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Laparoscopic cholecystectomy under field conditions in Asiatic black bears (Ursus thibetanus) rescued from illegal bile farming in VietnamR. Pizzi, J. Cracknell, S. David, D. Laughlin, N. Broadis, M. Rouffignac, D. V. Duong, S. Girling, M. Hunt

Nine adult Asiatic black bears (Ursus thibetanus) previously rescued from illegal bile farming in Vietnam were examined via abdominal ultrasound and exploratory laparoscopy for liver and gall bladder pathology. Three bears demonstrated notable gall bladder pathology, and minimally invasive cholecystectomies were performed using an open laparoscopic access approach, standard 10 to 12 mmHg carbon dioxide pneumoperitoneum and a four-port technique. A single bear required insertion of an additional 5 mm port and use of a flexible liver retractor due to the presence of extensive adhesions between the gall bladder and quadrate and left and right medial liver lobes. The cystic duct was dissected free and this and the cystic artery were ligated by means of extracorporeal tied Meltzer knot sutures. The gall bladder was dissected free of the liver by blunt and sharp dissection, aided by 3.8 MHz monopolar radiosurgery. Bears that have had open abdominal cholecystectomies are reported as taking four to six weeks before a return to normal activity postoperatively. In contrast, these bears demonstrated rapid unremarkable healing, and were allowed unrestricted access to outside enclosures to climb trees, swim and interact normally with other bears within seven days of surgery.

THE Asiatic black bear (Ursus thibetanus), also commonly referred to as the ‘Moon bear’ due to the white crescent on its chest, is a medium-sized bear, classified as vulnerable by the International Union for the Conservation of Nature. The main threats to wild populations are deforestation and hunting for body parts (Garshelis and Steinmetz 2008). Vietnamese black bear populations have declined rapidly (Servheen and others 1999) and there may be fewer than 100 remain-ing in the wild (Robinson and others 2006).

R. Pizzi, BVSc, MSc, DZooMed, FRES,

MACVSc (Surg), MRCVS,

J. Cracknell, BVMS, CertVA,

CertZooMed, MRCVS,

S. Girling, BVMS (Hons), DZooMed,

CBiol, MSB, MRCVS,

Royal Zoological Society of Scotland,

Edinburgh Zoo, 134 Corstorphine Road,

Edinburgh, EH12 6TS, UK

S. David, DVM

D. Laughlin, RVN

N. Broadis, BSc,

M. Rouffignac, VN

M. Hunt,Free The Bears Fund, Mekong Delta

Bear Sanctuary, Near Rach Gia, Vietnam

D. V. Duong, MD,

Center of Pathology, Bach Mai Hospital,

Hanoi Medical University, Vietnam

J. Cracknell is also at Free The Bears

Fund, Mekong Delta Bear Sanctuary,

Near Rach Gia, Vietnam and Longleat

Safari and Adventure Park, Warminster,

Wiltshire, BA12 7NW, UK

E-mail for correspondence:

rpizzi@rzss.org.uk

Provenance: not commissioned;

externally peer reviewed

Veterinary Record doi: 10.1136/vr.d4985

There are an estimated 4000 Asiatic black bears kept illegally in captivity for bile farming in Vietnam (Dang 2006). Bears are legally protected under Vietnamese law, with bear farming and bile extrac-tion banned since 1992. Captive bear numbers have, however, contin-ued to increase due to poor enforcement. Robinson and others (2006) reported no active bear farm breeding, with all bears being wild caught and smuggled from Laos and Cambodia.

Bear bile has been used in Traditional Chinese Medicine for over 2000 years to treat various ailments (Lee 1999, Pong and others 1999, Liu 2004), but farming bears for bile collection is relatively recent, starting in China in 1984 (Haikui and Zhi 2006). The Traditional Chinese Medicine Pharmacopoeia lists more than 50 herbal products with which to treat the same conditions for which bear bile is indi-cated (Pong and others 1999, Liu 2004), and the active ingredient in bear bile, ursodeoxycholic acid, is manufactured synthetically for use in standard allopathic medicine (Loeffler and others 2009). However, a cultural perception of the superiority of bear bile remains. Bile is now also added to other non-traditional non-medical products such as wine, due to the increase in bear bile farming, combined with increased eco-nomic prosperity in Asia (Loeffler and others 2009).

In Vietnam, bile collection differs from the gall bladder cannula-tion and fistula methods that have been used in China (Loeffler and others 2009), and bile is collected via needle percutaneous cholecysto-centesis, usually under ultrasound guidance. Hygiene is generally poor, with no aseptic technique (Dang 2006). This may be performed every two to three months (Dang 2006) or as frequently as several times weekly (Hunt, personal communication). Bile collection via this method results in pathology such as chronic cholecystitis and cholelithiasis, and bears rescued from bile farming have been reported

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A full clinical examination and an abdominal ultrasonography with a 3.5 MHz probe (GE Logic 100; General Electric) were per-formed under anaesthesia and blood was taken for haematology and biochemistry, which were analysed postoperatively. Bears were select-ed for surgery on the same criteria currently used by various rescue centres in South East Asia for open cholecystectomy, including nota-ble thickening of the gall bladder wall, presence of gallstones, presence of notable bile sludge, abnormal gall bladder appearance (as assessed on ultrasonography or laparoscopy) and visualisation of notable adhe-sions between the gall bladder and body wall or liver lobes.

Bears were positioned in dorsal recumbency. No tilting was performed and no repositioning was needed during the procedures. The screen was positioned at the bear’s head and the surgeon stood between the bear’s hind legs. An open approach was used to place a 10 mm primary (optical) cannula (YelloPort; Surgical Innovations). This was placed in the caudal third of the umbilical scar. The abdo-men was initially examined with a 10 mm 30° laparoscope (Karl Storz), after insufflation with carbon dioxide at a pressure of 10 to 12 mmHg. In all cases, a 5 mm secondary instrument cannula was inserted in the right upper quadrant under visualisation. Two 5 mm laparoscopic liver edge biopsies were taken for histological examina-tion. In the three cases judged to have diseased or abnormal gall blad-ders and notable adhesions, a 10 mm port with 5 to 10 mm reduction valve was inserted in the cranial midline, just caudal to the xiphoid, and a second 5 mm port in the right mid-abdominal region. The instrument ports were placed under visual examination of the abdo-men in relation to the position of the gall bladder, rather than using strict anatomic landmarks. Bariatric 45 cm length instruments in addi-tion to standard 30 cm length laparoscopic instruments were used. A single bear required insertion of an additional 5 mm port in the left upper cranial abdomen to allow the use of a flexible liver retractor (DiamondFlex; Surgical Innovations), due to the presence of exten-sive adhesions between the gall bladder and quadrate and right and left medial liver lobes (Fig 1). Port placement was similar to that used as standard in human laparoscopic cholecystectomy (McLatchie and Leaper 2006, Sindram and Ben-David 2007).

Toothed single-action grasping forceps were inserted in the right upper quadrant port and used to grasp the apex of the gall bladder. This was elevated to allow exposure of the length of the gall bladder and the hepatobiliary triangle was exposed for careful dissection by gentle lateral traction of the gall bladder neck with atraumatic forceps inserted via the right mid-abdominal/caudal port (Fig 2). Scissors were inserted in the 10 mm cranial midline port via the 5 mm reduction cap to allow careful blunt dissection of the cystic duct and judicious use of monopolar radiosurgery (Surgitron; Ellman) dissection with the closed laparoscopic scissor tips on low-power coagulation setting. Instruments were changed between ports as needed. Once a suitable sized window had been created in the hepatobiliary triangle, start-ing at the gall bladder neck and working proximally, 4 metric gauge

to suffer from a high incidence of hepatic and gall bladder neoplasia (Loeffler and others 2009). Bears kept for bile farming in Vietnam do not generally survive more than four to five years of exploitation (Dang 2006). Asiatic black bears may live up to 30 years in captivity when not kept for bile farming (Garshelis and Steinmetz 2008).

Almost all bears rescued from Chinese bile farming have dem-onstrated cholecystitis and other notable hepatobiliary pathology, necessitating cholecystectomy (Loeffler and others 2009). The exact incidence of hepatobiliary pathology associated with the Vietnamese method of bile collection and the proportion of rescued bears needing cholecystectomy have not yet been reported.

Materials and methodsA group of nine rescued Asiatic black bears kept in a rescue centre in southern Vietnam were examined by ultrasound and laparoscopy for hepatobiliary disease. Laparoscopic cholecystectomies were performed in three of these adult Asiatic black bears, weighing 150, 125 and 108 kg. All bears had previously been confiscated and rehabilitated. The bears’ exact ages were unknown and it was uncertain how frequently they had been illegally ‘milked for bile’ before their admission to the rescue centre.

Anaesthesia was induced using a combination of tiletamine-zolazepam (100 mg/ml Zoletil; Virbac) reconstituted with medeto-midine (1 mg/ml Domitor; Pfizer) at a dose of 1.25 mg/kg tiletamine-zolazepam and 12.5 μg/kg medetomidine, which is equivalent to 1.25 ml/100 kg of the tiletamine-zolazepam-medetomidine combina-tion (Caulkett 2007). The induction agents were administered via intra-muscular injection using remote chemical immobilisation (VARIO 1V Blowpipe-pistol; Telinject). Bears were then intubated using 16 mm internal diameter, low-volume, high-pressure cuffed red rubber endotra-cheal tubes (Arnolds) under head torch (Petzl) illumination. The bears were maintained with spontaneous ventilation with isoflurane (IsoFlo; Abbot Laboratories) and oxygen on a large animal circle. Anaesthesia was additionally monitored with side-stream capnography (Capnovet-10; Vetronics), arterial blood gases (EPOC; Woodley Equipment), rectal/oesophageal thermistor probe (International Animal Rescue) and a respirometer (Wright Mark 14; Spire). At the end of surgery, 20 μg/kg atipamezole (Antisedan; Pfizer) was given intravenously and 40 μg/kg atipamezole intramuscularly once the bear was returned to its enclosure.

FIG 1: Ventral laparoscopic cholecystectomy port insertion sites in the bears. The white cross indicates the extra port site used for the 5 mm flexible liver retractor used in a single bear with extensive adhesions

FIG 2: Retraction for initial dissection of the hepatobiliary triangle starting at the neck of the gall bladder

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braided polyglactin 910 (Vicryl; Ethicon) suture was passed around the cystic duct and extracorporeal Weston knot loop ligatures were placed with a knot pusher. Two ligatures were placed proximally and two ligatures distally (Fig 3). In two bears, the cystic artery was closely associated with the cystic duct and was included in the ligature. In one bear, a tortuous cystic artery was present, well separated from the cystic duct. Haemorrhage from this vessel occurred during dissection and was controlled by application of laparoscopic haemostatic tita-nium clips (Endo clip titanium; Auto Suture), two applied proximally and a single clip applied distally. In this bear, the abdominal cavity was lavaged with warm physiological saline and suctioned.

The cystic duct was carefully sectioned with laparoscopic curved double action scissors and the cystic artery was further cauterised with monopolar radiosurgery. Tension was applied to the neck of the gall bladder to lift this away from the liver bed, while the gall bladder was dissected free of the liver with monopolar surgery and blunt and sharp scissor dissection (Fig 4). The liver bed was then again carefully inspected for any possible bile leakage or minor haemorrhage. The gall bladder was placed into a 225 ml volume, impervious, lightweight rip-stop polyethylene-coated nylon bag (E-sac; Espiner Medical), inserted via the cranial 10 mm port and removed (Fig 5). Bile was sampled for bacteriology and the removed gall bladder examined for pathology. Sections of gall bladder were stored in 10 per cent neutral-buffered for-malin for later histopathological examination. All ports were closed with muscular layer suture of 3.5 mm polydioxanone (PDS II; Ethicon) and intradermal 3 metric poliglecaprone (Monocryl, Ethicon).

Two laparoscopic procedures were performed in a day. The bears that only had laparoscopic liver biopsies performed were given 15 mg/kg oral amoxicillin (Amoxil; GlaxoSmithKline) twice daily for five days and 0.1 mg/kg meloxicam (Metacam; Boehringher-Inglheim) orally once daily for three days. The bears that had laparoscopic chole-cystectomies performed were given 15 mg/kg oral amoxicillin twice daily for seven days and 0.1 mg/kg meloxicam orally once daily for five days; a single bear was also given 1 mg/kg paracetamol/codeine (Solpadol; Sanofi) orally twice daily for three days, as it was slightly more subdued.

ResultsAll bears undergoing exploratory laparoscopy and liver biopsy made rapid recoveries, climbing within their indoor dens and standing on their hind legs normally within 12 hours. Of the three bears that underwent laparoscopic cholecystectomy, two made a similar rapid recovery to the bears only having had laparoscopic liver biopsy, whereas one bear was subdued for three days postoperatively. This bear had demonstrated on previous behavioural observations to be very sensitive to any changes in routine. Because postoperative pain, as a contributing factor, could not be ruled out, the bear was given paracetamol/codeine as additional postoperative analgesia. All bears were allowed unrestricted access to climb, stand and walk around

in their indoor enclosures immediately postoperatively and for the first five days. All bears returned to normal outdoor access, access to swimming pools, climbing trees and normal physical contact such as wrestling with other bears by day 7. All bears have remained clinically unremarkable ten months postoperatively.

Histopathology confirmed chronic inflammatory changes and mucosal degeneration in the three bears that underwent laparoscopic cholecystectomy. Microbiological culture failed to isolate any organ-isms. All three bears also had moderate hepatic steatosis. Two of the other bears that only had laparoscopic liver biopsies demonstrated mild hepatic fibrosis on histopathology.

DiscussionMinimally invasive surgical techniques such as laparoscopy hold nota-ble advantages over open abdominal surgery in captive wild animals. These advantages include small wounds, reduced postoperative pain, rapid recoveries, low rates of postoperative infection and low risk of wound dehiscence. Endosurgery also provides magnified visualisa-tion of target organs (Bailey and Pablo 1999, Cook and Stoloff 1999, Freeman 1999, Lhermette and Sorbel 2008). In dogs, laparoscopic cholecystectomy has been demonstrated to result in less postopera-tive inflammatory response and hence adhesion formation than open cholecystectomy (Szabó and others 2006). Gamal and others (2001) found in an experimental group that no dogs undergoing laparoscopic cholecystectomy developed postoperative adhesions unless liver bed

FIG 3: Extracorporeal ligation of the distal and proximal cystic duct using a Meltzer extracorporeal knot, 4 metric polyglactin 910 suture and a laparoscopic knot pusher

FIG 4: Dissection of the gall bladder free from the liver bed with blunt and sharp dissection using 3.8 MHz monopolar radiosurgery (Surgitron; Ellman) applied via laparoscopic scissors

FIG 5: The gall bladder is placed in an impervious ripstop polyethylene-coated nylon bag (E-sac; Espiner Medical) intact for extraction

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lacerations or significant haemorrhage occurred. In contrast, a higher rate of abdominal adhesions was found after open cholecystectomy.

The laparoscopic surgical approach described here is similar to that currently used in human surgery (McLatchie and Leaper 2006, Sindram and Ben-David 2007). Mayhew and others (2008) also described a similar four-portal technique for laparoscopic cholecys-tectomy in dogs for the management of uncomplicated gall bladder mucocele. However, they reported the need for a 10 mm fan liver retractor. A liver retractor was not needed in two of the bears in this study, despite the large liver size and the abdominal and liver adhe-sions encountered. In human and canine laparoscopic cholecystecto-mies, the cystic duct can be ligated with the use of laparoscopically applied ligating clips. This was not possible in the bears due to the wide diameter of the cystic duct, and thick fibrous nature of the cystic duct wall, and extracorporeal knotted absorbable ligatures were used instead. Gurusamy and others (2010) reported no increase in postop-erative morbidity related to absorbable bile duct occlusion methods in human beings.

Extrahepatic biliary surgery, such as cholecystectomy, in domestic dogs has been associated with high postoperative morbidity and mor-tality. Reported survival rates range from 68 to 78 per cent (Mehler and others 2004, Pike and others 2004, Worley and others 2004). These rates are believed to be associated with the severity of the underlying diseases such as necrotizing cholangitis and their effects on the ani-mals, such as septic or bile peritonitis, rather than complications of the surgery (Mehler and others 2004). Laparoscopic cholecystectomies in human beings have lower postoperative morbidity and mortality than in dogs, likely in part due to the differing pathology. The procedure is most commonly performed in human beings for symptomatic chole-lithiasis (Sindram and Ben-David 2007). McLatchie and Leaper (2006) reported the postoperative mortality as 0.1 to 0.5 per cent.

Anomalous ductal anatomy and aberrant anatomy of the hepat-ic artery, particularly, the right hepatic artery is present in up to 20 per cent of human cases. The most frequent serious complications are common bile duct injuries, which occur in less than 1 per cent of cases, but are life threatening (McLatchie and others 2007). These injuries may be due to misidentification and complete transection of the common bile duct, or damage from indiscriminate cautery, hae-mostatic clip application, careless dissection or applying inappropri-ate tension (Portenier and Sindram 2007). Postoperative bile leakage is reported in 0.02 to 2.7 per cent of human beings, and may originate from the gall bladder bed, the cystic duct, if clips slip or are incorrectly placed, or from injury to the common bile duct (McLatchie and Leaper 2006). Other complications include bleeding in up to 2 per cent of cases, and the need to convert to open surgery, with conversion rates of 5 to 10 per cent reported, dependent on the experience of the sur-geon (McLatchie and others 2007).

The common anomalies of the hepatic arterial and biliary ductal anatomy that increase the hazards of laparoscopic cholecystectomy in human beings are well described, as are classification systems for the different types of biliary injury and their avoidance during laparo-scopic cholecystectomy in human beings (Strasberg and others 1995, Meyers and others 1996, Strasberg and others 2000, Strasberg 2002, Portenier and Sindram 2007). This is essential knowledge, as while the prevalence of different hepatic arterial and biliary ductal anatomic anomalies in Asiatic black bears is unknown, the differences seen in the three bears suggest that similar anatomic variation as encountered in human beings occurs and should be anticipated and planned for. Prevention of injury to the common bile duct relies on careful dissec-tion of the hepatobiliary triangle, starting from the neck of the gall bladder, with appropriate tension and retraction direction to compen-sate for the two-dimensional visual nature of laparoscopic surgery.

While none of the bears demonstrated icterus that would be sus-pect for a common bile duct obstruction such as calculi, laparoscopy under these types of field conditions cannot always determine the patency of the common bile duct. Careful dissection of the hepato-biliary angle and a ‘critical view of safety’(Sanjay and other 2010), as well as careful preoperative ultrasonography and gentle pressure on the gall bladder during laparoscopy to empty a small amount of bile via the common bile duct, can help decrease the risk of missing an obstruction. Intraoperative fluoroscopic cholangiography or other

recent diagnostic modalities such as magnetic resonance cholangio-pancreatography, endoscopic ultrasound and endoscopic retrograde cholangiopancreatography would be the method of choice (Khan and others 2011), but are not feasible under field conditions.

Further data are still needed to evaluate the long-term clinical significance of chronic cholecystitis and associated changes after the ultrasound bile farming method used in Vietnam. Several bear species appear to have a high incidence of liver and gall bladder neoplasia in captivity, even if they have never been tapped for bile (Miller and oth-ers 1985, Hellmann and others 1991, Matsuda and others 2010). Blake and Collins (2002) found that 40 per cent of digestive pathology seen in ursid species captive in 50 institutions was neoplasia and Gosselin and Kramer (1984) found that all sloth bears examined postmortem from the Ohio zoos between 1974 to 1980 had extrahepatic biliary carcinomas.

It is unclear whether the failure to culture any microrganisms from the bile in these cases was due to the logistics in transporting samples to the laboratory or genuinely reflects an absence of an active bacterial cholecystitis. The bears had all been rescued and may have previously been treated with antibiotics.

Further work is needed to determine what level of gall bladder pathology necessitates surgical intervention, compared with medical management and monitoring. This is somewhat hampered by the limitations of diagnostics in the field, and particularly the sensitivity of veterinary ultrasonography and the portable units available local-ly in evaluating biliary tract pathology. Several studies in dogs have found a limited or poor correlation between preoperative ultrasonogra-phy and gall bladder and biliary tract pathology such as cholecystitis, abdominal adhesions and gall bladder perforation (Vörös and others 2001, Pike and others 2004, Worley and others 2004, O’Neill and others 2006, Uno and others 2009). In the field conditions that this work was performed under, the decision to remove the gall bladders of bears was subjective. None of the bears demonstrated signs of icterus. The presence or absence of chronic biliary tact pain could not be deter-mined from the bears’ behaviour or eating records. It was difficult to compare the ultrasonographic and histological findings as gall blad-ders were only removed from bears in which the gall bladder appeared to be markedly thickened on ultrasonography, and/or in those having notable adhesions present between the gall bladder and body wall or liver on initial laparoscopic examination. As the gall bladders judged subjectively to be more normal in ultrasonographic and laparoscopic appearance were not removed, these could not be assessed histologi-cally for comparison.

Minimally invasive cholecystectomy is viable in Asiatic black bears rescued from Vietnamese bile farms and holds notable welfare advantages for bears over open abdominal cholecystectomies. More data are needed on the indications for and long-term consequences and sequelae of the procedure.

AcknowledgementsSurgical instruments were donated by Surgical Innovations, laparos-copy equipment by Zoological Medicine Ltd and the Royal Zoological Society of Scotland, anaesthesia equipment by Woodleys Equipment and Vetronics Services Ltd, extraction sacs by Espiner Medical Ltd, the ultrasound machine was donated by Nola Criddle Foundation and the funds to build the veterinary treatment room were donated by the Bridgette Bardot Foundation.

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doi: 10.1136/vr.d4985 published online September 6, 2011Veterinary Record

 R. Pizzi, J. Cracknell, S. David, et al. farming in Vietnam

) rescued from illegal bilethibetanusUrsusconditions in Asiatic black bears (

Laparoscopic cholecystectomy under field

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