McPherson, J Primatol 2013, 2:2 http://dx.doi.org/10.4172/2167-6801.

1000112

Primatology
Research Article Review Article Open Access Open Access

Normal Blood Parameters, Common Diseases and Parasites Affecting Captive Non-human Primates
Franoise 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 Introduction

Primates are studied extensively in their wild habitat as well as in captivity. Indeed, there are colonies of captive primates of different species ranging from the diminutive tamarins (Saguinus sp) to chimpanzees (Pan troglodytes) and many other species on a global basis. In the USA alone, up to 30,000 cotton-top tamarins (S.oedipus) were imported for biomedical research up to 1973 when the species was declared to be endangered and importation of wild tamarins ceased [1]. In 2003, there were more than 35,863 primates held in 22 research institutions across the USA [2]. In a research setting, primates such as tamarins (Saguinus sp), capuchins (Cebus sp), baboons (Papio sp) and rhesus macaques (Macaca mulatta) have immense value in studies relating to xenotransplantation [3], social and cognitive behaviour [4] and human disease models [5]. Until the practice of obtaining wild primates destined for captivity was outlawed, mortality rates were high due to the effects of stress after capture, inadequate diet and injury or illness [6]. Most zoos and many university animal houses these days provide captive primates with naturalistic habitats including trees, ropes and climbing structures for arboreal species and food scattered throughout the exhibit to stimulate foraging behaviour [7] and there are guidelines designed to optimize captive primate health and well-being [8]. Indeed, survivorship of captive orangutans (Pongo pygmaeus) has increased over the years so that instead of captive orangutans dying at an earlier age than their wild counterparts, there is now no difference in survivorship between captive and wild orangutans due to superior management practices [9]. Even so, captive primates are often kept in close contact with humans and/or animals of other species (such as rodents) which means they can be at greater risk of contracting and spreading pathogens and parasites 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 which could have catastrophic outcomes [11]. Primates differ in their social needs also so some species, such as baboons (Papio sp), gibbons (Hylobates sp), howlers (Alouetta sp), chimpanzees (P. troglodytes) and gorillas (Gorilla gorilla), naturally function best in stable social groups [12,13] of different sizes [14] while others, such as tamarins (Saguinus sp) and capuchins (Cebus sp) need to be housed as bonded breeding pairs with their offspring [15]. However, not all privately owned primates are housed in optimum conditions so that boredom and (self)-destructive behaviour can occur
J Primatol ISSN: 2167-6801 JPMT, an open access journal

[16]. Housing social primates in isolation for prolonged periods of time can cause behavioral pathologies such as spinning in place or self-mutilation [17]. Self-biting and other self-directed stereotypic behaviors are significantly less common in primates kept in outdoor enclosures than in indoor enclosures [18]. Primates which are housed and cared for under optimum conditions are more likely to be healthy and unstressed. Thus, their value as research animals is increased due to their physiological and behavioral measurements being representative of what is normal for the species. Monkeys and great apes, although all are classified as primates, vary immensely in terms of physical [19,20] and physiological parameters [21] such as differential blood counts and biochemical measurements such as sodium or calcium in serum. These parameters are, in turn, influenced by age, sex and health status. It is beneficial for researchers, veterinarians and zoo personnel to know what is normal for the species in question so that intervention can be provided when the animal/s deviate from the normal parameters. Problems with previous studies include the use of only a singular blood sample per animal or very limited number of animals per study group. However, there are now comprehensive published studies where animals have been sampled repeatedly over a period of years including both sexes [22], wild vs. captive animals [21] and animals of different ages [23,24] to provide a more accurate picture of what is normal or abnormal. It is the aim of this review to collate data regarding common diseases and parasites affecting non-human primates to assist anyone caring for and researching primates.

Diet and Its Effect on Primate Health

Commercially prepared primate foods are now available for many species of monkeys to ensure they receive a balanced diet optimum for their health and reproduction. However, it has been shown that

*Corresponding author: Franoise J McPherson, School of Agriculture and Wine Sciences, Charles Sturt University, Wagga Wagga, New South Wales 2850, Australia, Tel: +61 2 6925 8083; E-mail: fmcpherson@csu.edu.au ReceivedMarch 23 2013; Accepted April 23, 2013; Published April 27, 2013 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 Copyright: 2013 McPherson FJ. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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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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captive lemurs are prone to hepatic iron accumulation (hemosiderosis) when fed a commercial primate diet which can contain excessive iron for their requirements. Hemosiderosis can, in turn, lead to hepatic disease [11]. Diet also can impact on the health of captive primates as evidenced by increased cholesterol levels and cardiovascular disease in apes such as gorillas (G. gorilla) and orangutans (P. pygmaeus) [21]. It has been established that captive gorillas consume different foods or certain plant parts as opposed to their wild counterparts. Captive 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 may adversely affect their health [25]. However, dietary fibre content is not the only important factor in the diets provided to captive primates. The type of plants available for consumption is important not only for nutrition but also for self-medication. Self-medication through consumption of plants with pharmaceutical properties (such as nettles) has also been observed to occur in wild chimpanzees (P. troglodytes) more than in wild gorillas. Therefore, the ingestion of unusual plants and other foods may serve a need other than nutrition [26] such as ridding themselves of gastrointestinal parasites [27]. A common plant (Aframomum) eaten by Western Lowland (G. gorilla) and Mountain gorillas (G. gorilla beringei) is thought to have anti-parasite properties as is another plant, combretum [27]. Chimpanzees in Nigeria were observed to swallow Desmodium gangeticum leaves and sharp-edged grass blades without chewing which were recovered undigested in fecal samples together with parasitic worms [28]. This suggests that the leaves serve a medicinal rather than nutritional purpose and in particular, aided in gastrointestinal parasite removal [28]. Wild chimpanzees (P. troglodytes) in Uganda have also been observed to consume Trichilia rubescens, a plant which contains anti-malarial compounds [29]. Captive gorillas are usually denied the plants they would normally seek out in the wild for self-medication and are in fact often fed a frugivorous diet rather than a more natural herbivorous diet [27]. Lack of provision of medicinal herbage may therefore possibly aid parasite proliferation and cause ill health in captive primates. Propagation of plants with medicinal properties in zoological parks may thus be a feasible option to maintain optimum health and encourage normal behavior in their captive primates.

Therefore, to optimize the validity of the data, physiological parameters should preferably be measured on animals of different ages and both sexes as well in order to be most useful to the field of primatology. In addition, comparing values from anesthetized and non-anesthetized would show what effect the anesthetizing agent potentially has on the physiological parameter being measured. One way to achieve this is to train some individuals within a primate colony to subject to blood sampling in return for a reward such as food so that chemical restraint is not required while the other animals are physically captured and anesthetized. Another useful study would be to use different anesthetic agents to determine which one/s least affect the blood chemistry and hematology parameters. Likewise, physiological measurements such as hematology and blood biochemistry made between animals that are suffering from a known pathogen or parasite burden and compared to healthy individuals of the same species and age can potentially highlight the effect the pathogen or pathogen has on the host animals of a given species. Hematology values: Table 1 shows the normal means and standard deviations of haematological values of a range of primate species commonly kept in captivity. Only parameters from adult animals are given in table 1 and readers should bear in mind that there can be large variations in haematological values when comparing adults to juveniles or aged individuals. For instance, an 8-year study in captive tufted capuchin (Cebus apella) monkeys showed that erythrocytes, hemoglobin, calcium, alkaline phosphatase, glucose and serum iron were all significantly higher in juvenile females than adult females [23]. Likewise, juvenile males had significantly higher values for phosphorus and glucose compared to adult males. However, adult male tufted capuchins (C. apella) had higher values for leucocytes, PCV, hemoglobin, neutrophils and creatinine [23] while capuchin (C. apella) adult males have higher levels of neutrophils and lower values for lymphocytes compared to juveniles [32]. In some cases, there are no differences between adults and juveniles [6]. Some parameter changes such as PCV, hemoglobin or MCV are not uniform across the animals lifespan i.e., the reduction or increase may slow down or reverse postpuberty [22]. However, not all species show sex-specifc differences in hematology or biochemical values such as free ranging brown lemurs (Eulemur albifrons) or ring-tailed lemurs (Lemur catta) [11,35]. Significant differences in hematological values were observed between the sexes also where female juvenile tufted capuchins (C. apella) had significantly higher values for neutrophils than juvenile males. Adult males had higher values for erythrocytes, hemoglobin and PCV compared to adult females [23], similarly male capuchin monkeys (C. apella) also have significantly higher PCV, erythrocytes and hemoglobin [32] as did cotton-top tamarins (Saguinus oedipus) [1], golden lion tamarins (Leontopithecus rosalia) [36], adult vervet monkeys (Chlorocebus aethiops) although not juvenile vervets [30]. Male apes such as chimpanzees (Pan troglodytes) also have significantly higher values for PCV, erythrocytes, hemoglobin while females have significantly higher values for total white blood cell counts (WBC), lymphocytes and eosinophils [22]. It is thought that males have higher erythrocyte counts, PCV and hemoglobin concentrations due to the greater muscle mass and male reproductive hormones in male monkeys [37] as well as the menstrual blood loss in females [24]. Blood profiles change as animals age as shown in cotton-top tamarins (S. oedipus) where PCV and hemoglobin decreased significantly in older females while age did not affect these parameters in aging males [1]. Hematology parameters also change from what is normal for wildcaught primates, during the post-capture adaption period and life

Hematology and blood biochemical parameters

There is wide variation in hematological and blood biochemical parameters among primate species from prosimians to great apes. Published results need to be interpreted with caution as factors such as capture stress [1,30,31], anesthetic agents [32], parasitism [33] and reproductive status (barren, pregnant or lactating) can all potentially influence the results. For example, creatinine kinase is located in skeletal, cardiac and smooth muscles and greater amounts are released in response to stress, which can be due to being captured. Thus, stress can account for highly variable results in this enzyme concentration when animals are captured for blood sampling [6]. In addition, as can be expected, it has been shown that there are significant differences in hematology and blood biochemical parameters during different stages of development in a primate such as neonatal, juvenile, adult and aged animals [24,32]. However, many hematological studies in primates fail to include aged individuals in their study animal cohort [22]. Data is also scarce for pregnant and lactating primates although one research group investigated the effect of iron supplementation of commercial diets for pregnant and lactating rhesus monkeys on infant monkey hematology profiles and iron status [34]. More research is needed to provide physiology measurements on pregnant and lactating primates of different species, ages and parity to fill the current large gap of knowledge in this area.
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

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Species M. mulatta M. mulatta S. oedipus S. oedipus S. labiatus S. labiatus S. leucopus C.apella C. apella C. aethiops C. aethiops P. troglodytes P. troglodytes L. catta M or F F M F M F M F& M F M F M F M F&M Erythrocytes (106/L) 5.2 0.44 5.51 0.40 6.13 0.35 6.42 0.2 6.9 0.5 7.0 0.3 6.74 0.8 5.37 0.43 5.92 0.45 5.4 0.5 6.5 0.8 5.06 0.34 5.4 0.42 n/e Lymphocytes (103/L) 8.69 2.72 9.27 2.10 2.96 1.40 2.37 1.09 6.85 1.85 5.91 2.75 51.1 13.5* 29.95 6.78* 33.21 9.74* 3.4 1.5 3.5 1.9 4.72 2.01 4.58 1.45 3.75 2.14 Neutrophils (103/ L) 7.17 2.31 4.86 1.85 3.42 1.16 2.88 1.17 5.58 3.02 4.48 2.27 46.6 14* 67.19 6.1* 63.89 9.23* 3.6 2.1# 2.5 1.3# 0.07 0.07 0.07 0.01 4.27 2.94 Monocytes (103/L) Basophils (103/L) 0.40 0.20 0.29 0.19 0.36 0.21 0.38 0.20 0.40 0.18 0.27 0.19 n/e 1.95 1.73* 2.06 2.16* 0.6 0.2 0.6 0.3 0.32 0.19 0.33 0.15 0.37 0.47 0.02 006 0.0 0.0 0.07 0.06 0.06 0.06 0.08 0.12 0.08 0.07 n/e 0.21 0.22* 0.21 0.27* n/e n/e 0.02 0.03 0.01 0.02 0.15 0.68 Eosinophils (103/L) 0.09 0.10 0.03 0.06 0.16 0.14 0.18 0.14 0.13 0.18 0.08 0.13 n/e 0.60 0.63* 0.82 1.01* n/e n/e 0.24 0.16 0.22 0.1 0.33 0.32 PCV (%) 0.41 0.03 0.43 0.02 50.22 3.00 53.13 1.92 0.04 0.41 0.52 0.03 49.0 4.4 38.77 3.57 42.58 3.54 40.3 4.0 50.6 6.2 42.05 1.8 45.04 4.17 50.5 6.2 Reference (n) 40 (36) 40,1 (36, 38) 1 (38) 1 (38) 33 (39) 33 (39) 6 (29) 23 (44) 23 (44) 30 (50) 30 (50) 22 (252) 22 (252) 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. aethiops) where there was a significant rise in packed cell volume (PCV) and mean corpuscular volume (MCV) for sexes, adults and juveniles, during the 4 months post-capture adaption period i.e. while the wild caught animals adapted to captivity. Similarly, the WBC and platelet 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 stress levels and decline thereafter due to the monkeys being exposed to many microbes in the wild as well as being linked to higher levels of cortisol in circulation as a stress response during and immediately after capture [38]. Likewise, platelet counts tend to decrease during adaptation to captive life as platelet release from the spleen takes place in response to fright [30]. Diet has an effect on hematological parameters also and it has been shown that a high protein diet as fed in captivity to vervet monkeys (C. aethiops) significantly elevates PCV, MCV as well as hemoglobin [39]. Illness changes the hematological profile and sick golden lion tamarins (L. rosalia) showed a reduction in monocytes and eosinophils and a concurrent increase in WBC, neutrophils and basophils [36]. Biochemical blood values: Table 2 shows the normal means and standard deviations of biochemical values of a range of primate species commonly kept in captivity. There is immense variation between the different species as well as the sexes. Striking differences are found in blood biochemical values when comparing the different primate species in table 2. For example, creatinine ranges from 0.33 mg/dL for Saguinus Oedipusto 4.36 mg/dL in Papio hamadryas. Cholesterol values range from 45.4 mg/dL in P. hamadryas to 224.7 mg/dL in P. troglodytes. Rhesus macaque (M. mulatta) males had lower sodium (149.7 3.1 mmol/l) and potassium (4.7 0.6 mmol/l) concentrations than females (153.7 3.5 mmol/l and 4.9 0.8 mmol/l respectively) [36]. However, in white-footed tamarins (S. leucopus), there was no difference in serum sodium concentrations between the sexes but serum chloride concentrations in males (94 5.1 mEq/L) was significantly lower than for females at 99 5.4 mEq/L [6]. Male capuchin (C. apella) monkeys had significantly more creatinine while females had higher values for BUN, AST and GGT [32].Cotton-top tamarin (S. oedipus) males also showed significantly elevated values for creatinine compared to females [1]. The most striking difference between the sexes was seen in
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total serum bile acids where Rhesus macaque (M. mulatta) males had twice as much than females at 24.9 16.7 mol/l vs 12.8 10.3 mol/l respectively [40]. Juvenile primates are still growing therefore they show differences in blood biochemical values compared to adults. One example of this is in alkaline phosphatase which is an enzyme that is present in elevated concentrations due to increased bone growth in juveniles [6,24,32]. Likewise, juvenile capuchin monkeys (C. apella) have significantly higher values for calcium, inorganic phosphorus (both also required for bone growth and development) and glucose than adults [32]. Male cotton-top tamarins (S. oedipus) had less calcium as they aged but this effect was not seen in females [1]. Age-related changes in blood biochemistry values may increase or decrease exponentially as with hematologic values. Both alkaline phosphatase and creatinine are greatest in juvenile animals. The alkaline phosphatase concentration curve flattens out at about 8 years of age in baboons (P. hamadryas) while creatinine does not show any sex-based differences until 5 years of age [24]. This is when baboons undergo puberty and males undergo a disproportionate increase in muscle mass compared to similar-aged females [41]. When studied by two different research groups, captive tufted capuchins (C. apella) showed significant differences between juvenile and adult animals in terms of alkaline phosphatase, calcium, glucose, inorganic phosphorus, aspartate aminotransferase and some serum proteins [23,32] although iron and alanine aminotransferase were also significantly different [23]. There can also be differences based on where animals are housed, presumably due to different diets and husbandry. This was the case in white-footed tamarins (S. leucopus) which were housed in three different facilities in Colombia and blood testing revealed significant differences in values for haemoglobin, serum total protein, albumin, glucose and alkaline phosphatase [6]. Differences also exist between captive animals and their wild counterparts in terms of biochemical parameters as was demonstrated in ring-tailed lemurs (L. catta). Furthermore, captive lemurs, possibly due to a diet high in ascorbic acid and low in tannins, can be more prone to hemosiderosis then wild lemurs [11,35]. It is also noteworthy that prosimians metabolize vitamins differently to other primates so, for example, carotenoids may be undetectable in lemurs but present in otherprimate species [11].

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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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Species Albumin (g/ dL) Calcium (mg/ dL) 48.96 3.06 47.34 2.34 9.02 0.50 8.69 0.59 2.60 0.17 2.5 0.2 8.7 1.1 2.39 0.17 2.33 0.12 9.14 42.71 93.02 30.44 288.9 186.3 540.83 429.49 627.33 428.73 2.41 13.14 5.43 10.8 13.4 81.18 30.06 92.7 28.62 0.33 9.15 0.81 8.46 1.32 42.66 2.88 42.48 2.88 Cholesterol (mg/dL) 55.08 7.2 51.3 10.98 134.67 31.04 153.94 51.04 n/e n/e 79.0 19.6 145.33 38.44 138.42 18.74 224.72 36.83 222.58 31.8 161.9 165. 45.54 11.88 45.36 9.54 89.0 26.0 10.3 100.33 15.18 118.7 47.5 103.32 31.86 95.04 24.3 142.0 0.2 2.43 Potassium (mmol/L) 4.90 0.76 4.67 0.62 4.04 0.44 4.25 0.64 4.5 0.78 4.0 0.95 4.9 1.0 3.92 0.36 4.2 0.56 3.39 0.43 97.04 1.67 3.43 0.34 97.5 1.63 108.98 22.52 107.86 4.23 108.0 6.0 4.55 97.5 3.58 0.53 3.7 0.53 4.4 0.6 Sodium (mmol/L) 153.74 3.47 149.71 3.07 150.50 2.12 150.06 2.54 156.0 6.3 159.0 5.0 148.3 13.5 148.02 2.13 148.95 2.29 139.97 1.68 140.93 2.33 135.5 4.55 145.69 3.69 146.35 3.5 148.0 5.0 3.74 0.87 4.36 2.88 1.0 0.3 24 (160 24 (160) 35 (903) 0.14 1.12 0.21 1.4 2.2 22 (252) 31 (44)

M. mulatta (F) 54.31 2.73 M. mulatta (M) 53.43 2.60 S. oedipus (F) 4.06 0.31 S. oedipus (M) 3.97 0.30 S. labiatus (F) 4.0 0.42 S. labiatus (M) 3.9 0.47 S. leucopus (M 3.1 0.49 & F) C. apella (F) C. apella (M) P. troglodytes (F) P. troglodytes (M) P. pygmaeus (F & M) 61.76 2.68* 61.22 3.43* 3.34 0.21 3.36 0.37 4.07 0.55

P. hamadryas 4.09 0.46 (F) P. hamadryas 4.17 0.41 (M) L. catta 5.7 0.9

222.0 109.0 22.0 8.0 9.7 0.9

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) from a mean value of 45 mg/dL in baboons (P. hamadryas) to 225 mg/ dl in chimpanzees (P. troglodytes) which exceeds the recommended maximum values for humans at <200 mg/dL [42]. Hypercholesterolemia in humans is implicated in coronary heart disease and cardiovascular disease is also a major cause of death in captive adult gorillas (G. gorilla [43]) and orangutans (P.pygmaeus; [44]) while 77% of adult chimpanzees (P. troglodytes; [45]) and 46% of adult bonobos (Pan paniscus; [46]) have died in zoos from cardiovascular diseasesince records were kept of causes of death up to 2003. Captive gorillas (G. gorilla) were found to have significantly higher (approximately 1.5x) cholesterol concentrations than free-ranging gorillas while both sexes of captive orangutans (P. pygmaeus) had significantly higher total cholesterol concentrations than free-ranging female orangutans [21]. The component of cholesterol which is linked to elevated risk of cardiovascular disease is low-density lipoprotein or LDL. The recommended concentration of LDL cholesterol in humans is <2.59 mmol/L [21]. In a study of captive apes comprising of Western lowland gorillas (G. gorilla gorilla), orangutans ( P. pygmaeus, P.abeli), chimpanzees ( P. troglodytes) and bonobos (P. paniscus), only bonobos had a mean cholesterol LDL value of 2.25 mmol/L which is below what is recommended for humans. The highest mean value of 3.8 mmol/L for cholesterol LDL was recorded for gorillas [21] while other researchers have documented similar high findings for gorilla serum cholesterol [47], presumably due to obesity, which is in turn due to inactivity and high dietary carbohydrate intake, insulin resistance and type 2 diabetes as well as progestins and androgens [42]. These are all risk factors which are in greater abundance for captive great apes compared to free-ranging primates. It would be beneficial to establish a database of known blood lipid values for captive gorillas (G. gorilla)
J Primatol ISSN: 2167-6801 JPMT, an open access journal

to better assess the risk of arteriosclerosis and coronary heart disease so that early intervention is possible [48].

Parasites
Nematode, cestode and trematode parasites
The use of captive primates as research animals could potentially be jeopardised by internal parasites causing ill health and possibly death. Likewise, endangered species survival may be further threatened by the presence of heavy loads of parasites [49] although it has also been proven that threatened species of primates which live in small groups harbour fewer parasites (helminths, protozoa, arthropods, bacteria and viruses) than non-threatened species where more individuals living in a smaller area facilitate parasite exchange [50]. Most information on parasite infections in primates comes from non-invasive fecal sampling of wild animals. Data concerning endoparasite loads in captive primates are scarce even though heavy infestations can cause diarrhea and even death in the host animals [51]. Internal parasites are found primarily in wild primates, since captive primates are often treated with anthelmintics as a preventative strategy [52] such as ivermectin which are used routinely to kill gastrointestinal parasites of domestic animals [53]. Even so, captive primates, like their wild counterparts, have been shown to harbor an extensive variety of internal parasites as outlined in table 3 however, in another study, no significant differences were found in parasite prevalence between wild and captive Olive baboons (P. cyanocephalus anubis)and Sykes (Cercopithecus mitis) monkeys [52]. Sampling 40 animals belonging to 7 lemur species kept in captivity at two zoos in Madagascar revealed significant differences between the two sites in the prevalence of strongylids, possibly due to one zoo using

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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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Primate (W/C) P. cyanocephalus (W) P. cyanocephalus (C) C. mitis (W) C. mitis (C) C. aethiops (C) C. guereza(W) C. angolensis(W) P. tephrosceles(W) P. cyanocephalus(W & C) C. aethiops(W & C) C. mitis(W & C) C. neglectus(W & C) C. albigena(W & C) C. torquatus(W & C) P. pygmaeus(C) S. fulleborni S. stercoralis Trichuris sp Oesophagostomum sp Trichostrongylus sp S. mansoni Streptopharagus sp Ascaris 63.0 17.3 61.8 32.5 44.0 4.2 5.26 3.54 30.6 16.3 23.5 0.0 0 12.5 39.0* n/e n/e n/e n/e n/e 0.0 0.0 0.44 9.0 22.8 32.5 17.7 50 62.5 n/e 73.9 69.3 60.0 51.2 50.0 79.0 100.0 37.75 38.7 47.1 50 50 37.5 62.5 7.0 76.0 17.3 47.2 20.9 0.0 6.09 0.00 2.8 n/a n/a n/a n/e n/e n/e n/e 43.5 16.0 38.2 0.0 0.0 n/e n/e n/e n/a n/a n/a n/e n/e n/e 3.0 4.3 0.0 0.0 0.0 0.0 n/e n/e n/e 3.6 4.9 0.0 0.0 0.0 0.0 n/e 42.2 0.0 52.7 0.0 0.0 n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e 1.26 0.00 0.12 n/e n/e n/e n/e n/e n/e 1 Reference (n) 52 (92) 52 (75) 52 (55) 52 (43) 52 (50) 63 (476) 63 (19) 63 (1608) 49 (111) 49 (123) 49 (34) 49 (12) 49 (8) 49 (8) 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 that can increase parasite loads in primates, wild and captive, include unwashed food items such as fruits and vegetables [51] and inbreeding since outbred animals are less prone to parasite infections than inbred individuals [54]. Out of 15 human workers taking care of captive infant orangutans (P. pygmaeus), only 3 tested negative for intestinal parasites and both humans and apes were infected with the same parasite species [55]. This cross-infection was enhanced by the workers not using protective clothing and infant apes (P. pygmaeus) being kept in large groups, which is an unnatural living arrangement, so that soil and floor contamination levels were high [55]. Many primate intestinal parasites are pathogenic in humans. Cross infection from primates to humans can occur with those who work with captive primates and also as a result of ecotourism where humans enter the wild habitat of infected primates. A colony of 39 semi-captive chimpanzees (P. troglodytes) in Uganda were found to be extensively infected (seroprevalence rate >90%) with the trematode Schistosoma mansoni while many of the 37 humans who came into close contact with the animals also harboured this parasite [56]. Captive olive baboons (Papio cyanocephalus) were found to have significantly lower parasite infection prevalence compared to their wild counterparts with the exception of Trichuris sp. where both populations had similar infection prevalence [52]. A coprological study of wild guenons in Western Uganda showed that parasite infection of blue monkeys (C. mitis) varied by location so most prevalence was found in Kenya for S. fulleborni, Trichostrongylus sp., Oesophagostomum sp. while there was no difference for Trichuris sp. and more prevalence of Streptopharagus and Bertiella sp. in South Africa [57]. Environmental conditions such as rainfall are most likely the cause for the difference in prevalence of intestinal parasites [58]. Housing conditions can influence parasite infections. For example, the prevalence of S. fulleborni is greatest in primates housed on gravel/dirt floor enclosures, moderate in cement floor enclosures while primates in cages suspended above the floor did not have any S. fulleborni [52]. Wild baboons for aging on the ground, especially near livestock and human settlements, are more susceptible to becoming infected than captive baboons that do not forage [59]. Arboreal primate species do not show significant differences in parasite prevalence
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between wild and captive animals since they tend to avoid coming into contact with contaminated soil [60]. Sex-differences can occur as in the case of only adult female guenons (Cercopithecus sp.) being infected with Oesophagostomum sp. and S. fulleborni [57], a findingthat could be due to females being pregnant and experiencing compromised immunity as a result [61,62]. However male red colobus (Piliocolobus sp.) showed higher infection rates with S. fulleborni than females [63]. Wild male orangutans (P. pygmaeus) had a significantly higher hookworm infection rate than wild females however there was no difference between dominant flanged males and subservient non-flanged males [55]. When taking into account total intestinal parasite loads, wild females had a higher total intestinal prevalence than males, presumably because the females have more contact with other orang utans, both with other females and their offspring [55]. However, a coprological survey of wild mountain gorillas (G. gorilla beringei) in Rwanda revealed no significant sex differences in parasite load or species of parasite harboured although dominant silverback males tended to have a higher prevalence of the pinworm Probstmayria sp. [64]. When two primate species co-inhabit the same region, parasite infestation can be similar between the different primate populations as determined in wild guenons of Western Uganda [57] or remarkably different between the species as shown in a coprological survey performed on western lowland gorillas (Gorilla g. gorilla)and chimpanzees (Pan t.troglodytes) in Gabon. While 84% of the gorilla fecal samples were positive for parasites, only 56% of the chimpanzee samples contained evidence of intestinal parasites [65].The same could potentially apply to primates of different species co-habitating the same enclosure. When closely related colobus monkey species were sampled; Eastern black and white colobus, (Colobus guereza); Angolan black and white colobus (C. angolensis) and red colobus (Piliocolobus tephrosceles), host species effects were found for the prevalence of Trichuris, Ascaris, unidentified strongyle sp. and Oesophagostomum sp. Overall, eastern black and white colobus monkeys (C. guereza) were more susceptible to parasite infection than red colobus (P. tephrosceles) [63]. However, other researchers found that while black and white colobus monkeys (C. guereza) harboured only a single species of parasite (Trichuris sp.), the other 5 species of primates that were sampled harboured

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multiple concurrent parasite infections [49]. Mountain gorillas (G. gorilla beringei) harboured cestodes such as Anoplocephala gorilla in abundance (51-92%) while lowland gorillas in different geographical areas did not have any, possibly due to the lack of intermediate hosts in their environment [66].

However, while P. knowlesi tends to infect mainly long-tailed macaques (Macaca fascicularis) and pig-tailed macaques (Macaca nemestrina), humans can be infected also [70]. Likewise, malaria sporozoites can be transferred from infected humans to primates as demonstrated in gibbons (Hylobates lar [71]).

Protozoan parasites
Protozoal infections such as Balantidium coli and Entamoeba colican are more common in captive primates, which could be due to contaminated water and housing [52] (Table 4). However, free ranging primates can also become infected when drinking water contaminated by infected fecal material from ruminants, other primates or humans. Free-ranging baboons (Papio sp.) had a lower rate of protozoal infection than captive baboons for E. histolytica and B. coli but the reverse was true for Entamoeba coli [52]. Captive Sykes (C. albogularis) monkeys had a lower rate of infection for all three protozoal parasites compared to free ranging Sykes monkeys [52]. Free-ranging arboreal species such as colobus monkeys (Colobus sp. [63] and Ugandan guenons (Cercopithecus sp. [57]) showed low prevalence of protozoan infections. In another study of captive, semi-captive and wild orangutans (P. pygmaeus), the prevalence rates of 3 genera of Protozoa was >10% of which 2 are pathogenic (Entamoeba histolytica and Balantidium sp.) while the third (Entamoeba coli) is non-pathogenic [55]. Balantidium sp. was most prevalent at 39% and 41% prevalence in captive and semicaptive orangutans (P. pygmaeus) respectively. Entamoeba coli was equally prevalent in captive and semi-captive populations at 22% and 32% respectively however, E. histolytica, with a prevalence rate of 3% in captive vs 35% in semi-captive orangutans was not equally distributed [55]. In a study comparing wild and captive ring-tailed lemurs (L. catta), captive and wild animals harbored different parasite species with Entamoeba coli being the only parasite common to both populations [67]. Giardia was only present in captive lemurs (L. catta), despite no clinical signs being present, while only wild ring-tailed lemurs tested positive for Cryptosporidium [67]. Malaria is a potentially fatal disease caused by the zoonotic protozoan parasite Plasmodium sp that is transmitted not through direct contact with infected animals or infected feces but by mosquito vectors [68]. A blood smear survey and polymerase chain reaction analyzes for Plasmodium sp. revealed that 29 out of 31 captive orangutans (P. pygmaeus) and 5 out of 43 wild orangutans tested positive for malaria. The greater prevalence in captive apes was possibly due to a 50-fold increase in population density in captivity compared to the wild population which facilitated transfer of the parasite by mosquitoes [69]. Malaria can be host-specific, for example,orangutans (P. pygmaeus) are naturally infected with either P. pitheci or P. silvaticum.
Primate species P. pygmaeus (C) P. cyanocephalus (W) P. cyanocephalus (C) C. mitis (W) C. mitis (C) C. aethiops (C) C. guereza(W) C. angolensis (W) P. tephrosceles(W) L. catta(C) L. catta(W) Entamoebahistolytica 3 26.1 26.6 23.6 16.3 25.4 7.56 10.53 3.48 0.02 0.0 Entamoeba coli 22 78.3 66.7 54.5 34.9 74.0 7.77 15.79 4.35 0.0 0.0 Endolimax 9 n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e

Microsporidian parasites
Encephalitozoon cuniculi is a fungal obligate intracellular parasite that can exist in infected individuals for years and quickly kill others. In an affected colony of captive emperor tamarins (Saguinus imperator), all infants died after showing obvious signs of disease such as infections and systemic vasculitis as well as high titres for encephalitozoon [72]. Respiratory distress and acute onset of cardiac failure were symptoms of microsporidia in an affected captive adult male Goeldis monkey (Callimico goeldii). At autopsy,findings were multicentric arteritis and aortitis [73]. Subsequent serosurveys of monkeys imported into the USA in the same consignment and potentially exposed to the infected individual revealed that multiple animals tested positive for E. cuniculi antibodies against genotype II [73]. Other New World primates harboured genoptype III E. cuniculi such as squirrel monkeys (Saimiri sciureus) that were bred in captivity in Japan [74].

External parasites
Primates are prone to similar exoparasites as other animals such as fleas and lice, potentially causing sarcoptic mange. Alopecia is not always due to exoparasites and can be a form of self-mutilation when hair loss is apparent. External parasites are not usually problematic unless primates are housed in isolation since mutual grooming serves to not only strengthen and reaffirm social bonds [75,76] but also rid the fur of exoparasites such as lice which are eaten by the groomer animal [77]. Indeed, mite infestation in wild brown lemurs (E. fulvus albifrons) was not associated with alopecia or pruritis [11].

Infectious Viral Diseases

Primates and humans share susceptibility to a range of pathogens which makes it a challenge to work with these animals and prevent transfer of zoonoses. One such example is the mumpsvirus (Epidemic parotidis) where apes can be infected from a human [78]. As a precaution, infected animals should be quarantined and protective gear worn by their carers such as gloves, face mask and surgical apron or overalls. Likewise, when a researcher, veterinarian or zoo worker is ill, he or she should either refrain from coming into contact with healthy primates or take all the necessary precautions to avoid spreading infectious agents throughout the primate colony. In wild primates, sudden deaths en-masse can be a sentinel message.
Iodamoeba 4 n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e Balantidium 39 43.6 23.2 43.6 23.2 30 n/e n/e n/e 0.0 0.04 Giardia 3 n/e n/e n/e n/e n/e 0.0 0.0 0.81 0.1 0.0 Blastocystis 15 n/e n/e n/e n/e n/e n/e n/e n/e n/e n/e Reference (n) 55 (119) 52 (92) 52 (75 52 (55) 52 (43) 52 (50) 63 (476) 63 (19) 63 (1608) 67 (50) 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] in Howler monkeys (Alouatta sp) and Kyasanur Forest disease virus in bonnet macaques (Macaca radiata) and hanuman langurs (Presbytis entellus) in India which later infected humans living near the forest [80]. Since it is probable that the human immunodeficiency virus (HIV) originated from simian immunodeficiency virus (SIV) through direct contact between affected primates and humans [81] and especially from chimpanzees and sooty mangabeys [82,83], the threat of zoonoses is especially high for humans working with primates.

and gorillas (G. gorilla), is most likely the reason why it is the most commonly transmitted retrovirus from primates to humans through infected saliva and blood when zoo workers, veterinarians and animal researchers are bitten or through needlestick injury when the needle contains infected blood [90]. Even so, many SFV-infected humans show no apparent signs of ill health for many years after exposure to the virus which seems to remain latent in the blood peripheral lymphocytes. Transmission between humans is not as prevalent as between primate and human [81]. Another retrovirus, simian type D retrovirus (SRV), is a highly prevalent virus with >90% of captive Asian macques infected and displaying symptoms similar to AIDS [91]. On the other hand, herpesvirus papio2 (HVP2) is not as prevalent with only 3.8% of captive baboon (Papio sp) swabs being positive for HVP2 over a period of 1.5 years with twice yearly testing of 128 baboons [92] although another captive colony of baboons (P. anubis and P. cyanocephalus) 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 cavity [92]. Of the 31 wild-caught baboons that were swabbed before being added to the colony, none were shedding the virus although >93% of these animals were seropositive for the virus. Another captive colony of baboons had a HVP2 infection rate of ~33% with half of the baboons shedding the virus into the oral cavity and the other half into the genital tract [92]. HPV2 appears to be present predominantly in the oral cavity of young baboons and is transmitted sexually in adults [92]. In another study, >90% of wild caught adult olive baboons (P. anubis) and chacma baboons (P. ursinus) were seropositive for HPV2 although there were no differences in immune sera reactivity to HPV2 between the baboon species [93].

Arboviruses
Arboviruses infecting primates include dengue, Japanese encephalitis, Langat, Sinbis, Tembusu and Zika. It is considered to be beyond the scope of this review to cover every single virus known to infect primates so only a select few of greatest importance will be covered here. The incidence of primates testing positive to any virus is variable among wild and captive animals. No animals tested positive for any of the 33 viruses tested for out of their sample population of 44 semicaptive and 54 free-ranging orang-utans (P. pymaeus) in Malaysia [31]. However, in another study of wild and semi-captive orangutans in Borneo, one out of 71 apes (1.4%) tested positive to all flaviviruses examined [84]. Wild and semi-captive orangutans were both infected with dengue-2, Zika, Tembusu and Japanese encephalitis virus. Sindbis virus was found only in wild orangutans (P. pygmaeus) while only semi-captive orangutans tested positive to Langat virus. Humans living near the forest were infected with all viruses except Sindbis virus [84]. The difference in prevalence could be due to the wild ape cohort being primarily adults while the semi-captive orangutans were mostly juveniles. Adults showed a greater seroprevalence for all 6 viruses examined than juveniles [84]. Dengue-2 and Japanese encephalitis were the two most common flaviviruses among both orangutan groups [84]. Both viruses are not species-specific and infect other mammal species and birds [85,86].

Infectious Bacterial Diseases

Leptospirosis
Leptospirosis is a zoonotic bacterial disease spread through infected urine that infects domestic and wild animals as well as humans [94]. Primates, even in captivity, may become infected when they come into contact with seropositive animals such as rodents. Humans coming into contact with primates can transfer or become infected with the bacteria [95]. Primates destined for release back into the wild are not routinely tested for anti-Leptospirosis antibodies during their rehabilitation period so there is a real risk of introducing the disease into nave wild populations. In a captive population of 44 marmosets and capuchins (C. jacchus, C. pennicilata and Cebus sp) in Brazil, 56.8% tested positive for the presence of Leptospirosis antibodies despite no signs of clinical disease being present [96]. The prevalence of leptospiral antibodies in 73 captive lion tamarins (l. rosalia) elsewhere in Brazil was much lower at only 15% [97] suggesting that there may be a species-effect in antibody prevalence rates.However, at a Colombian Zoo, not only was the seroprevalence 23% in the resident Neotropical monkeys, 25% of zoo workers also tested positive for Leptospirosis antibodies despite most of the zoo workers wearing protective clothing to minimise transmission risk between animals to humans [95]. Most reactivity was found in Black spider monkeys (Ateles fusciceps), whitefronted capuchin (Cebus albifrons) and white-footed tamarin (Saguinus leucopus). Monkeys and zoo workers had different predominant serovars [95] which may be due to serovar conversion within a new host. Stress levels can influence prevalence of protozoan, as well as helminth, infections [98]. An example of this was found in semi-captive lactating orangutan females which were rescued and experienced

Non-Arboviruses
Non-arbovirusesthat can infect primates include rotavirus SA11, respiratory syncytial, parainfluenza 3, mumps, foamy, Ebstein-Barr, Coxackie B-4, herpes, hepatitis A and B, poliomyelitis, rubella,and monkey pox. The prevalence of Simian Foamy Virus (SFV) is captive nonhuman primates is very high at approximately 70% while the prevalence of simian immunodeficiency virus (SIV) is up to 36% in wild primates [81]. SFV is the most transmitted primate retrovirus to humans working with primates [80] and people who hunt and eat primates [87]. In a sample of wild-caught primates, 5 out of 27 gorillas (G. gorilla; 19%), 7 out of 11 mandrills (Mandrillus sphinx; 64%) and 2 out of 6 drills (Mandrillus leucophaeus; 33%) tested positive to SFV although not all harboured the same viral strain with the drills being infected with two different strains and the gorillas having 3 strains of SFV [88]. Chimpanzees (P. troglodytes) were found to be source of SFV infection in 9 out of 10 infected human workers with the remaining person infected by a baboon [81]. Prevalence of SFV in captive primates is 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 contact [81]. The high prevalence of SFV among captive and wild primates, especially baboons (Papio sp), chimpanzees (P. troglodytes)
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unstable grouping arrangements from constant introductions of newly rescued individuals. These animals had a high prevalence rate of 76% (55) and this is a similar finding as in red colobus monkeys with high stress levels, lowered immune response and high prevalence of parasite infections [99].

References
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Other ailments
Although great advances have been made over the years in terms of knowledge of primate husbandry, mortality can still be high. For example, half of the gorillas which died in zoos did so before reaching maturity at 8 years of age [100]. Reproductive failures such as rejection of newborns and stillbirths account for some of these deaths while pathogenic infections and internal parasites are preventable causes of death. Dental disease and cardiac disease are also threats to captive gorilla (G. gorilla) health [100]. Captive primates can be prone to boredom and social stress due to being kept in groups without the possibility of subordinates leaving at their free will when they are the repeated recipient of aggressive behaviour directed at them. Captive great apes are prone to obesity when opportunity to exercise and forage for food is denied. Obesity is also linked to cardiac disease which is currently a main cause of mortality in captive gorillas [101]. Male gorillas (G. gorilla and G. beringei) are more prone to cardiac disease than females and the most common conditions are progressive left ventricular (LV) hypertrophy and depressed LV ejection fraction [102]. Vitamin D deficiency due to lack of adequate exposure to natural sunlight is a potential problem documented in captive primates, especially in juvenile and prime adult primates housed only indoors [103]. Effects such as lowered serum calcium and phosphorus concentrations seem to affect female chimpanzees (P. troglodytes) more profoundly than males. In juvenile primates, vitamin D deficiency manifests as rickets and pathologic fractures, symptoms that can be reversed by daily oral administration of vitamin D2 following an injection of vitamin D2 in sesame seed oil [104]. Prevention of rickets in juvenile apes raised indoors under sky lights was achieved with a single injection of slow release vitamin D at a rate of 5000 IU intramuscularly at 4 months old followed by a daily oral vitamin D supplement [104]. It should be noted that male ring-tailed lemurs (L. catta) tend to have significantly higher serum vitamin D concentrations than females which could be due to differential sunning behavior or consumption of different foodstuffs between the sexes [35]. Similar findings could apply to other lemur species also.

Summary
In conclusion, the health and welfare of captive non-human primates has improved over the years so that mortality rates have declined however, the main causes of death for great apes include cardiovascular disease and diabetes which is directly linked to a sedentary lifestyle in captivity. There are significant differences in physiological parameters such as blood biochemistry, even between closely related species while endoparasite loads can vary between species in a given location or between the sexes. The risk of zoonoses remains high for humans coming into close contact with primates with regards to endoparasites and infectious diseases. Therefore, it remains prudent to take precautionary measures such as protective clothing to prevent transmission of pathogens and parasites between primates and humans. The data presented in this review could assist in improving the health of captive primates.
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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

J Primatol ISSN: 2167-6801 JPMT, an open access journal

Volume 2 Issue 2 1000112