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PAPERS & ARTICLES

Scabies in free-ranging mountain gorillas

(Gorilla beringei beringei) in Bwindi
Impenetrable National Park, Uganda
G. KALEMA-ZIKUSOKA, R. A. KOCK, E. J. MACFIE
Between August and December 1996, there was an outbreak of a debilitating skin disease attributed to
Sarcoptes scabiei infection in mountain gorillas (Gorilla beringei beringe,) in Bwindi Impenetrable National
Park in Uganda. All four members of a gorilla group which had been habituated to tourists were clinically
affected; the infant male gorilla was most severely affected and died, the juvenile male showed serious
manifestations of the disease and the two adult animals showed milder signs. The three older animals
recovered after a single intramuscular dose of ivermectin. S scabiei mites were observed on skin scrapings
and biopsies taken while the juvenile was immobilised and in postmortem samples taken from the infant.
The clinical signs did not recur during the following year, and no other gorilla groups in the park were
observed to be clinically affected.

MOUNTAIN gorillas (Gorilla beringei beringei) are an CASE REPORT

endangered species, with only approximately 650 remaining
in Rwanda, the Democratic Republic of Congo and Uganda. Study area and invesfigation of the outbreak
Approximately 290 gorillas live in Bwindi Impenetrable The outbreak occurred during the wet season of 1996 in
National Park, Uganda, where two of 28 gorilla groups have Bwindi Impenetrable National Park, south-western Uganda,
been habituated for tourism and one for behavioural a tropical montane and lowland forest covering an area of 330
research (McNeilage and others 1998). The policy adopted km2 and ranging in altitude from 1190 to 2607 m.
by the government agency responsible for gorilla health, the Temperatures range from 7 to 15°C at night, to 20 to 27°C
Uganda Wildlife Authority, limits any veterinary interven- during the day. The affected gorilla group, known as the
tions to diseases caused by human beings or life-threatening Katendegyere group, was ranging at 0.960 south longitude and
conditions, to minimise the disturbance to the animals' nat- 29.60 east latitude where gorillas were occupying the ground
ural behaviour. Gorillas are considered to be susceptible to in thick, dense and mainly secondary forest, and there was a
many human diseases because of their close genetic simi- tourist site, Buhoma, adjacent to its range. Veterinary Record (2002)
larity and suspected naivety to most human pathogens (Ott- 150, 12-15
Joslin 1993, Osborn and Lowenstein 1998, Wallis and Rick Clinical history of the Katendegyere mountain
Lee 1999). Intense efforts are made to prevent the trans- gorilla tourist group G. Kalema-Zikusoka,
mission of disease between people and gorillas during the At the beginning of 1996 the Katendegyere group had six mem- BVetMed, MRCVS,
visits of tourists and in the course of research; they includebers. However, in May, the lead silverback, Mugurusi, died of Veterinary Unit, Uganda
limiting human approaches to more than 5 m, burying old age-related changes including renal and cardiac failure. Wildlife Authority,
human excreta at least 30 cm deep, and restricting entry to After his death, a young silverback, Kalema, left the group. At PO Box 3530, Kampala,
clinically healthy visitors (Macfie 1992). Other measures the time of the disease outbreak, the group consisted of one Uganda
include chasing gorillas from private land surrounding the adult male silverback, one adult female, one juvenile male and R. A. Kock, MA, VetMB,
park, especially when the gorillas are feeding on people's one infant male. The observers believed the group to be more MRCVS, Field
banana plants. stressed during tourist visits, possibly because the usual tourist Conservation and
Scabies or sarcoptic mange is a contagious skin disease groups of six people outnumbered the gorillas. In May 1996, Consultancy Zoological
caused by Sarcoptes scabiei mites, which are generally con- the gorilla group crossed the border into the Democratic Society of London, c/o
sidered host-specific, but can cause disease in other hosts. Republic of Congo and raided banana plants in an area where OAU IBAR Pan African
The pathogenesis of sarcoptic mange is well known the local farmers have been reported to have rough skin. Programme for the
(Soulsby 1982, Wall and Shearer 1997) and the disease has In August, the field staff reported that the Katendegyere Control of Epizootics,
been recorded in a wide variety of species including human gorillas were losing hair and developing white, scaly skin. The PO Box 30786, Nairobi,
beings, and domestic and wild animals. Mange is becoming condition had never been observed in these animals since Kenya
an important disease of free-ranging wildlife (Valenzuela their habituation had begun in 1992. A health check was made E. J. Macfie, DVM, MS,
and others 2000) and reported hosts in Africa include by observing the gorillas at a distance of approximately 5 m International Gorilla
wild chimpanzees (Pan troglodytes schweinfurthii) (Pusey with and without binoculars. The seven-month-old infant Conservation
1998, Wallis and Rick Lee 1999), and cheetahs (Acinonyx male had lost hair on its back and most of its body and was Programme, PO Box
jubatus) (Mwanzia and others 1995). Scabies is said to be exceptionally pale and emaciated, but it was still alive and 10950, Kampala, Uganda
commonly diagnosed in people in the vicinity of Bwindi clung on to its mother. The infant was heard crying on sev-
Park. eral occasions, and may have been in discomfort. The juvenile Mrs Kalema-Zikusoka's
The species of mite involved, the host's immune status male had lost hair on the back of his legs, and on his inner present address is
and degree of exposure, the parasite burden and stressors elbow and neck. The adult female in the group had also lost Environmental Medicine
are thought to influence the severity of the clinical disease hair on the back of her legs and chest, where she carried her Consortium and
(Soulsby 1982, Wall and Shearer 1997). This paper describes infant. The silverback male did not show any outward signs Department of Clinical
the management of an isolated outbreak of scabies in a free- of disease, but appeared to be scratching more frequently than Sciences, North Carolina
ranging group of mountain gorillas which were habituated usual, as did the female and the juvenile. State University College of
to visitors. The outbreak resulted in morbidity and mor- Veterinary Medicine, 4700
tality, but the clinical signs resolved after treatment. Immobilisation and anaesthesia of the juvenile Hillsborough Street,
The implications for the health of people and gorillas are gorilla Raleigh, North Carolina
discussed. On the basis of the clinical signs shown by the group it was 27606, USA

12 The Veterinary Record, January 5, 2002

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FIG 1: (a)
Photomicrograph of the
skin from the ear pinna
of an infant mountain
gorilla with marked
parakeratotic
hyperkeratosis
associated with scabies.
Parts of three mites and
one egg are visible
within tunnels in the
thickened stratum
corneum. There is also
intracellular oedema of
the basal layer and mild
dermal oedema with
minimal inflammation.
Haematoxylin and
eosin. Bar = 70 pm.
(b) Photomicrograph of
skin from the ear pinna
of an infant mountain
gorilla with scabies. A
female mite and three
eggs are visible in an
epidermal tunnel,
confirming that the
mites were replicating
on the host.
Haematoxylin and
eosin. Bar = 35 pm
decided to immobilise the juvenile male gorilla. The infant
was the worst affected of the group but it was decided not to
sample it because its mother was very shy and difficult to
approach for her to be immobilised. The juvenile gorilla, with
an estimated bodyweight of 30 kg, was immobilised with 310
mg of ketamine (100 mg/ml ketamine hydrochloride, Ketaset;
Fort Dodge Laboratories). The drug was administered intra-
muscularly from approximately 4 m by means of a 3 ml dart
with a heavy duty, cuffed steel 38 mm x 0 I mm gauge needle,
fired from a carbon dioxide-powered pistol and blowpipe
pressurised to 3 5 bar (Telinject; Sauger). Anaesthesia was
induced after four-and-a-half minutes. Twenty minutes after
the first dose, an additional 200 mg of ketamine was admin-
istered intramuscularly because the gorilla was waking up and
pulling out the stitches at the site of its biopsy. During the pro-
cedure the gorilla's body temperature was 36 8°C, its heart
rate was 100 bpm and its respiration rate was 16 bpm. The
time from induction to when the animal was eating and walk-
ing towards the rest of the group was one-and-a-half hours.
Clinical examination and treatment of the
juvenile gorilla
The gorilla had signs of muscle atrophy and it was in poor
body condition. The skin showed generalised chronic der-
matitis and alopecia on the back of the legs, inner elbows,
hips, axilla, groin and neck area, with thinning hair over
approximately 90 per cent of the body. The skin was excori-
ated, thickened and scaly. There was evidence of secondary
trauma, and the animal was scratching even under the effects
of ketamine.
A 2 cm x 0 5 cm full thickness epidermal biopsy was taken
from the anteriolateral aspect of the right foot at the junction
of normal and affected skin, using a number 22 blade. The
biopsy site was closed with three simple interrupted 3-0 (2
metric) dexon (polyglycolic acid) sutures (Davis and Geck).
The biopsy was preserved in 10 per cent formalin in saline.
Skin scrapes were collected from the left hip, back and ante-
riolateral aspect of the right foot, and put directly into saline-
The Veterinary Record, January 5, 2002
PAPERS & ARTICLES
moistened test tubes and kept cool. Blood samples were col-
lected from the tarsal vein because the usual site for
venepuncture, the femoral vein, was difficult to locate owing
to the thickening of the skin in the inguinal area. The 10 ml
samples were placed in tubes containing ethylenediamine
tetra-acetic acid and heparin and in uncoated vacuum tubes.
A urine sample was collected from the immobilised animal
when it urinated during the procedure. Faecal samples col-
lected during tracking and while the gorilla was immobilised
were examined for parasites and cultured for aerobic bacte-
ria. All the samples were kept at 40C for 24 hours.
The gorilla was given 0 5 ml, approximately 0 17 mg/kg
of ivermectin 1 per cent (Ivomec 10 mg/ml; Merck) intra-
muscularly for the suspected mite infection. It was also given
2 ml of long-acting streptopenicillin antibiotics (Streptopen
250,000 iu; Bremer Pharma; procaine penicillin G 200 mg and
dihydrostreptomycin sulphate 250 mg, equivalent to 200 mg
base streptopenicillin, which provided 167,000 iu/kg and 16-7
mg/kg, respectively) intramuscularly for a suspected sec-
ondary bacterial infection. Oxytetracycline gentian violet
spray (Oxytetracycline 5 0 per cent and gentian violet 0 4 per
cent OTC-Spray; Bremer Pharma) was applied to the crusted
areas which accounted for approximately 50 per cent of the
gorilla's body surface. In addition, 0 5 ml of Ferrum 10 per
cent + vitamin B12 (100 mg iron in the form of ferric iron dex-
tran complex and 1-5 [tg vitamin B,2, Cyanocobalamin;
Bremer Pharma) were administered intramuscularly.
The skin scrapes revealed numerous mites resembling
S scabiei. The bodies of the mites were circular with short legs
and the third and fourth pairs of legs did not project beyond
the margin of the body. Cultures of the scrapes did not grow
fungal organisms. Bacterial cultures of the skin scrapes iso-
lated Gram-positive streptococci. The faecal samples con-
tained numerous eggs of Ascaris lumbricoides, Strongyloides
species and Oesophagostomum species, similar to those which
have previously been found in Bwindi and Virunga gorillas
(Ashford and others 1990, Hastings and others 1992, Kalema
1995).
The abnormal haematological findings were limited to a
mild eosinophilia of 6 per cent, compared with a mean (sd)
of 2-6 (2.5) per cent in captive western lowland gorillas
(Gorilla gorilla gorilla). The concentration of total bilirubin
(0.60 mg/dl), and the activity of aspartate aminotransferase
(32 iu/litre) were slightly above the baseline values of 0 17
(0-11) mg/dl and 10 1 (5 1) iu/litre recorded in captive west-
ern lowland gorillas (Fowler 1986). The urine sample con-
tained calcium oxalate crystals rather than the calcium
phosphate crystals routinely observed in free-ranging Virunga
mountain gorillas (Sleeman and Mudakikwa 1998).
Treatment of the rest of the Katendegyere
gorilla group
One week after the immobilisation of the juvenile, the group
was tracked to treat the other gorillas. Although the infant was
the first priority, the infant's mother, with an estimated weight
of 45 kg, could not be immobilised on the first day, but was
given an intramuscular injection of ivermectin (30 mg). The
male silverback, with an estimated weight of 100 kg, also
received an intramuscular injection of ivermectin (32 mg).
The following day the eight-month-old infant's dead body
was found on the trail. The body showed no signs of decom-
position or maggots, but it was emaciated and weighed 2-8 kg.
Its skin was thickened with scaling and crusts over the entire
body, and the neck, back, legs, chest and arms were devoid of
hair. The only hair on the head was on top of the cranium.
The eyes were very sunken and the ears heavily scaled and
crusted. There was evidence of inanition and pneumonia but
no other abnormal findings.
Skin scrapes from the dead infant revealed numerous
S scabiei mites, some of which were still alive and with eggs.
13
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PAPERS & ARTICLES
The skin sections showed severe cutaneous acariasis, associ-
ated with marked acanthosis, spongiosis, ballooning degen-
eration, and hyperkeratosis, but few signs of inflammation
(Fig 1).
The gorillas' behaviour made it impossible to dart them
again, so observations were made from a distance of 5 m or
more to monitor the progress of the treatment. The only
potentially adverse effect of the ivermectin treatment
observed was profuse watery diarrhoea passed by the juvenile
gorilla after the treatment, which cleared up within a week.
All three gorillas improved after one treatment with iver-
mectin. The hair on the juvenile and adult female started to
grow back within three months, and they all stopped scratch-
ing excessively within a month. Follow-up health checks were
continued for a year.
Veterinary health checks on other Bwindi gorillas
During the investigation of the disease in the Katendegyere
group, health checks were made monthly by visual observa-
tion with and without binoculars on the two other habituated
groups of gorillas. No pruritus, alopecia or scaling of skin was
observed. These groups were the Mubare group, the neigh-
bouring tourist gorilla group of Buhoma, which had 16 goril-
las with a ratio of young to adult gorillas of 1:1, and the
research group of mountain gorillas, Kyagurillo, at Ruhija in
the south east of the park, further away from the border with
the Democratic Republic of Congo, which had 12 gorillas,
also with a ratio of young to adult gorillas of 1:1.
DISCUSSION
This report is the first record of sarcoptic mange in free-rang-
ing gorillas. The outbreak was treated successfully with a sin-
gle intramuscular injection of ivermectin which relieved the
clinical signs for up to a year. Chimpanzees in Gombe,
Tanzania, have been successfully treated for scabies with oral
doses of ivermectin given in bananas (Pusey 1998), a practi-
cal method because they were routinely provided with food
(Wallis and Rick Lee 1999). The mountain gorillas in Uganda
are not fed, and the delivery of multiple doses by dart to these
gorillas is extremely difficult. The delivery of ivermectin to all
the gorillas in the group is thought to have been an important
factor in preventing them from becoming reinfected. On the
basis of the clinical findings it is difficult to understand why
a single dose of ivermectin was effective in relieving the clin-
ical signs of scabies.
The cause of the disease outbreak is unknown and further
outbreaks may occur. Possible sources of the mite include ani-
mals that the gorillas come into close contact with, includ-
ing human beings and domestic and wild animals. No signs
of scabies were observed in other animal species which came
into close contact with the gorillas in Bwindi Impenetrable
National Park. However, the possibility that other wild ani-
mal species could have been the source of scabies cannot be
ruled out, because other species in the park are not monitored
as intensively as the gorillas.
There is an apparently high prevalence of scabies in peo-
ple living close to Bwindi Impenetrable National Park, who
are poor and have poor standards of hygiene (Ministry of
Planning and Economic Development, Uganda 1997, Hall
and others 1998). The gorillas could have been exposed to
contaminated clothing or other fomites of infected people
either during tourist visits or when the gorillas went outside
the park boundary to raid banana crops. The distribution of
scabies lesions in the infant and juvenile gorillas was similar
to that in human beings, whose head and neck are most
severely affected (Sullivan and others 1997). The scabies could
be endemic and exacerbated by stressors, including the larger
numbers of people visiting the gorillas during each tourist
14
visit, and the reduction in the size of the group during the pre-
vious three months from six to four. As a result, this gorilla
group was observed to be less tolerant of human observation
than other tourist-habituated groups. A similar stressor may
have been responsible for the fact that Masai Mara cheetahs
in areas with a large number of human visitors developed
mange whereas those in areas with less tourist disturbance did
not (Mwanzia and others 1995).
The severity of clinical sarcoptic mange depends on the
species of mite involved, the burden of the parasites, and the
immunity of the host. The species of mite in this outbreak was
identified as S scabiei, but its source was not identified. This
mite is ubiquitous and can cause mild disease in a normal
host, but may settle in a temporary host and cause severe dis-
ease (Soulsby 1982). The youngest animal died and the juve-
nile was more affected than the adults. The slight eosinophilia
observed in the juvenile gorilla also occurs in cases of acari-
asis (Wall and Shearer 1997), and may indicate a reaction to
the mites in the skin.
Endangered species with small populations and low pop-
ulation densities may be severely affected by a non-lethal epi-
zootic disease when it is combined with other factors such as
poaching and, in the case of the mountain gorilla, habitat
destruction (Caughley and Gunn 1996, Harcourt 1996,
Valenzuela and others 2000). To manage the disease effec-
tively, it is necessary to educate rangers and trackers to observe
for signs of ill health in gorillas and other species. Improving
public health is also important (Wallis and Rick Lee 1999).
Veterinarians are working with medical personnel in the dis-
trict to educate the community about the risk of disease trans-
mission between people and gorillas and how to control it.
The Health and Wildlife sectors of the Ugandan government
are being urged to increase development and health care in
the local communities which share habitats with endangered
great apes like the mountain gorilla, which are an important
source of tourism revenue to the country.
ACKNOWLEDGEMENTS
The authors are grateful to Uganda Wildlife Authority (uWA),
the International Gorilla Conservation Programme, and to Dr
Eric Miller, Dr Jonathan Sleeman, Dr Tony Mudakikwa, Dr
Ludwig Siefert and Dr Johnston Acon for their assistance in this
investigation. In particular they thank UWA Deputy Director,
John Otekat, and field staff at Bwindi Impenetrable National
Park, including the senior park warden, Ignatius Achoka, peace
corps volunteer, Karen Archibald, and the ranger guides and
trackers. The authors thank Dr Linda Lowenstein, Dr Nancy
Kock and Professor John Cooper for the histopathology, and
Dr Chris Whittier and Dr Michael Stoskopf for editorial assis-
tance and comments on the manuscript.
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SHORT COMMUNICATIONS_
Initial investigations
into two viruses isolated
from marine food fish
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S. F. CHANG, G. H. NGOH-LIM, L. F. S. KUEH,
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THE rapid expansion of the aquaculture industry in south-
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The Veterinary Record, January 5, 2002
PAPERS & ARTICLES
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death of fish showing lethargy and anorexia with no other
clinical signs.
The fish were examined for ectoparasites on the skin and
gills. Bacterial cultures were grown from samples of spleen tis-
sue inoculated on to tryptic soy agar with 1 per cent salt and
incubated at 25°C for two days. Spleen, heart, liver, kidney and
intestine samples were fixed in 10 per cent buffered formalin,
processed and stained with haematoxylin and eosin for
microscopic examination.
Virus isolation was carried out as described by Chong and
others (1990). Proportionate samples of brain, eye, liver, kid-
ney and spleen tissue were collected, and 1 g of the pooled
samples was homogenised for inoculation into cell lines. The
threadfin samples were inoculated into BF2 (ATCC) and GF
(ATCC) fish cell lines, while the grouper samples were inocu-
lated into SB (Chong and others 1987) and GP (Chew-Lim and
others 1994) fish cell lines. The cell lines were incubated at
23°C and observed for cytopathic effect (CPE) daily for 10 days.
In the threadfins, concurrent infection with Moraxella
species and Streptococcus species was detected on one and two
occasions, respectively. Hepatic congestion and multifocal
areas of renal tubular degeneration were observed histologi-
cally. Five of six groupers were concurrently infected with flat-
worms and Trichodina species. Infection with Vibrio species
was detected in one fish. The spleens of the fish were enlarged.
On histological examination, multifocal areas of degenera-
tion were observed in the spleen. Large, round, basophilic cells
with displaced nuclei were also found, predominantly in the
spleen and kidney. A mononuclear infiltrate was observed
occasionally in heart tissue.
CPE was observed in BF2 cell lines inoculated with the sam-
ples from the threadfin on six of eight occasions. Syncytia for-
mation followed by detachment was observed. This was
similar to the CPE described by Wolf (1988) in aquatic
reoviruses. No CPE was observed in the GF cell line after 10
days. Five of six samples from the groupers produced a CPE in
the GP cell line but not the SB cell line. The CPE consisted of
round, refractile cells, which gradually affected the entire
monolayer. In both cases, the CPE was reproduced on further
passages through the respective cell lines. Both isolates were
further studied by treatment with 5-iodo-2'-deoxyuridine
15
 Downloaded from http://veterinaryrecord.bmj.com/ on June 16, 2015 - Published by group.bmj.com

Scabies in free-ranging mountain gorillas (

Gorilla beringei beringei) in Bwindi
Impenetrable National Park, Uganda
G. Kalema-Zikusoka, R. A. Kock and E. J. Macfie

Veterinary Record 2002 150: 12-15

doi: 10.1136/vr.150.1.12

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