Abstract

A female 27-day-old mother-reared western lowland gorilla (Gorilla gorilla gorilla) that was raised in a naturalistic outdoor enclosure, in a group where social dynamics were unstable, became acutely septicemic with Aeromonas hydrophila. The infection resulted in an encephalopathy. Treatment extended over the course of 1 year and involved numerous specialists, neurologic examinations, a computerized axial topography (CAT) scan, magnetic resonance imaging (MRI), and physical therapy. Despite the treatments, motor development was significantly delayed and paralleled human infant symptoms associated with cerebral palsy. At 1 year of age the gorilla started to seizure.

The gorilla was euthanatized at 13 months of age. Necropsy revealed the posterior bilateral cerebral convexities to be severely atrophic with focally corresponding diminished white matter and dilated posterior horns of the lateral ventricles and subarachnoid spaces. There was evidence of a 0.5 cm depressed area consistent with an old infarct in the superior aspect of the left cerebellar hemisphere. Histopathology showed neuron loss and gliosis with the most severe atrophy in the depths of the sulci in the posterior parietal occipital cortex. The affected areas had mineralized neurons and macrophages. The lesion in the left cerebellar hemisphere revealed a loss of cerebellar cortical neurons.

Introduction

Aeromonas hydrophila is a gram-negative bacillus that is commonly found in soil, sewage, and in fresh or brackish water in most of the United States.^14,21,22 It has been reported to infect amphibians, fish, turtles, birds, rabbits, grey seals, and nonhuman primates through ingestion of contaminated food or water.^{1-5,10,11,13,18} A. hydrophila can infect any human and cause gastrointestinal signs. However young children, those with impaired immune systems, or people with malignant neoplasia may suffer from septicemia.^7,9,13,15 Septicemic conditions from this bacteria have also been reported in amphibians, a grey seal, turtles, a dog, rabbits, and a ground hornbill.^{1-5,9,11,12,14,15-17}

In addition, myonecrosis due to A. hydrophila infection has been reported in human patients, particularly those who are immunocompromised or have neoplasia.^6,7,11,15,23 Ischemic insult to the cerebral cortex due to septic shock can lead to permanent damage and can result in motor developmental delays similar to cerebral palsy in human infants.^14,20 Infections of A. hydrophila have been reported in seven species of Old and New World Primates. In these species A. hydrophila showed both a septicemic form as well as peritonitis.² A septicemic condition and resulting encephalopathy from this organism has not been reported in gorillas at this time.

Case Report

The female western lowland gorilla neonate had been raised for 3 weeks in the summer, in a naturalistic outdoor enclosure, that occasionally had standing water. Its mother was primiparous, was part of a group with two young but mature males, and another first-time mother. The social dynamics of this young group led to group instability at times. There were numerous minor altercations between group members, and the neonate gorilla from this report sustained several scratches on its head as a result. These are speculated to be possible points of entry for the bacterial organism. When the neonate was 27 days old it became acutely weak and lethargic. The gorilla infant was pulled from the mother and upon examination and diagnostic work-up was found to have an Aeromonas hydrophila septicemia. This resulted in an ischemic encephalopathy that caused the neonate to have delayed motor responses, a hemiparesis of the left arm, and minimal use of the legs. The muscular weakness was suspected to be caused from myonecrosis, (creatine phosphokinase (CPK) = 65,142 IU/L; normal 363 ± 407 IU/L), shock, and heart damage. Treatment consisted of ampicillin sodium (Ampicillin Sodium, Lilly, IN, USA) administered at 170 mg IV BID, together with amikacin sulfate (Amiglyde-V, Fort Dodge, IA, USA) at 12.5 mg IV TID, and digoxin (Digoxin injection, Elkins-Sinn, NJ, USA) at 6.8 µg IV once followed by 17.22 µg IV SID q 48 days. However, the organism was later found to be resistant to ampicillin, so only amikacin sulfate was continued. The gorilla was further maintained with a percutaneous indwelling catheter and total parenteral nutrition.

The clinical weakness and motor impairment gradually improved from a generalized severe paresis to a state resembling cerebral palsy motor development in humans. These similarities include delayed developmental skills and physical findings such as abnormal muscle tone, abnormal movement, and abnormal reflexes.¹⁴

A Haberman nipple was used to aid in feeding the gorilla since it initially lacked the ability to suckle properly. Once it began eating, treatment changed from crisis care and therapy to long-term management and supportive care. Daily physical therapy was used to aid in the development of motor skills. However, the age of development of her skills was considerably delayed in comparison to previous Toledo Zoo gorilla neonates and other neonatal gorillas (Table 1).

Table 1. Motor development of Western Lowland gorillas (Gorilla gorilla gorilla)

Cerebral damage was monitored using CAT scan, MRI, and periodic neurologic examinations. The initial CAT scan at 31 days of age showed possible temporal lobe attenuation. At this point the gorilla had an improved grip and no suckle reflex. An MRI at 45 days of age showed diffuse brain swelling and global hypoxia of the cerebral hemispheres. There was also extensive atrophy in the parietal area and bilateral subdural hygroma. Cortical function impairment was anticipated due to these findings. The motor development at this age included an asymmetric posture, decreased tone of the right arm and leg, and continued inability to grasp. Assistance with feeding was still required. The MRI at 94 days of age showed focal subdural collection of fluid on the left side of the brain. The gyri and the sulci were prominent and there was more generalized subarachnoid space present. The gorilla was having generalized twitching, was apraxic or dyskinetic of the right arm, and used the left arm less than the right arm. The gorilla was able to scoot at this age. An MRI at 287 days of age showed possible shrinkage of the brain in areas associated with cognitive function. Motor development by this age included rolling over, reaching randomly, and placing objects in the mouth. The lack of normal gorilla brain scans available for comparison made diagnosis difficult, but human pediatric neurologists assisted in interpretation of the scans by comparing them to human neonates.

At 1 year of age the neonate started to seizure and the antiseizure medication phenytoin (Dilantin, Parke-Davis, Morris Plains, NJ, USA) was prescribed at a dose of 20.42 mg PO BID. The medication ceased the seizures, but due to the continued lack of motor development and need for physical assistance with many skills, a decision was made by a committee named the “Sindiswa Care Committee” after the gorilla infant, to euthanatize the gorilla. The Sindiswa Care Committee was formed early on due to the high-profile nature of this case (an endangered species and an infant gorilla that was very endearing to the public and staff). The committee was formed to assess this gorilla’s progress, treatment, goals for recovery, and prognosis. The Sindiswa Care Committee consisted of the veterinary staff, mammal curatorial and gorilla keeper staff, human medical specialists, the zoo’s director and assistant director, and several members of the Toledo Zoological Society’s Board of Directors.

Necropsy revealed the posterior bilateral cerebral convexities to be severely atrophic with focally corresponding diminished white matter and dilated posterior horns of the lateral ventricles and subarachnoid spaces. There was also evidence of a 0.5-cm depressed area consistent with an old infarct in the superior aspect of the left cerebellar hemisphere. Histopathology showed neuron loss and gliosis with the most severe atrophy in the depths of the sulci in the posterior parietal occipital cortex. The affected areas had mineralized neurons and macrophages. The lesion in the left cerebellar hemisphere shows a loss of cerebellar cortical neurons.

Discussion

Collaborations were made with numerous human and medical specialists, including a neonatologist, pediatric neurologist, speech therapist, occupational therapist, and a physical therapist. These individuals worked closely with the zoo veterinary, curatorial, and keeper staff and numerous volunteers to care for the infant gorilla. They all worked in conjunction to develop plans for treatment and goals for motor development. Comparisons of human infant MRI and CRT images with those of the gorilla from this report proved very valuable for diagnostic interpretation due to lack of “normal” gorilla infant images available.²¹ The establishment of a physical therapy regimen based on those used in people was felt to have aided the progress and development of the motor skills this neonate did achieve. A motor development chart (Table 1) was created by the zoo’s gorilla keeper staff for comparison of this gorilla’s motor development progress versus that of a normal infant gorilla. These comparisons helped in assessment of clinical progress and also became prognostic indicators for the zoo’s veterinarians and staff.

This case was unique in light of the consensus-building approach and numerous people involved in making decisions on the gorilla’s care and ultimate outcome. Anthropomorphization is a natural tendency when humans and gorillas or other apes interact significantly, especially a gorilla infant under human care. Having a larger decision-making body made up partially of animal care staff very knowledgeable of normal gorilla behavior, development, and social structure helped to temper this tendency. Quality of life, animal welfare, and human safety issues were primary considerations in the Sindiswa Care Committee discussions regarding long-term condition and care. The final decision to euthanatize this animal was the result of a consensus from the Sindiswa Care Committee and the Toledo Zoological Society’s Board of Directors together. The high profile and sensitive nature of this case also required the involvement of the zoo’s public relations department in dealing with local media and a special reporter from the local newspaper.

This case demonstrates the potential severe septicemic capabilities of Aeromonas hydrophila in a neonatal western lowland gorilla, beginning with an initial insult of septic shock requiring intensive care and resulting in cerebral damage with long-term therapy. All of these led to a gorilla that never attained full sensory-motor development and was incapable of existing without human assistance. This condition has never been reported in a gorilla before, nor has the resulting encephalopathy been reported.

The gorilla was slowly making improvements, but probably would not have attained the ability to walk until at least 4–5 years of age, if ever. This would have led to a situation where the animal would not have been able to be assisted safely by humans, and would not have been able to maintain itself within a gorilla group.

The fact that this animal was being reared by a first-time mother in a socially unstable group in an outdoor enclosure may have led to increased stress for the mother and infant, subsequent development of weakness in the infant, compromised immunity, and increased susceptibility to infection.

Acknowledgments

The authors would like to thank the following people for their assistance and involvement: Dr. Howard Stein, Dr. Donald Cameron, Bobbi Miller, Char Petiniot, Andrea Walters, Deborah Paperd LVT, Diana Lydick LVT, Tim French, Donna Colcord, Betsy Hyde, Dr. E.R. Savolaine, Terry Webb, Sheri Hensley, Dr. Haynes Robinson, the staff of the Toledo Zoo, and the numerous Toledo Zoo volunteers.

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