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Bakker, J. Unintentional Intoxications of Nonhuman Primates: Miscellaneous. Encyclopedia. Available online: https://encyclopedia.pub/entry/22239 (accessed on 07 December 2024).
Bakker J. Unintentional Intoxications of Nonhuman Primates: Miscellaneous. Encyclopedia. Available at: https://encyclopedia.pub/entry/22239. Accessed December 07, 2024.
Bakker, Jaco. "Unintentional Intoxications of Nonhuman Primates: Miscellaneous" Encyclopedia, https://encyclopedia.pub/entry/22239 (accessed December 07, 2024).
Bakker, J. (2022, April 25). Unintentional Intoxications of Nonhuman Primates: Miscellaneous. In Encyclopedia. https://encyclopedia.pub/entry/22239
Bakker, Jaco. "Unintentional Intoxications of Nonhuman Primates: Miscellaneous." Encyclopedia. Web. 25 April, 2022.
Unintentional Intoxications of Nonhuman Primates: Miscellaneous
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Wild and captive nonhuman primates (NHP) are exposed and potentially vulnerable to many natural and man-made toxic threats. Nevertheless, wild NHP are capable of coping with these threats using strategies, namely avoidance, dilution, gastrointestinal degradation, or detoxification, which require genetic potential, learning from parents and conspecifics in their social group, or prior experience through random food sampling and experimentation. Captive NHP are also at high risk for intoxications when they are often housed in an outdoor enclosure in a vivarium or zoo that is in or close to a large urban and industrial city. These NHP are potentially exposed to urban-industrial air pollution due to industrial and vehicle exhausts, waste incineration, and the domestic and industrial use of petroleum-based products, cleaners, pesticides, and paints, amongst others.

nonhuman primates poisoning

1. Pesticides

A pesticide is a naturally occurring or synthetic chemical or biological agent that is used to control pests. About 700 pesticides are in current use and these pesticides can be classified according to (a) the type of target pest (organism), such as a herbicide, an insecticide, a nematicide, a rodenticide, a fungicide, and a bactericide; (b) the chemical structure, such as organophosphates, organochlorines, carbamates, and pyrethroids; and (c) the mechanism (mode) of action, such as enzyme inhibitors, disruptors of cellular signaling pathways, and generators of reactive molecules that destroy cellular components, amongst others. To be acceptable, a pesticide must be toxic to the intended target and not toxic to any non-target organism.
Wilderness areas are vital refuges where natural ecological and evolutionary processes can operate with minimal human disturbance. Humans have appropriated much land and altered terrestrial ecosystems for agriculture. Agricultural frontiers are dynamic environments that are characterized by the conversion of native habitats to agriculture and the highest incidence of species loss occurs on an agricultural frontier. Therefore, habitat loss is a burgeoning threat to a population of wild NHP and other terrestrial vertebrates that live on an agricultural frontier. Furthermore, the use of pesticides on an agricultural frontier has the potential to detrimentally affect wild NHP populations, the local biodiversity, and ecosystem’s structure and function.
An overview of the reported cases of pesticide poisonings in wild NHP are presented in Table 1A,B. Since these poisonings occurred mostly on agricultural frontiers, pesticides, which were used to control agricultural pests, were the suspected cause of these poisonings in non-target wild NHP. The main reported outcome of an acute poisoning by a pesticide was death (Table 1A). Continual exposure to a pesticide on an agricultural frontier may also be hazardous for wild NHP populations because of the possible teratogenic effects of the pesticide: birth (congenital) defects have been reported in the offspring of pesticide-exposed pregnant mothers (Table 1B). These effects were usually documented in the reports of research projects whose aims were to (a) determine the cause of the phenotypical harm to wild NHP and (b) understand whether these harms were linked to environmental pollution of their habitat. Unfortunately, no definitive links between pesticide exposure and reproduction or frequency of stillbirths could be made. Interestingly, many health authorities advise pregnant women or women who are planning to become pregnant avoid contact with or exposure to pesticides because some pesticides may cross the placental barrier and lead to miscarriages, pre-term births, infants with low birth weights, birth defects, and congenital anomalies.
Table 1. (A) Summary of the reported cases of death in wild NHP due to acute pesticide poisoning on agricultural frontiers. (B) Summary of the reported birth defects and congenital anomalies in wild NHP due to suspected continual pesticide exposure on agricultural frontiers. * The clinical signs and main laboratory findings and pathology were often not performed and documented in the report.
(A)
NHP Species Suspected Pesticide Clinical Signs Laboratory and Main Postmortem Findings Reference
Not specified Anticoagulant
rodenticide
Not provided Not performed Bates, 2016 [1]
Vervet monkeys (Chlorocebus pygerythrus) Aldicarb, carbofuran Sudden death Not performed Botha et al., 2015 [2]
Golden Langurs (Trachypithecus geei) Organochlorine
insecticide
Sudden death Insecticide was detected in the liver, kidney, and intestinal contents Pathak, 2011 [3]
Bonnet macaque (Macaca radiata) Carbofuran (a
carbamate insecticide)
Sudden death Cyanosis, severe pulmonary congestion, splenomegaly and dark purplish-blue granules, identified as carbofuran, in the gastric contents Radhakrishnan, 2017, 2018 [4][5]
Cynomolgus monkeys (Macaca fascicularis) Anticoagulant bromadiolone and
difenacoum
Sudden death extensive subcutaneous and internal hemorrhages. Bromadiolone and difenacoum were detected in frozen liver samples IJzer et al., 2009 [6]
Squirrel Monkey (Saimiri sciureus) Fipronil Ranging from sudden death to symptoms of depression, inappetence, lethargy and body weight loss, which progressively disappear over time Fipronil and fipronil sulfone were detected in cutaneous and brain tissue Demir et al., 2021 [7]
Tantalus monkeys (Cercopithecus aethiops) Dieldrin Sudden death Not performed Koeman et al., 1978 [8]
(B)
NHP Species Suspected Pesticide Clinical Signs Laboratory and Main Postmortem Findings Reference
Ring-tailed lemurs Organochlorine
pesticides
* * Rainwater et al., 2009 [9];
Dutton et al., 2003 [10]; Miller et al., 2007 [11]
Chimpanzees and baboons Several different pesticides (Congenital) facial and nasal deformities (i.e., reduced nostrils, cleft lip), limb deformities, reproductive problems, and hypopigmentation * Krief et al., 2017 [12]; Lacroux et al., 2019 [13]
Baboons, howler monkeys, chimpanzees, red-tailed monkeys, red colobus Pesticides,
halogenated flame retardants, and
organophosphate flame retardants
* * Wang et al., 2020 [14]
Douc langurs (Pygathrix spp.) Dioxins (i.e., Agent Orange, tetrachlorodibenzo-p-dioxin) and dioxin-related compounds Two animals exhibited developmental consequences of possible dioxin exposure * Brockman et al., 2009 [15];
Brockman & Harrison, 2013 [16]
Baboons (Papio spp.), Tantalus monkeys (Chlorocebus tantalus), red tail monkeys (Cercopithecus ascanius), vervet monkeys (C. pygerythrus), Campbell’s monkeys (Cercopithecus campbelli lowei), Zanzibar red colobus (Procolobus kirkii), and chimpanzees (Pan troglodytes) Pesticides * * Ogada, 2014 [17]; Naughton-Treves, 1998 [18];
Eniang et al., 2011 [19]; Nowak et al., 2009 [20]; Sai et al., 2006 [21]
Japanese monkeys (Macaca fuscata) Dieldrin and heptacholorepoxide Congenital defects such as abnormal limbs in offspring Elevated concentration of dieldrin and heptacholorepoxide in the liver and kidney of female monkeys whose babies were born with malformations Minezawa et al., 1990 [22]

2. Botulism

Botulinum toxins are neurotoxins that are produced by spores of the anaerobic bacterium, Clostridium botulinum. There are seven botulinum toxins, namely, A, B, C, D, E, F, and G. Types A, B, E, and F cause botulism in humans and types C, D, and E are the causes of botulism in other mammals and vertebrates. Since the spores are resistant to heat, botulism usually occurs after the ingestion of improperly processed food or spore-contaminated water (food-borne and water-borne botulism). However, botulism can also occur when a wound becomes infected with the spores or inhalation of the spores. The main clinical signs of food-borne botulism are an initial ataxia, which is followed by flaccid paralysis of the legs and neck muscles and respiratory depression and failure [23]. Botulism is a rarely reported disease in NHP. The published reports on botulism in captive NHP indicate that the cases were food- and water-borne botulism caused by the type C toxin [24][25][26]. Diagnosis is usually based on the history and clinical signs, and laboratory confirmation of the toxin’s presence in the suspected source and blood, body fluids, and excretions of affected animals. Treatment comprises administration of antitoxin, mechanical ventilation, and other supportive treatments. Untreated botulism is fatal.

3. Polychlorinated Biphenyls

Polychlorinated biphenyls (PCBs) are human-made chlorinated organic chemicals and were widely used in innumerable industrial and commercial applications. Since PCBs are chemically stable and non-inflammable and have electrical insulating properties, they (a) were present in electrical transfer and hydraulic equipment, (b) used as plasticizers in paints and rubber products, and (c) constituents of pigments, dyes, and carbonless copy paper, amongst others. PCBs were manufactured worldwide from 1929 until the late 1970s and early 1980s, when their manufacture was terminated when authorities realized that PCBs were persistent environmental and toxic contaminants. The primary sources of environmental PCBs include their vaporization after undisclosed uses in unenclosed areas, inappropriate disposal practices, volatilization and runoff from landfills that have PCB-containing wastes, accidental release of PCBs from facilities where they are used, and incineration of PCB-containing wastes.
PCBs have become ubiquitous environmental contaminants because they do not easily degrade in the environment. PCBs can bioaccumulate in adipose tissue of NHP because they are lipophilic. PCB congeners such as polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) are carcinogenic.
Several reports on PCB toxicity in captive NHP have been published [27][28][29][30]. This toxicity is a chronic and progressive disease, which is characterized initially by diarrhea, weight loss, dehydration, weakness, lethargy, inappetence, followed by alopecia, acne, facial edema, swelling and reddening of the eyelids, gingivitis, and emaciation, and then death. PCBs also possess teratogenic properties. The infants of PCB-exposed mothers are small and unthrifty, and the infant mortality rate is high. Laboratory and main postmortem findings of PCB toxicity were hypertrophic and hyperplastic mucinous gastropathy and the presence of PCBs in the livers of the dead NHP [31][32][33]. The source of the PCBs was the concrete sealers that were used during building (re)construction [27][28][29][30]. The treatment comprised the removal of the PCB-containing sealer and resurfacing the floors of the NHP’s housing facility.

4. Snake and Spider Venoms

Snakes are ectothermic limbless reptiles that regulate and maintain their body temperature by relying on the environment. Venomous snakes are found in most parts of the world except in very cold regions and many islands and have been identified in only five families: ElapidaeHydrophiidaeViperidaeCrotalidae, and Colubridae. Venom is produced and secreted by the snake’s oral glands in order to immobilize and kill its prey and aid in its digestion. The composition of snake venom has a large degree of variability: enzymes and proteins of various sizes (phospholipases, serine proteases, catalase, hyaluronidase, and collagenase), amines, lipids, nucleosides, and carbohydrates. Venoms act on many cell types and their actions include cell and cell membrane digestion, disruption of the functional role of the procoagulant and anticoagulant systems in blood, production of reactive oxidizing agents, breakdown of collagen and the intercellular matrix, and neurotoxicity. Venoms can also be classified according to their main toxin, namely a neurotoxin, a hemotoxin, a cardiotoxin, a cytotoxin, or a myotoxin and the target organ because they cause paralysis, coagulopathy, rhabdomyolysis, and organ failure.
There are only a few published reports of (fatal) attacks on wild NHP by venomous snakes, usually terrestrial vipers [34][35][36][37]. A bite from a Crotalus adamanteus has immediate local and systemic effects. The local effects at or near the site of the bite include marked edema (and apparently marked pain), followed by rupture of the skin, and tissue and muscle necrosis. The systemic effects are dependent upon the venom’s composition and confined to general lethargy, salivation, bloody diarrhea, and death in an irreversible coma. Hydrocortisone treatment is probably therapeutically beneficial for NHP following a venomous snake bite [38].
Spider venoms are a mixture of many active compounds, some of which have cytolytic or neurotoxic activity. The Australian funnel-web spider, which has been designated as the world’s deadliest spider, is named so because its venom contains a lethal neurotoxic polypeptide, robustoxin [39]. This neurotoxin is a δ-hexatoxin (δ-HXTXs) and this family of toxins is responsible for the human envenomation syndrome. In human bite victims, δ-HXTXs cause disturbances in respiration, blood pressure, and heart rate, followed by severe hypotension. Without treatment with commercial antivenom, fatalities can occur by respiratory and circulatory failure within a few hours of the bite. Wiener [40] reported on the death of and the main post-mortem findings in a captive cynomolgus monkey (Macaca fascicularis) that died within 36 h after being bitten by a funnel-web spider. The main post-mortem findings were areas of emphysema, hemorrhage, and edema in the lungs. Although Gray and Sutherland [41] reported that a captive monkey may sometimes die after being bitten by a female funnel-web spider, there is no certainty that venom has been injected after a spider bite [40]. It has also been reported that captive cynomolgus monkeys can be protected against the lethal effects of male funnel-web spider venom by immunization with robustoxin glutaraldehyde-polymerized toxoid [42][43] or a synthetic robustoxin derivative lacking disulfide bridges [44].

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