Comparison and Contrast Between Recent Pregnancies, Cesarean Sections, And Reintroductions of Neonates in Two Great Ape Species at Busch Gardens Tampa Bay
Ray L. Ball, DVM,1 Cathy Lynch2, MD; Mike S. Burton1, VMD; Genny Dumonceaux1, DVM; John H. Olsen1, DVM
Cesarean sections are relatively uncommon procedures in captive great apes. In the period of less than 3 years, two such procedures were performed at Busch Gardens Tampa Bay; one in a Bornean orangutan (Pongo pygmaeus) and another in a western lowland gorilla (Gorilla gorilla). In both cases the female recovered well, and the infant was successfully returned to the mother after a limited amount of hand rearing.
A captive-born 16-year-old female Bornean orangutan was diagnosed as being pregnant with an over-the-counter home pregnancy test (Clearview Home Pregnancy Test, Unipath Ltd., Bedford, UK) on September 4, 2002. Labial tumescence allowed an estimated gestational age of 4 weeks which coincided well with the last observed breeding. Oral progesterone (R.P. Scherer North America, St. Petersburg, FL, USA), 100 mg PO SID along with prenatal vitamins (PreCare, Ther-Rx Corp., St. Louis, MO, USA) was started to help support the pregnancy. Transabdominal ultrasound training was instituted, and at week 16 the fetus could be visualized. The ultrasound exams occurred at irregular intervals to monitor the progression of the pregnancy. Prenatal care also included training to allow visualization and potential manipulation of the nipples along with presenting an infant.
At 7:30 a.m. on March 11, 2003 the orangutan was seen to start labor with some pushing efforts. By 1:00 p.m. she had passed about 200 ml of clear fluid and continued to push. By 5:30 p.m., the contractions had weakened after having her water break. She was monitored all night, and by mid-morning on March 13, 2003 she had not delivered and the contractions had stopped. The orangutan was immobilized with a combination of 150 mg tiletamine/zolazepam (Telazol, Fort Dodge Laboratories Inc., Fort Dodge, IA, USA), and 32 mg xylazine (Xylazine 100, The Butler Co., Columbus, OH, USA) via blow dart. Ketamine hydrochloride, 500 mg (Ketaset, Fort Dodge Laboratories Inc., Fort Dodge, IA, USA), was administered to facilitate handling and transportation to the zoo hospital. Intravenous catheters were placed in both brachial veins and 0.5% isoflurane (IsoSol®, Vedco, Inc., St. Joseph, MO, USA) was delivered at a low flow of oxygen with the airway maintained with a jaw thrust. Examination by the consulting obstetrician revealed a viable fetus with a strong heart rate and fluid in the vaginal vault consistent with placental fluid. The orangutan was prepped for abdominal surgery. A 20-cm midline incision was made from just caudal to the umbilicus to the pubis. Intravenous 100 mg ketamine hydrochloride boluses were given every 15 minutes PRN during surgery to supplement the isoflurane. The bladder was iatrogenically incised, but this allowed visualization of the uterus. The fetal head was located cranial to the brim of the pelvis. The uterus had a tight muscular ring around the fetal head, preventing its passage. A low transverse incision was made into the uterus and a viable female fetus removed. The infant was attended to by a neonatologist but had no complications. The uterus was cleaned out and closed in two layers. The bladder was closed in two layers as well. Closure was in two layers in the linea, with additional closure in the subcutaneous and intradermal layers. The infant was allowed to nurse before being placed in recovery. The infant was placed in an Isolette in the holding facility. The following day (day 1 post surgery), the adult female was given hydrocodone/acetaminophen combination (Vicodin 5/500 mg, Abbott Laboratories, North Chicago, IL, USA) for analgesia. On Day 2, the adult appeared more depressed. The incision looked good, her mucus membranes were bright and pink, her mammary glands were swollen, and she was taking fluids from staff. A re-introduction with the infant was attempted but she displayed no interest. Additional attempts on day 3 and day 4 were made to reintroduce the infant to the adult with essentially no interest. The infant was hand reared until February 3, 2004 when she was successfully reunited with the mother. The female allowed bottles to be given to the infant/juvenile through the mesh as she was no longer lactating. Today the juvenile and female are with another adult female and continue to do well.
A captive-born primigravid 33-year-old female western lowland gorilla was diagnosed pregnant on April 24, 2005 with an over-the-counter home pregnancy test (EPT, Pfizer Consumer Healthcare, Morris Plains, NJ, USA). This gorilla had a history of a pelvic fracture in February 2004 and had a spontaneous pregnancy termination in January of 2005. Three days later the gorilla was immobilized with 185 mg tiletamine/zolazepam (Fort Dodge Laboratories Inc.), and 45 mg xylazine (The Butler Company) via a hand syringe for evaluation of the pelvis. Computed tomography showed excellent callus formation of the fractures. Pelvic exam revealed a smooth ring, but a small notch was palpated on the right side. The consulting obstetrician was concerned about a vaginal delivery at this point. Prenatal vitamins and oral progesterone were supplemented as in the orangutan case above. Prenatal training consisted of transabdominal ultrasounds and presentation of the mammary glands to the mesh for examination. The pregnancy was monitored with intermittent sonograms. There was virtually no weight gained during the course of this pregnancy (96 kg versus 98 kg). On November 15, 2005, hemorrhage was noted in the female’s holding area. No signs of labor were observed. Placenta previa or possibly cervicitis was thought to be responsible for the bleeding. The next day, (November 16), a sonogram revealed a viable fetus, but the placenta may have moved partially in front of the internal os. The gorilla showed no signs of discomfort and was otherwise well. A cesarean section was planned for in 2 weeks, pending her progression to the expected due date. The following evening, (November 17), a considerable amount of hemorrhage was noted in the holding area. Again, there was neither distress nor contractions evident. A sonogram was attempted, but the gorilla was not cooperative for this procedure. On November 18, a sonogram was performed across the mesh, but only echogenic images consistent with blood clots could be seen. The gorilla was immobilized as above, intubated, and maintained on 1.5% isoflurane. Ultrasound imaging discovered a term fetus with a slow heart rate (40 bpm) and confirmed a diagnosis of placenta previa. A midline abdominal incision was made from the umbilicus to the pubis. A vertical incision was made in the uterus and a healthy 2154-g male infant was delivered. Closure was routine. Ketoprofen 400 mg IM was given intraoperatively for analgesia, and the female recovered uneventfully. The next morning she was essentially normal.
The neonate was managed by the attending neonatologist and the veterinary staff. The infant was bradypneic and bradycardic and was immediately intubated with a 3.0 Cole tube and manually ventilated with 100% oxygen. Atipamezole, 0.4 mg, was administered IM. Within 1 minute the breathing rate increased as did the mucus membrane color and refill. The umbilicus was ligated with chromic gut, and he was extubated. The infant was placed on the female’s nipple until she was placed in recovery. The infant was fed 7 ml of a commercial human milk replacer every 2 h overnight. The following morning the infant was placed alongside the female’s holding pen. The infant was fed for the next 10 days in close proximity to the female. The staff was able to massage the nipples and maintain lactation. On day 11 post surgery the two were reintroduced without complication.
Cesarean sections are uncommon in great apes. A few reports on gorillas and no reports on the procedure in orangutans were found in the scientific literature. The prenatal care and training were similar in both cases. Both animals were conditioned to allow transabdominal ultrasound which proved useful in both cases. Both animals allowed some manipulation of the mammary glands although this was much more successful in the gorilla. The use of progesterone was done in both cases to help support the pregnancy to term as a safeguard against inadequate production by the fetal-maternal unit. The gorilla also routinely allowed hand injections.
The anesthetic and postoperative management did vary between the two animals. Low-dose tiletamine/zolazepam (∼1.5 mg/kg) with xylazine (∼0.4 mg/kg) has provided good inductions for all great apes at the facility. The gorilla was well trained for hand injection which made for a smooth and quick induction. The orangutan needed to be darted and was obese which slowed the induction. The orangutan was maintained during surgery with ketamine boluses and a low flow of isoflurane to help with muscle relaxation. It was thought that ketamine would have the least adverse effect on the infant and due to its short half-life, provide a quicker recovery. This technique had been used previously when a quicker recovery was desired or in cases where isoflurane was not available. The gorilla was intubated and managed only with isoflurane. This appeared to make the uterus much more compliant and easier to close. The use of hydrocodone may have had a negative impact on the recovery of the orangutan as well, as she appeared to be depressed while on this drug and inattentive to the neonate when early introductions were made. Ketoprofen appeared to provide excellent postoperative analgesia, as the gorilla was fully recovered the next morning and receptive to the infant. Tiletamine/zolazepam combinations have been thought to be the reason for neonatal hypoxia. In the case of the gorilla, the dose was lower than that reported and the response to atipamezole implicates xylazine as the cause for the neonatal respiratory depression.
The gorilla had an offspring 10 years earlier at another facility but failed to care for it properly. The orangutan had never given birth before, but both animals had experience with neonates in other facilities. The close proximity of the neonate to the mother was thought to be essential. The use of the opiates in the orangutan may have hindered her response to the infant.
Risk factors for the gorilla included a healed pelvic fracture, a previous miscarriage, and her age. Pelvic trauma and advanced age are both risk factors for placenta previa in women. The major risk to the orangutan was her obesity with her conception weight of 160 lb. Obesity is a risk factor for term delivery as well as anesthetic management. While both cases resulted in the return of the infant to the mothers, differences in the management may have resulted in a quicker return in the gorilla.