout the surgery (20 mg/kg i.v. every 90

min), and gentamicin-impregnated polymethylmethacrylate was molded around the plate for localized delivery of antibiotic. To minimize anesthetic time, the fibular fracture was left untreated. The wound was closed in three layers, with size 3-0 PDS for the muscle fascia and size 30 CaprosynTM for the subcutis and intradermal layers. Meloxicam (0.1 mg/kg s.i.d. p.o.), marbofloxacin (5 mg/kg s.i.d. i.m.), and clindamycin (30 mg/kg b.i.d. p.o.) were administered during the postoperative recovery period. By 2.5 mo postoperatively, bony healing of the tibial and fibular fractures was evident on CT examination, with no signs of injury to the distal tibial growth plate or osteomyelitis observed. The seal was able to swim and hunt normally and was successfully released into the wild 3 mo postoperatively. Surgical treatment of elbow luxation in a 15-yrold female California sea lion has also been reported.42 The animal presented with acute lameness of the left forelimb following a suspected traumatic event. Carprofen and tramadol were prescribed and radiographs revealed a severe elbow luxation. Manual reduction under anesthesia was unsuccessful. It was determined that the animal would not regain proper function and quality of life would be adversely affected, so an open reduction surgery was subsequently performed. The sea lion was premedicated with the muscle relaxant methocarbamol 2 days prior to surgery. Despite this treatment, the luxation was difficult to reduce due to fibrosis and damage to the joint capsule. Ultimately reduction was achieved, bone tunnels were made in the ulna and humerus, and LigaFibat was used to stabilize the joint with a lateral suture. The incision was closed in three layers. Muscle was closed with size 2-0 PDS, subcutaneous tissues with 2-0 and 3-0 DexonTM, and skin with 3-0 and 5-0 EthilonTM as well as surgical glue. Radiographs and a CT scan were performed to confirm proper alignment of the joint. Recovery of function progressed well following surgery, demonstrating the success of the surgical procedure. Mandibular fractures are also commonly observed in pinnipeds. They can occur as a result of blows to the head during play or fighting behaviors.62 Mandibular fractures can also occur as a result of biting of objects in the exhibit. A case report of mandibular fracture repair is included above in the discussion of oral surgeries.38 Surgical contraception Although few case reports of the procedure exist in the literature, castration is commonly


performed in captive pinnipeds for the management of social dynamics within exhibits. Vasectomies are less commonly employed.4 Miscellaneous surgical procedures Several additional case reports of surgical procedures in pinnipeds can be found in the literature that do not fit clearly into the categories discussed above. One such case report is that of partial penile amputation in two Cape fur seals housed in different marine parks in Europe following persistent paraphimosis.36 The animals presented with persistent, partially exteriorized penises that were edematous, necrotic, and painful. The cases were attributed to both high bodyweight and possible traumatic injury while entering or exiting the pool in their exhibits. Medical treatment was unsuccessful at maintaining the penises in the preputial opening and surgical treatment became necessary. Both animals were anesthetized with medetomidine (0.02 mg/kg i.m.) and Zoletilt (0.7 mg/kg i.m.) followed by isoflurane administration (0.8–2%). Complete amputation of the tip of the penis was required in one animal. Partial penile bone amputation and urethra reconstruction were performed in the second sea lion. Both animals were also castrated; however, detailed description of the procedure was not provided. Postoperative treatment included administration of fluids and furosemide (2 mg/kg b.i.d. for 4 days) to promote urination. The animals were also prescribed doxycycline (2.5 mg/kg b.i.d. p.o.) and carprofen (4 mg/kg b.i.d. p.o.). Following surgery, the preputial opening was disinfected and the penis exteriorized daily to prevent the formation of adhesions. The only postoperative complication reported was infection in one animal, which was treated successfully with enrofloxacin (5 mg/kg b.i.d. p.o.). The surgical treatment of paraphimosis was ultimately successful in both sea lions. Superficial biopsy and mass removal from pinniped species is also reported in the literature. One case report is of a 7-mo-old stranded harbor seal rehabilitated at a facility in the Netherlands.52 The seal presented with signs consistent with parasitic bronchopneumonia. Upon initial physical examination, a subcutaneous mass was also observed on the animal’s head. Palpation of the mass did not elicit pain and it did not appear to be attached to the calvarium. It was assumed to be an incidental finding unrelated to the cause of stranding. Over a 2-mo course of rehabilitation, however, this mass grew steadily in size and

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a fine needle aspirate and biopsy were performed. Cytologic and histopathologic analyses revealed a dermal melanoma. This is believed to be the first report of a melanoma in a harbor seal. Due to steady growth of the tumor and its location near the right eye and pinna of the seal, surgical excision was elected. Complete excision of the mass was achieved; however, the seal suffered cardiac arrest and died during final closure of the wound 95 min after induction of anesthesia. It is difficult to infer the most likely cause of death when analyzing this case report. Anesthetic and surgical causes must be considered as well as underlying disease. Complications with the surgical procedure itself were not reported. The authors did not describe the anesthetic protocol and whether ventilatory support was used. Anesthetic-related death must therefore be considered. Necropsy showed no gross or microscopic abnormalities other than the cutaneous melanoma and parasitic bronchopneumonia. While there was no evidence of metastasis, underlying disease also cannot be ruled out as a cause of death. Perianesthetic mortality has been previously documented in a seal with parasitic bronchopneumonia undergoing mandibular fracture repair.30 Abdominal surgery Limitations: While risks associated with anesthesia in pinnipeds present a formidable challenge to conducting surgery in seals and sea lions, the case reports presented above demonstrate that many successful surgical procedures have been performed. It is evident from the cases presented, however, that surgical procedures that require entering the abdominal cavity are less-commonly performed. Laparotomy is associated with additional challenges due to anatomic considerations and challenges with postsurgical healing within an aquatic environment. In pinnipeds, closure of a surgical incision in the abdominal wall presents several challenges. The outermost layer of the abdominal wall consists of blubber in all but the fur seals. Blubber is poorly vascularized and thus surgical wound healing is prolonged. This results in an increased risk for dehiscence of the surgical site and penetration of water into the wound from the aquatic environment. In pinnipeds, internal to the blubber is a thin sheet of rectus abdominis muscle and a thin peritoneum. The blubber, rectus abdominis, and peritoneum all have poor holding properties for placement of suture material.62 This, combined with the method by which pinnipeds slide their body across the ground,

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results in a real risk for evisceration following abdominal surgery.54 Applying a body bandage and maintaining animals in a dry environment for several days postsurgery is possible with pinniped species and can help minimize the risks of dehiscence.62 Other authors prefer to allow animals access to water, as this can decrease patient stress and minimize abrasion on the incision site from the movement of the animal on land.54 Traditional abdominal surgery: The first case report of a laparotomy in a pinniped was published in 1982.54 An 11-yr-old Australian sea lion (Neophoca cinerea) at a marine park in Australia presented with vaginal prolapse. Reduction of the prolapse under physical restraint and local analgesia was initially attempted. The prolapse was successfully reduced; however, the horizontal mattress of size 2-0 ProleneTM placed in the vulval lips broke down after 1 wk. At this point an ovariohysterectomy was elected for. While this is the first published case report of abdominal surgery in a pinniped, according to the authors there had apparently been several similar cases of vaginal prolapse in harp seals (Pagophilus groenlandicus) that had been treated successfully by ovariohysterectomy. The same procedure was thus chosen for this sea lion. Anesthesia was induced with ketamine (4.5 mg/kg i.m.) and atropine (0.0075 mg/kg i.m.). To achieve adequate sedation, an additional dose of ketamine (0.75 mg/kg i.m.) was needed. Mask induction with halothane (5%, O2 6 L/min) was then performed to facilitate endotracheal intubation. The animal was maintained on 1–1.5% halothane (O2 6 L/min) throughout the procedure. Few complications with anesthesia were reported during the 3.5-hr surgery. The only anestheticassociated problem encountered was hyperthermia, which was successfully treated by application of ice packs on the flipper. Hyperthermia is commonly observed during anesthetic procedures in pinnipeds and if not corrected can cause cardiac dysrhythmias. The surgical procedure was executed in a similar manner as an ovariohysterectomy in domestic animals. Several surgical challenges were encountered; however, whether these were due to species differences or the moderately advanced pregnancy that was discovered upon opening the abdominal cavity is unknown. The authors cited considerable difficulty with ligation of the ovarian vessels. Simple ligatures tended to slip off the pedicle and multiple overlapping transfixation ligatures were required. Many vessels in the broad ligament of the uterus also required separate ligation. All

vessels were ligated with size 1 chromic gut. The uterine body measured 12 cm in diameter at the level of transection near the cervix. This large diameter prevented the use of a simple ligation technique, and a horizontal mattress of size 1 chromic gut was used to provide adequate hemostasis. The stump was oversewn with a simple continuous pattern of size 2-0 gut. The incision was closed in four layers. The abdominal wall was closed with a simple interrupted pattern and oversewn with simple continuous sutures. The thick subcutaneous fat required a 2-layer closure to minimize dead space. The skin was closed with a subcuticular pattern in an attempt to minimize rubbing of the sutures on the ground and the possibility of suture breakdown. All layers were closed with either size 0 or 2-0 Dexon. Recovery from anesthesia was uneventful. The authors reported that the main challenge of this case was not anesthesia or the surgical procedure but postoperative management. Five days postoperatively the skin and subcutaneous sutures broke down, leaving only the thin abdominal wall intact. The sea lion was again placed under anesthesia to repair closure of the abdominal incision. Instead of a subcuticular pattern, a horizontal mattress was used to close the skin. A row of deep vertical mattress sutures was also placed in the skin to relieve tension. Nonabsorbable Prolene suture was used in place of the initial absorbable Dexon skin sutures. These sutures were ultimately more resistant to dehiscence, and within 3 wk all but the most posterior 3–4 mm of the wound had healed well. The gap at the end of the wound did eventually heal by second intention. The ovariohysterectomy proved successful at treating the vaginal prolapse. While this case report was published 3 decades ago, surgical contraception techniques are still rarely performed in female pinnipeds.4 In addition to providing contraception and treatment of vaginal prolapse, ovariohysterectomy is also an important means of treating tumors of the reproductive tract. Ovarian and uterine neoplasias are common in California sea lions; however, laparotomy procedures for biopsy and removal of tumors by ovariohysterectomy are infrequently performed.21 Another potential application of abdominal surgery in pinnipeds is for treatment of gastrointestinal lesions. Gastric and intestinal obstructions secondary to foreign body ingestion are widely reported in both captive and wild marine mammals.22 Endoscopic diagnostic techniques are readily available. Although easier to apply in many cetaceans, because these species can be


behaviorally trained to accept a flexible endoscope, endoscopy can be performed in pinnipeds under anesthesia. While removal of small foreign objects is often possible endoscopically, abdominal surgery may still be necessary. A rare case report of traditional abdominal surgery in a pinniped outlines one such procedure. In 2002 at the National Veterinary School of Nantes in France, a gastrotomy was performed on a 4-yr-old captive harp seal.35 The seal presented with dysorexia of several months duration and showed a significant delay in growth. Diagnosis of gastric foreign bodies was made radiographically. The seal was anesthetized with midazolam (0.2 mg/kg i.m.) followed by isoflurane administration. The animal was then intubated and maintained on 2% isoflurane in oxygen. Ventilatory assistance was needed throughout the procedure. Several metallic objects and silicone joints were successfully removed by gastrotomy. The authors stated that the skin incision was closed using sutures that ‘‘were resistant to the friction due to locomotion of the seal over the ground.’’ However, the specific suture type and suture pattern were not described. The seal recovered well with complete return of appetite and no report of complications associated with closure of the incision. Another surgical procedure reported in the literature in which the abdominal cavity of pinnipeds was entered describes the implantation of telemetry transmitters.29 While external and subcutaneous radio transmitters have been implanted in pinniped species previously, this was the first time intraperitoneal implantation in pinnipeds was performed.26 Although manipulation of the viscera is unnecessary, the surgical implantation of telemetry devices into the abdomen of pinnipeds presents significant risks because all the challenges of closure of the incision into the abdominal wall discussed above apply. In this study, satellite transmitters were implanted into the caudoventral abdominal cavity of four rehabilitated California sea lions and 15 wild Steller sea lions. Anesthesia in the California sea lions was induced with medetomidine (0.07 mg/ kg i.m.) and Telazol (1 mg/kg i.m.). Stellar sea lions were induced with 5% isoflurane delivered via mask after the animals voluntarily entered squeeze cages. All animals were intubated and maintained on 1–3% isoflurane in oxygen. Assisted ventilation was necessary in some animals throughout the procedure. An 8.5 to 12-cm incision was made along ventral midline for insertion of the transmitters. The incision was closed with size 1 or 0 PDS sutures and skin glue

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or staples in six layers. First, the thin peritoneum was closed with a simple continuous pattern. Second, the internal abdominal oblique muscle, linea alba, and external abdominal oblique muscle were closed together with a simple interrupted or interrupted cruciate pattern. Third, subcutaneous fat was closed with a simple continuous pattern. Fourth, intradermal fat (blubber) was closed in a continuous mattress pattern to relieve tension in the blubber and aid in apposition of the layers. Fifth, a subcuticular pattern combined with an interrupted cruciate pattern was used in the skin over the mattress pattern to achieve a watertight closure. The subcuticular pattern was chosen to avoid exposure of sutures to the environment, which would have made them susceptible to compromise by the friction of the sea lions moving over the ground. Finally, surgical staples or skin glue were used to secure the skin incision in some animals. Mean surgical time was 90 min and, in the 19 sea lions in which the abdominal surgery was performed, no mortalities were reported. The intraperitoneal implantation of transmitters in this study likely represents the vast majority of any type of abdominal surgeries performed in pinniped species to date. Laparoscopic procedures—indications: Over the past decade, the application of laparoscopy in pinniped species has expanded the number of abdominal surgeries performed. Although, admittedly, the number of laparoscopic procedures performed in marine mammals is still small, this technique has the potential to increase the feasibility of performing invasive diagnostic and treatment procedures in pinnipeds and cetaceans. Laparoscopy, a subset of MIS techniques, is being increasingly applied in veterinary medicine including the fields of zoologic and wildlife medicine. Many exotic animal diseases are diagnosed by direct visualization of organs and biopsy due to the limited availability of serologic tests. Laparoscopy has been increasingly used in exotic pets as a minimally invasive means of obtaining tissue samples for histopathology and microbial culture. Application of this technique has led to improved diagnosis and treatment of disease.9 These principles apply to pinnipeds as well because diagnostic modalities are limited in the field of marine mammal medicine. While laparoscopy will not replace open abdominal exploratory surgery, this minimally invasive technique is now commonly used in small domestic animals for performing liver, intestinal, pancreatic, and kidney biopsies as well as for diagnosis and management of neoplasia. Laparoscopic surgical

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techniques commonly performed in small domestic animal and equine medicine include gastropexy, ovariohysterectomy and ovariectomy, cryptorchid surgery, gastric foreign body removal, and mass removal.27,51 When diseased tissue, organs, or large foreign bodies are removed laparoscopically, a portal site incision can be extended to allow for removal of the tissue. Alternatively, a morcellator can be used to cut the large tissue section into smaller pieces for removal through the portal site.3 The advantages of laparoscopy compared to conventional open abdominal surgery include decreased recovery time, improved wound healing, lower rates of infection, and decreased postoperative pain.51 In addition, laparoscopic techniques often offer improved visualization compared to open exploratory surgeries because structures are magnified on a video screen. The small diameter of the laparoscope also allows visualization of recesses in the abdominal cavity that would be inaccessible via an open approach, and insufflation allows for separation of abdominal structures. These advantages of MIS are especially of value in the field of marine mammal medicine. As discussed previously, the anatomical challenges of closing the abdominal wall of pinnipeds and their method of moving across the ground has resulted in wound dehiscence.54 Dehiscence can result in loss of a watertight closure, allowing pathogens from the aquatic environment to enter the abdominal cavity, as well as lead to evisceration. The surgical wounds resulting from laparoscopic procedures are typically less than 1 cm in size.17 This, together with new MIS techniques that enable closure of the abdominal wall underlying the small skin incision, allow for achievement of a watertight closure. Marine mammal species can thus be immediately returned to the water postoperatively and the risk of dehiscence is greatly reduced. The improved visualization of abdominal structures associated with laparoscopy is also greatly beneficial in marine mammals. The thick blubber layer of pinnipeds and cetaceans is relatively inelastic, significantly restricting access to the abdominal cavity during conventional open abdominal surgery unless a large incision is made.62 Another potential benefit of laparoscopy in marine mammals is the possibility of performing laparoscopic procedures with only heavy sedation and local anesthesia, eliminating the risks of general anesthesia in these animals. Standing laparoscopies are commonly performed with neuroleptanalgesia in horses and cattle.3,27 Laparoscopic procedures have also been performed in

severely debilitated small animal patients using only local anesthesia and sedation in cases when general anesthesia and laparotomy were considered too risky.51 In cetaceans the combined use of diazepam (0.1 mg/kg) and meperidine (1 mg/kg) with a local anesthetic at the surgical site has been previously reported to produce almost total immobility for 45 min, with the maintenance of consciousness and low–normal respiration.62 This anesthetic technique may be applicable to laparoscopic procedures in marine mammals. As with any surgical technique, complications can occur during laparoscopic procedures. The most common major surgical complications reported in small animal and equine laparoscopic surgeries include intestinal, splenic, urinary bladder, and vessel puncture during trocar insertion.27 Surgeons should be familiar with methods to prevent these complications as well as how to manage them should they occur. Complications associated with anesthesia during laparoscopic procedures have also been documented. Studies in humans and domestic animals have shown an increase in end tidal CO2 and acidosis in patients following insufflation of the abdominal cavity with CO2. The increase in intra-abdominal pressure from pneumoperitoneum can also interfere with movement of the diaphragm. These changes are easily managed in healthy patients with positive-pressure ventilation.27,51 While challenges with hypoventilation, hypercarbia, and acidosis have not been specifically reported in the few cases of laparoscopic surgeries performed in marine mammals, these complications should be monitored closely.14,16,18,37,49,59 It is possible that marine mammals may be particularly prone to these complications due to their predisposition for apnea and high end tidal CO2 during anesthetic procedures. An additional disadvantage associated with laparoscopy is the greater requirement for training with this technique. Tissue handling skills, manipulation of instruments, and laparoscopic suturing all require specialized training.9,27 Surgical time associated with laparoscopic procedures is comparable to that of open laparotomies if performed by an experienced laparoscopic surgeon. Surgical time can be prolonged, thus increasing anesthetic risk, in laparoscopic surgeries performed by veterinarians less experienced with MIS techniques. Finally, laparoscopy requires the use of sophisticated and costly technology. As with any procedure, the complications and disadvantages of laparoscopic techniques must be balanced against the value of the procedure. Overall the complication rate associ-


ated with laparoscopy is reported to be less than 2% in small domestic animals.51 The main indications for laparoscopy in marine mammals are direct visual examination of abdominal organs, tissue biopsy, reproductive manipulation, and in some cases surgical treatment of gastrointestinal and urogenital diseases. Over the past decade, there have been several reports of laparoscopic procedures performed in pinniped species. MIS techniques have been applied for diagnostics and treatment of genital, hepatic, and gastrointestinal lesions.16,18,37,59 Laparoscopic procedures—ovarian disease: As described previously, ovariohysterectomies have rarely been performed in pinniped species.4 Laparoscopic techniques are now expanding the options for diagnosis and treatment of ovarian and uterine disease and have the potential to make ovariectomy or ovariohysterectomy a viable method of contraception in female pinnipeds. One report of laparoscopic ovariectomy is described for treatment of polycystic ovaries.16 A female grey seal presented with bone marrow suppression and a severe nonregenerative anemia secondary to hyperestrogenism. Ultrasound examination determined the source of estrogen to be polycystic ovaries and an ovariectomy was performed laparoscopically. The seal was anesthetized with midazolam and isoflurane; however, additional details of the anesthetic protocol were not provided by the author. The animal was positioned in dorsal recumbency, a 1-cm incision made through the skin and subcutaneous fat and fascia caudal to the umbilicus, and a Veress needle inserted into the peritoneal cavity. Insufflation was performed with sterile CO2. The Veress needle was replaced with a cannula to allow insertion of a telescope attached to an endoscopic camera. Two additional cannulas for instrumentation were inserted into the abdominal cavity. Visualization of the ovaries showed both to be enlarged, polycystic, and highly vascularized. Ovariectomy was performed by first bluntly dissecting the ovarian pedicle to expose the ovarian artery and vein. Three loop ligatures were placed on each of the ovarian pedicles with size 0 PDS and the ovaries were excised. Cautery was used on vessels less than 2 mm in diameter. The ovaries were removed from the peritoneal cavity through the incision made for one of the instrument cannulas after the incision was slightly enlarged. Liver biopsies were also performed. For each cannula incision the fascia, subcutaneous tissue, and skin were closed in two layers. Absorbable suture material

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applied in a single cruciate suture was used to close the underlying layers. The skin was closed using nylon suture in a single cruciate pattern and then sealed with surgical glue. The surgery was successful and recovery was uneventful. There are two case reports of attempted laparoscopic diagnosis and treatment of ovarian tumors in which both procedures were ultimately unsuccessful. In 2002 a 27-yr-old female South American sea lion presented with anorexia, lethargy, coprostasis, tenesmus, and perineal tumefaction.59 While gastrointestinal disease may be suspected with these clinical signs, clinical pathological abnormalities, including hypernatremia (Na 176 mEq/L), hyperchloremia (Cl . 140 mEq/ L), and hyperprogesteronemia (306.22 ng/ml), led to the suspicion of adrenal or ovarian disease. After medical approaches failed to improve clinical signs and other diagnostic tests proved inconclusive, an exploratory laparoscopy was attempted in order to make a definitive diagnosis. The ovaries and adrenal glands were reported to be of normal appearance on laparoscopic observation, and no biopsies were reported to be taken. The sea lion was recovered from anesthesia; however, she was found dead the following morning. Findings on necropsy included ovarian neoplasia, chronic interstitial nephritis, atelectasis, and lung emphysema. The adrenal glands appeared normal. The animal likely died from cardiopulmonary failure during the recovery period from anesthesia. This sea lion was an older animal with increased anesthetic risk. Chronic renal disease may also have led to decreased clearance of anesthetic agents. Duration of anesthesia was reported to be 10 hr; however, the anesthetic protocol was not described by the authors. Given the risks associated with anesthesia in pinnipeds, surgical procedures must always be performed as efficiently as possible in these species. For the inexperienced surgeon, laparoscopy can result in prolonged anesthetic procedures. This case emphasizes the fact that one challenge to laparoscopic surgery in marine mammals is sufficient training. Training in laparoscopic techniques may take the form of special workshops, use of cadavers for simulation of techniques, or formation of a traveling team of clinicians with proper MIS experience, equipment, and funding. There are several recent examples of efforts initiated to make laparoscopy a safe and effective treatment option for marine mammals. One dolphin MIS workshop has previously been taught at the Colorado State University Veterinary Teaching Hospital.11 Veterinarians

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at the San Diego Wild Animal Park and Karl Storz Veterinary Endoscopy, Inc. have collaborated with other facilities needing assistance with laparoscopic procedures in megavertebrates. In addition, a traveling team of surgeons with experience in laparoscopy has been formed to perform laparoscopic surgeries in terrestrial wildlife species and could serve as a model for the field of marine mammal medicine.53 The second case report of ovarian tumor removal is also in a South American sea lion.37 A rapidly growing mass was identified on a routine ultrasound exam associated with either the kidney or ovary. An exploratory laparoscopy with possible excision was performed. Anesthesia was induced with medetomidine (0.02 mg/kg) and Zoletil (0.7 mg/kg). The animal was then intubated and maintained on isoflurane (0.6–1.5%) in oxygen. Although the laparoscopic approach allowed good visualization of the mass, it was difficult to determine whether it was associated with the kidney or ovary due to extensive connective tissue that had developed between the organs. Excision of the tumor was started, but the connections proved very complex. Bradycardia (50 bpm) was also observed, and the decision was made to end the surgery and wake the patient. The sea lion went into cardiac arrest while still under anesthesia and attempts at resuscitation ultimately failed. To gain further knowledge for future procedures, the surgery was continued after the animal’s death. The mass was excised successfully from the ovary, the kidney was observed to have an enlarged hiatus, and the lungs, observed through a trans-diaphragmatic approach, had a cottage cheese-like appearance. The observed lung pathology suggests the presence of an underlying infection which may have increased anesthetic risk and contributed to the perianesthetic death. Laparoscopic procedures—hepatic disease: Laparoscopic procedures for diagnosis of hepatic disease have also been described in the literature. One such procedure was performed on a stranded adult northern elephant seal (Mirounga angustirostris) admitted to a rehabilitation hospital (The Marine Mammal Center, California, USA).18 The animal was lethargic, underweight, icteric, and dehydrated on presentation. Serum biochemical abnormalities included marked elevation of bilirubin (28 mg/dl) and gamma-glutamyl transferase (GGT; 1,070 U/L) as well as a moderate elevation of alanine aminotransferase (ALT; 196 U/L). The animal was treated with antibiotics, corticosteroids,

anthelmintics, and supportive care but remained inappetant and lethargic. Laparoscopy was performed in an attempt to diagnose the cause of hyperbilirubinemia and elevations in liver enzymes. The animal was premedicated with atropine (0.02 mg/kg i.m.) and anesthesia was induced with Telazol (0.7 mg/kg i.v.). The seal was maintained on isoflurane (0.5–1.5%, O2 6 L/ min). The procedure allowed for good visualization of the spleen and liver. Splenomegaly was observed and both the spleen and liver had generalized, multifocal, raised, pale yellow, nodular masses. Green serous fluid was observed in the abdomen. Due to the extent of the lesions and poor prognosis for rehabilitation and release of the stranded animal, euthanasia was elected. The masses were identified to be biliary adenocarcinoma with metastasis to the liver, spleen, lymph nodes, adrenal gland, and pancreas. The biliary tumors likely caused bile duct rupture and the observed peritonitis. Laparoscopic procedures—gastrointestinal disease: Veterinarians at The Marine Mammal Center performed another laparoscopic surgery on a stranded northern elephant seal in 2011. Details on the procedure have not yet been published, but a description of the case can be found on the rehabilitation center’s website (www.marinemammalcenter.org/patients/ success-stories/wildoctric.html). A stranded elephant seal pup suffering from severe malnutrition was brought to the rehabilitation center. The animal would frequently vomit after feeding and remained underweight despite 3 wk of supportive care. Survey radiographs, a contrast study, and endoscopy were used to diagnose a sliding hiatal hernia. A laparoscopic gastropexy was successfully performed and the animal was ultimately rehabilitated and released. This procedure demonstrates the progress that has been made in laparoscopy in pinniped species over the past decade. Laparoscopic procedures have progressed from being used simply for direct observation and biopsy of organs to more-complex surgical procedures such as tumor removal, ovariectomy, and gastropexy. Gastropexy is commonly performed laparoscopically in domestic animals, especially for prevention of gastric dilation– volvulus in dogs and treatment of displaced abomasum in cattle.3,51 It should be noted that only five laparoscopic procedures in pinnipeds are described in this review because these are the only case reports described in the literature or in conference


proceedings. A handful of additional minimally invasive surgeries, however, have likely been performed. Dr. Samuel Dover at Sea World of Florida, for example, mentions that his group has successfully performed laparoscopic procedures in harbor seals, Pacific walrus (Odobenus rosmarus divergens), and Florida manatee (Trichechus manatus latirostris) as early as 1998; however, published descriptions of these procedures could not be located.15

CASE REPORTS OF SURGICAL PROCEDURES IN CETACEANS While several surgeries are likely performed in pinnipeds every year at aquariums, zoologic parks, rehabilitation facilities, and veterinary hospitals worldwide, surgical procedures are only rarely considered a treatment option in cetacean species. A brief discussion of the challenges associated with surgery in cetaceans is thus warranted before surgical procedures in these species are reviewed. Challenges and limitations Anesthesia: The first major challenge that must be overcome is successful anesthesia and recovery. Cetaceans are one of the most-challenging surgical candidates due to complications associated with anesthesia. General anesthesia in cetaceans has likely been induced fewer than 100 times.12 Intubation in cetaceans is more complicated than that in pinnipeds or terrestrial mammals. The anatomy of the cetacean upper respiratory tract is modified to allow for respiration through the blowhole. Intubation is achieved by first reaching into the mouth of the animal and manually dislocating the laryngeal goosebeak. The endotracheal tube can then be slid into the trachea via the oral cavity.24 Adequate ventilation is also more difficult to maintain in cetaceans as compared to pinniped species. When cetaceans lose consciousness under anesthesia, they fail to respire and require mechanical ventilation. Cetaceans’ loss of voluntarily ventilatory drive during anesthesia has been explained by a lack of central chemoreceptors to detect changes in blood pCO2 and pH.62 Special equipment is generally required for mechanical ventilation of cetaceans. These animals breathe in an apneustic plateau pattern in which air is not being inhaled or exhaled for a large percentage of the respiratory cycle. Cetaceans will breathe very deeply, filling their lungs to 80–90% capacity, breath hold for a period of time, and then exhale

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very forcefully allowing for almost complete emptying of the lung.12 Mechanical ventilation of cetaceans during general anesthesia has been performed with a respirator that is modified to include an apneustic plateau control unit. For procedures lasting 4 hr or more, respiratory acidosis and cardiovascular depression have been observed in cetaceans mechanically ventilated without this apneustic plateau modification. For shorter procedures, however, the apneustic plateau ventilatory cycle may be unnecessary.12 Recovery of cetaceans from anesthesia can be even more challenging than induction and maintenance of anesthesia. Depth of anesthesia is difficult to gauge, and the reflexes that control respiratory activity, including blowhole opening, nasopharyngeal sphincter integrity, and thoracic and diaphragmatic muscular activity, are among the last to return during the recovery process.62 The animal is often moving around and may require physical restraint before it has recovered sufficient respiratory reflex activity. The replacement of the laryngeal goosebeak is also necessary before voluntary respiration can occur.12 Thus, it must be precisely gauged when the animal has regained a sufficient level of consciousness, mechanical ventilation stopped, the endotracheal tube quickly removed, and the goosebeak replaced in order for the animal to begin breathing on its own after surgery. Anatomical and disease conditions can also compromise respiration during anesthesia and the subsequent recovery period. When removed from an aquatic environment, the bodyweight of cetaceans can crush their internal organs. The relatively flexible thoracic skeleton of these animals does not provide much protection for the lungs, and compression can lead to markedly decreased lung function. Depending on surgical approach, some animals have been maintained in specially designed surgical tanks to prevent compression of vital organs. If the surgical approach, such as a ventral midline approach, does not allow the animal to be maintained in a fluid environment, a special stretcher or a padded area can be used to optimize positioning. Underlying disease conditions can also lead to compromised lung function. Pneumonia is likely the most common serious disease of dolphins.43 Cetaceans mask signs of disease well and, thus, there is the risk that a patient may have underlying respiratory disease that compromises pulmonary function and oxygenation during anesthesia. Although cetaceans present a number of unique challenges to successful anesthesia that are not

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encountered with terrestrial mammalian or pinniped species, anesthesia has been successfully performed in cetaceans approximately 100 times.12 There have also been many additional cases in which heavy sedation has been achieved to allow for advanced diagnostic techniques. By combining sedation with local anesthesia, several major surgical procedures have been performed in cetaceans without the need for general anesthesia.62 Surgical challenges: Challenges associated with surgical procedures in cetaceans go beyond those of anesthesia. The anatomy of cetacean species presents a number of obstacles to abdominal surgery, namely limited exposure gained during the surgical approach to the abdomen and difficulty in achieving a watertight closure. The cetacean rib cage covers a greater portion of the abdominal organs in comparison to terrestrial mammals, making it difficult to visualize and manipulate these tissues during surgery. Compounding this problem is the thick abdominal wall of cetaceans, consisting of 2 cm of blubber and 5 cm of rectus abdominis muscle even in the smaller cetacean species. The layers of this thick abdominal wall lack elasticity, restricting surgical access to abdominal organs. Further complicating exposure of an abdominal lesion is the tightly packed nature of abdominal organs. Unlike in terrestrial animals, there is very limited free peritoneal space in the abdomen of cetaceans. The combination of these factors creates a situation in which a large surgical incision must be made to gain sufficient exposure. This in itself is problematic, as a major obstacle to surgery in cetaceans, similar to that discussed in pinnipeds, is the ability to achieve a watertight closure. Like pinnipeds, cetaceans lack a strong holding layer for sutures within the abdominal wall, and healing is delayed by the poor vascularity of blubber. Unlike pinnipeds, however, cetaceans cannot be maintained out of the water for several days to allow for healing of the incision in a dry environment. The strong muscular activity of the rectus abdominis muscle during normal swimming and the pressure of the tightly packed abdominal contents of cetaceans place a tremendous amount of strain on the incision. The tendency towards dehiscence is one of the greatest deterrents to abdominal surgery in cetaceans.62 The use of laparoscopic techniques would allow many of these surgical challenges to be minimized. With laparoscopy, incisions are around 1 cm in length, making a secure water-

tight closure more easily obtainable. At the same time, laparoscopy optimizes exposure. Early surgical procedures Many of the cases of general anesthesia and major surgical procedures in cetaceans occurred in the late 1960s and 1970s through pioneering efforts of Sam Ridgway and James McCormick. General anesthesia was first achieved in dolphins with thiopental induction and halothane maintenance.57 In a series of experiments a total of 18 Atlantic bottlenose dolphins (Tursiops truncatus) and Pacific white-sided dolphins (Lagenorhynchus obliquidens) were successfully anesthetized. Recovery in all animals was uneventful. Following the pioneering work of Ridgway and McCormick in 1967, many additional dolphins were anesthetized over the next decade for studies of dolphin sleep, brain activity, and hearing. In one study of dolphin sleep published by McCormick, 35 dolphins were successfully anesthetized.44 Many of the scientific studies conducted at the time also involved surgical procedures. In studies of dolphin hearing, for example, a complicated surgical approach to the ear was necessary for exposure of the round window of the cochlea.58 Animals were often maintained under anesthesia for 24 hr to allow measurement of cochlear potentials. Mortality rate was not reported in these studies but was apparently low. Monitoring techniques employed during the surgeries included blood gas analysis, capnography, electrocardiography, and urine output measurement as an estimation of renal perfusion. Liver enzyme measurement and histopathologic analysis of liver biopsies taken from dolphins during a 24hr anesthetic protocol did not reveal any significant abnormalities resulting from the prolonged period of anesthesia.48 Induction of general anesthesia in dolphins during the late 1960s and 1970s was not only for the purpose of scientific research. Ridgway and McCormick performed two successful ovariohysterectomies on adult Atlantic bottlenose dolphins in the late 1960s. A castration surgery was also performed. Although this surgery was successful, this dolphin died 6 days postoperatively of an infection that was aggravated by surgery.57 These remain the only reports of surgical contraception in the literature. While castration is routinely performed in some pinniped species, the testicles of cetacean species are intra-abdominal and, thus, surgical contraception has not been considered. Ridgway and


McCormick also report a laparotomy that was successfully performed for the removal of a cyst, the location of which was not described.57 Surgical treatment of oral disease Since the early abdominal surgeries carried out by Ridgway and McCormick, the surgical procedures performed in cetaceans have primarily been limited to treatment of oral and ocular disease and superficial lesions. Tooth extraction is commonly performed. Fracture of teeth and exposure of the pulp cavity can occur from trauma to the mouth. Degenerative changes also occur. Exposure of the pulp cavity will ultimately lead to infection and periapical abscesses, and extraction of the teeth is often necessary to prevent systemic infection (P. Kertesz, www. zoodent.com). Extraction of the tooth itself is usually a relatively simple procedure as all the teeth are single-rooted. Immobilization and logistical issues complicate treatment, however. General anesthesia is not required, and chemical restraint is achieved with a combination of sedation and local anesthesia. Anesthetization of the mandible is achieved by infiltrating lidocaine around the mandibular nerve as it passes through the mandibular foramen. Innervation of the mandible and anatomic landmarks for local anesthetization were worked out by Ridgway and others by anatomic dissection of the lower jaw of a bottlenose dolphin.56 A combination of benzodiazepines and opioids are most commonly used for sedation. In earlier case reports published on tooth extraction in bottlenose dolphins, diazepam alone or a combination of diazepam and meperidine were used to achieve reliable and safe sedation.32,61 More recently, butorphanol (0.05–0.13 mg/kg i.m.) has also been used for chemical restraint during minor procedures including tooth extraction.5 Several case reports also exist of oral squamous cell carcinoma (SCC) in dolphins. SCC typically presents as a nonhealing ulcerative lesion on the lips, hard palate, frenulum, or tongue in cetaceans. Various surgical and medical treatments have been applied in the management of these animals including cryosurgery, conventional surgical excision, chemotherapy, laser surgery, radiation, and brachytherapy.10,13,45,46,47,55,60 SCCs are locally aggressive and destructive tumors but rarely metastasize. Repeated treatments are often necessary to control growth or prevent reoccurrence. One of the earliest reports of cetacean oral SCC describes

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the use of laser surgery for ablation of lesions in the upper lip and rostral hard palate of a 16-yrold Pacific white-sided dolphin.13 SCC had been diagnosed histopathologically in this animal. Difficulty in achieving hemostasis was noted during the biopsy and, for this reason, the authors elected for laser ablation instead of conventional surgical excision. Although a small amount of tumor remained after debridement with the laser, and likely would require further treatment, this early case demonstrated the effectiveness of laser surgery in the management of SCC in cetaceans. Laser treatment has since been utilized in dolphins with extensive SCC lesions, especially when the tumor has been found to infiltrate the frenulum precluding complete surgical excision.45,46 In advanced cases laser treatment has been performed every 2–3 mo in an effort to control tumor growth. Laser surgery has been successfully supplemented with intralesional chemotherapy in a case with rapid tumor growth.46 Two case reports of radical surgical excision of SCC from the oral cavity of cetaceans have been published. In the first case a 22-yr-old Atlantic bottlenose dolphin presented with a 3 3 1 cm sublingual ulcer.55 SCC was diagnosed following biopsy of the lesion. The animal was sedated with meperidine (1.1 mg/kg i.m.) and midazolam (0.06 mg/kg i.m.) and the ulcer was infiltrated with lidocaine. The entire ulcerative lesion was excised with wide margins. The incision was closed in two layers. Head, neck, thoracic, and abdominal radiographs as well as a whole-body ultrasound exam were subsequently performed to look for metastasis. No evidence of local invasion or metastasis was observed, and the surgical site healed well with no reoccurrence of the lesion. In a more recent case report, complete surgical excision also was successfully performed with no recurrence of the ulcerative lesion.10 The authors of this report describe the use of electrocautery, electroligation, and ligation with size 3-0 silk to control hemorrhage, a common complication associated with the excision of SCC lesions. Radiation has been used to slow the growth of aggressive SCC lesions in cases where surgical incision, laser surgery, and chemotherapy have been unsuccessful. A brachytherapy implant of Iodine-125 was used in a 27-yr-old Atlantic bottlenose dolphin with an ulcerative lesion that invaded the intermandibular space and undermined the tongue.47 External beam photon radiation was performed in a 39-yr-old Atlantic

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bottlenose dolphin with uncontrolled growth of SCC lesions.60 The procedure was performed weekly over the course of 2 mo. For each treatment, the dolphin was premedicated with oral diazepam (0.25 mg/kg) prior to transport to the radiation center. Additional sedation with midazolam (0.045 mg/kg i.m.) was administered just before the procedure. The animal tolerated radiation therapy well with no change in appetite reported. In this case radiation therapy allowed for control of tumor growth, even after surgical excision and chemotherapy failed to significantly slow disease progression. Surgical treatment of ocular disease While degenerative changes of the cornea and lens are ubiquitous in pinnipeds, these lesions are rarely observed in cetaceans. Two case reports exist, however, of surgical debridement and repair of corneal ulcers in dolphins. Ridgway and McCormick describe the use of thiopental and halothane in a dolphin for repair of a corneal ulcer.57 In a more recent case report, propofol and isoflurane were used to induce general anesthesia in an Atlantic bottlenose dolphin for the treatment of an ocular lesion.39 The animal presented with blepharospasm and photophobia. Severe conjunctival inflammation and scleral injection were observed on ophthalmic examination. Despite two treatments of gentamicin (50 mg) administered into the bulbar conjunctiva, the animal continued to hold her eye shut and became anorexic. A corneal lesion was suspected, and examination and treatment of the lesion under general anesthesia was elected. Propofol was used for induction of anesthesia at a dose of 3.5 mg/kg administered intravenously in 40-mg increments to effect. The animal was intubated and maintained on 2% isoflurane in oxygen. Assisted respiration was performed throughout the procedure with an apneustic control device. Examination of the eye revealed an opaque, hyperemic cornea with mucopurulent discharge from a large ulcer. The lesion was cultured, flushed, and debrided. Another dose of gentamicin was administered into the bulbar conjunctiva before the termination of anesthesia. No complications with propofol–isoflurane anesthesia were reported by the authors. Total anesthetic time was 1.5 hr. A heart rate of 80–120 bpm and an O2 saturation of 96–98% were measured throughout the course of the procedure. Postoperative treatments included enrofloxacin (5 mg/ kg b.i.d. p.o.) and topical ophthalmic medication

(Dexasporin). The animal was opening her eye 2 wk after surgery with subsequent decrease in corneal opacity and return of vision over the next several months. This remains one of the few reports of general anesthesia in cetaceans since the pioneering days of Ridgway and McCormick. Abdominal surgery—laparoscopy After the early laparotomies performed by Ridgway and McCormick, no additional abdominal surgeries were reported in the literature until 1998 when the first laparoscopic procedure was performed in a cetacean.14 This pioneering surgery was performed at SeaWorld on a 27-yr-old female Atlantic bottlenose dolphin with a history of chronic hematuria unresponsive to medical management. The laparoscopic procedure was performed in order to obtain a renal biopsy. Anesthesia was induced with intravenous administration of propofol allowing for dislocation of the laryngeal goosebeak and intubation. Maintenance was with isoflurane in oxygen. Insufflation of the peritoneal cavity was achieved with a Veress needle inserted into the peritoneal cavity at the level of the umbilicus lateral to the rectus abdominis. The Veress needle was replaced with a 12-mm trocar for insertion of a 30 degree, 60 cm 3 10 mm telescope. Two additional 5 mm trocars were placed in the lateral abdominal wall for introduction of instruments. An incision was made in the renal capsule and a reniculus dissected free from the remainder of the renal parenchyma. A size 2-0 Vicryl ligature was placed around the base of the dissected reniculus for hemostasis before excision of two small biopsy samples. The trocar sites were closed in two layers. For the larger incision the peritoneum, fascia, and subcutaneous tissue were closed together with size 1-0 PDS followed by closure of the skin with size 2-0 nylon. For the two smaller incisions only the subcutaneous tissue was closed beneath the skin. Surgical glue was used over the skin sutures for further security. Recovery from anesthesia was uneventful, and within 1 hr of extubation the animal was returned to a medical pool and was able to swim without assistance. No complications were associated with the surgery. While histopathology and microbial culture results from the renal biopsy did not provide a definitive diagnosis for this animal’s condition (immune complex deposition of unknown etiology was diagnosed), the surgical procedure represented a major advance in cetacean medicine. This was the first abdominal


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surgery performed on a cetacean in 30 yr and the first laparoscopy performed. The success of this procedure proved that MIS is a viable option for the marine mammal veterinarian and that laparoscopic techniques have the potential to greatly expand diagnostic and treatment options for cetacean species. In 2011, another laparoscopic procedure was performed in a dolphin for the purpose of diagnosis and treatment of renal disease.49 The surgery was on a 31-yr-old male bottlenose dolphin with a history of chronic nephrolithiasis. A previous urolith in the left ureter, which the animal eventually passed on his own, left the animal with unilateral kidney atrophy and decreased function. The animal presented again with azotemia consistent with acute renal disease, and another ureteral stone obstruction was suspected. Ultrasound, CT scan, and renal scintigraphy were performed. Observation of hydronephrosis, proximal dilation of the ureter, and delayed excretion suggested obstruction of the right ureter. Medical treatment and an attempt at removal of the urolith by retrograde ureteroscopy all proved unsuccessful. As a final treatment option, a laparoscopicassisted ureterotomy was performed. General anesthesia was induced; however, the anesthetic protocol was not described by the authors of the case report. The ureter was located and incised to allow for removal of the ureteral stone. The animal suddenly arrested during the surgery and attempts at resuscitation were ultimately unsuccessful. The compromised condition of the patient at the time of surgery likely contributed to his death. Important lessons can be taken away from these two laparoscopic procedures. First is proof of principle of laparoscopic surgery in cetaceans. This technique has been proven to be a viable option for diagnosis and treatment of intraabdominal lesions in small cetacean species and, in many cases, may be the only alternative for treatment. Second, the unfortunate outcome of the most recent cetacean laparoscopic procedure illustrates the increased risk associated with general anesthesia and surgery in systemically compromised patients.

cetaceans are fraught with complications and are thus not typically considered a feasible treatment option. Laparoscopy allows veterinarians to overcome some of these anatomical constraints. The primary indications for MIS include direct visualization of abdominal organs for diagnostic purposes and subsequent biopsy collection as well as surgical treatment of some diseases. In particular, laparoscopy may hold the most promise for diagnosis and treatment of renal disease in cetaceans, treatment of perforated gastric ulcers in cetacean and pinniped species, and reproductive manipulation. In order for the potential of laparoscopic techniques to be realized, a greater effort must be made. Laparoscopic procedures have now been performed in pinniped and cetacean species for about 15 yr, yet the technique has not gained wide acceptance and is rarely performed. A number of limitations exist: risks of anesthesia, challenges with wound closure, environmental constraints, a shortage of veterinarians trained in laparoscopic techniques in these species, equipment limitations, expense, and perceived risks. Steps have been taken in an attempt to address each of these limitations. For example, advances in general anesthetic techniques have been made as well as safe chemical sedation protocols developed. Increasing experience with chemical restraint may create the possibility of performing laparoscopic procedures with heavy sedation and regional anesthesia, as they are often performed in the horse. This would greatly decrease anesthetic risks associated with laparoscopies. Advances have also been made in laparoscopic techniques that allow for better wound closure. Training workshops have been organized in attempts to increase the number of veterinarians with experience in laparoscopic techniques in pinniped and cetacean species. Perhaps most crucial to the acceptance and application of minimally invasive surgical procedures, however, is the sharing of knowledge. It is vital that case reports and advances in technique be shared among the marine mammal medical community for the full potential of laparoscopy to be realized.

CONCLUSIONS

LITERATURE CITED

The application of laparoscopic techniques in pinnipeds and cetaceans has the potential to expand diagnostic and treatment capabilities in these species. Due to anatomical challenges, traditional abdominal surgeries in pinnipeds and

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Received for publication 6 December 2012

Conservation of polymorphic simple sequence loci in cetacean species.

Surgical procedures and hemophilia.

Pinniped splenic volumes.

Pinniped visual pigments.

Aspirin and elective surgical procedures.

Surgical-mechanical procedures.

Cetacean vocal learning and communication.

Knee rehabilitation following surgical procedures.

[Surgical procedures in gallstone-ileus (author's transl)].

Fundamental Ethical Issues in Unnecessary Surgical Procedures.

Major gynecologic surgical procedures in the aged.

Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast.

Prosthodontic procedures for implant reconstruction. 2. Post-surgical procedures.

Genomic organization and differential signature of positive selection in the alpha and beta globin gene clusters in two cetacean species.

Cetacean morbillivirus in Northern and Southern Hemispheres.

Brown adipose tissue in cetacean blubber.

Surgical complications and procedures in neonates on extracorporeal membrane oxygenation.

Tooth Size Variation in Pinniped Dentitions.

Cetacean morbillivirus: current knowledge and future directions.

Predicting postoperative delirium after vascular surgical procedures.

Preoperative testing before low-risk surgical procedures.

Randomised trial support for orthopaedic surgical procedures.

Surgical site infections following ambulatory surgery procedures.

Day surgical anaesthesia: which patients? Which procedures?