EXPLORATORY RIGID LAPAROSCOPY IN AN AFRICAN ELEPHANT (LOXODONTA AFRICANA) Author(s): Julia Sweet, R.V.T., C.V.T., Dean A. Hendrickson, D.V.M., M.S., Dipl. A.C.V.S., Mark Stetter, D.V.M., Dipl A.C.Z.M., and Donald L. Neiffer, V.M.D., C.V.A., Dipl. A.C.Z.M. Source: Journal of Zoo and Wildlife Medicine, 45(4):941-946. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0299.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0299.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(4): 941–946, 2014 Copyright 2014 by American Association of Zoo Veterinarians
EXPLORATORY RIGID LAPAROSCOPY IN AN AFRICAN ELEPHANT (LOXODONTA AFRICANA) Julia Sweet, R.V.T., C.V.T., Dean A. Hendrickson, D.V.M., M.S., Dipl. A.C.V.S., Mark Stetter, D.V.M., Dipl A.C.Z.M., and Donald L. Neiffer, V.M.D., C.V.A., Dipl. A.C.Z.M.
Abstract: In March 2009, a 25-yr-old captive female African elephant (Loxodonta africana) underwent an exploratory laparoscopy after several weeks of diarrhea, submandibular and ventral edema, and swelling on medial and lateral aspects of all feet. Although there have been recent advances in laparoscopic vasectomies in free-ranging African elephants in South Africa utilizing specially designed rigid laparoscopes and insufflation devices, this was the first attempt at using these same techniques for an exploratory purpose. The elephant was sedated in a static restraint chute and remained standing for the duration of the procedure. Laparoscopy provided visibility of the dorsal abdomen, enabled collection of reproductive tract biopsies and peritoneal fluid samples, and allowed for instillation of antibiotics and crystalloid fluids directly into the abdominal cavity. Abdominal exploration, collection of tissue samples, and local therapy is possible via standing laparoscopy in megavertebrates. Key words: African elephant, exploratory, laparoscopy, Loxodonta africana.
BRIEF COMMUNICATION Although commonly used in human and veterinary medicine, challenges exist with the use of laparoscopic techniques in megavertebrates.7 Specialized laparoscopes, cannulas, and instruments have been developed (Karl Storz Endoscopy, Goleta, California 93117, USA) for use in the field to perform vasectomies on African elephants (Loxodonta africana).3–7 Specialized long instruments have also been employed for uterine biopsy in a white rhinoceros (Ceratotherium simum).1,2 Such equipment was used for the first time for diagnostic purposes in an African elephant in 2009 at Disney’s Animal Kingdomt. In early February of 2009, a 25-yr-old female African elephant was examined, using behavioral conditioning, for submandibular edema. Routine bloodwork was performed and differential diagnoses included allergy, vasculitis, and trauma. Flunixin meglumine paste (Banaminet Intervet International B.V., Merck & Co., Inc., WhiteFrom the Department of Animal Health, Disney’s Animal Kingdomt, 1200 North Savannah Circle, Bay Lake, Florida 32830, USA (Sweet and Neiffer); and the College of Veterinary Medicine and Biological Sciences, Colorado State University, 1601 Campus Delivery, Fort Collins, Colorado 80523-1601, USA (Hendrickson and Stetter). Present addresses (Sweet): Los Angeles Zoo, 5333 Zoo Drive, Los Angeles, California 90027, USA; (Neiffer): Center for Animal Care Sciences, Smithsonian’s National Zoo, Smithsonian Conservation Biology Institute, 3001 Connecticut Ave NW, Washington, D.C. 20008, USA. Correspondence should be directed to Julia Sweet ([email protected]).
house Station, New Jersey 08889, USA; 1.1 mg/ kg p.o.) was prescribed for 3 days. Bloodwork revealed values that were within normal limits. Edema progressed over the next weeks to include the entire facial area, as well as the elephant’s ventrum. Watery diarrhea, which was noted occasionally in early February, became a daily occurrence. Appetite decreased and the elephant developed additional edema on the medial and lateral aspects of all feet. Treatments during this time included diphenhydramine (Qualitest Pharmaceuticals Inc., Huntsville, Alabama 35811, USA; 1mg/kg), continued flunixin meglumine, pentoxifylline (Apotex Inc., Toronto, Ontario, Canada M9L1T9; 2.5mg/kg), gabapentin (InvaGen Pharmaceuticals Inc., Hauppauge, New York 11788, USA; 2.3 mg/kg), trimethoprim sulfa (Uniprimt, Macleod Pharmaceuticals, Inc., Fort Collins, Colorado 80525, USA; 18 mg/kg), and an equine gastrointestinal health supplement (Biosponget, Platinum Performance Inc., Buellton, California 93427, USA), all given orally. Repeated blood testing, fecal analyses (direct and float examination, fecal cultures, gram stain, fecal cytology), and fecal sand checks did not provide additional information to assist diagnosis. Further diagnostic testing of the abdominal and thoracic cavity was elected, and the elephant was immobilized for bronchoalveolar lavage, transabdominal ultrasound, and abdominocentesis; however, the results of these procedures were unremarkable. In another attempt to secure a diagnosis, an exploratory laparoscopy was performed in early March. Reproductive disease, peritonitis, and
941
942
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 1. Drawing shows the positioning of an African elephant and the location of the spinal needles to determine incision placement for left flank laparoscopy (close up, posterior view).
gastrointestinal or other abdominal problems were possible differential diagnoses explored through laparoscopy. The elephant was handinjected with a combination of detomidine (Dormosedan, Pfizer Animal Health, Exton Pennsylvania 19341, USA; 0.014 mg/kg) and butorphanol (ZooPharm, Laramie, Wyoming, 82070, USA; 0.014 mg/kg) intramuscularly in the left hind limb. An additional 30 mg of each drug was injected via both the intravenous and intramuscular routes to achieve the appropriate level of sedation for standing surgery. The elephant was moved into a static chute (restraint stall) for the surgery, and remained standing for the duration of the procedure (about 3.5 hr). To maintain an adequate level of sedation, the elephant received 20-mg increments each of detomidine and butorphanol intravenously throughout the procedure for a total of 300 mg detomidine and 300 mg butorphanol. Surgeons and equipment were placed on an elevated table to facilitate access. Surgical preparation, consisting of alternating scrubs with povidone–iodine and isopropyl alcohol, was performed just cranial to the left tuber coxae and sterile drapes were placed over the area. A line block was performed using 300 ml of 2% lidocaine (PhoenixTM, Clipper Distributing Company LLC, St. Joseph, Missouri 64507, USA) in multiple areas.
Two 10-ga spinal needles were placed perpendicular in the skin 10 cm rostral to the tuber coxae, with the first needle placed at the expected ventral border of the nearest rib (Figs. 1–3). The second needle was placed 15 cm ventral to the first, and both were advanced slowly into the muscles of the paralumbar fossa to confirm lack of bone at the planned incision site. Using a number 22 scalpel blade, a 10-cm vertical incision was made through the skin and subcutaneous tissues into the paralumbar fossa of the left flank. Chest retractors (Miltex Instruments, Lake Success, New York 10042, USA) were placed to aid in visualizing the muscle. The external and internal abdominal oblique muscle layers were sharply incised and modified Finocetto chest retractors (Miltex) (retractor blades were replaced in-house with blades lengthened to 6 inches) were used to retract the skin and muscle layers. The transverse abdominus muscle layer was separated along the natural fiber plane. The fibroelastic portion of the peritoneum was exteriorized through the flank incision by the use of vulsullem forceps. The fibroelastic layer as well as retroperitoneal fat was excised to reveal the peritoneum. A 3-cm incision was made into the peritoneum and number 2 polydioxanone (PDS II 3.0 metric, 70 cm on a reverse cutting needle, Ethicon Inc., Guaynabo, Puerto Rico 00969, USA) suture was used to place a purse-string suture in the peritoneum and around the laparoscopic cannula. Insufflation commenced at 52–78 mm Hg (1–1.5 pounds/inch2), using a specially designed insufflator (designed by a member of the surgical team) with ambient air. A laparoscope designed for use in elephants was placed through the cannula for visualization of the caudal dorsal abdomen, left kidney, and ovaries, which all appeared normal. The broad ligament in conjunction with the uterus had numerous small firm pedunculate structures, and biopsies of these were taken for histopathology, culture, and banking (freezing). Surgeons did not note gross evidence of peritonitis. Samples of free fluid in the abdomen were collected for cytology and culture. After samples were collected, 25 L of crystalloid fluids (Lactated Ringers Solution, Abbott Laboratories, North Chicago, Illinois 60064, USA) instilled with 20,000 mg amikacin sulfate (Amiglyde-V, Fort Dodge Animal Health, Fort Dodge, Iowa 50501, USA) and 6 million units of penicillin G potassium (GC Hanford Manufacturing Company, Syracuse, New York 13201, USA) were delivered into the peritoneal cavity using a large-animal intravenous set attached to the laparoscopic cannula. The
SWEET ET AL.—LAPAROSCOPY IN AN AFRICAN ELEPHANT
943
Figure 2. Drawing shows the positioning of an African elephant and the location of the spinal needles to determine incision placement for left flank laparoscopy (posterior view).
944
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 3. Drawing of the lateral aspect of an African elephant showing the spinal needles (placed to determine incision placement for left flank laparoscopy) in relationship to the tuber coxae (dashed line).
elephant was given flunixin meglumine (Flunazine, Bimeda, LeSueur, Minnesota 56058, USA; 1.1 mg/kg) and ceftiofur crystalline free acid (Excedet, Pfizer, New York, New York 10017, USA; 5.4 mg/kg) intramuscularly. Peritoneal and muscle layers were closed with size 2 polydioxanone II suture in a simple continuous pattern. The skin layer was closed with number 5 stainless steel suture (Ethicon 7.0 metric, 75 cm conventional cutting surgical steel monofilament, Ciudad Juarez, Chihuahua 32574, Mexico) in a horizontal mattress pattern with stents made from extension-set tubing (Abbott Laboratories) cut into 1.27-cm (0.5-inch) lengths and sterilized in ethylene oxide (Fig. 4). Additional appositional skin sutures were placed in a simple interrupted pattern using size 2 monofilament nylon suture (Monosof, Syneture/Covidien Mansfield, Massachusetts 02048, USA). Naltrexone (Taylor’s Pharmacy, Winter Park, Florida 32789, USA; 0.09 mg/kg) and yohimbine (Premier Pharmacy Labs, Inc, Weeki Wachee, Florida 34613, USA; 0.09 mg/kg) were given intravenously as reversal agents. An additional dose of
naltrexone (0.16 mg/kg) and yohimbine (0.07 mg/kg) were injected intramuscularly at the end of the procedure. The elephant walked out of the stall 7 min following the last intramuscular injections. Eight days later, the elephant was euthanized due to quality of life concerns. Lack of response to therapy coupled with worsening diarrhea, edema in all limbs, lameness, and overall discomfort led to the decision to humanely euthanize the animal. Gross necropsy and histopathologic examination revealed a wide range of pathology with the most significant lesions found in the stomach, proximal small intestine, colon, and kidneys. The most consistent lesion found in the stomach, upper small intestine, and colon was mucosal damage (including ulceration) not associated with any identifiable infectious etiology. Bacteria and yeast were noted in some areas and were considered secondary invaders of the damaged mucosa. The histologic appearance of these lesions supported an acute to subacute timeframe (days to weeks). All of the lesions in the gastrointestinal tract had the appearance of ischemic damage with fibrin,
SWEET ET AL.—LAPAROSCOPY IN AN AFRICAN ELEPHANT
Figure 4. Appearance of 10-cm vertical incision site showing surgical closure with stents in an African elephant that underwent exploratory left flank laparoscopy.
thrombi, and vascular lesions leading to loss of the overlying mucosa, and their character suggested a toxic exposure. Renal lesions were characterized by acute to subacute, multifocal, and moderate to severe renal papillary necrosis with associated tubular mineralization, scattered tubular epithelium regeneration, and squamous metaplasia. Other significant lesions included a single focus of hepatocellular necrosis with intralesional yeast bodies, a focal deep tongue ulcer, and whole body edema with severe subcutaneous edema and mechanical rupture of the epidermis in all four feet. The structures biopsied from the broad ligament were diagnosed as leiomyomas, benign smooth muscle tumors, unrelated to the primary disease. Considering potential toxins and the fact that the renal lesions noted are pathognomonic for nonsteroidal anti-inflammatory drug (NSAID)– induced papillary necrosis, the drug history of NSAID administration in this elephant in combi-
945
nation with an endogenous stress steroid response was considered the most likely cause for the gastrointestinal and renal pathology. Based on bloodwork, renal papillary necrosis did not cause significant renal impairment in this elephant. The major lesion that cannot be explained by gross or histopathologic findings is the presence of edema of the subcutaneous tissue and limbs. The basic pathogenesis of edema indicates that it results from decreased oncotic pressure (low protein), increased hydrostatic pressure, microvascular leakage, or decreased lymphatic drainage. Bloodwork examined throughout the animal’s illness did not reveal hypoproteinemia, and the absence of cardiac disease does not support increased hydrostatic pressure as the cause of edema. Vascular lesions were noted in the gastrointestinal tract, yet were not a feature in other organs and tissues affected by edema, and therefore microvascular damage is unlikely. Decreased lymphatic drainage due to reduced mobility may have contributed to the edema in this elephant; however, a diagnosis was not obtained. Decreased mobility would certainly help to explain the severe edema of the limbs and feet at necropsy. Unfortunately, no etiology responsible for the initial clinical signs could be determined. This procedure would not have been possible without the previous work done in the field by the Elephant Population and Management Program (EPMP), an international collaboration of wildlife specialists, veterinarians, veterinary technicians, industry partners, and game reserve/national park managers who are working together to address elephant overpopulation in southern Africa. These techniques and specialized equipment were first used in the field in South Africa to perform vasectomies on elephants in small game reserves, a project which started in 2005.3–7 According to a report summarizing the important considerations of laparoscopy in megavertebrates from experience gained in a white rhinoceros,2 having the ability to utilize these megavertebrate instruments was essential to advancing laparoscopic methodologies in these species. In that case, the author found that specialized insufflation equipment is also invaluable for successful visualization of the abdominal cavity. His subsequent design and implementation of this unit proved invaluable for the EPMP as well as for this exploratory laparoscopy. Laparoscopy allowed for evaluation of part of the reproductive and gastrointestinal tracts and peritoneal cavity in this elephant. Surgical time as well as anesthesia time was minimized. Looking to the future, laparoscopy is
946
JOURNAL OF ZOO AND WILDLIFE MEDICINE
feasible in megavertebrates and may be employed for abdominal exploration as well as organ or other tissue biopsy in such animals.
LITERATURE CITED 1. Radcliffe RM, Hendrickson DA, Richardson LG, Zuba JR, Radcliffe RW. Considerations for laparoscopy in megavertebrates. In: Proc Am Assoc Zoo Vet, Int Assoc Aquatic Anim Med, joint conference; 2000. p. 81–82. 2. Radcliffe RM, Hendrickson DA, Richardson LG, Zuba JR, Radcliffe RW. Standing laparoscopic-guided uterine biopsy in a southern white rhinoceros (Ceratotherium simum simum) J Zoo Wildl Med. 2000;31:201– 207. 3. Stetter M. Laparoscopy as an aid to animal care and conservation in elephants. J Elephant Managers Assoc. 2004;15(2):44–47. 4. Stetter M, Grobler D, Zuba JR, Hendrickson DA, Briggs M, Castro L, Neiffer D, Terrell S, Robbins PK, Stetter K, Ament BS, Wheeler L. Laparoscopic repro-
ductive sterilization as a method of population control in free-ranging African elephants (Loxodonta africana). In: Proc Am Assoc Zoo Vet, Am Assoc Wildl Vet, Assoc of Zoos, and Aquar, Nutr Advisory Group; 2005. p. 199–200. 5. Stetter M, Hendrickson DA. Laparoscopic surgery in the elephant and rhinoceros. In: Miller RE, Fowler ME (eds.). Fowler’s zoo and wild animal medicine, Volume 7, Current therapy. St. Louis (MO): Elsevier; 2011. p. 524–530. 6. Stetter M., Hendrickson DA, Zuba JR, Stetter K, Grobler D, van Altena JJ, Small LA. Laparoscopic vasectomy as a potential population control method in free ranging African elephants (Loxodonta africana). In: Proc International Elephant Conservation and Research Symposium; 2006. p. 177. 7. Zuba JR, Stetter MD, Dover SR, Briggs M. Development of rigid laparoscopy techniques in elephants and rhinoceros. In: Proc Am Assoc Zoo Vet, Annual Meeting; 2003. p. 223–227. Received for publication 6 January 2014
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(4): 941–946, 2014 Copyright 2014 by American Association of Zoo Veterinarians
EXPLORATORY RIGID LAPAROSCOPY IN AN AFRICAN ELEPHANT (LOXODONTA AFRICANA) Julia Sweet, R.V.T., C.V.T., Dean A. Hendrickson, D.V.M., M.S., Dipl. A.C.V.S., Mark Stetter, D.V.M., Dipl A.C.Z.M., and Donald L. Neiffer, V.M.D., C.V.A., Dipl. A.C.Z.M.
Abstract: In March 2009, a 25-yr-old captive female African elephant (Loxodonta africana) underwent an exploratory laparoscopy after several weeks of diarrhea, submandibular and ventral edema, and swelling on medial and lateral aspects of all feet. Although there have been recent advances in laparoscopic vasectomies in free-ranging African elephants in South Africa utilizing specially designed rigid laparoscopes and insufflation devices, this was the first attempt at using these same techniques for an exploratory purpose. The elephant was sedated in a static restraint chute and remained standing for the duration of the procedure. Laparoscopy provided visibility of the dorsal abdomen, enabled collection of reproductive tract biopsies and peritoneal fluid samples, and allowed for instillation of antibiotics and crystalloid fluids directly into the abdominal cavity. Abdominal exploration, collection of tissue samples, and local therapy is possible via standing laparoscopy in megavertebrates. Key words: African elephant, exploratory, laparoscopy, Loxodonta africana.
BRIEF COMMUNICATION Although commonly used in human and veterinary medicine, challenges exist with the use of laparoscopic techniques in megavertebrates.7 Specialized laparoscopes, cannulas, and instruments have been developed (Karl Storz Endoscopy, Goleta, California 93117, USA) for use in the field to perform vasectomies on African elephants (Loxodonta africana).3–7 Specialized long instruments have also been employed for uterine biopsy in a white rhinoceros (Ceratotherium simum).1,2 Such equipment was used for the first time for diagnostic purposes in an African elephant in 2009 at Disney’s Animal Kingdomt. In early February of 2009, a 25-yr-old female African elephant was examined, using behavioral conditioning, for submandibular edema. Routine bloodwork was performed and differential diagnoses included allergy, vasculitis, and trauma. Flunixin meglumine paste (Banaminet Intervet International B.V., Merck & Co., Inc., WhiteFrom the Department of Animal Health, Disney’s Animal Kingdomt, 1200 North Savannah Circle, Bay Lake, Florida 32830, USA (Sweet and Neiffer); and the College of Veterinary Medicine and Biological Sciences, Colorado State University, 1601 Campus Delivery, Fort Collins, Colorado 80523-1601, USA (Hendrickson and Stetter). Present addresses (Sweet): Los Angeles Zoo, 5333 Zoo Drive, Los Angeles, California 90027, USA; (Neiffer): Center for Animal Care Sciences, Smithsonian’s National Zoo, Smithsonian Conservation Biology Institute, 3001 Connecticut Ave NW, Washington, D.C. 20008, USA. Correspondence should be directed to Julia Sweet ([email protected]).
house Station, New Jersey 08889, USA; 1.1 mg/ kg p.o.) was prescribed for 3 days. Bloodwork revealed values that were within normal limits. Edema progressed over the next weeks to include the entire facial area, as well as the elephant’s ventrum. Watery diarrhea, which was noted occasionally in early February, became a daily occurrence. Appetite decreased and the elephant developed additional edema on the medial and lateral aspects of all feet. Treatments during this time included diphenhydramine (Qualitest Pharmaceuticals Inc., Huntsville, Alabama 35811, USA; 1mg/kg), continued flunixin meglumine, pentoxifylline (Apotex Inc., Toronto, Ontario, Canada M9L1T9; 2.5mg/kg), gabapentin (InvaGen Pharmaceuticals Inc., Hauppauge, New York 11788, USA; 2.3 mg/kg), trimethoprim sulfa (Uniprimt, Macleod Pharmaceuticals, Inc., Fort Collins, Colorado 80525, USA; 18 mg/kg), and an equine gastrointestinal health supplement (Biosponget, Platinum Performance Inc., Buellton, California 93427, USA), all given orally. Repeated blood testing, fecal analyses (direct and float examination, fecal cultures, gram stain, fecal cytology), and fecal sand checks did not provide additional information to assist diagnosis. Further diagnostic testing of the abdominal and thoracic cavity was elected, and the elephant was immobilized for bronchoalveolar lavage, transabdominal ultrasound, and abdominocentesis; however, the results of these procedures were unremarkable. In another attempt to secure a diagnosis, an exploratory laparoscopy was performed in early March. Reproductive disease, peritonitis, and
941
942
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 1. Drawing shows the positioning of an African elephant and the location of the spinal needles to determine incision placement for left flank laparoscopy (close up, posterior view).
gastrointestinal or other abdominal problems were possible differential diagnoses explored through laparoscopy. The elephant was handinjected with a combination of detomidine (Dormosedan, Pfizer Animal Health, Exton Pennsylvania 19341, USA; 0.014 mg/kg) and butorphanol (ZooPharm, Laramie, Wyoming, 82070, USA; 0.014 mg/kg) intramuscularly in the left hind limb. An additional 30 mg of each drug was injected via both the intravenous and intramuscular routes to achieve the appropriate level of sedation for standing surgery. The elephant was moved into a static chute (restraint stall) for the surgery, and remained standing for the duration of the procedure (about 3.5 hr). To maintain an adequate level of sedation, the elephant received 20-mg increments each of detomidine and butorphanol intravenously throughout the procedure for a total of 300 mg detomidine and 300 mg butorphanol. Surgeons and equipment were placed on an elevated table to facilitate access. Surgical preparation, consisting of alternating scrubs with povidone–iodine and isopropyl alcohol, was performed just cranial to the left tuber coxae and sterile drapes were placed over the area. A line block was performed using 300 ml of 2% lidocaine (PhoenixTM, Clipper Distributing Company LLC, St. Joseph, Missouri 64507, USA) in multiple areas.
Two 10-ga spinal needles were placed perpendicular in the skin 10 cm rostral to the tuber coxae, with the first needle placed at the expected ventral border of the nearest rib (Figs. 1–3). The second needle was placed 15 cm ventral to the first, and both were advanced slowly into the muscles of the paralumbar fossa to confirm lack of bone at the planned incision site. Using a number 22 scalpel blade, a 10-cm vertical incision was made through the skin and subcutaneous tissues into the paralumbar fossa of the left flank. Chest retractors (Miltex Instruments, Lake Success, New York 10042, USA) were placed to aid in visualizing the muscle. The external and internal abdominal oblique muscle layers were sharply incised and modified Finocetto chest retractors (Miltex) (retractor blades were replaced in-house with blades lengthened to 6 inches) were used to retract the skin and muscle layers. The transverse abdominus muscle layer was separated along the natural fiber plane. The fibroelastic portion of the peritoneum was exteriorized through the flank incision by the use of vulsullem forceps. The fibroelastic layer as well as retroperitoneal fat was excised to reveal the peritoneum. A 3-cm incision was made into the peritoneum and number 2 polydioxanone (PDS II 3.0 metric, 70 cm on a reverse cutting needle, Ethicon Inc., Guaynabo, Puerto Rico 00969, USA) suture was used to place a purse-string suture in the peritoneum and around the laparoscopic cannula. Insufflation commenced at 52–78 mm Hg (1–1.5 pounds/inch2), using a specially designed insufflator (designed by a member of the surgical team) with ambient air. A laparoscope designed for use in elephants was placed through the cannula for visualization of the caudal dorsal abdomen, left kidney, and ovaries, which all appeared normal. The broad ligament in conjunction with the uterus had numerous small firm pedunculate structures, and biopsies of these were taken for histopathology, culture, and banking (freezing). Surgeons did not note gross evidence of peritonitis. Samples of free fluid in the abdomen were collected for cytology and culture. After samples were collected, 25 L of crystalloid fluids (Lactated Ringers Solution, Abbott Laboratories, North Chicago, Illinois 60064, USA) instilled with 20,000 mg amikacin sulfate (Amiglyde-V, Fort Dodge Animal Health, Fort Dodge, Iowa 50501, USA) and 6 million units of penicillin G potassium (GC Hanford Manufacturing Company, Syracuse, New York 13201, USA) were delivered into the peritoneal cavity using a large-animal intravenous set attached to the laparoscopic cannula. The
SWEET ET AL.—LAPAROSCOPY IN AN AFRICAN ELEPHANT
943
Figure 2. Drawing shows the positioning of an African elephant and the location of the spinal needles to determine incision placement for left flank laparoscopy (posterior view).
944
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 3. Drawing of the lateral aspect of an African elephant showing the spinal needles (placed to determine incision placement for left flank laparoscopy) in relationship to the tuber coxae (dashed line).
elephant was given flunixin meglumine (Flunazine, Bimeda, LeSueur, Minnesota 56058, USA; 1.1 mg/kg) and ceftiofur crystalline free acid (Excedet, Pfizer, New York, New York 10017, USA; 5.4 mg/kg) intramuscularly. Peritoneal and muscle layers were closed with size 2 polydioxanone II suture in a simple continuous pattern. The skin layer was closed with number 5 stainless steel suture (Ethicon 7.0 metric, 75 cm conventional cutting surgical steel monofilament, Ciudad Juarez, Chihuahua 32574, Mexico) in a horizontal mattress pattern with stents made from extension-set tubing (Abbott Laboratories) cut into 1.27-cm (0.5-inch) lengths and sterilized in ethylene oxide (Fig. 4). Additional appositional skin sutures were placed in a simple interrupted pattern using size 2 monofilament nylon suture (Monosof, Syneture/Covidien Mansfield, Massachusetts 02048, USA). Naltrexone (Taylor’s Pharmacy, Winter Park, Florida 32789, USA; 0.09 mg/kg) and yohimbine (Premier Pharmacy Labs, Inc, Weeki Wachee, Florida 34613, USA; 0.09 mg/kg) were given intravenously as reversal agents. An additional dose of
naltrexone (0.16 mg/kg) and yohimbine (0.07 mg/kg) were injected intramuscularly at the end of the procedure. The elephant walked out of the stall 7 min following the last intramuscular injections. Eight days later, the elephant was euthanized due to quality of life concerns. Lack of response to therapy coupled with worsening diarrhea, edema in all limbs, lameness, and overall discomfort led to the decision to humanely euthanize the animal. Gross necropsy and histopathologic examination revealed a wide range of pathology with the most significant lesions found in the stomach, proximal small intestine, colon, and kidneys. The most consistent lesion found in the stomach, upper small intestine, and colon was mucosal damage (including ulceration) not associated with any identifiable infectious etiology. Bacteria and yeast were noted in some areas and were considered secondary invaders of the damaged mucosa. The histologic appearance of these lesions supported an acute to subacute timeframe (days to weeks). All of the lesions in the gastrointestinal tract had the appearance of ischemic damage with fibrin,
SWEET ET AL.—LAPAROSCOPY IN AN AFRICAN ELEPHANT
Figure 4. Appearance of 10-cm vertical incision site showing surgical closure with stents in an African elephant that underwent exploratory left flank laparoscopy.
thrombi, and vascular lesions leading to loss of the overlying mucosa, and their character suggested a toxic exposure. Renal lesions were characterized by acute to subacute, multifocal, and moderate to severe renal papillary necrosis with associated tubular mineralization, scattered tubular epithelium regeneration, and squamous metaplasia. Other significant lesions included a single focus of hepatocellular necrosis with intralesional yeast bodies, a focal deep tongue ulcer, and whole body edema with severe subcutaneous edema and mechanical rupture of the epidermis in all four feet. The structures biopsied from the broad ligament were diagnosed as leiomyomas, benign smooth muscle tumors, unrelated to the primary disease. Considering potential toxins and the fact that the renal lesions noted are pathognomonic for nonsteroidal anti-inflammatory drug (NSAID)– induced papillary necrosis, the drug history of NSAID administration in this elephant in combi-
945
nation with an endogenous stress steroid response was considered the most likely cause for the gastrointestinal and renal pathology. Based on bloodwork, renal papillary necrosis did not cause significant renal impairment in this elephant. The major lesion that cannot be explained by gross or histopathologic findings is the presence of edema of the subcutaneous tissue and limbs. The basic pathogenesis of edema indicates that it results from decreased oncotic pressure (low protein), increased hydrostatic pressure, microvascular leakage, or decreased lymphatic drainage. Bloodwork examined throughout the animal’s illness did not reveal hypoproteinemia, and the absence of cardiac disease does not support increased hydrostatic pressure as the cause of edema. Vascular lesions were noted in the gastrointestinal tract, yet were not a feature in other organs and tissues affected by edema, and therefore microvascular damage is unlikely. Decreased lymphatic drainage due to reduced mobility may have contributed to the edema in this elephant; however, a diagnosis was not obtained. Decreased mobility would certainly help to explain the severe edema of the limbs and feet at necropsy. Unfortunately, no etiology responsible for the initial clinical signs could be determined. This procedure would not have been possible without the previous work done in the field by the Elephant Population and Management Program (EPMP), an international collaboration of wildlife specialists, veterinarians, veterinary technicians, industry partners, and game reserve/national park managers who are working together to address elephant overpopulation in southern Africa. These techniques and specialized equipment were first used in the field in South Africa to perform vasectomies on elephants in small game reserves, a project which started in 2005.3–7 According to a report summarizing the important considerations of laparoscopy in megavertebrates from experience gained in a white rhinoceros,2 having the ability to utilize these megavertebrate instruments was essential to advancing laparoscopic methodologies in these species. In that case, the author found that specialized insufflation equipment is also invaluable for successful visualization of the abdominal cavity. His subsequent design and implementation of this unit proved invaluable for the EPMP as well as for this exploratory laparoscopy. Laparoscopy allowed for evaluation of part of the reproductive and gastrointestinal tracts and peritoneal cavity in this elephant. Surgical time as well as anesthesia time was minimized. Looking to the future, laparoscopy is
946
JOURNAL OF ZOO AND WILDLIFE MEDICINE
feasible in megavertebrates and may be employed for abdominal exploration as well as organ or other tissue biopsy in such animals.
LITERATURE CITED 1. Radcliffe RM, Hendrickson DA, Richardson LG, Zuba JR, Radcliffe RW. Considerations for laparoscopy in megavertebrates. In: Proc Am Assoc Zoo Vet, Int Assoc Aquatic Anim Med, joint conference; 2000. p. 81–82. 2. Radcliffe RM, Hendrickson DA, Richardson LG, Zuba JR, Radcliffe RW. Standing laparoscopic-guided uterine biopsy in a southern white rhinoceros (Ceratotherium simum simum) J Zoo Wildl Med. 2000;31:201– 207. 3. Stetter M. Laparoscopy as an aid to animal care and conservation in elephants. J Elephant Managers Assoc. 2004;15(2):44–47. 4. Stetter M, Grobler D, Zuba JR, Hendrickson DA, Briggs M, Castro L, Neiffer D, Terrell S, Robbins PK, Stetter K, Ament BS, Wheeler L. Laparoscopic repro-
ductive sterilization as a method of population control in free-ranging African elephants (Loxodonta africana). In: Proc Am Assoc Zoo Vet, Am Assoc Wildl Vet, Assoc of Zoos, and Aquar, Nutr Advisory Group; 2005. p. 199–200. 5. Stetter M, Hendrickson DA. Laparoscopic surgery in the elephant and rhinoceros. In: Miller RE, Fowler ME (eds.). Fowler’s zoo and wild animal medicine, Volume 7, Current therapy. St. Louis (MO): Elsevier; 2011. p. 524–530. 6. Stetter M., Hendrickson DA, Zuba JR, Stetter K, Grobler D, van Altena JJ, Small LA. Laparoscopic vasectomy as a potential population control method in free ranging African elephants (Loxodonta africana). In: Proc International Elephant Conservation and Research Symposium; 2006. p. 177. 7. Zuba JR, Stetter MD, Dover SR, Briggs M. Development of rigid laparoscopy techniques in elephants and rhinoceros. In: Proc Am Assoc Zoo Vet, Annual Meeting; 2003. p. 223–227. Received for publication 6 January 2014
