Abstract
First time pregnancies of two western lowland gorillas (Gorilla gorilla gorilla) resulted in the live births of both neonates. The first case describes a 26-year-old wild-caught gorilla with vaginal bleeding during the third trimester of its pregnancy. Operant conditioning allowed the transpelvic ultrasonographic assessment of fetal health and placental integrity. The term pregnancy and unassisted parturition resulted with the neonate dead at 4 days of age with a cleft palate and complications from sepsis. The cleft palate was believed to be a sporadic congenital malformation. The second case describes a 10-year-old captive-born gorilla with a protracted labor requiring immobilization and labor management to vaginally deliver a normal term fetus. The neonate was resuscitated immediately upon delivery and has survived without complications. Both neonates were the only progeny of a 36-year-old wild-caught male that has since died of an aortic aneurysm.
Introduction
A perinatal team of specialists, including veterinarians, obstetricians, a radiologist, a neonatologist, and anesthesiologists worked together to oversee obstetrical conditions during the pregnancies of two western lowland gorillas. Each pregnancy and potential birth was important for these genetically unrepresented individuals.
Case Report One
A 25-year-old primiparous western lowland gorilla presented with episodes of vaginal bleeding. Both parents were wild caught with no histories of reproductively related disease. Gestational age at the onset of bleeding was 120 days and continued intermittently through 210 days of gestation. The expected range of gestational period for gorillas is 237–285 days, with a mean of 255 days, or 8.5 months.6 Urinary progesterones measured by radioimmunoassay (RIA) and chorionic gonadotropin (CG) detection (OvuQuick, Quidel Corp., San Diego, CA, USA) had confirmed the pregnancy. The gorilla had been trained to give daily urine samples upon request by the gorilla keeper. Urinary reagent strips (Hemastix, Bayer Corp., Elkhart, IN, USA) indicated consecutive days of 1+ (slight) to 2+ (moderate) blood in the animal’s urine. Urine cultures were negative for bacterial growth and urinalysis results were not consistent with cystitis. The pair had continued to copulate throughout the pregnancy and a vaginitis was suspected. Sonographic monitoring (UltraMark 4, Advanced Technology Laboratories, Bothell, WA, USA) was performed to rule out a placental or other cause of bleeding.
The gorilla was conditioned to accept the 2.25-MHz transducer probe against its ventral pelvis for 3–5-minute periods while receiving a juice or milk reward. The handheld probe was introduced between the cage bars while the animal sat on a large, end-on-end PVC pipe with an opening cut along the rim to allow the probe to be extended into the center of the PVC pipe. The gorilla was only comfortable having the gorilla keeper manipulating the probe. The sonographer was stationed with the ultrasound monitor 3 m away so that he could view the images and tell the gorilla keeper how to direct the probe placement.
During four separate exams within a 1-week period, a single living intrauterine gestation was identified in cephalic position. The cranium was fairly low in the pelvic vault and obscured the cervix internal os. The biparietal diameter (BPD) of 7.3 cm was estimated since the cavum septum and thalami were not identified. The placenta was left lateral, fundal, and tapered normally making a placenta previa very unlikely. The amniotic fluid volume was normal. The four chambered heart with a rate of 150 bpm was noted. No placental cause for the observed bleeding was determined and no fetal anomalies were detected. The value of the sonography was minimized due to the sonographer not directly performing the examination since many structures were not visualized. The vaginal bleeding resolved without treatment.
The neonate delivered unassisted during an observed parturition. The length of gestation was 262 days. The neonate was assessed as normal and determined to be suckling by experienced veterinary and gorilla keeper observations. The maternal level of care was judged as excellent. The neonate’s condition deteriorated suddenly on day four requiring a physical examination. The mother gorilla was immobilized with 5 mg/kg IM blow dart injection of ketamine hydrochloride (Ketaset, Fort Dodge, Fort Dodge, IA, USA). The presence of breast milk was confirmed. The 2.2 kg male neonate was removed for examination in a dehydrated, moribund state and died several hours later.
Gross findings at necropsy included a right-sided cleft of the hard and soft palate, subcutaneous and subdural hemorrhage with severe cerebral edema, and a mild myxomatous degeneration of the right atrioventricular valve. The right-sided cleft palate communicated with the nasal cavity as confirmed by the passage of a blunt probe through the right nostril and into the oral cavity. The u-shaped cleft tapered posteriorly to involve the distal edge of the hard palate and proximal soft palate. Postmortem three-dimensional reconstruction of computerized tomographic scans demonstrated a cleft maxilla, asymmetrical inferior turbinates, intact premaxilla, and vomer. No anomalies of the dentition, cranial base, or calvaria were noted. It was felt that the cleft palate defect had prevented any intraoral suction by the neonate during nursing attempts and no breast milk had been ingested.
Histopathology revealed a suppurative omphalophlebitis and focal suppurative encephalitis with cerebral edema. Adipose tissues, hepatocytes, and pancreatic acinar cells were atrophic.
Case Report Two
A 10-year-old, 129 kg primiparous western lowland gorilla experienced a protracted labor. Urinary progesterone levels measured by RIA and CG levels (Ovuquick) had confirmed the pregnancy and approximate date of conception. Length of gestation was estimated at 275 days. Birth watch observations by experienced gorilla keepers were ongoing from the onset of labor signaled by a watery fluid discharge presumed to be amniotic fluid covering the gorilla’s rump. Contractions and labor activities were light and infrequent (one/15 minutes). This animal had been unresponsive to attempts at conditioning for elective sonography.
The gorilla was described 24 hours later to be uncomfortable, restless, unable to sleep, and taking small amounts of oral fluids. The animal would repeatedly change position, roll over, and would often remain on its back lifting its rump slightly during each contraction. Approximately 36 hours after the onset of labor the animal was immobilized to assess fetal viability and position, amniotic fluid volume, and cervical dilation.
The gorilla was immobilized with a 5 mg/kg IM blow dart injection of ketamine hydrochloride (Ketaset) and an intravenous catheter was placed. Anesthesia was induced with isoflurane (Isoflo, Abbott Laboratories, North Chicago, IL, USA) in oxygen via face mask, followed by endotracheal intubation. The isoflurane levels required for immobilization varied from 0.5–2.5% depending on the amount of manipulation by the obstetrician. No muscle relaxant was used. The animal was monitored using a pulse oximeter (Model N-100, Nellcor, Hayword, CA, USA), automated blood pressure monitor, and EKG. Complete blood counts and serum chemistries were all within normal limits.5 Uterine contractions were abolished by the anesthesia.
Transpelvic scanning (UltraMark 4) was obtained using 2.25-MHz mechanical and 3.5-MHz curvilinear array transducers. A 1.5-cm pocket of amniotic fluid was initially present, but disappeared after additional labor. This severe oligohydramnios made the sonographic exam difficult and incomplete. A single viable intrauterine fetus was identified in cephalic, occipitoposterior position. The fetal head was in the vagina which precluded sonographic visualization and measurements of the cranium, orbits, and neck. No maternal uterine or ovarian masses were identified.
Initial attempts with vacuum extraction were unsuccessful. The stable condition of the fetus allowed the labor to be augmented with IV oxytocin (Syntocinon, Sandoz Pharmaceuticals, East Hanover, NJ, USA) at a starting dose of 6 mU/minute and increased by 6 mU every 15 minutes. The induced uterine contractions were monitored both by palpation and with sonography. The fetal pulse rate measured from the abdominal aorta dropped from 180 bpm at the initiation of the oxytocin to 130 bpm after 85 minutes. The contraction frequency, strength, and duration increased and the fetal head could be felt to be descending.
After approximately 1.3 minutes on oxytocin, the head was clearly under the pelvic symphysis and close to the pelvic floor. The vacuum extractor was reapplied without problems and was used for pulling with the contractions. The gorilla was noticeably contracting from an increase in its respiratory rate and facial grimacing. After approximately three contractions, the widest point of the head emerged through the pelvic canal. The patient sustained a vaginal laceration at this time. With gentle traction the head was delivered in the occipitoanterior position. There was no evidence of any nuchal cord. The shoulders delivered easily. The cord was clamped and cut.
The 2.54 kg anesthetized female neonate required ventilatory support with 100% oxygen. Immediately after birth, the neonate had a low heart rate with no respiratory efforts or muscle tone. The neonate was intubated with a 3.5 mm oral endotracheal tube. The neonate exhibited a markedly compressed anterior ribcage, but had no other physical abnormalities. Auscultation of the lung fields revealed adequate breath sounds, symmetric chest movement, and normal heart sounds. The neonate started to spontaneously breathe after 45 minutes and the airway was decannulated. The neonate was gavage-fed premature infant formula (Enfamil, Mead Johnson & Company, Evansville, IN, USA) to maintain its blood glucose. At 4 hours of age it was able to take small amounts of formula by nipple and progressed to a full intake during the first 24 hours. The animal has survived to date without complications.
Discussion
We describe the observations of a perinatal team of specialists surrounding the events that occurred with the pregnancies of two western lowland gorillas. Fetal growth, development, and health assessment during gestation are monitored routinely in human medicine. These same techniques can be applied to the nonhuman primate patient with expected limitations that arise from working with animals.
With the cleft palate case, the suppurative nature of the inflammation suggested the presence of a bacterial sepsis most likely originating from the inflamed umbilicus. It was not felt that the cleft palate was involved with the sepsis or the cerebral edema. There was no evidence of bronchopneumonia to suggest aspiration pneumonia. The failure of passive transfer due to the functional dysphagia of the cleft palate most likely lead to humoral immunosuppression, with a suppurative omphalophlebitis and encephalitis. The atrophy of fat, pancreas, and liver implied a malnutritional state in the neonate.
Anatomically, the cleft found in the gorilla was identical to those observed in humans with congenital disorders involving the palate. Dietary, teratogenic, and genetic causes of cleft palate are recognized. The prevalence for humans is approximately 0.4–0.8/1000 for liveborn infants in the USA but remains undetermined for nonhuman primates. Oral-facial clefts are among the most frequent congenital anomalies reported in nonhuman primates.2 The spontaneous appearance of cleft palates, with or without cleft lip, has been reported for the macaque,8 squirrel monkey,1 and tamarin3. Cleft lip and palate have also occurred in fetal macaques following intrauterine exposure to ethanol.7
The contribution of ultrasonography in the assessment of fetal health and prediction of parturition can be particularly useful when animal management changes, such as isolation or intervention, are planned for the periparturient period. Sonography could have potentially detected the cleft palate defect in the fetus, allowing zoo staff and perinatal consultants to intervene at the time of birth. Fetal BPD measurements have been published for the gorilla.10 Continued measurements of multiple fetal parameters in gorillas will assist future attempts to assess fetal growth and health. Operant conditioning of gorillas for sonography to determine fetal growth measurements needs to be completed as has been reported in other species.4,9
Acknowledgments
The authors recognize gorilla keepers, Violet Sunde and Judy Sievert, for their efforts in the operant conditioning of the gorillas to voluntarily assist with routine veterinary procedures; the zoo nursery technician staff, Harmony Frazier, Linda Shipe, and Carol Simkins; and the Departments of Neonatology, Obstetrics, and Gynecology from Swedish Hospital.
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