Surveillance of emerging infectious diseases in wild non-human primates in Kenya: Successes and challenges

doi:10.21203/rs.3.rs-923002/v1

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Systematic Review

Surveillance of emerging infectious diseases in wild non-human primates in Kenya: Successes and challenges

https://doi.org/10.21203/rs.3.rs-923002/v1

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Emerging infectious diseases (EIDs) originating from wildlife present a significant threat to global health, security, and economic growth, thus combatting their emergence is a public health priority. Humans and non-human primates (NHPs) exhibit a high degree of overlap in their genetic and physiological similarities, hence making them susceptible to majority of pathogens that can cross the primate species boundaries. However, efforts to understand the potential infectious disease-causing pathogens harbored by wild primate populations has lagged and is yet to be fully explored. Disease surveillance in wildlife to identify probable infectious disease outbreaks has remained a challenge especially in developing countries due to logistical and financial constrains associated with both periodic and longitudinal sample collection. Such loopholes have hampered the preparedness to handle the emerging infectious diseases whenever they arise. In this review we focus on successes, challenges, and proposed solutions for EID surveillance in non-human primate populations in Kenya. We discuss,1) mechanisms of cross species transmission of EIDs, 2) the role of NHPS in EID transmission, 3) results from past NHP pathogen surveillance projects in Kenya and 4) challenges and proposed solutions for NHP-EID surveillance. Finally, we propose that more studies need to include investigations into understanding how cross species transmission occurs in diverse NHP populations and how this impacts one health.

Zoonoses

Wildlife Biology

Veterinary Epidemiology

Parasitology

Virology

Conservation Biology

non-human primates

emerging infectious diseases

Kenya

wildlife

zoonoses

We report on wild primate species and their locations in Kenya.
We highlight results from EID surveillance projects in Kenyan wild primates.
We discuss challenges and propose solutions for EID surveillance of wild primates

In early 2020 the world woke up to the reality of a pandemic of coronavirus disease (COVID-19) induced by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) whose origin was thought to be from animals. The emergence of a global pandemic was always predicted but efforts that included improving public health capacity and surveillance of diseases both in animals and humans through phylogenetic studies, ecological overlap and reports to contain and manage proved unsuccessful (Gómez and Nichols, 2013; Paules et al., 2017; Sands et al., 2016; Yamey et al., 2017). As the world population continues to expand, human encroachment into wildlife habitats, changes in climatic conditions and adverse anthropogenic activities favor increased contact between wild animals and humans leading to a high risk for more emerging infectious diseases (EIDs).

At the dawn of the 21st century, many EIDs emerged in Africa where majority could be traced to animal origin such as HIV and malaria (Calvignac-Spencer et al., 2012), monkey pox (Yinka-Ogunleye et al., 2018), Ebola (Rouquet et al., 2005); (Barry et al., 2018), Rift valley fever (http://www.who.int/newsroom/fact-sheets/detail/rift-valley-fever ), hepatitis B (Sa-Nguanmoo et al., 2009), Chikungunya (Wahid et al., 2017; Zeller et al., 2016), Marburg (Bengis et al., 2004), West Nile virus (Bengis et al., 2004; Wang and Crameri, 2014a), Dengue (Kemunto et al., 2018), Zika virus (Freire et al., 2018; Gubler et al., 2017). While in Asia, highly pathogenic avian influenza (H5N1 and H7N9), severe acute respiratory syndrome (SARS) (Drosten et al., 2003), influenza A (H1N1) (Gao et al., 2013) zoonotic malaria (Plasmodium knowlesi), Nipah virus were the major outbreaks (Wang and Crameri, 2014b). In Mediterranean region, EID outbreaks included the Middle East respiratory syndrome (Zaki et al., 2012) and in Australia Q fever was described (Bengis et al., 2004; Sivabalan et al., 2017). Lastly, there is speculation that SARS-CoV-2, the pathogen responsible for the on-going pandemic is a zoonotic disease that originated from bats (Zhou et al., 2020).

Africa clearly bears the greatest burden of EIDs due to its poor health infrastructural development, weak economies and governance structures, and inadequate surveillance systems (Lamarque et al., 2009). Despite such foreseeable adverse effects of EIDs, wildlife surveillance for potential infectious disease outbreaks in developing countries has remained a challenge. This has been attributed to logistical and financial constraints associated with both periodic and longitudinal sample collection. To aid the public health sector in their management and preparedness of disease outbreaks, there is need to set up a robust pathogen surveillance system of EIDs, that would allow for timely detection, identification, and effective control measures (Nsubuga et al., 2006). In this review we focus on successes, challenges and proposed solutions for EID surveillance specifically in non-human primate populations in Kenya. We discuss,1) mechanisms of cross species transmission of EIDs, 2) the role of NHPS in EID transmission, 3) results from past NHP pathogen surveillance projects in Kenya and 4) challenges and proposed solutions for NHP-EID surveillance.

Mechanisms of cross species transmission of EIDs

Wildlife including NHPs are well known reservoirs of parasites, viruses, bacteria and fungi and with the continuous interaction between humans and wildlife, a zoonotic spill over is likely to happen (Wolfe et al., 1998). Despite an increase in infectious disease emergence, the mechanisms by which EID pathogens cross the species barrier to infect humans still remains poorly understood (Dennehy, 2017). However, EID emergence and transmission are dependent on multiple risk factors that interact at the levels of the pathogen, host and the environment (Raina K Plowright et al., 2017; Wolfe et al., 1998). Figure 1 summarizes risk factors that influence disease emergence and transmission.

Figure 1

Risk factors that influence disease emergence and transmission

Firstly, pathogens can evolve and adapt to varying conditions and this plays a significant role in zoonotic spillovers. Some pathogens have acquired the ability to jump species barriers and infect new hosts by adapting novel replication and evasion mechanisms to host immune defenses (Sharp and Hahn, 2011a). Host plasticity is an important pathogen factor that allows for infection of a wide host range and hence increases the probability of infection into novel hosts (Kreuder Johnson et al., 2015). The ability of pathogens to invade hosts is dependent on available receptors, biology of the pathogen, various point mutations and pathogen recombination (Sharp and Hahn, 2011a). For example, viral receptors that exist on the host that support entry for SARS-CoV-2 in humans, have also been described in NHPs(Liu et al., 2020; Schmitt et al., 2020; Tung et al., 2007) and studies on HTLV-1 have shown that glucose transporter GLUT1, heparan sulfate proteoglycans, and neuropilin-1 act as receptors for both human and NHP infections(Hoshino, 2012). Pathogen genetics is also integral in disease transmission dynamics. Mutations and recombination lead to genetic variation of pathogens and hence facilitate entry and establishment of infections in new hosts. In the case of point mutations, SARS-CoV virus exhibited Spike protein mutations that allowed it to exist in an animal host and this eventually spilled over to humans causing SARS in 2003 (Sheahan et al., 2008). Virus recombination allows for formation of a new genetic material that provides a host receptor gene to the virus or results in novel and more virulent viral variants (Dennehy, 2017). The H1N1 in swine that spilled over to humans is believed to have originated from a reassortment of three Avian influenza viruses where viruses from birds, swine and humans were combined resulting in H3N2.

Secondly, various host factors facilitate zoonotic spillovers that eventually cause infectious disease emergence. Humans and animals have an elaborate and robust immune system that helps them evade the pathogens they encounter in their environments on a day to day basis. A number of host restriction actors are encoded and adapted as part of the innate immune system response, and these factors form barriers that guard against most viral and other pathogens (Kajaste-Rudnitski et al., 2010; Neil and Bieniasz, 2009). However, several host factors may also weaken the restriction barrier towards pathogens. For instance, a weakened immune status exposes hosts to new pathogens as the body is unable to stop entry or replication of the pathogen. Weakened immunity may arise due to existing infections, host age or genetics and this allows for rapid disease progression as seen in SARS-CoV-2 infections (Sahebnasagh et al., 2020). Risky behaviour by hosts also play a key role in cross species transmission of infections as they increase the frequency of contact between reservoirs and the hosts. Human beings through their socio-economic activities, leisure activities and occupations interact with wildlife. Hunting and consumption of bushmeat for instance is a risky activity that exposes human beings to direct transmission of pathogens e.g. HTLV-1(Mossoun et al., 2017) Ebola(Leroy et al., 2004a) and Simian foamy virus (Betsem et al., 2011). This occurs mainly through ingestion or exchange of body fluids containing pathogen between human beings and NHPs. Anthropogenic activities that have detrimental effects on the environment such has forest degradation, fragmentation and loss increases the rate of contact and interactions between wildlife, livestock and humans (Acevedo-Whitehouse and Duffus, 2009).These habitat changes potentially increases pathogen host ranges and hence expose humans to contraction of pathogens shared by both wild and domesticated animals (Kreuder Johnson et al., 2015). EIDs that are caused by drug resistant microbes have been exacerbated by misuse of antimicrobials used for treating humans, food and domesticated animals (Jones et al., 2008). Wildlife living in close proximity to humans and domestic animals harboring resistant pathogens are likely to acquire the same and hence act as reservoirs of these pathogens (Arnold et al., 2016). In addition, globalization and technological advances in transport, movement of human populations, animal products, and live animal specimens across the continents continues to occur at very high frequencies (Wu et al., 2016).These factors have played a fundamental role in proliferation of disease emergence particularly by efficiently increasing dispersion of pathogens and diseases across geographical regions and human races (Hassell et al., 2017). This has been observed during the ongoing COVID-19 pandemic, where in less than one year, the virus has spread to all corners of the globe infecting humans and wildlife (da Silva et al., 2020).

Thirdly, environmental factors have direct and indirect consequences on parameters that allow for cross species transmission of pathogens (Lindahl and Grace, 2015) and EID emergence by dictating disease dynamics in reservoir hosts, vectors and human beings (Estrada-Peña et al., 2014). Environmental stress can alter movement of vectors and/or hosts. This could increase contact rates between the two and hence facilitate pathogen transmission (Estrada-Peña et al., 2014). The amount of pathogen available in the environment at a given time, that can infect humans (pathogen pressure) is a key determinant in cross species transmission of pathogens (Raina K. Plowright et al., 2017). The viability of the pathogens in the host reservoirs’ relevant tissues is equally important for pathogen release in the environment either directly through shedding or indirectly through vectors. (Ducatez et al., 2008). Consequently, this release of the pathogens from the reservoir hosts coupled with the duration of survival of the pathogens in the environment provides an opportunity for a potential cross over as this dictates the route of disease transmission (Raina K Plowright et al., 2017). Wildlife biodiversity provides different host reservoirs for various pathogens (Jones et al., 2008; Keesing et al., 2010).These reservoir hosts provide for intermediary hosts that facilitate indirect contact as for the case in SARS-CoV, HIV and Nipah Virus (Mandl et al., 2015). The role of intermediate hosts in Simian Immunodeficiency Virus (SIV) jump to humans is clearly seen when comparisons are made between SIV and HIV sequences (Sharp and Hahn, 2011b) Climate change may also bring about emergence of diseases that are dependent on vectors that are influenced by environmental conditions (Patz et al., 2005). Vectors such as mosquitoes are abundant during wet seasons and they bridge the gap between animal reservoirs and human beings thus facilitating the spread of pathogens e.g., P. knowlesi agent of zoonotic malaria (Singh and Daneshvar, 2013), Dengue Virus, Zika virus, Chikungunya Virus (Estrada-Peña et al., 2014). Moreover, with climate change, shifts in pathogen conducive conditions are observed resulting in expansion of a wide range of disease-causing vectors spreading the infectious disease wider than areas of known occurrence (Ogden, 2017). Anthropogenic activities such as deforestation cause changes in climate and loss of habitat (Morris, 2010)which affects the diversity of local animal communities and hence influences pathogen host plasticity, i.e pathogens infecting new hosts to survive (Alexander et al., 2018). These activities also lead to constant human-wildlife interactions and hence provide multiple opportunities for pathogen spillover (Estrada-Peña et al., 2014).

Host, pathogen and environment factors are independently necessary for zoonotic spillages and disease emergence but are not independently sufficient to bring about such events. Their interactions and overlaps allow for adaptation and susceptibility that facilitates cross species transmission and are yet to be fully studied in NHPs.

The role of non-human primates (nhps) in emerging infectious diseases transmission

Humans and NHPs exhibit a high degree of overlap in their genetic and physiological similarities, thus, making them susceptible to majority of pathogens that are capable of crossing the primate species boundaries (Johnson et al., 2020; Wolfe et al., 1998). This close relationship provides a new environment for maintenance and transmission of pathogens (Wolfe et al., 1998). Emerging disease hotspots are found in the tropical regions of the world (Africa and Asia), where there is good forest cover and these are habitats for many primate species. However, these areas are also associated with increased human-wildlife interactions, which has led to pathogen spill-over events from NHPs to humans. Relative to wildlife, NHPs harbor a high diversity of parasites with zoonosis potential (Ogden, 2017; Rothschild, 2015). The Global Mammal Parasite Database, records over 300 parasite species (including viruses, bacteria, helminths, protozoa, arthropods, and fungi) infecting 140 primate hosts (Nunn and Altizer, 2005a). A subset of these pathogens are zoonotic and have been reported in wild or captive primates (Table 1 adopted and updated from Rothschild et al. 2015).

Table 1

**Non-human primate zoonoses** (Adopted and updated from Rothschild et al. 2015)
Pathogen Class	Pathogens	References
Bacteria	Bacillus anthracis, Bartonella Quintana, Campylobacter jejunii, Escherichia coli, Helobacter, Pasturella multocida, Salmonella, Shigella, streptococcus pneumonae, Yersinia pseudotuberculosis, Mycobacterium tuberculosis, Mycobacterium avium-intracellulare, Mycobacterium bovis, Actinomycetes Treponema pallidium	(Appel et al., 2006), (Leendertz et al., 2004), (Russon and Wallis, 2014a), (Nizeyi et al., 2001) (Rothschild, 2015) (Mladenova-Hristova et al., 2017) (Köndgen et al., 2011) (Tegner et al., 2019) (Kennedy et al., 1992) (Devaux et al., 2019) (Bielli et al., 2013) (Biet et al., 2005) (Leendertz et al., 2004),(Rothschild, 2015), (Witmer, n.d.) (Russon and Wallis, 2014b) (Zimmerman et al., 2019)
Fungi	Candida albicans, Coccidiomycosis, Cryptococcus, Cryptosporidium parvum, Dermatophilus congolenseis, Nocardia, Trichophyton mentagrophytes,	(Russon and Wallis, 2014b), (Koistinen et al., 2018) (Li et al., 2019) (Nizeyi et al., 2001)(Muriuki et al., 1998) (Russon and Wallis, 2014b), (Ferrecchia et al., 2015) (Gugnani, 1971)
Rickettsia	Anaplasmosis, Babesiosis, Colorado tick fever, Erhlichiosis, Q fever, Rocky mountain spotted fever, Tick borne encephalitis, Tularemia, Typhus	(Nakayima et al., 2014) (Nakayima et al., 2014) (Maamun et al., 2011) (Nakayima et al., 2014) (Nakayima et al., 2014) (Mafra et al., 2015) (Bewley, 2013)(Njeru et al., 2016) (Nakayima et al., 2014) (Süss et al., 2007) (Mätz-Rensing et al., 2007) (Paris et al., 2015)
Viruses	Adenoviruses, Herpes Simplex B virus, Influenza, Measles, Metapneumovirus, Polio, Varicella, Yellow fever, Prion, Coronavirus, Dengue, Chikungunya, Marburg, Ebola, HIV/AIDS	(Wevers et al., 2011)(Lange et al., 2019) (Huff and Barry, 1932) (Control, 1998) (Kock and Macfie, 2002), (News, n.d.) (Kock and Macfie, 2002)(Slater et al., 2014) (Palacios et al., 2011) (Potkay et al., 1966) (Kock and Macfie, 2002), (Russon and Wallis, 2014b), (HEUSCHELE, 1960) (Muhammad and Saqib, 2011) (Kock and Macfie, 2002), (Russon and Wallis, 2014b), (Ye et al., 2020)(Al-Osail and Al-Wazzah, 2017) (Choumet and Desprès, 2015) (Powers and Logue, 2007)(Eastwood et al., 2017) (Schou and Hansen, 2000) (Schou and Hansen, 2000) (Hahn et al., 2000)
Parasites	Entamoeba, Cryptosporidium, Dracunculia, Encephalitozoon intestinalis, Filaria, Giardia, Hymenolepsis nana, Leishmania, Schistosoma, Strongyloides, Taenia, Trypanosoma cruzi	(Dong et al., 2017)(Muriuki et al., 1998) (Dong et al., 2017) (Russon and Wallis, 2014b), (Kock and Macfie, 2002) (Nizeyi et al., 2001) (Wamae and Odongo, 1990) (Nizeyi et al., 2001) (Russon and Wallis, 2014b), (Quinnell and Courtenay, 2009) (Richards et al., 2019)(Kebede et al., 2020) (Medkour et al., 2020) (Nguyen et al., 2015) (Marcili et al., 2009)

These zoonotic pathogens spill over to humans occur through multiple transmission routes. For instance, human contact with dead NHP carcasses facilitates transmission of filoviruses such as Ebola and Marburg viruses which cause haemorrhagic fever and are characterized by high fatality rates in both human and NHPs (Formenty et al., 1999). Using serological screening for antibodies against Ebola in NHPs, (Leroy et al., 2004b) and (Johnson et al., 1982) found that multiple NHP species have been exposed to the virus including Pan troglodytes sp, Gorilla sp, Cercopithecus sp, Papio sp, Mandrill sp., while genetic lineage studies revealed that the Ebola virus has spilled over to humans’ multiple times from its reservoir host and intermediate NHP hosts (Wittmann et al., 2007). Other pathogens that are transmitted from NHPs to humans by contact include Herpes virus (Control, 1998; Huff and Barry, 1932), Simian foamy virus (Betsem et al., 2011b).

Vector mediated transmission of EIDs from NHPs to humans is also common. An example being Plasmodium knowlesi (a zoonotic malaria) that is transmitted by mosquitoes of the Anopheles leucosphyrus group (Singh and Daneshvar, 2013). P. knowlesi is maintained in the environment by Macaca fascicularis, Macaca nemestrina and Macaca leonine which acquire the infection naturally but they do not develop clinical signs (Coatney, 1971). Other vector transmitted EID pathogens that have been reported in NHPs include arboviruses such as Dengue virus (DENV), Zika virus (ZIKV), yellow fever virus (YFV) and chikungunya virus (CHIKV) (Table 1). These viruses are maintained in sylvatic cycles between NHPs and mosquitoes. Other vector-mediated zoonoses include tick borne diseases such as Rickettsia (Table 1).

Another alternative mode of zoonoses transmission is via fecal-oral route which is a common occurrence with gastrointestinal parasites. Some of the most important and well-known human zoonosis are caused by helminths including, Ascaris, Strongyloides, Ancylostoma, Trichuris, Oesophagostomus, Enterobius, Hymenolepis species (Rothschild, 2015). These are common human intestinal parasites and have been found in free ranging as well as NHPs near human settlements (Murray et al., 2000; Weyher et al., 2006). Emerging Infectious Diseases can also be transmitted through respiratory droplets. For instance, Mycobacterium tuberculosis, bovis and avium species are transmitted easily between humans and NHPs through aerosols (MA et al., 2004)

Primate disease studies provide information on the origins of human pathogens, mechanisms by which pathogens emerge and how they are maintained in the environment (Wolfe et al., 1998). Genomic surveillance of closely related pathogens in NHPs and humans provide information on antigen diversity and mutation events which can impact vaccine development and emergence of drug resistance (Wolfe et al., 1998). For instance, drug resistance studies have reported less sensitivity of Plasmodium knowlesi to some anti-malarial drugs due to mutations (Fatih et al., 2013). These mutant Plasmodium parasites can be maintained in NHP reservoirs thus hindering malaria eradication efforts. Likewise, antimicrobial resistance studies in Papio sp. have reported resistance of E. coli isolated from the gut to a subset of commonly used antibiotics such as Ampicillin (Kenneth Kariuki et al., 2018). This is a worrying trend because NHPs can maintain antibiotic resistant plasmids in the environment and hence further facilitate their transmission to other animals and humans (Kenneth Kariuki et al., 2018). Zoonotic RNA viruses such as Dengue, CHIKV, Yellow fever, Ebola which are also maintained in the population by NHP hosts can easily mutate to variants that might pose more risk to the human population.

Results from past NHP-EID surveillance projects in Kenya

Over the last decade, Kenya has witnessed a high rise in the number of EIDS including the on-going pandemic SARS-COV-2 (Uyoga et al., 2020), influenza cases(Onyango et al., 2012) and in the past, populations have exhibited high antibody levels to Marburg virus(Johnson et al., 1996; Smith et al., 1982) and Ebola virus(Johnson et al., 1982; Teepe et al., 1983) (Johnson et al., 1986). Arboviruses that include Dengue, West Nile Viruses, Chikungunya and Yellow Fever virus transmission have also been reported in the Kenyan population (Inziani et al., 2020; LaBeaud et al., 2015). The rise in EID cases in Kenya necessitates a one health approach towards prevention, detection and rapid response to infected populations. Prevention and early detection of EIDs can be easily accomplished by periodic surveillance of human and animal populations for known and novel pathogens with zoonotic potential (Chomel et al., 2007). Thus, Kenya embraced this one health approach through the establishment of the Zoonotic Disease Unit (ZDU) in 2012 whose overall aim was to conduct zoonotic disease research and to support public health (Mbabu et al., 2014; Munyua et al., 2019). The ZDU focuses mainly on disease surveillance in livestock and companion animals. Despite this disease surveillance effort there is scarce research on wildlife including NHPs.

Africa is home to several species of NHPs (Groves, 2016; Grubb et al., 2003), with 25 genera and 94 species (De Jong and Butynski, 2012a). East Africa supports 68% of Africa’s primate genera and 41% of Africa’s primate species. Tanzania holds the largest number of primate species (27), followed by Uganda (23), Kenya (19), Rwanda (15) and Burundi (13). In Kenya NHPs, comprise of 12 genera, 19 species and 23 sub-species (Table S1) and this represents one of the most diverse taxonomic groups of wild mammals. The family Cercopithecidae is the largest with 16 species that include African green monkeys and olive baboons which have the widest distribution and are more common in Kenya. These species are distributed across the country with some endemic to specific regions. Some of the key primate hotspots in the country include; the Tana River National Primate Reserve, Kakamega Forest Complex, and Mathew’s Range Forest Reserve. These areas support more than five different primate species constituting key primate communities in the country. However, majority of the primate species that are of least conservation concern and considered abundant such as baboons, vervet monkeys, sykes monkeys and galagoes are distributed in various habitats throughout the country (De Jong and Butynski, 2012b) (Table S1).

In the last 25 years, Kenya’s population has doubled to over 40 million and with suburban development, deforestation and destruction of wildlife habitat has increased. This in turn has created an ecological proximity between phylogenetically closely related NHPs and humans, which results in increased potential for exchange of pathogens (Gillespie, 2006). In line with the one health approach, primatologists in Kenya have conducted epidemiological surveillance of both captive and wild primate populations. In this review, we summarize parasite screening projects in wild NHP populations in Kenya. To determine the total number of studies that have conducted surveillance on primates, we carried out searches from multiple databases including: the Global Mammal Parasite Database (https://parasites.nunn-lab.org/); PubMed; Google scholar and; Institute of Primate Research library publication records (http://primateresearch.org/download/ipr-publications-2017/). The global mammal parasite database is a compilation of parasites and pathogens from wild primates, carnivores and ungulates obtained from published scientific works (Nunn and Altizer, 2005b; Stephens et al., 2017). The search terms contained the following words “primates” and “monkeys” and “parasites” and “diseases” and “Kenya”. The above databases retrieved a total of 67 published papers out of which we omitted 11 review papers (Fig. 2, Supplemental table S2).

Figure 2

Flow chart summarizing published NHP studies in Kenya and pathogens surveyed.

Sampled NHP locations in Kenya

We found that the number of NHP surveillance studies had steadily increased over the past two decades (Fig. 3). The most sampled locations included Amboseli, Kibwezi, and Laikipia. While, moderately sampled areas were Tana River, Naivasha, Kajiado, Aberdares and Maasai Mara. Figure 4 highlights the most frequently sampled NHP sites in Kenya. These most sampled locations comprise of long-term field study sites managed by the Amboseli Baboon Research Project (ABRP), Mpala Wildlife Conservancy in Laikipia, Tana River National Primate Reserve (TRNPR), Ewaso-Nyiro baboon project and the Kakamega Monkey Project. These long-term field projects are unique in that they provide rare opportunities to investigate how multiple risk factors impact disease transmission in the wild. Part of the long-term data collected focuses on population demographics and non-invasive sampling to answer multiple research questions including disease transmission dynamics. For instance, studies conducted by ABRP have revealed how social networks impact the gut microbiome (Tung et al., 2015), and the complexities of how risk factors operate in multiple levels to influence helminth infections, (Akinyi et al., 2019; Habig et al., 2019). Notably, NHPs in the northern and southeastern parts of Kenya have not been studied because of the remoteness of NHP geographical ranges, and poor road networks and insecurity brought about by human conflicts. These specific areas include; Mathews ranges, Mt kuraal, Marsabit Forest, Kirisia forest, Ndotos Mountains, Bura forests in Tana River (e.g.,Tune, Mambo leo etc), and Shetani Matwari and Masewe forest complex in Tana Delta region. Also, the dryland forest and woodlands in same areas in the same regions support baboon and vervet populations that are unexplored. A few studies conducted multi-site disease surveillance, which is useful for understanding population level risk factors that influence disease transmission or emergence. One limitation of the selected papers is that some of the data retrieved from the scientific literature did not indicate the specific areas sampled and this hence limits the knowledge on which populations have been sampled (Table S2).

Figure 3

Number of published NHP studies in Kenya from 1960–2020

Figure 4

Kenyan map showing protected areas and sites of sample collection for published NHP studies.

NHP Species studied in Kenya

Out of the 12 genera and19 species of primates in Kenya, our search indicated that Papio, Chlorocebus and Cercopithecus species were the most sampled NHPs (Table 2). The endemic and endangered monkey species or subspecies, which include the Tana River mangabey (Cercocebus galeritus), Tana River red colobus (Piliocolobus ruformitratus), Percival’s black and white colobus (Colobus gurereza spp. percivalii), and Kilimanjaro guereza (Colobus guereza spp. caudatus) were rarely sampled. For instance, apart from gastro-intestinal parasites in the Tana Primates(Mbora and McPeek, 2009) surveillance for other pathogen types remains scanty. Non-invasive sampling techniques such as stool sample collection can be used to monitor other pathogen types in threatened and endangered populations. Multiple NHP studies conducted in endangered species such as apes have used cutting edge diagnostic tools screen for viruses (Speranza et al., 2020), bacteria (Yildirim et al., 2010), protozoa(Miró et al., 2018) from stool and urine samples. Table 2 summarizes all the primate species and subspecies in the country and indicates species that have undergone infectious or zoonotic disease surveillance. However, the primate populations sampled may represent a small proportion of NHPs that are at risk of contracting, maintaining and transmitting disease-causing pathogens. In addition, understanding pathogen transmission for the threatened and endangered species can inform management strategies for conservation purposes.

Table 2

Summary of NHP species sampled 1960–2020
NHP Genus	Species	Common name	Conservation status	Number of surveillance studies	Pathogen types surveilled
Papio	Papio anubis and papio cynocephalus	Olive and yellow baboons	Least concern	33	Gastrointestinal parasites Haemoprotozoans Flaviviruses, Filoviruses, Alphaviruses, Coronaviruses, Influenza virus, Fungi, STLV, Herpes Virus, Coronaviruses, Papilloma Viruses
Chlorocebus	Chlorocebus aethiops	Vervet monkeys	Least concern	14	Gastrointestinal parasites Haemoprotozoans, Simian Immunodeficiency Virus, Retroviruses, Flavivirus, STLV,
Cercopithecus	Cercopithecus mitis	Syke monkeys	Least concern	13	Gastrointestinal parasites Haemoprotozoans, Lentivirus, Simian Immunodeficiency Virus, Flavivirus, Alphaviruses, STLV
	Cercopithecus ascanis	Red tailed monkeys	Least concern	2	Gastrointestinal parasites Alphaviruses
	Cercocebus galeritus	Crested mangabey	Critically threatened	2	Gastrointestinal parasites
	Cercopithecus neglectus	De Brazza monkey	Least concern	3	Gastrointestinal parasites, Filoviruses
Colobus	Colobus badius (P. rufomitratus)	Red colobus	Critically threatened	2	Gastrointestinal parasites
	Colobus angolensis	Angola colobus	Least concern	1	Gastrointestinal parasites
	Colobus guereza	Black and white colobus	Least concern	2	Gastrointestinal parasites, Filoviruses
Erythrocebus	Erythrocebus patas	Patas monkey	Near threatened	1	Gastrointestinal parasites

Pathogen types surveyed

Majority of the pathogen surveillance projects in Kenya focused on screening for gastrointestinal parasites (helminths and protozoa), followed by viruses, other protozoa (e.g. haemoprotozoans), and only a single study investigated fungi, (Fig. 5). Gastrointestinal parasite surveillance is common due to the non-invasive nature of stool sample collection and the availability of affordable diagnostics methods such as microscopy. On the other hand, virus families screened in NHPs to date included Flaviviruses, Lentiviruses, Retroviruses, Filoviruses, Herpes Virus, Papilloma virus and Influenza viruses. Only one study screened for Filoviruses (Marburg and Ebola) in wild NHP populations more than 3 decades ago (Johnson et al., 1982) yet studies in bats have shown that these viruses are present in the Kenyan bat populations (Kuzmin et al., 2010).Therefore, it remains to be seen if filoviruses are still present in NHPs even now. Multiple studies have screened for Flaviviruses, e.g yellow fever (Haddow, 1969) and more recently surveillance of Dengue Virus and an alphavirus (Chikungunya viruses) among wild populations of Papio anubis, Papio cynocephalus, Chlorocebus aethiops, Cercopithecus mitis and Cercopithecus ascanius was accomplished (Ambala, 2014; Eastwood et al., 2017). Other Alphaviruses such as Onyong’nyong’, Sindbis and Semiliki viruses have been reported in humans in Kenya but to the best of our knowledge no one has screened for the same in wild NHPs to date (LaBeaud et al., 2015; Tigoi et al., 2015). Available data indicated that the following vector-borne zoonotic haemoparasites constitute what so far has been reported in Kenya; Trypanosoma (Jeneby et al., 2002), Leishmania (Gicheru et al., 2009) and Babesia (Akinyi et al., 2013; Maamun et al., 2011).

Figure 5

Pathogen types surveyed in Kenyan NHPs

Diagnostic techniques employed for Kenyan NHP surveillance

Both conventional and advanced diagnostic techniques have been employed towards NHP emerging disease surveillance in Kenya. These wide spectra of diagnostic methods are of different specificity and sensitivity associated with both merits and demerits. There are two basic diagnostic approaches: 1) Direct detection and identification, also known as classical diagnostic methods, that involves the revealing of zoonotic agents and/or their associated constituents from collected NHP samples. Examples are microbial cultures and microscopy. 2.) Indirect detection and identification involve the detection of antibodies of zoonotic agents (Granberg et al., 2015a). Below, we discuss the diagnostic tools utilized by the above studies (Supplementary Table S2).

Microscopy is the most used diagnostic tool for gastrointestinal parasites (helminth and protozoa), haemoparasites and bacteria screening in NHP populations in Kenya (Table S2). Histology diagnostic techniques also utilize microscopy. Microscopy is employed by most studies because its associated consumables and equipment are readily available and cheaper compared to other diagnostic options. However, microscopic diagnosis has demerits, it is time consuming, requires personnel training and often prone to human error. In addition, it has low specificity when it comes to accurate pathogen identification to the species or subspecies level. For example, because identification of strongyle eggs through microscopy provides results to the genus level, most researchers are forced to conduct additional diagnostic assays such as larval culture or PCR to determine the species of interest (Gillespie, 2006). In addition, microscopy also has low sensitivity, especially when screening for haemoparasites whose appearance under a microscope will depend on the parasite density. This leads to many false negative results. Few NHP field studies have employed histology and necropsy diagnostics because they are invasive techniques that are difficult to perform in the field.

Most NHP projects conducting surveillance of viruses use serological assays for diagnostics. Enzyme-linked immunosorbent assay (ELISA) is the most common assay (see supplementary table S2) and it is used to detect pathogen antigens and determine specific antibodies circulating in blood samples. Serological tests can detect acute and past infections. In some scenarios, they have low specificity due to cross reactivity of different pathogens and may result in false positives. One of the significant advancements in serological diagnostic techniques is the development of genetic engineered antibodies which are used for Western blotting and immunochromatographic tests which have the ability to detect viral antigens. These advanced tests have enabled the classification of parasite serotypes within a species (Gicheru et al., 2009;Jeneby et al., 2002). More so, the advances have enabled the identification of new virulence factors in zoonotic disease process (Granberg et al., 2015b). Other serological assays used for monitoring diseases in NHPs include agglutination assays (Ball, 1966; D.M. et al., 2019), indirect immunofluorescence (Eley et al., 1989; Johnson et al., 1982; Mwenda et al., 1999). See supplementary table S2 for a complete list of serological assays used by different Kenyan NHP projects.

With the inception of genomic era, numerous technologies have been developed to enable manipulation of nucleic acids of zoonotic agents. Molecular assays are popular because of the uniqueness of every microorganism genome which contributes to the high sensitivity and specificity of the approach (Granberg et al., 2015b). NHPs surveillance studies on haemoparasites and viruses have used conventional polymerase chain reaction (PCR) as a diagnostic tool (Ambala, 2014; Chepkwony et al., 2016; Eberhard et al., 2001; Mahieux et al., 1998). Nested PCR, a technique that involves a second PCR assay which targets a more specific inner region of target sequence has been employed by(Maamun et al., 2011) in detecting Babesia microti-like parasites by targeting Babesia β-tubulin gene. However, this technique might be limited especially if the target genome is highly variable. Another demerit is that there is need for a subsequent stage of performing gel electrophoresis which is tedious method of detecting PCR amplicons. Reverse transcriptase polymerase chain reaction (RT-PCR) has been applied in screening viruses such as H1N1, H3N2 influenza viruses and coronaviruses in NHPs present in Kenya (Bunuma et al., 2018; Gambo, 2018). More recently, High resolution melting PCR (PCR_HRM) has been introduced and used for detection of multiple parasite species in NHPs that are within the same genus (Mbuthia Peris et al., 2020; Nyamota et al., 2020). This approach cuts out the need for sequencing and hence reduces diagnostic costs. Sanger sequencing and pyrosequencing techniques have been used to characterize viruses, Bacteria, helminths and protozoans in Kenyan NHPS (Table S2). Only one study has used metagenomics to characterize NHP gut microbiome (Tung et al., 2015).

Challenges and proposed solutions for NHP-EID surveillance

In the last decade efforts in building laboratory capacity to enhance healthcare across Africa have increased with the establishment of CDC (http://africacdc.org) and African society for laboratory medicine (ASLM) (https://aslm.org), seedling labs ((www.seedinglabs.org)). However, zoonotic disease surveillance and reporting still remains rudimentary and information sharing between human health and animal health sectors is rarely undertaken. There is therefore, an urgent need as defined by WHO (WHO, 2008)to set up an ongoing systematic and timely collection, analysis, interpretation, and dissemination of information about the occurrence, distribution, and determinants of zoonotic diseases for timely dissemination of public health information for assessment and public health response. Current obstacles to effective disease surveillance and control system include (i) limited financial resources, ii) lack of well-equipped laboratories, (iii) limited number of trained personnel and iv) lack of biological resource centres. The emergence of infectious diseases (MERS, Ebola, Zika, SARS, SARSCoV-2) suggest that the frequency of disease events that are zoonotic in nature will not lessen in the future. Thus, to better predict and prevent zoonotic disease outbreaks, disease surveillance is imperative to gather and understand information about the nature of disease appearance and spread, and to understand genetic-, population-, social-, and ecological-level characteristics that enable zoonotic pathogens to jump species and spread easily to humans. Here we highlight challenges hampering disease surveillance in NHPs and possible solutions.

Limited financial resources

The most reported barrier to zoonotic disease surveillance especially in sub-Saharan Africa (SSA) is lack of research funding (Dhalla and Guirguis, 2018; Kokwaro and Kariuki, 2001). The quantity of funds available for disease surveillance through local institutions is quite limited. Countries in SSA rely on self-funds through loans or rely on the international donor community for funding (Viergever et al., 2016). Consequently, any decrease in the level of global funding may have a significant and immediate impact in these countries. Additionally, the grants are extremely competitive and often require collaboration from donor countries and institutions who determine the domains of interest and consequently set the surveillance and ultimately the public health agenda. While it is not possible for SSA governments to adequately fund zoonotic diseases surveillance systems given their limited resources and competing budgeting priorities, it is possible to rethink the funding model by engaging local foundations and major industry stakeholders to secure funding. A recently established funding initiative Alliance for accelerating Excellence in Science in Africa (www.aasciences.africa.aesa) through partnership with the African academy of Sciences and African Union development agency and other global partners is taking big strides in meeting the gaps in funding and building research capacity on the continent. Other ways of mobilizing funding is through improved communication. One way of achieving this is by communication, a sustained presence on social media and dissemination of findings through non-scientific means (TV/Radio appearances, banners, webinars, and visual abstracts) (“The beginning of a new era: science communication in Africa – AfricArXiv,” n.d.).This will help policy makers pursue and sustain the effort, mechanisms, and build sustainable capabilities around disease surveillance. Ultimately, investments in sustainable surveillance programs must be linked to tangible health improvement outcomes.

Lack of well-equipped laboratories

Laboratory confirmation of etiological cause of zoonotic disease whether emerging or reemerging is a vital part of any disease surveillance system. Although rapid field tests are available for a select group of infectious agents (such as influenza A), laboratory confirmation is typically required for pathogen characterization, confirmation of infection, and further preventive actions. Given the multiple problems caused by false-positive reports, laboratory-confirmed cases increasingly provide the bulk of actionable alerts (Rodier et al., 2007). However, in SSA, where rapid assays may not be available conventional methods of confirmation result in significant time delays. Most advanced analysis such as sequencing, is outsourced to countries outside of Africa because of the expensive nature of equipment maintenance and purchase of consumables. This continued outsourcing contributes to slow transfer of knowledge and expertise thus limiting the ability to detect known and unknown pathogens in a timely fashion. Field surveillance should consider fairly new but affordable technologies such as Loop-Mediated Isothermal DNA Amplification whose cycling process does not necessarily require a specified thermal profile but it is highly rapid, effective and with high specificity. There is also a need to embrace new ways of collecting and transmitting epidemiological, clinical, demographical, and other information in the field. Use of handheld computers, cell phones, remote sensing, and internet searches for instance are being used to collect and transmit information from even the most remote and resource-challenged countries (Beck et al., 2000; Lobitz et al., 2000).

Limited number of trained personnel

Integration of surveillance capacities across human and animal health sectors is urgently needed. Crucially, disease surveillance and the implementation and evaluation of interventions to contain the disease threat must be linked. This will require multidisciplinary professionals; who are trained in basic clinical diagnosis of emerging zoonotic diseases, veterinary medicine, epidemiology, laboratory sciences, molecular genetics, animal ecology, environmental science, geographical Information system, social sciences, information technology, and communications at national, regional, and global levels. In addition, personnel are needed who have leadership and management skills; who have a vision and understand the need for a national and global integrated system; who have the interpersonal skills to work with experts from different disciplines; and who understand public–private partnerships (Pappaioanou et al., 2003). Laboratory expertise is needed for correctly obtaining samples, for data collection from the field, for laboratory sample analysis and interpreting and communicating laboratory-based information to others who have responsibility for determining the best response to the threat. Surveillance data will inform control measures, preparedness of EIDs and useful responses incentivize future data collection and reporting. Importantly, protocols have to be developed to allow for collaboration between laboratory personnel, medical professionals and veterinarians for quick identification and mitigation of agents causing outbreaks.

Lack of biological resource centers

Biological resource centers are an important component of scientific research and infrastructure. Few institutions in Africa are limited in terms of collection, transport, storage space and equipment to archive samples. Detection of past and current zoonotic pathogens depends on the availability of biological samples. Sample availability can be enhanced by the creation of biological repositories, also known as biobanks. Biobanking is important because it provides samples that can be used in future biological, biomedical and industrial research and for laboratory diagnostics (De Paoli, 2005). This in turn leads to improved global networks and that can respond rapidly and effectively to biological threats of international concern. Long term outcomes of biobanking enables researchers to compare samples collected at different time points and different locations, increase sample sizes for research that provides meaningful data analysis, modeling, and predictions on potential disease outbreaks or any other interpretations. This data may also contribute towards development of human and animal cell lines for and towards development of new diagnostic methods that may increase sensitivity or specificity of infectious disease detection. With the looming threat of primates and other biodiversity extinctions, storage of archived samples might provide a useful resource for synthetic biology and invitro-fertilization to help in recovery of the endangered species.

Technological advances have increased the availability of sensitive and specific techniques that allow for quick identification, accurate analysis of infectious disease activity, monitoring of disease dynamics and epidemic prediction. However, periodic surveillance of EIDs in Kenya in wild NHP populations is rarely undertaken despite the availability of the new diagnostic tools. This is further complicated by the fact that biomedical research using primates has predominantly focused on only two species (baboons, vervets) as common appropriate models to study different infections. Thus, sample collection has overtime concentrated on these two species with low or no representation of the remaining 17 species. Nonetheless, nonhuman primate surveillance for EIDs has been conducted in some wild primate populations. There is need to expand the surveys in under-represented areas as well as carrying out complete NHP distribution surveys in the entire country to facilitate equitable sample collection. Kenyan primatologists need to establish additional long-term study sites of other primate species rather than baboons and vervet monkeys to allow for collection of demographic and behavioural data that will inform disease emergence and transmission dynamics. Future studies should embrace an interdisciplinary and one health approach towards disease surveillance by incorporating concurrent sampling of NHPs, humans and livestock. In addition, research scientists should adopt non-invasive sampling methods and cutting-edge diagnostic technologies to screen for a broader spectrum of pathogens.

Overall, improved EID surveillance in NHPs will contribute data towards understanding mechanisms of EID transmission and allow predictions of possible outbreaks and support our national and global preparedness to prevent or handle the EID pandemics. Further, outcomes of EID surveillance remain key in informing the development of conservation strategies especially for critically endangered NHP species and mitigating their risk of extinction.

ACKNOWLEDGEMENTS

We thank the Kenya Wildlife Services, Institute of Primate Research, National Museums of Kenya and National Council for Science and Technology. Mercy Akinyi was supported through the DELTAS Africa Initiative an independent funding scheme of the African Academy of Sciences (AAS) Alliance for Accelerating Excellence in Science in Africa (AESA), (DELGEME Grant No. DEL-15-003 number and Global Health Fund, Duke University, USA. LO is funded by the African Research Network for Neglected Tropical Diseases (ARNTD) small grants program Reference SGPIII/0210/351. We thank Beth Archie for her invaluable advice.

CONLICT OF INTEREST STATEMENT

The authors declare no conflict of interest

AUTHOR CONTRIBUTIONS

MYA and LO contributed to the original idea and structure of this manuscript. All authors contributed to write and revise the final version of the manuscript including the preparation of Tables and Figures.

SUPPLEMENTARY INFORMATION

Supporting Information on Primate diversity and distribution in Kenya (Table S1) and List of all primate studies in Kenya (Table S2) are available online.

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SupplementarytableS12021.docx
Supporting Information on Primate diversity and distribution in Kenya
SupplementarytableS22021.xlsx
List of all primate studies in Kenya

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Surveillance of emerging infectious diseases in wild non-human primates in Kenya: Successes and challenges

Status:

Version 1

Abstract

Figures

Impacts

Introduction

Mechanisms of cross species transmission of EIDs

The role of non-human primates (nhps) in emerging infectious diseases transmission

Methodology And Results

Results from past NHP-EID surveillance projects in Kenya

Sampled NHP locations in Kenya

NHP Species studied in Kenya

Pathogen types surveyed

Diagnostic techniques employed for Kenyan NHP surveillance

Challenges and proposed solutions for NHP-EID surveillance

Limited financial resources

Lack of well-equipped laboratories

Limited number of trained personnel

Lack of biological resource centers

Conclusion And Further Directions

Declarations

References

Supplementary Files

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﻿Surveillance of emerging infectious diseases in wild non-human primates in Kenya: Successes and challenges

Status:

Version 1

Abstract

Figures

Impacts

Introduction

Mechanisms of cross species transmission of EIDs

The role of non-human primates (nhps) in emerging infectious diseases transmission

Methodology And Results

Results from past NHP-EID surveillance projects in Kenya

Sampled NHP locations in Kenya

NHP Species studied in Kenya

Pathogen types surveyed

Diagnostic techniques employed for Kenyan NHP surveillance

Challenges and proposed solutions for NHP-EID surveillance

Limited financial resources

Lack of well-equipped laboratories

Limited number of trained personnel

Lack of biological resource centers

Conclusion And Further Directions

Declarations

References

Supplementary Files

Status:

Version 1

Surveillance of emerging infectious diseases in wild non-human primates in Kenya: Successes and challenges