The Primate Zoonoses

Culture Change and Emerging Diseases

Loretta A. Cormier, Pauline E. Jolly

• Publisher: Taylor & Francis
• Year: 2017
• Print ISBN: 9780367607326
• eBook ISBN: 9781315414874
• Edition: 1
• Topic: Social Sciences
• Subtopic: Anthropology
• Index: Social Sciences

This book offers an accessible and up-to-date reference on primate zoonoses. Recent years have witnessed a rise in human diseases zoonotically transferred from animals, with wild primates implicated in the spread of numerous newly emerging infections. The authors go beyond simply providing an inventory of diseases, helping readers to understand how and why they are transmitted. Important consideration is given to the contemporary cultural and ecological factors involved.

1
The ecological context

Emerging infectious disease

Nonhuman primates contribute substantially to emerging infectious diseases in humans. Of the approximately 75% of emerging pathogens that are also zoonotic, nearly 25% are found in nonhuman primates (Cleave-land et al. 2007; Taylor et al. 2001). Both the major taxa of the organisms (viruses, bacteria, protozoa, and helminths) and their mode of transmission play important roles in the potential for a given parasite to become an emerging infection in humans. According to Taylor et al. (2001), although virtually all of the helminths (parasitic worms) can be considered potentially zoonotic, they are far less likely to be the source of an emerging infection than viruses or protozoa are. More narrowly, considering helminth cross-transmission among human and nonhuman primates, the literature review for this book identified numerous studies demonstrating broad susceptibility among species in the order Primates to each other’s helminths. However, they are rarely the source of emerging infections. Two notable exceptions are the lymphatic filariasis and the larvae (cercariae) of schistosomiasis, which are both vector-borne. All vector-borne parasites have a higher risk of becoming emerging infectious disease than parasites transmitted through other means have (Taylor et al. 2001). The ecological context is also of paramount importance in understanding under what conditions any given parasite may potentially be spread among species.

Zoonoses and anthroponoses

The World Health Organization (WHO) defines a zoonosis as any disease or infection that is naturally transmissible from vertebrate animals to humans (WHO 2016a). The phrase “naturally transmitted” excludes infections that are intentionally induced in laboratory settings. In the past, humans have also been the subject of experimental infection with animal pathogens. One example involves studies in the 1960s when over 200 prisoners were inoculated with various strains of wild primate malarias to determine if infections could be established in humans (Coatney 1968; Cormier 2011). Many species of wild primates have been used as models in the study of human diseases, particularly Rhesus macaques, chimpanzees, owl monkeys, and squirrel monkeys. However, acquisition under experimental conditions should not technically be considered cases of zoonotic or anthroponotic disease, although such studies can provide information about potential susceptibility.

A gray area exists when considering parasite exchange among captive nonhuman primates. In the literature, the phrase “natural transmission” or “natural infection” is sometimes applied to situations where human and non-human primates have been exposed to and acquired each other’s parasites, such as in zoos and in primate research centers. Describing such infections as natural is problematic and can be misleading, for although the infections were not acquired through experimental induction of parasites, they are also not natural settings. One example is the protozoa Trypanosoma cruzi, the agent of Chagas disease. The protozoa is indigenous to the Neotropics, but can also survive in the southernmost areas of the United States. In southern U.S. zoos, Asian and African species of primates have been found to harbor the parasite (see Chapter 3, but the parasite does not exist in their natural habitats. Primate sanctuaries with semi-captive primates also represent a gray area. These facilities often take in rescued orphans or former pets that would not be able to survive independently in the wild. Although they have access to natural habitat, they are also often in frequent contact with humans. In some contexts, even primates in wildlife preserves that sponsor ecotourism may not be in entirely natural conditions for they may become well habituated to humans.

Anthroponoses are infectious diseases of humans that can be naturally transmitted to animals. In the broadest sense, the term “primate zoonosis” can elide the distinction between anthroponosis and zoonosis. Because humans are primates, the primate zoonoses are those diseases that may cross between members of the taxonomic order Primates. In many cases among primate species, the barrier preventing an infectious agent in a host species from cross-infecting a novel species may not be due as much to biological differences as to ecological differences that prevent two primate species from coming into contact. For our purposes here, the primary focus is on wild primate diseases that cross over into human populations.

The term “pathogen” is often used to describe an infectious agent, but some caution should be used, for not all infectious agents cause pathogenic symptoms in their hosts. In Nunn and Altizer’s (2006:3) work on primate infectious disease, they prefer the broad term “parasite,” defined as any organism that lives on and draws nutrients from a host, including both microparasites and macroparasites, drawing on the distinction made by Anderson and May (1991). Microparasites have direct reproduction within a host and include viruses, bacteria, fungi, and protozoa. Macro-parasites are those that do not have direct reproduction within the host and include helminths (e.g., parasitic worms) and arthropods (e.g., ticks and mites).

A parasite may infect several different types of hosts, differentiated below (Hubálek and Rudolf 2010; Salfeder et al. 1992; Soloman et al. 2015). Broadly, the term “host” refers to any species that has been detected to harbor a parasite. A reservoir is one or more species that serve as the natural, long-term host of a parasite, and ensures the persistence of the parasite. Some parasites, such as those involved in vector-borne diseases, have both a primary (definitive) and secondary (intermediate) host. The host in which a parasite completes sexual maturity is the primary host, while other stages of the life cycle occur in the secondary host. For example, among the plasmodia that cause malaria, mosquitoes are the primary host while a variety of vertebrates serve as secondary hosts. An amplifying host is a species that harbors the parasite in sufficient concentrations such that it is able to propagate the parasite. In contrast, a dead-end host is one that may be infected, but is not able to transmit the parasite to others. Accidental hosts are those in which the parasite is not usually found; such hosts may be dead-end hosts or could potentially become amplifying hosts.

Due to long-term host and parasite co-evolution, infections may be relatively benign among members of the reservoir population. Parasites that are virulent enough to kill their hosts are less likely to spread than those whose hosts can survive to continue to propagate the organism. However, in vector-borne diseases, parasites may continue to be quite virulent in human reservoirs, who serve as secondary hosts. McNeill (1976) has argued that in vector-borne diseases, in the triad of the host-vector-parasite, “benignness” can only be accomplished in the relationship between the parasite and the vector or the parasite and the secondary host, but not both. Further, given that vectors are short-lived, it is more likely that benignness would involve in the vector-parasite relationship than in the human-parasite relationship. Ewald (1994) proposed the adaptive severity hypothesis to explain the persistence of virulence in vector-borne diseases. He argues that in non-vector-borne diseases, the host has to be well enough to move and spread the disease. But in vector-borne diseases, it is not necessary for the secondary host to be well enough to be mobile, for the vector itself is mobile and is able to spread the parasite. Moreover, virulence is associated with higher parasite densities, which means that vectors can be more readily infected. Thus, virulence in the secondary host may benefit the parasite. Incapacitated secondary hosts are also easy targets for the vector.

Spillover, spillback, and spread

Parasite amplification in a host population is necessary for the parasite to achieve sufficient densities to be effectively transmitted. Reservoir hosts are amplification hosts, but amplification may also occur in spillover infections. In spillover infections, a parasite of a reservoir population comes in contact with a novel host population (Weaver 2005). Spillover infections may result in high levels of virulence, and secondary spillovers are also possible.

Cleaveland et al. (2007) make an important distinction between “samplers” and “spreaders” in spillover events. Samplers are involved in situations where spillover occurs in a localized population, while spreaders are involved in pandemic disease, such as in the case of HIV and Ebola viruses.

In the case of pandemic HIV, most scholars attribute its origin to a host switch from chimpanzees to humans (see Chapter 2). Its propagation in the human population from samples in rural sub-Saharan Africa to spreaders in urban cities in Africa and then globally are due to a number of social and cultural factors (Mayer et al. 2008; Reid 2009). These include the development and urbanization of Africa, which increased communication and travel between rural and urban areas. Medical technology also played a role in the early spread of HIV through the reuse of contaminated needles and blood transfusions. Intravenous drug users also became spreaders due to needle sharing. Human sexual behaviors contributed to the spread of HIV for individuals who had contact with multiple partners, particularly homosexual men and sex workers and their clients. And critical to the spread of HIV was globalization with its consequent ease of international travel, which spread the virus worldwide. More recent emerging diseases may have similar potential. Two examples are Zika and chikungunya viruses. Both were first isolated in the mid-20th century in both African wild primates and human populations (see Chapter 2), but they resulted in relatively benign illnesses that did not spread widely. In recent years, global epidemics have occurred with both of these viruses, which have diversified with potential for neurotoxicity in humans.

The spread of Ebola shares many characteristics with HIV since it may be transmitted through blood and body fluids, but it may involve a longer infection chain (from bats to apes to humans), similar to the Hendra virus in bats, horses, and humans. Quammen (2012) describes a case study of a Hendra virus outbreak in a horse stable in eastern Australia (Quammen 2012). Fruit bats, which are the reservoir, had been roosting in fig trees in a horse pasture, and a horse likely was exposed to the virus by eating grass contaminated with bat urine, feces, or saliva. The virus then spilled over into other horses at the stables, manifesting in virulent infection, with half a dozen horses dying within 12 hours. The horses became effective amplifying agents, and the virus had a secondary spillover into three men who were caretakers of the horses, one of whom died.

This case study of the Hendra virus is relevant to understanding the transmission of Ebola virus in humans. The reservoir for the Ebola virus remains unknown but is suspected to be in fruit bats (Cárdenas and Basler 2013). The virus is virulent in chimpanzees and gorillas, and there are documented cases of humans acquiring the virus from great apes (see Chapter 2). One might argue that Ebola is not a true primate zoonosis, because the known primate amplifiers were not the reservoir hosts. However, if some humans acquire Ebola directly from wild primates, arguably it qualifies as a primate zoonosis, for in these cases, the end of the infection chain is from wild primate to human. Thus, it is not necessary for a primate to be the natural reservoir for a primate zoonotic infection to occur.

Modes of transmission

Zoonotic parasites are transmitted to humans through three key routes: direct contact, indirect contact, or shared vectors (Taylor et al. 2001). Direct contact involves contact with blood or body fluids. Such direct contact typically occurs in hunting contexts through exposure to blood and body fluids but may also occur through bites and scratches from animals. Pet-keeping also provides a context for exposure to blood and body fluids, but due to close contact may also include inhalation. Indirect contact most often occurs with exposure to contact with animals feces, particularly those that are water-borne, but may also include contact with fomites or distant consumption of bushmeat. Vector-borne zoonotic diseases involve agents that transmit parasites between animals and humans. The primary vectors responsible are arthropods, but gastropod vectors and helminth parasites are involved in schistosomiasis. After infection, some parasites may also be transmitted vertically from mother to child during pregnancy or childbirth.

Direct contact and indirect contact

Hunting activities are the primary means through which humans have direct contact with nonhuman primates. Potential for parasite transfer occurs when hunters are exposed to blood, body fluids, or other body tissues through handling bushmeat. Hunters also risk being bitten or scratched by frightened or wounded animals. Individuals involved in the butchering of bushmeat are at even greater risk through accidental cuts. Once a parasite spills over into the human population, human-to-human contact may continue through routes including sexual contact, blood donation, organ transfer, or other exposure to body fluids, depending on the particular parasite involved.

Primate pet-keeping poses risks for parasite transmission. Direct exposure may occur from bites and scratches from pets, but close contact may also pose risk of transmission of parasites in air-borne droplets. Occupational exposure is another context where direct contact occurs with nonhuman primates, including workers in zoos, primate sanctuaries, and primate research centers. Laboratory workers who handle nonhuman primate blood products are at risk for accidental exposure and also for bites and injuries when they handle animals. Laboratory and zoo workers are also responsible for maintaining the hygiene of the animals kept and come into contact with feces, urine, and other body fluids when cleaning cages.

An additional means of direct contact with potential to spread parasites is xenotransplantation. The World Health Organization defines animal-to-human xenotransplantation as

living cells, tissues, or organs of animal origin and have human body fluids, cells, tissues or organs that have ex vivo with these living, xenogeneic materials, has the potential to constitute an alternative to the material of human origin and bridge the shortfall in human material for transplantation.

(WHO 2016b)

A number of such procedures have used nonhuman primates. Keith Reemtsma made one of the first attempts involving transplantation of chimpanzee kidneys into patients with renal failure (Reemtsma et al. 1964). Reemtsma performed 13 of these transplants and most failed within 4–8 weeks due to either rejection or infection; however, one patient survived 9 months (Cooper et al. 2015). In 1984, an infant, “Baby Fae,” made international headlines when she received a baboon heart transplant, but she survived only 20 days after the procedure (Bailey et al. 1985). In 1992, a baboon-to-human liver transplant was attempted, but the patient survived only 70 days (Starzl et al. 1993). A baboon-to-human bone marrow transplant was attempted in 1995 in an AIDS patient (Ildstad 1996). Although it failed to engraft, the patient did show temporary improvement after the procedure (Fricker 1996). As of March 2016, over 120,000 people in the U.S. were awaiting organ donation (HRSA 2016). Despite failures, potential still exists for procedures to be modified in the future. However, this raises ethical considerations, for it would require a mass breeding program of wild primates to meet the needs. Additionally, there is increasing concern, particularly for nonhuman primates, that known or unknown parasites may be spread.

The most significant way that parasites can be transmitted indirectly between humans and animals is through water-borne infections (Cotruvo et al. 2004). Here, parasites are typically transmitted through the fecal-oral route, but transmission may also involve exposure to urine or animal carcasses through parasites in the soil. Risk is highest in rural areas, where sanitation may be poor and humans and nonhuman primates share the same water sources. Human infections may arise from utilizing contaminated water for drinking, food preparation, or bathing. Keeping pets in the household may involve direct exposure to primate species. When raised near primate habitats, livestock may also be a source of infection for primates. Indirect contact may also occur through exposure to fomites, which are any objects contaminated with parasites that remain infectious for a period of time. A wide range of objects can carry fomites, including skin cells, clothing and bedding, eating utensils, and furniture surfaces.

Vector-borne transmission

Vector-borne parasites have the most complicated ecologies, for transmission involves the triad of the vector (primary host), animal host (secondary host), and the parasite. Vector-borne parasites also present some of the most serious challenges in controlling zoonotic disease due to the mobility of the vector. Mosquitoes are responsible for most of the vector-borne diseases; most others are caused by other arthropods. Vector-borne parasites that share human and wild primate hosts include viruses, protozoa, and helminths.

Of the approximately 49 genera and over 3,000 species of known mosquitoes, only a few are important in parasite transmission between humans and wild primates. Aedes species are most important for the transmission of viral diseases such as dengue, chikungunya, yellow fever, and Zika. Anopheles species are most important for the transmission of malarial diseases.

Two key cycles, sylvatic and urban, have been described for vector-borne infections, but a variety of intermediate stages may also come into play (e.g., Harper 2011; Higgs and Beaty 2005; Weaver 2005). The sylvatic or jungle cycle is enzootic with parasites circulating between mosquitoes and a single or multiple reservoir host species. In the strictest sense, the sylvatic cycles only involves infection of wild animals. However, hum...

Table of contents

• Cover
• Title
• Copyright
• Contents
• Tables
• Preface
• 1 The ecological context
• 2 Viruses
• 3 Protozoa
• 4 Bacteria
• 5 Helminths
• 6 Concluding remarks
• References
• Index