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Detection of antibodies to selected human pathogens among wild and pet macaques (Macaca tonkeana) in Sulawesi Indonesia.

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American Journal of Primatology 54:171–178 (2001)
BRIEF REPORT
Detection of Antibodies to Selected Human Pathogens
Among Wild and Pet Macaques (Macaca tonkeana) in
Sulawesi, Indonesia
LISA JONES-ENGEL1*, GREGORY A. ENGEL2, MICHAEL A. SCHILLACI1,
ROSNANY BABO3, AND JEFFERY FROEHLICH1
1
Department of Anthropology, University of New Mexico, Albuquerque, New Mexico
2
Department of Family and Community Medicine, University of New Mexico, Albuquerque,
New Mexico
3
Sulawesi Natural Resources Conservation Information Center, Makassar, Sulawesi,
Indonesia
Human-to-primate disease transmission can potentially cause significant morbidity and mortality among wild primate populations and thus constitutes an
important conservation issue. Our cross-sectional study examines serological
evidence of exposure to human pathogens among wild and pet macaques in
Sulawesi. Serum samples taken from 11 pet and 15 wild macaques (Macaca
tonkeana) were analyzed for antibodies to a panel of viruses commonly encountered in human populations. Antibodies to measles, influenza A, and
parainfluenza 1 were detected in sera of both pet and wild macaques. Antibodies to parainfluenza 2 and 3 were found in the sera of wild macaques only.
Possible routes of exposure, as well as implications for conservation are discussed. Am. J. Primatol. 54:171–178, 2001. © 2001 Wiley-Liss, Inc.
Key words: viral antibodies; human pathogens; primate conservation;
Sulawesi macaques
INTRODUCTION
Pathogens endemic in human populations can decimate primate populations
[Fiennes, 1967]. This phenomenon has been observed repeatedly over the past
decades in captive settings, in which epidemics of influenza, tuberculosis, chicken
pox, and measles have caused mortality rates exceeding 90% among primates,
including animals newly captured from the wild [Gibson, 1998; Mansfield & King,
1998; Ott-Joslin, 1993; Remfry, 1976].
Human-to-primate disease transmission is becoming an increasingly important issue to primate conservationists as human society encroaches on the planet’s
tropical forests [American Society of Primatologists Bulletin, 2000]. Yet, in contrast to poaching and habitat destruction, which are well-recognized dangers to
wild primates, the threat posed by human-to-primate disease transmission in
Contract grant sponsor: University of New Mexico Student Research and Allocations Committee;
Contract grant sponsor: University of New Mexico School of Graduate Studies.
*Correspondence to: Lisa Jones-Engel, Department of Anthropology, University of New Mexico, Albuquerque, NM 87131. E-mail: Jones-Engel2@worldnet.att.net
Received 11 September 2000; revision accepted 21 March 2001
© 2001 Wiley-Liss, Inc.
172 / Jones-Engel et al.
wild primate populations is not well studied [Wolfe et al., 1998]. The published
evidence for disease transmission from humans to wild primates remains largely
anecdotal and unsubstantiated by diagnostic tests and epidemiological analysis
[for review see Wallis & Lee, 1999]. Little work has been done to confirm diagnoses, establish causality, or describe conditions that influence pathogen transmission between humans and primates [but see Warren et al., 1998].
To mitigate the impact of human-originating disease on primates, it is important to understand which human pathogens are involved and how they are
transmitted from humans to primates. Epidemiological data characterizing pathogen exposures among both human and nonhuman primate populations in areas
where the two come into contact can be used to assess which pathogens are being transmitted, and to develop hypotheses regarding the likely routes of transmission. The ultimate aim is to design strategies to prevent future epidemics
among wild primates—epidemics that could further compromise species already
endangered or on the brink of extinction. These data may also advance the study
of emerging infectious diseases that potentially threaten human populations.
The present study takes a first step toward learning about human-to-primate disease transmission by examining pathogen exposures among nonhuman
primates in an area in which human settlement is expanding into the tropical
forest. We examine the seroprevalence of antibodies to a panel of viruses considered to be endemic in human populations among pet and wild macaques on the
Indonesian island of Sulawesi.
METHODS
Study Population
The third largest island in the Indonesian archipelago [Whitten et al., 1987],
Sulawesi still contains large tracts of virgin forest that support a unique fauna.
The island is home to at least seven morphologically distinct taxa of macaques
[Fooden, 1969]. As in many areas that contain populations of wild primates,
Sulawesi’s ecosystems are under pressure from human populations.
Eleven pet and 15 wild macaques (Macaca tonkeana) were sampled over a 3wk period during July and August 1999. Table I characterizes each study animal
in terms of age, weight, location, and status (i.e., pet or wild). Wild-caught
macaques were trapped near the village of Kayutanyo, towards the eastern end
of Sulawesi’s central peninsula (Fig. 1). An official census of the macaque population at Kayutanyo has not been conducted, but villagers estimate the population to be approximately 60 monkeys, which range through diverse habitats that
include mangrove forest, secondary forest, coconut and banana plantations, and
small farms. The results of an ethnographic survey administered to villagers
who live near the macaques indicate that the monkeys frequently raid their crops,
prompting farmers to drive them away by throwing stones or setting dogs after
them. Pet monkeys were sampled in villages along the tip of the east-central
peninsula (Fig. 1). Pets are usually acquired from the wild through opportunistic
trappings of mother–infant pairs. The infants are typically fitted with a belt made
of cloth, rope, or wire, and kept chained to a post in the front of their owner’s
compound. This prominent location allows virtually everyone in the village to
have contact with the macaque.
Trapping and Specimen Collection
Wild macaques were trapped in a locally constructed, wood and bamboo trap
measuring 13 m × 6 m × 2 m, with a narrow 1 m × 1 m × 1 m chute at one end.
TABLE I. Animal Characteristics and Serologic Results
Status
Location
C5
C6
C7
C8
C9
C10
C19
C20
C21
C22
C28
CF1
CF2
CF11
CF12
CF13
CF14
CF15
CF16
CF17
CF18
CF23
CF24
CF25
CF26
CF27
Pet
Pet
Pet
Pet
Pet
Pet
Pet
Pet
Pet
Pet
Pet
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Wild
Lauwan
Balantak
Bollo
Eteng
Eteng
Bantalyan
Bali Satu
Bali Satu
Lauwan
Kayutanyo
Padang
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
Kayutanyo
a
Infant
Juvenile
Subadult
Juvenile
Juvenile
Juvenile
Juvenile
Juvenile
Infant
Juvenile
Juvenile
Adult
Juvenile
Adult
Adult
Adult
Subadult
Juvenile
Subadult
Juvenile
Infant
Adult
Adult
Adult
Subadult
Subadult
Herpes simplex virus type 1.
Respiratory syncitial virus.
+, Antibody positive; –, Antibody negative.
b
Sex Weight
M
M
M
M
M
F
M
F
M
M
M
M
M
F
F
M
F
M
F
M
F
F
F
F
F
M
.30k
1.8k
4.5k
3.0k
3.0k
3.2k
4.0k
2.5k
1.1k
4.0k
2.8k
13.5k
3.5k
7.5k
7.8k
12.5k
4.0k
3.5k
5.2k
3.2k
.49k
8.2k
8.2k
7.1k
4.0k
4.2k
HSV-1a
Measles
Parainfluenza
1
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
+
+
+
+
–
+
–
–
–
–
+
+
+
–
+
–
–
–
–
–
–
–
–
+
–
+
–
–
–
–
–
–
–
–
–
–
+
–
–
–
+
–
–
–
–
–
+
+
+
+
–
Parainfluenza
2
Parainfluenza
3
Influenza
A
Influenza
B
RSVb
–
–
–
–
–
–
–
–
–
–
–
+
–
–
–
–
–
–
–
–
–
+
+
–
–
–
–
–
–
–
–
–
–
–
–
–
–
+
–
–
–
+
–
–
–
–
–
+
–
–
–
–
–
–
+
–
–
+
–
–
–
–
–
+
–
–
–
+
–
–
–
–
–
+
–
+
+
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
Macaques Exposed to Human Pathogens / 173
Identifier
Age
class
174 / Jones-Engel et al.
Fig. 1. Study site locations. Map locations: 1 = Luwuk; 2 = Kayutanyo; 3 = Lauwan; 4 = Bali Satu; 5 =
Bantalyan; 6 = Eteng; 7 = Padang; 8 = Bollo; 9 = Balantak.
The door to the trap could be closed remotely by observers who continuously
monitored the trap during daylight hours. After capture, the macaques were
hand injected with <5 mg/kg of Telazol® (tiletamine hydrochloride/zolazepam
hydrochloride). Three ml of blood were withdrawn from the femoral vein, placed
in a serum separator tube, and centrifuged in the field to extract the serum.
Sera were frozen and stored at –20°C. No macaques sustained injury during
this study.
Eleven pets from small villages east of Kayutanyo were sampled using the
same protocols as those employed for the wild macaques. Dental eruption sequences were recorded for each animal and used for age estimation [Sirianni &
Swindler, 1985].
Serologic Tests and Data Analysis
Serum samples were sent to the Simian Diagnostic Laboratory of the Virus
Reference Laboratory (VRL) in San Antonio, Texas, and analyzed by rapid dotimmunobinding assay [Kalter et al., 1997] for the presence of immunoglobulin
antibodies to measles; influenza A and B; parainfluenza 1, 2, and 3; Herpes simplex virus type 1 (HSV-1); and respiratory syncytial virus (RSV). Sera were diluted prior to testing to 1:5 in phosphate-buffered saline (pH 7.4). Titers are not
provided; results are indicated as either positive or negative.
RESULTS
Seroprevalence results are presented in Table I and summarized in Table II.
Antibodies to measles, influenza A, and parainfluenza 1 were detected in the
sera of both pet and wild macaques; antibodies to parainfluenza 2 and 3 were
detected only in wild macaques. No animal tested positive for antibodies to HSV1, RSV, or influenza B.
TABLE II. Percent Seroprevalence of Antibodies to Viruses Among Macaques
Measles
Parainfluenza 1
Parainfluenza 2
Parainfluenza 3
RSVa
Influenza A
Influenza B
HSV-1b
a
b
Pets
N=11
Wild
N=15
Infant
pets
N=2
Juvenile
pets
N=8
38.5
26.9
11.5
11.5
0.0
26.9
0.0
0.0
45.5
9.1
0.0
0.0
0.0
18.2
0.0
0.0
33.3
40.0
20.0
20.0
0.0
33.3
0.0
0.0
0.0
50.0
0.0
0.0
0.0
0.0
0.0
0.0
50.0
0.0
0.0
0.0
0.0
12.5
0.0
0.0
RSV = respiratory syncitial virus.
HSV-1 = herpes simplex virus type 1.
Subadult
pets
N=1
100.0
0.0
0.0
0.0
0.0
100.0
0.0
0.0
Infant
wild
N=1
Juvenile
wild
N=3
Subadult
wild
N=4
Adult
wild
N=7
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
33.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
25.0
25.0
0.0
0.0
0.0
25.0
0.0
0.0
42.9
71.4
42.9
42.9
0.0
57.1
0.0
0.0
Macaques Exposed to Human Pathogens / 175
Virus
Total
population
N=26
176 / Jones-Engel et al.
DISCUSSION
The results described above indicate seropositivity for antibodies to measles,
influenza A, and parainfluenza viruses 1, 2, and 3 among pet and wild macaques.
Older macaques possessed antibodies against more of the selected viral agents
than their younger counterparts, suggesting that animals may accumulate exposures to these pathogens over time.
Because individuals with these diseases remain infectious for only days or
weeks, the wild macaque population is probably too small and geographically
diffuse to serve as a pathogen reservoir for continuous epizootic transmission. As
a result the probable source of these exposures was likely direct or indirect contact with the human population, which constitutes the most likely reservoir for
these viruses, or through contact with pet macaques infected with human pathogens. Furthermore, it is unlikely that any given macaque with antibodies to several pathogens was exposed simultaneously to all of those pathogens; rather,
they probably accumulated exposures over time through multiple contacts. The
results of this study suggest that there have been multiple, distinct occurrences
of wild macaques at Kayutanyo being exposed to human pathogens.
Significance of Exposure to Human Pathogens
Measles, influenza, and parainfluenza are highly contagious diseases of the
respiratory tract spread mainly by aerosolized droplets [Benenson, 1990]. In
humans—the definitive host—the heaviest burden of infection falls upon children, though these diseases can strike at any age. In macaques, measles is
associated with high levels of mortality—particularly among immunosuppressed
and stressed individuals—and can cause pregnant females infected with the
virus to abort their fetuses [Lowenstine, 1993; Renne et al., 1973]. While infection with measles usually confers lifetime immunity in humans and macaques,
reoccurrence of infection with influenza and parainfluenza is common and can
cause considerable morbidity in primate species, including macaques [Acha &
Szyfres, 1980; Brack, 1987]. The bacterial superinfection of the respiratory and
gastrointestinal tracts associated with these viruses can be extremely debilitating for wild primates who must forage, compete for resources, and protect
themselves from predators.
Previous work with paramyxoviruses—antigenically related to measles virus—has raised the speculation that measles seropositivity could actually reflect prior exposure to canine distemper virus (CDV). However, experimental
research with CDV has shown that monkeys inoculated with CDV did not develop serologic evidence of measles infection [Delay et al., 1965]. More recently,
Yoshikawa and colleagues [1989] have reported immunological data on a group
of Japanese macaques (Macaca fuscata) in which one monkey was found to be
naturally infected with CDV and 22 members of its group developed high titers
of neutralizing antibodies to CDV but not to the measles virus. These data suggest that it is unlikely that measles seropositivity in the current study reflects
infection with CDV.
While humans are considered hosts for influenza and parainfluenza viruses
[Ott-Joslin, 1993] other potential reservoirs exist [Mansfield & King, 1998]. Fowl
and swine have been reported to be infected with the influenza A virus, while
infection to parainfluenza viruses have been seen in rodents, dogs, and cattle.
Thus, it is important to consider that exposure to these pathogens from reservoirs other than human populations may be responsible for the observed seropositivity among the monkeys included in our study.
Macaques Exposed to Human Pathogens / 177
Implications for Primate Conservation
This study provides evidence that wild macaques living around human settlements can be exposed to human pathogens. In Sulawesi, human–primate contact
occurs in a number of contexts. Pet ownership is quite common, and as macaques
pass through adolescence their increasingly aggressive behavior causes their owners in almost all cases to sell, release, or kill them. Pet macaques may acquire
pathogens from close interaction with their owners and subsequently come into
contact with wild macaques, thereby introducing pathogens into the wild population. Interaction between pets and wild macaques has indeed been observed in
Sulawesi. Pets are sometimes targets of aggression or sexual attention from wild
primates [Jones-Engel et al., in preparation].
Other contexts for disease transmission must also be considered. For example,
macaques are often attracted to human settlements as they search for food. In
this environment they may come into contact with human pathogens through
direct contact with humans or through contact with fomites, such as refuse, or
with contaminated water sources. Farmers generally regard primates as pests,
owing to their crop-raiding propensities, and may come into contact with wild
macaques as they chase the monkeys away from crops. Pathogens may be transmitted from trappers to wild macaques after animals escape from traps. Finally,
contact with primate researchers must also be considered a potential source of
exposure to human pathogens.
CONCLUSIONS
The results of our analysis provide evidence that wild and pet macaques are
exposed to pathogens endemic in human populations. These findings have important implications for primate conservation and suggest a variety of directions
for further research. Future work should examine evidence of exposure to other
pathogens, including mumps, rubella, polio, varicella, and hepatitis viruses. Studies comparing seroprevalence among human populations to seroprevalence among
contiguous macaque populations are also needed, as are studies comparing
seroprevalence in macaque populations remote from human populations to
seroprevalence in wild macaques living in close proximity to human settlements.
Ethnoprimatological research into pet ownership practices would help to elucidate the dynamics of this potential route of interspecies pathogen transmission.
Also of great value are studies linking primate die-offs with serologic studies of
both primate and contiguous human populations.
ACKNOWLEDGMENTS
The University of New Mexico’s IACUC approved the research protocols presented here, which were designed to minimize the risk of pathogen transmission
between the researchers and the study animals. We are grateful to R. Heberling
and A. Cooke of the Simian Diagnostic Laboratory, Virus Reference Laboratory,
San Antonio, Texas, for performing dot immunobinding assays. We thank D. Cohn,
J. Heidrich, and E. Bedrick for their technical support, and D. Babo and the
UNM undergraduates who participated in the 1999 field school for their help in
data collection. We thank J. Supriatna and the Indonesian Directorate of Nature
Conservation and Wildlife Management for their support in conducting field research. We also thank the anonymous reviewers for their constructive comments
on earlier versions of this manuscript.
178 / Jones-Engel et al.
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