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Normal Blood Parameters, Common Diseases and Parasites Affecting Captive


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McPherson, J Primatol 2013, 2:2
http://dx.doi.org/10.4172/2167-6801.1000112

Primatology
Research
Review Article
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Normal Blood Parameters, Common Diseases and Parasites Affecting


Captive Non-human Primates
Françoise J McPherson*
School of Agriculture and Wine Sciences, Charles Sturt University, Wagga Wagga, New South Wales 2850, Australia

Abstract
Non-human primates are kept in captivity as zoological exhibits as well as being used for research purposes
and as breeding colonies of endangered species with the aim of eventual release back into the wild. The aim
of this review is to collate data obtained for blood parameters for healthy animals as well as common diseases
and parasites encountered in captive non-human primates. This information can be used as a reference for
veterinarians, researchers and animal care workers working with primates. Comparisons to wild primates are made
where appropriate.

Keywords: Captive; Primate; Health, Hematology; Parasites [16]. Housing social primates in isolation for prolonged periods of
time can cause behavioral pathologies such as spinning in place or
Introduction self-mutilation [17]. Self-biting and other self-directed stereotypic
Primates are studied extensively in their wild habitat as well as in behaviors are significantly less common in primates kept in outdoor
captivity. Indeed, there are colonies of captive primates of different enclosures than in indoor enclosures [18]. Primates which are housed
species ranging from the diminutive tamarins (Saguinus sp) to and cared for under optimum conditions are more likely to be healthy
chimpanzees (Pan troglodytes) and many other species on a global and unstressed. Thus, their value as research animals is increased due to
basis. In the USA alone, up to 30,000 cotton-top tamarins (S.oedipus) their physiological and behavioral measurements being representative
were imported for biomedical research up to 1973 when the species was of what is normal for the species.
declared to be endangered and importation of wild tamarins ceased Monkeys and great apes, although all are classified as primates,
[1]. In 2003, there were more than 35,863 primates held in 22 research vary immensely in terms of physical [19,20] and physiological
institutions across the USA [2]. In a research setting, primates such parameters [21] such as differential blood counts and biochemical
as tamarins (Saguinus sp), capuchins (Cebus sp), baboons (Papio sp) measurements such as sodium or calcium in serum. These parameters
and rhesus macaques (Macaca mulatta) have immense value in studies are, in turn, influenced by age, sex and health status. It is beneficial for
relating to xenotransplantation [3], social and cognitive behaviour [4] researchers, veterinarians and zoo personnel to know what is normal
and human disease models [5]. for the species in question so that intervention can be provided when
Until the practice of obtaining wild primates destined for captivity the animal/s deviate from the normal parameters. Problems with
was outlawed, mortality rates were high due to the effects of stress after previous studies include the use of only a singular blood sample per
capture, inadequate diet and injury or illness [6]. Most zoos and many animal or very limited number of animals per study group. However,
university animal houses these days provide captive primates with there are now comprehensive published studies where animals have
naturalistic habitats including trees, ropes and climbing structures for been sampled repeatedly over a period of years including both sexes
arboreal species and food scattered throughout the exhibit to stimulate [22], wild vs. captive animals [21] and animals of different ages [23,24]
foraging behaviour [7] and there are guidelines designed to optimize to provide a more accurate picture of what is normal or abnormal. It is
captive primate health and well-being [8]. Indeed, survivorship of the aim of this review to collate data regarding common diseases and
captive orangutans (Pongo pygmaeus) has increased over the years so parasites affecting non-human primates to assist anyone caring for and
that instead of captive orangutans dying at an earlier age than their researching primates.
wild counterparts, there is now no difference in survivorship between
captive and wild orangutans due to superior management practices [9]. Diet and Its Effect on Primate Health
Even so, captive primates are often kept in close contact with humans Commercially prepared primate foods are now available for many
and/or animals of other species (such as rodents) which means they can species of monkeys to ensure they receive a balanced diet optimum
be at greater risk of contracting and spreading pathogens and parasites for their health and reproduction. However, it has been shown that
than primates in the wild [10]. In addition, some wild populations
are becoming more fragmented due to habitat loss and human
encroachment and are thus more vulnerable to disease outbreaks *Corresponding author: Françoise J McPherson, School of Agriculture and
which could have catastrophic outcomes [11]. Wine Sciences, Charles Sturt University, Wagga Wagga, New South Wales 2850,
Australia, Tel: +61 2 6925 8083; E-mail: fmcpherson@csu.edu.au
Primates differ in their social needs also so some species, such as
Received March 23 2013; Accepted April 23, 2013; Published April 27, 2013
baboons (Papio sp), gibbons (Hylobates sp), howlers (Alouetta sp),
chimpanzees (P. troglodytes) and gorillas (Gorilla gorilla), naturally Citation: McPherson FJ (2013) Normal Blood Parameters, Common Diseases
and Parasites Affecting Captive Non-human Primates. J Primatol 2: 112.
function best in stable social groups [12,13] of different sizes [14] doi:10.4172/2167-6801.1000112
while others, such as tamarins (Saguinus sp) and capuchins (Cebus sp)
Copyright: © 2013 McPherson FJ. This is an open-access article distributed under
need to be housed as bonded breeding pairs with their offspring [15].
the terms of the Creative Commons Attribution License, which permits unrestricted
However, not all privately owned primates are housed in optimum use, distribution, and reproduction in any medium, provided the original author and
conditions so that boredom and (self)-destructive behaviour can occur source are credited.

J Primatol
ISSN: 2167-6801 JPMT, an open access journal Volume 2 • Issue 2 • 1000112
Citation: McPherson FJ (2013) Normal Blood Parameters, Common Diseases and Parasites Affecting Captive Non-human Primates. J Primatol 2:
112. doi:10.4172/2167-6801.1000112

Page 2 of 10

captive lemurs are prone to hepatic iron accumulation (hemosiderosis) Therefore, to optimize the validity of the data, physiological
when fed a commercial primate diet which can contain excessive iron parameters should preferably be measured on animals of different
for their requirements. Hemosiderosis can, in turn, lead to hepatic ages and both sexes as well in order to be most useful to the field of
disease [11]. Diet also can impact on the health of captive primates as primatology. In addition, comparing values from anesthetized and
evidenced by increased cholesterol levels and cardiovascular disease in non-anesthetized would show what effect the anesthetizing agent
apes such as gorillas (G. gorilla) and orangutans (P. pygmaeus) [21]. potentially has on the physiological parameter being measured. One
way to achieve this is to train some individuals within a primate colony
It has been established that captive gorillas consume different foods
to subject to blood sampling in return for a reward such as food so
or certain plant parts as opposed to their wild counterparts. Captive
that chemical restraint is not required while the other animals are
gorillas (G. gorilla), being hindgut fermenters, tend to be provided with
a diet lower in fibre than what they would consume in the wild which physically captured and anesthetized. Another useful study would be to
may adversely affect their health [25]. However, dietary fibre content is use different anesthetic agents to determine which one/s least affect the
not the only important factor in the diets provided to captive primates. blood chemistry and hematology parameters. Likewise, physiological
The type of plants available for consumption is important not only measurements such as hematology and blood biochemistry made
for nutrition but also for self-medication. Self-medication through between animals that are suffering from a known pathogen or parasite
consumption of plants with pharmaceutical properties (such as nettles) burden and compared to healthy individuals of the same species and
has also been observed to occur in wild chimpanzees (P. troglodytes) age can potentially highlight the effect the pathogen or pathogen has
more than in wild gorillas. Therefore, the ingestion of unusual plants on the host animals of a given species.
and other foods may serve a need other than nutrition [26] such as Hematology values: Table 1 shows the normal means and
ridding themselves of gastrointestinal parasites [27]. A common plant standard deviations of haematological values of a range of primate
(Aframomum) eaten by Western Lowland (G. gorilla) and Mountain species commonly kept in captivity. Only parameters from adult
gorillas (G. gorilla beringei) is thought to have anti-parasite properties animals are given in table 1 and readers should bear in mind that there
as is another plant, combretum [27]. Chimpanzees in Nigeria were can be large variations in haematological values when comparing
observed to swallow Desmodium gangeticum leaves and sharp-edged adults to juveniles or aged individuals. For instance, an 8-year study
grass blades without chewing which were recovered undigested in fecal in captive tufted capuchin (Cebus apella) monkeys showed that
samples together with parasitic worms [28]. This suggests that the leaves erythrocytes, hemoglobin, calcium, alkaline phosphatase, glucose and
serve a medicinal rather than nutritional purpose and in particular, serum iron were all significantly higher in juvenile females than adult
aided in gastrointestinal parasite removal [28]. Wild chimpanzees (P.
females [23]. Likewise, juvenile males had significantly higher values
troglodytes) in Uganda have also been observed to consume Trichilia
for phosphorus and glucose compared to adult males. However, adult
rubescens, a plant which contains anti-malarial compounds [29].
male tufted capuchins (C. apella) had higher values for leucocytes,
Captive gorillas are usually denied the plants they would normally seek
PCV, hemoglobin, neutrophils and creatinine [23] while capuchin (C.
out in the wild for self-medication and are in fact often fed a frugivorous
apella) adult males have higher levels of neutrophils and lower values
diet rather than a more natural herbivorous diet [27]. Lack of provision
for lymphocytes compared to juveniles [32]. In some cases, there are no
of medicinal herbage may therefore possibly aid parasite proliferation
differences between adults and juveniles [6]. Some parameter changes
and cause ill health in captive primates. Propagation of plants with
such as PCV, hemoglobin or MCV are not uniform across the animal’s
medicinal properties in zoological parks may thus be a feasible option
to maintain optimum health and encourage normal behavior in their lifespan i.e., the reduction or increase may slow down or reverse post-
captive primates. puberty [22]. However, not all species show sex-specifc differences in
hematology or biochemical values such as free ranging brown lemurs
Hematology and blood biochemical parameters (Eulemur albifrons) or ring-tailed lemurs (Lemur catta) [11,35].
There is wide variation in hematological and blood biochemical Significant differences in hematological values were observed
parameters among primate species from prosimians to great apes. between the sexes also where female juvenile tufted capuchins (C.
Published results need to be interpreted with caution as factors such apella) had significantly higher values for neutrophils than juvenile
as capture stress [1,30,31], anesthetic agents [32], parasitism [33] and males. Adult males had higher values for erythrocytes, hemoglobin
reproductive status (barren, pregnant or lactating) can all potentially and PCV compared to adult females [23], similarly male capuchin
influence the results. For example, creatinine kinase is located in monkeys (C. apella) also have significantly higher PCV, erythrocytes
skeletal, cardiac and smooth muscles and greater amounts are released and hemoglobin [32] as did cotton-top tamarins (Saguinus oedipus)
in response to stress, which can be due to being captured. Thus, stress [1], golden lion tamarins (Leontopithecus rosalia) [36], adult vervet
can account for highly variable results in this enzyme concentration monkeys (Chlorocebus aethiops) although not juvenile vervets [30].
when animals are captured for blood sampling [6]. In addition, as can Male apes such as chimpanzees (Pan troglodytes) also have significantly
be expected, it has been shown that there are significant differences in higher values for PCV, erythrocytes, hemoglobin while females have
hematology and blood biochemical parameters during different stages significantly higher values for total white blood cell counts (WBC),
of development in a primate such as neonatal, juvenile, adult and aged lymphocytes and eosinophils [22]. It is thought that males have higher
animals [24,32]. However, many hematological studies in primates fail erythrocyte counts, PCV and hemoglobin concentrations due to the
to include aged individuals in their study animal cohort [22]. Data is greater muscle mass and male reproductive hormones in male monkeys
also scarce for pregnant and lactating primates although one research [37] as well as the menstrual blood loss in females [24]. Blood profiles
group investigated the effect of iron supplementation of commercial change as animals age as shown in cotton-top tamarins (S. oedipus)
diets for pregnant and lactating rhesus monkeys on infant monkey where PCV and hemoglobin decreased significantly in older females
hematology profiles and iron status [34]. More research is needed to while age did not affect these parameters in aging males [1].
provide physiology measurements on pregnant and lactating primates
of different species, ages and parity to fill the current large gap of Hematology parameters also change from what is normal for wild-
knowledge in this area. caught primates, during the post-capture adaption period and life

J Primatol
ISSN: 2167-6801 JPMT, an open access journal Volume 2 • Issue 2 • 1000112
Citation: McPherson FJ (2013) Normal Blood Parameters, Common Diseases and Parasites Affecting Captive Non-human Primates. J Primatol 2:
112. doi:10.4172/2167-6801.1000112

Page 3 of 10

Erythrocytes Lymphocytes Neutrophils (×103/ Eosinophils Reference


Species M or F Monocytes (×103/μL) Basophils (×103/μL) PCV (%)
(×106/μL) (×103/μL) μL) (×103/μL) (n)
M. mulatta F 5.2 ± 0.44 8.69 ± 2.72 7.17 ± 2.31 0.40 ± 0.20 0.02 ± 006 0.09 ± 0.10 0.41 ± 0.03 40 (36)
40,1 (36,
M. mulatta M 5.51 ± 0.40 9.27 ± 2.10 4.86 ± 1.85 0.29 ± 0.19 0.0 ± 0.0 0.03 ± 0.06 0.43 ± 0.02
38)
S. oedipus F 6.13 ± 0.35 2.96 ± 1.40 3.42 ± 1.16 0.36 ± 0.21 0.07 ± 0.06 0.16 ± 0.14 50.22 ± 3.00 1 (38)
S. oedipus M 6.42 ± 0.2 2.37 ± 1.09 2.88 ± 1.17 0.38 ± 0.20 0.06 ± 0.06 0.18 ± 0.14 53.13 ± 1.92 1 (38)
S. labiatus F 6.9 ± 0.5 6.85 ± 1.85 5.58 ± 3.02 0.40 ± 0.18 0.08 ± 0.12 0.13± 0.18 0.04 ± 0.41 33 (39)
S. labiatus M 7.0 ± 0.3 5.91 ± 2.75 4.48 ± 2.27 0.27 ± 0.19 0.08 ± 0.07 0.08 ± 0.13 0.52 ± 0.03 33 (39)
S. leucopus F& M 6.74 ± 0.8 51.1 ± 13.5* 46.6 ± 14* n/e n/e n/e 49.0 ± 4.4 6 (29)
C.apella F 5.37 ± 0.43 29.95 ± 6.78* 67.19 ± 6.1* 1.95 ± 1.73* 0.21 ± 0.22* 0.60 ± 0.63* 38.77 ± 3.57 23 (44)
C. apella M 5.92 ± 0.45 33.21 ± 9.74* 63.89 ± 9.23* 2.06 ± 2.16* 0.21 ± 0.27* 0.82 ± 1.01* 42.58 ± 3.54 23 (44)
C. aethiops F 5.4 ± 0.5 3.4 ± 1.5 3.6 ± 2.1# 0.6 ± 0.2 n/e n/e 40.3 ± 4.0 30 (50)
C. aethiops M 6.5 ± 0.8 3.5 ± 1.9 2.5 ± 1.3# 0.6 ± 0.3 n/e n/e 50.6 ± 6.2 30 (50)
P. troglodytes F 5.06 ± 0.34 4.72 ± 2.01 0.07 ± 0.07 0.32 ± 0.19 0.02 ± 0.03 0.24 ± 0.16 42.05 ± 1.8 22 (252)
P. troglodytes M 5.4 ± 0.42 4.58 ± 1.45 0.07 ± 0.01 0.33 ± 0.15 0.01 ± 0.02 0.22 ± 0.1 45.04 ± 4.17 22 (252)
L. catta F&M n/e 3.75 ± 2.14 4.27 ± 2.94 0.37 ± 0.47 0.15 ± 0.68 0.33 ± 0.32 50.5 ± 6.2 35 (1249)
M=male; F=female. *results expressed as % of total leucocyte count.n/e=not examined. #measurement is for granulocytes which are neutrophils, basophils and eosinophils
combined.

Table 1: Normal mean and standard deviations of haematological parameters in the most commonly kept captive primate species of both sexes.

in captivity after habituation. This was shown in vervet monkeys (C. total serum bile acids where Rhesus macaque (M. mulatta) males had
aethiops) where there was a significant rise in packed cell volume (PCV) twice as much than females at 24.9 ± 16.7 µmol/l vs 12.8 ± 10.3 µmol/l
and mean corpuscular volume (MCV) for sexes, adults and juveniles, respectively [40].
during the 4 months post-capture adaption period i.e. while the wild
Juvenile primates are still growing therefore they show differences
caught animals adapted to captivity. Similarly, the WBC and platelet
in blood biochemical values compared to adults. One example of this is
counts both declined during the adaptation period in captivity [30]. It
is possible that WBC counts are high at capture which is a time of high in alkaline phosphatase which is an enzyme that is present in elevated
stress levels and decline thereafter due to the monkeys being exposed concentrations due to increased bone growth in juveniles [6,24,32].
to many microbes in the wild as well as being linked to higher levels Likewise, juvenile capuchin monkeys (C. apella) have significantly
of cortisol in circulation as a stress response during and immediately higher values for calcium, inorganic phosphorus (both also required
after capture [38]. Likewise, platelet counts tend to decrease during for bone growth and development) and glucose than adults [32]. Male
adaptation to captive life as platelet release from the spleen takes cotton-top tamarins (S. oedipus) had less calcium as they aged but this
place in response to fright [30]. Diet has an effect on hematological effect was not seen in females [1].
parameters also and it has been shown that a high protein diet as fed Age-related changes in blood biochemistry values may increase
in captivity to vervet monkeys (C. aethiops) significantly elevates PCV, or decrease exponentially as with hematologic values. Both alkaline
MCV as well as hemoglobin [39]. Illness changes the hematological phosphatase and creatinine are greatest in juvenile animals. The
profile and sick golden lion tamarins (L. rosalia) showed a reduction alkaline phosphatase concentration curve flattens out at about 8 years
in monocytes and eosinophils and a concurrent increase in WBC, of age in baboons (P. hamadryas) while creatinine does not show any
neutrophils and basophils [36]. sex-based differences until 5 years of age [24]. This is when baboons
Biochemical blood values: Table 2 shows the normal means and undergo puberty and males undergo a disproportionate increase in
standard deviations of biochemical values of a range of primate species muscle mass compared to similar-aged females [41]. When studied
commonly kept in captivity. There is immense variation between the by two different research groups, captive tufted capuchins (C. apella)
different species as well as the sexes. Striking differences are found showed significant differences between juvenile and adult animals in
in blood biochemical values when comparing the different primate terms of alkaline phosphatase, calcium, glucose, inorganic phosphorus,
species in table 2. For example, creatinine ranges from 0.33 mg/dL aspartate aminotransferase and some serum proteins [23,32] although
for Saguinus Oedipusto 4.36 mg/dL in Papio hamadryas. Cholesterol iron and alanine aminotransferase were also significantly different [23].
values range from 45.4 mg/dL in P. hamadryas to 224.7 mg/dL in P. There can also be differences based on where animals are housed,
troglodytes. presumably due to different diets and husbandry. This was the case
Rhesus macaque (M. mulatta) males had lower sodium (149.7 ± 3.1 in white-footed tamarins (S. leucopus) which were housed in three
mmol/l) and potassium (4.7 ± 0.6 mmol/l) concentrations than females different facilities in Colombia and blood testing revealed significant
(153.7 ± 3.5 mmol/l and 4.9 ± 0.8 mmol/l respectively) [36]. However, differences in values for haemoglobin, serum total protein, albumin,
in white-footed tamarins (S. leucopus), there was no difference in glucose and alkaline phosphatase [6]. Differences also exist between
serum sodium concentrations between the sexes but serum chloride captive animals and their wild counterparts in terms of biochemical
concentrations in males (94 ± 5.1 mEq/L) was significantly lower than parameters as was demonstrated in ring-tailed lemurs (L. catta).
for females at 99 ± 5.4 mEq/L [6]. Male capuchin (C. apella) monkeys Furthermore, captive lemurs, possibly due to a diet high in ascorbic
had significantly more creatinine while females had higher values acid and low in tannins, can be more prone to hemosiderosis then
for BUN, AST and GGT [32].Cotton-top tamarin (S. oedipus) males wild lemurs [11,35]. It is also noteworthy that prosimians metabolize
also showed significantly elevated values for creatinine compared to vitamins differently to other primates so, for example, carotenoids may
females [1]. The most striking difference between the sexes was seen in be undetectable in lemurs but present in otherprimate species [11].

J Primatol
ISSN: 2167-6801 JPMT, an open access journal Volume 2 • Issue 2 • 1000112
Citation: McPherson FJ (2013) Normal Blood Parameters, Common Diseases and Parasites Affecting Captive Non-human Primates. J Primatol 2:
112. doi:10.4172/2167-6801.1000112

Page 4 of 10

Albumin (g/ Calcium (mg/ Cholesterol Potassium Sodium


Species
dL) dL) (mg/dL) (mmol/L) (mmol/L)
153.74 ±
M. mulatta (F) 54.31 ± 2.73 48.96 ± 3.06 55.08 ± 7.2 4.90 ± 0.76
3.47
149.71 ±
M. mulatta (M) 53.43 ± 2.60 47.34 ± 2.34 51.3 ± 10.98 4.67 ± 0.62
3.07
134.67 ± 150.50 ±
S. oedipus (F) 4.06 ± 0.31 9.02 ± 0.50 4.04 ± 0.44
31.04 2.12
153.94 ± 150.06 ±
S. oedipus (M) 3.97 ± 0.30 8.69 ± 0.59 4.25 ± 0.64
51.04 2.54
S. labiatus (F) 4.0 ± 0.42 2.60± 0.17 n/e 4.5 ± 0.78 156.0 ± 6.3
S. labiatus (M) 3.9 ± 0.47 2.5 ± 0.2 n/e 4.0 ± 0.95 159.0 ± 5.0
S. leucopus (M
3.1 ± 0.49 8.7 ± 1.1 79.0 ± 19.6 4.9 ± 1.0 148.3 ± 13.5
& F)
145.33 ± 148.02 ±
C. apella (F) 61.76 ± 2.68* 2.39 ± 0.17 3.92 ± 0.36
38.44 2.13
138.42 ± 148.95 ±
C. apella (M) 61.22 ± 3.43* 2.33 ± 0.12 4.2 ± 0.56
18.74 2.29
P. troglodytes 3.34 ± 9.14 ± 224.72 ± 3.39 ± 139.97 ±
(F) 0.21 42.71 2.41 0.33 36.83 10.3 2.43 0.43 1.68 0.14
P. troglodytes 93.02 ± 13.14 ± 222.58 ± 100.33 ± 140.93 ± 1.12 ±
3.36 ± 0.37 9.15 ± 0.81 97.04 ± 1.67 3.43 ± 0.34 22 (252)
(M) 30.44 5.43 31.8 15.18 2.33 0.21
P. pygmaeus 4.07 ± 288.9 ± 10.8 ± 8.46 ± 161.9 ± 118.7 ± 97.5 ± 4.55 ± 135.5 ± 1.4 ± 2.2 31 (44)
(F & M) 0.55 186.3 13.4 1.32 165. 47.5 1.63 97.5 4.55
P. hamadryas 540.83 ± 81.18 ± 45.54 ± 103.32 ± 108.98 ± 145.69 ± 3.74 ±
4.09 ± 0.46 42.66 ± 2.88 3.58 ± 0.53 24 (160
(F) 429.49 30.06 11.88 31.86 22.52 3.69 0.87
P. hamadryas 627.33 ± 92.7 ± 107.86 ± 4.36 ± 24 (160)
4.17 ± 0.41 42.48 ± 2.88 45.36 ± 9.54 95.04 ± 24.3 3.7 ± 0.53 146.35 ± 3.5
(M) 428.73 28.62 4.23 2.88
L. catta 5.7 ± 0.9 222.0 ±109.0 22.0 ± 8.0 9.7 ± 0.9 89.0 ± 26.0 142.0 ± 0.2 108.0 ±6.0 4.4 ± 0.6 148.0 ± 5.0 1.0 ± 0.3 35 (903)
AP=alkaline phosphatase; BUN=blood urea nitrogen; n/e=not examined

Table 2: Normal mean and standard deviations of blood chemistry values for the most commonly kept species of captive primates of both sexes.

Cholesterol values vary widely among primate species (Table 2) to better assess the risk of arteriosclerosis and coronary heart disease so
from a mean value of 45 mg/dL in baboons (P. hamadryas) to 225 mg/ that early intervention is possible [48].
dl in chimpanzees (P. troglodytes) which exceeds the recommended
maximum values for humans at <200 mg/dL [42]. Hypercholesterolemia Parasites
in humans is implicated in coronary heart disease and cardiovascular Nematode, cestode and trematode parasites
disease is also a major cause of death in captive adult gorillas (G.
gorilla [43]) and orangutans (P.pygmaeus; [44]) while 77% of adult The use of captive primates as research animals could potentially be
chimpanzees (P. troglodytes; [45]) and 46% of adult bonobos (Pan jeopardised by internal parasites causing ill health and possibly death.
paniscus; [46]) have died in zoos from cardiovascular diseasesince Likewise, endangered species’ survival may be further threatened by
records were kept of causes of death up to 2003. the presence of heavy loads of parasites [49] although it has also been
proven that threatened species of primates which live in small groups
Captive gorillas (G. gorilla) were found to have significantly higher harbour fewer parasites (helminths, protozoa, arthropods, bacteria and
(approximately 1.5x) cholesterol concentrations than free-ranging viruses) than non-threatened species where more individuals living in
gorillas while both sexes of captive orangutans (P. pygmaeus) had a smaller area facilitate parasite exchange [50]. Most information on
significantly higher total cholesterol concentrations than free-ranging parasite infections in primates comes from non-invasive fecal sampling
female orangutans [21]. The component of cholesterol which is linked of wild animals. Data concerning endoparasite loads in captive primates
to elevated risk of cardiovascular disease is low-density lipoprotein are scarce even though heavy infestations can cause diarrhea and even
or LDL. The recommended concentration of LDL cholesterol in death in the host animals [51].
humans is <2.59 mmol/L [21]. In a study of captive apes comprising of
Western lowland gorillas (G. gorilla gorilla), orangutans ( P. pygmaeus, Internal parasites are found primarily in wild primates, since
P.abeli), chimpanzees ( P. troglodytes) and bonobos (P. paniscus), only captive primates are often treated with anthelmintics as a preventative
bonobos had a mean cholesterol LDL value of 2.25 mmol/L which is strategy [52] such as ivermectin which are used routinely to kill
below what is recommended for humans. The highest mean value of gastrointestinal parasites of domestic animals [53]. Even so, captive
3.8 mmol/L for cholesterol LDL was recorded for gorillas [21] while primates, like their wild counterparts, have been shown to harbor an
other researchers have documented similar high findings for gorilla extensive variety of internal parasites as outlined in table 3 however,
serum cholesterol [47], presumably due to obesity, which is in turn due in another study, no significant differences were found in parasite
to inactivity and high dietary carbohydrate intake, insulin resistance prevalence between wild and captive Olive baboons (P. cyanocephalus
and type 2 diabetes as well as progestins and androgens [42]. These are anubis)and Sykes (Cercopithecus mitis) monkeys [52]. Sampling 40
all risk factors which are in greater abundance for captive great apes animals belonging to 7 lemur species kept in captivity at two zoos
compared to free-ranging primates. It would be beneficial to establish in Madagascar revealed significant differences between the two
a database of known blood lipid values for captive gorillas (G. gorilla) sites in the prevalence of strongylids, possibly due to one zoo using

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Primate (W/C) S. fulleborni S. stercoralis Trichuris sp Oesophagostomum sp Trichostrongylus sp S. mansoni Streptopharagus sp Ascaris Reference (n)
P. cyanocephalus (W) 63.0 n/e 73.9 76.0 43.5 4.3 42.2 n/e 52 (92)
P. cyanocephalus (C) 17.3 n/e 69.3 17.3 16.0 0.0 0.0 n/e 52 (75)
C. mitis (W) 61.8 n/e 60.0 47.2 38.2 0.0 52.7 n/e 52 (55)
C. mitis (C) 32.5 n/e 51.2 20.9 0.0 0.0 0.0 n/e 52 (43)
C. aethiops (C) 44.0 n/e 50.0 0.0 0.0 0.0 0.0 n/e 52 (50)
C. guereza(W) 4.2 0.0 79.0 6.09 n/e n/e n/e 1.26 63 (476)
C. angolensis(W) 5.26 0.0 100.0 0.00 n/e n/e n/e 0.00 63 (19)
P. tephrosceles(W) 3.54 0.44 37.75 2.8 n/e n/e n/e 0.12 63 (1608)
P. cyanocephalus(W
30.6 9.0 38.7 n/a n/a 3.6 n/e n/e 49 (111)
& C)
C. aethiops(W & C) 16.3 22.8 47.1 n/a n/a 4.9 n/e n/e 49 (123)
C. mitis(W & C) 23.5 32.5 50 n/a n/a 0.0 n/e n/e 49 (34)
C. neglectus(W & C) 0.0 17.7 50 n/e n/e 0.0 n/e n/e 49 (12)
C. albigena(W & C) 0 50 37.5 n/e n/e 0.0 n/e n/e 49 (8)
C. torquatus(W & C) 12.5 62.5 62.5 n/e n/e 0.0 n/e n/e 49 (8)
P. pygmaeus(C) 39.0* n/e 7.0 n/e 3.0 n/e n/e 1 55 (119)
W=wild and C=captive. n/e=not examined. *includes all strongyloides sp.

Table 3: Percentage distribution of gastrointestinal parasites found in captive and wild primates.

anthelmintics and the different floor substrates used [51]. Other factors between wild and captive animals since they tend to avoid coming into
that can increase parasite loads in primates, wild and captive, include contact with contaminated soil [60].
unwashed food items such as fruits and vegetables [51] and inbreeding
Sex-differences can occur as in the case of only adult female
since outbred animals are less prone to parasite infections than inbred
guenons (Cercopithecus sp.) being infected with Oesophagostomum
individuals [54].
sp. and S. fulleborni [57], a findingthat could be due to females being
Out of 15 human workers taking care of captive infant orangutans pregnant and experiencing compromised immunity as a result [61,62].
(P. pygmaeus), only 3 tested negative for intestinal parasites and However male red colobus (Piliocolobus sp.) showed higher infection
both humans and apes were infected with the same parasite species rates with S. fulleborni than females [63]. Wild male orangutans (P.
[55]. This cross-infection was enhanced by the workers not using pygmaeus) had a significantly higher hookworm infection rate than
protective clothing and infant apes (P. pygmaeus) being kept in large wild females however there was no difference between dominant
groups, which is an unnatural living arrangement, so that soil and floor flanged males and subservient non-flanged males [55]. When taking
contamination levels were high [55]. into account total intestinal parasite loads, wild females had a higher
Many primate intestinal parasites are pathogenic in humans. Cross total intestinal prevalence than males, presumably because the females
infection from primates to humans can occur with those who work have more contact with other orang utans, both with other females and
with captive primates and also as a result of ecotourism where humans their offspring [55]. However, a coprological survey of wild mountain
enter the wild habitat of infected primates. A colony of 39 semi-captive gorillas (G. gorilla beringei) in Rwanda revealed no significant sex
chimpanzees (P. troglodytes) in Uganda were found to be extensively differences in parasite load or species of parasite harboured although
infected (seroprevalence rate >90%) with the trematode Schistosoma dominant silverback males tended to have a higher prevalence of the
mansoni while many of the 37 humans who came into close contact pinworm Probstmayria sp. [64].
with the animals also harboured this parasite [56]. When two primate species co-inhabit the same region, parasite
Captive olive baboons (Papio cyanocephalus) were found to have infestation can be similar between the different primate populations
significantly lower parasite infection prevalence compared to their wild as determined in wild guenons of Western Uganda [57] or remarkably
counterparts with the exception of Trichuris sp. where both populations different between the species as shown in a coprological survey
had similar infection prevalence [52]. A coprological study of wild performed on western lowland gorillas (Gorilla g. gorilla)and
guenons in Western Uganda showed that parasite infection of blue chimpanzees (Pan t.troglodytes) in Gabon. While 84% of the gorilla
monkeys (C. mitis) varied by location so most prevalence was found fecal samples were positive for parasites, only 56% of the chimpanzee
in Kenya for S. fulleborni, Trichostrongylus sp., Oesophagostomum sp. samples contained evidence of intestinal parasites [65].The same could
while there was no difference for Trichuris sp. and more prevalence of potentially apply to primates of different species co-habitating the same
Streptopharagus and Bertiella sp. in South Africa [57]. Environmental enclosure.
conditions such as rainfall are most likely the cause for the difference in When closely related colobus monkey species were sampled; Eastern
prevalence of intestinal parasites [58]. black and white colobus, (Colobus guereza); Angolan black and white
Housing conditions can influence parasite infections. For colobus (C. angolensis) and red colobus (Piliocolobus tephrosceles),
example, the prevalence of S. fulleborni is greatest in primates housed host species effects were found for the prevalence of Trichuris, Ascaris,
on gravel/dirt floor enclosures, moderate in cement floor enclosures unidentified strongyle sp. and Oesophagostomum sp. Overall, eastern
while primates in cages suspended above the floor did not have any S. black and white colobus monkeys (C. guereza) were more susceptible
fulleborni [52]. Wild baboons for aging on the ground, especially near to parasite infection than red colobus (P. tephrosceles) [63]. However,
livestock and human settlements, are more susceptible to becoming other researchers found that while black and white colobus monkeys
infected than captive baboons that do not forage [59]. Arboreal primate (C. guereza) harboured only a single species of parasite (Trichuris
species do not show significant differences in parasite prevalence sp.), the other 5 species of primates that were sampled harboured

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multiple concurrent parasite infections [49]. Mountain gorillas (G. However, while P. knowlesi tends to infect mainly long-tailed macaques
gorilla beringei) harboured cestodes such as Anoplocephala gorilla in (Macaca fascicularis) and pig-tailed macaques (Macaca nemestrina),
abundance (51-92%) while lowland gorillas in different geographical humans can be infected also [70]. Likewise, malaria sporozoites can
areas did not have any, possibly due to the lack of intermediate hosts in be transferred from infected humans to primates as demonstrated in
their environment [66]. gibbons (Hylobates lar [71]).
Protozoan parasites Microsporidian parasites
Protozoal infections such as Balantidium coli and Entamoeba Encephalitozoon cuniculi is a fungal obligate intracellular parasite
colican are more common in captive primates, which could be due to that can exist in infected individuals for years and quickly kill others. In
contaminated water and housing [52] (Table 4). However, free ranging an affected colony of captive emperor tamarins (Saguinus imperator),
primates can also become infected when drinking water contaminated all infants died after showing obvious signs of disease such as infections
by infected fecal material from ruminants, other primates or humans. and systemic vasculitis as well as high titres for encephalitozoon [72].
Free-ranging baboons (Papio sp.) had a lower rate of protozoal infection Respiratory distress and acute onset of cardiac failure were symptoms
than captive baboons for E. histolytica and B. coli but the reverse was of microsporidia in an affected captive adult male Goeldi’s monkey
true for Entamoeba coli [52]. Captive Sykes (C. albogularis) monkeys (Callimico goeldii). At autopsy,findings were multicentric arteritis and
had a lower rate of infection for all three protozoal parasites compared aortitis [73]. Subsequent serosurveys of monkeys imported into the
to free ranging Sykes monkeys [52]. Free-ranging arboreal species USA in the same consignment and potentially exposed to the infected
such as colobus monkeys (Colobus sp. [63] and Ugandan guenons individual revealed that multiple animals tested positive for E. cuniculi
(Cercopithecus sp. [57]) showed low prevalence of protozoan infections. antibodies against genotype II [73]. Other New World primates
In another study of captive, semi-captive and wild orangutans (P. harboured genoptype III E. cuniculi such as squirrel monkeys (Saimiri
pygmaeus), the prevalence rates of 3 genera of Protozoa was >10% of sciureus) that were bred in captivity in Japan [74].
which 2 are pathogenic (Entamoeba histolytica and Balantidium sp.) External parasites
while the third (Entamoeba coli) is non-pathogenic [55]. Balantidium
sp. was most prevalent at 39% and 41% prevalence in captive and semi- Primates are prone to similar exoparasites as other animals such
captive orangutans (P. pygmaeus) respectively. Entamoeba coli was as fleas and lice, potentially causing sarcoptic mange. Alopecia is not
equally prevalent in captive and semi-captive populations at 22% and always due to exoparasites and can be a form of self-mutilation when
32% respectively however, E. histolytica, with a prevalence rate of 3% in hair loss is apparent. External parasites are not usually problematic
captive vs 35% in semi-captive orangutans was not equally distributed unless primates are housed in isolation since mutual grooming serves
[55]. In a study comparing wild and captive ring-tailed lemurs (L. to not only strengthen and reaffirm social bonds [75,76] but also rid the
catta), captive and wild animals harbored different parasite species with fur of exoparasites such as lice which are eaten by the groomer animal
Entamoeba coli being the only parasite common to both populations [77]. Indeed, mite infestation in wild brown lemurs (E. fulvus albifrons)
[67]. Giardia was only present in captive lemurs (L. catta), despite no was not associated with alopecia or pruritis [11].
clinical signs being present, while only wild ring-tailed lemurs tested
Infectious Viral Diseases
positive for Cryptosporidium [67].
Primates and humans share susceptibility to a range of pathogens
Malaria is a potentially fatal disease caused by the zoonotic
which makes it a challenge to work with these animals and prevent
protozoan parasite Plasmodium sp that is transmitted not through direct
transfer of zoonoses. One such example is the mumpsvirus (Epidemic
contact with infected animals or infected feces but by mosquito vectors
parotidis) where apes can be infected from a human [78]. As a
[68]. A blood smear survey and polymerase chain reaction analyzes
precaution, infected animals should be quarantined and protective gear
for Plasmodium sp. revealed that 29 out of 31 captive orangutans (P.
worn by their carers such as gloves, face mask and surgical apron or
pygmaeus) and 5 out of 43 wild orangutans tested positive for malaria.
overalls. Likewise, when a researcher, veterinarian or zoo worker is ill,
The greater prevalence in captive apes was possibly due to a 50-fold
he or she should either refrain from coming into contact with healthy
increase in population density in captivity compared to the wild
primates or take all the necessary precautions to avoid spreading
population which facilitated transfer of the parasite by mosquitoes
infectious agents throughout the primate colony.
[69]. Malaria can be host-specific, for example,orangutans (P.
pygmaeus) are naturally infected with either P. pitheci or P. silvaticum. In wild primates, sudden deaths en-masse can be a sentinel message.

Primate species Entamoebahistolytica Entamoeba coli Endolimax Iodamoeba Balantidium Giardia Blastocystis Reference (n)
P. pygmaeus (C) 3 22 9 4 39 3 15 55 (119)
P. cyanocephalus (W) 26.1 78.3 n/e n/e 43.6 n/e n/e 52 (92)
P. cyanocephalus (C) 26.6 66.7 n/e n/e 23.2 n/e n/e 52 (75
C. mitis (W) 23.6 54.5 n/e n/e 43.6 n/e n/e 52 (55)
C. mitis (C) 16.3 34.9 n/e n/e 23.2 n/e n/e 52 (43)
C. aethiops (C) 25.4 74.0 n/e n/e 30 n/e n/e 52 (50)
C. guereza(W) 7.56 7.77 n/e n/e n/e 0.0 n/e 63 (476)
C. angolensis (W) 10.53 15.79 n/e n/e n/e 0.0 n/e 63 (19)
P. tephrosceles(W) 3.48 4.35 n/e n/e n/e 0.81 n/e 63 (1608)
L. catta(C) 0.02 0.0 n/e n/e 0.0 0.1 n/e 67 (50)
L. catta(W) 0.0 0.0 n/e n/e 0.04 0.0 n/e 67 (99)
W=wild and C=captive. n/e=not examined.

Table 4: Percentage distribution of common intestinal protozoan parasites found in wild and captive primates.

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This has occurred previously with fatal outbreaks of yellow fever [79] and gorillas (G. gorilla), is most likely the reason why it is the most
in Howler monkeys (Alouatta sp) and Kyasanur Forest disease virus in commonly transmitted retrovirus from primates to humans through
bonnet macaques (Macaca radiata) and hanuman langurs (Presbytis infected saliva and blood when zoo workers, veterinarians and animal
entellus) in India which later infected humans living near the forest researchers are bitten or through needlestick injury when the needle
[80]. contains infected blood [90]. Even so, many SFV-infected humans
show no apparent signs of ill health for many years after exposure
Since it is probable that the human immunodeficiency virus (HIV)
to the virus which seems to remain latent in the blood peripheral
originated from simian immunodeficiency virus (SIV) through direct
lymphocytes. Transmission between humans is not as prevalent as
contact between affected primates and humans [81] and especially
between primate and human [81].
from chimpanzees and sooty mangabeys [82,83], the threat of zoonoses
is especially high for humans working with primates. Another retrovirus, simian type D retrovirus (SRV), is a highly
prevalent virus with >90% of captive Asian macques infected and
Arboviruses displaying symptoms similar to AIDS [91]. On the other hand,
Arboviruses infecting primates include dengue, Japanese herpesvirus papio2 (HVP2) is not as prevalent with only 3.8% of
encephalitis, Langat, Sinbis, Tembusu and Zika. It is considered to captive baboon (Papio sp) swabs being positive for HVP2 over a period
be beyond the scope of this review to cover every single virus known of 1.5 years with twice yearly testing of 128 baboons [92] although
to infect primates so only a select few of greatest importance will be another captive colony of baboons (P. anubis and P. cyanocephalus)
covered here. had a HVP2 prevalence rate of 85% [93]. All animals (except for one)
shedding the virus were infants and the virus was isolated in the oral
The incidence of primates testing positive to any virus is variable cavity [92]. Of the 31 wild-caught baboons that were swabbed before
among wild and captive animals. No animals tested positive for any being added to the colony, none were shedding the virus although
of the 33 viruses tested for out of their sample population of 44 semi- >93% of these animals were seropositive for the virus. Another captive
captive and 54 free-ranging orang-utans (P. pymaeus) in Malaysia colony of baboons had a HVP2 infection rate of ~33% with half of the
[31]. However, in another study of wild and semi-captive orangutans baboons shedding the virus into the oral cavity and the other half into
in Borneo, one out of 71 apes (1.4%) tested positive to all flaviviruses the genital tract [92]. HPV2 appears to be present predominantly in the
examined [84]. Wild and semi-captive orangutans were both infected oral cavity of young baboons and is transmitted sexually in adults [92].
with dengue-2, Zika, Tembusu and Japanese encephalitis virus. Sindbis In another study, >90% of wild caught adult olive baboons (P. anubis)
virus was found only in wild orangutans (P. pygmaeus) while only and chacma baboons (P. ursinus) were seropositive for HPV2 although
semi-captive orangutans tested positive to Langat virus. Humans there were no differences in immune sera reactivity to HPV2 between
living near the forest were infected with all viruses except Sindbis virus the baboon species [93].
[84]. The difference in prevalence could be due to the wild ape cohort
being primarily adults while the semi-captive orangutans were mostly Infectious Bacterial Diseases
juveniles. Adults showed a greater seroprevalence for all 6 viruses Leptospirosis
examined than juveniles [84]. Dengue-2 and Japanese encephalitis
were the two most common flaviviruses among both orangutan groups Leptospirosis is a zoonotic bacterial disease spread through
[84]. Both viruses are not species-specific and infect other mammal infected urine that infects domestic and wild animals as well as humans
species and birds [85,86]. [94]. Primates, even in captivity, may become infected when they
come into contact with seropositive animals such as rodents. Humans
Non-Arboviruses coming into contact with primates can transfer or become infected
with the bacteria [95]. Primates destined for release back into the wild
Non-arbovirusesthat can infect primates include rotavirus SA11,
are not routinely tested for anti-Leptospirosis antibodies during their
respiratory syncytial, parainfluenza 3, mumps, foamy, Ebstein-Barr,
rehabilitation period so there is a real risk of introducing the disease
Coxackie B-4, herpes, hepatitis A and B, poliomyelitis, rubella,and
into naïve wild populations. In a captive population of 44 marmosets
monkey pox.
and capuchins (C. jacchus, C. pennicilata and Cebus sp) in Brazil,
The prevalence of Simian Foamy Virus (SFV) is captive nonhuman 56.8% tested positive for the presence of Leptospirosis antibodies
primates is very high at approximately 70% while the prevalence of despite no signs of clinical disease being present [96]. The prevalence of
simian immunodeficiency virus (SIV) is up to 36% in wild primates leptospiral antibodies in 73 captive lion tamarins (l. rosalia) elsewhere
[81]. SFV is the most transmitted primate retrovirus to humans in Brazil was much lower at only 15% [97] suggesting that there may be
working with primates [80] and people who hunt and eat primates [87]. a species-effect in antibody prevalence rates.However, at a Colombian
Zoo, not only was the seroprevalence 23% in the resident Neotropical
In a sample of wild-caught primates, 5 out of 27 gorillas (G. gorilla; monkeys, 25% of zoo workers also tested positive for Leptospirosis
19%), 7 out of 11 mandrills (Mandrillus sphinx; 64%) and 2 out of 6 antibodies despite most of the zoo workers wearing protective clothing
drills (Mandrillus leucophaeus; 33%) tested positive to SFV although to minimise transmission risk between animals to humans [95]. Most
not all harboured the same viral strain with the drills being infected reactivity was found in Black spider monkeys (Ateles fusciceps), white-
with two different strains and the gorillas having 3 strains of SFV [88]. fronted capuchin (Cebus albifrons) and white-footed tamarin (Saguinus
Chimpanzees (P. troglodytes) were found to be source of SFV infection leucopus). Monkeys and zoo workers had different predominant
in 9 out of 10 infected human workers with the remaining person serovars [95] which may be due to serovar conversion within a new
infected by a baboon [81]. Prevalence of SFV in captive primates is host.
also high at more than 70% of animals infected with this virus [89] and
this is most likely due to its transmission between primates by direct Stress levels can influence prevalence of protozoan, as well as
contact [81]. The high prevalence of SFV among captive and wild helminth, infections [98]. An example of this was found in semi-captive
primates, especially baboons (Papio sp), chimpanzees (P. troglodytes) lactating orangutan females which were rescued and experienced

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Citation: McPherson FJ (2013) Normal Blood Parameters, Common Diseases


and Parasites Affecting Captive Non-human Primates. J Primatol 2: 112.
doi:10.4172/2167-6801.1000112

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