Prevalence of gastrointestinal helminth parasites in rhesus macaques and local residents in the central mid-hills of Nepal

Gastrointestinal parasites like helminths and protozoans are ubiquitous in humans and non-human primates (NHPs) and are among the most prevailing infections worldwide (Sepahvand et al., 2022). Gastrointestinal (GI) helminth parasites, also known as geohelminths or soil-transmitted helminths, include species like Ascaris lumbricoides (roundworm), Trichiuris trichiuria (whipworm), Ancylostoma duodenale, Necator americanicus (hookworms), etc. (Haque, 2007). These parasites are found in the gastro-intestinal tract of the host and heavy parasitic infections can lead to anorexia, cachexia and severe ascites (Loukopoulos et al., 2007). Some of the parasites are non-pathogenic, however, large numbers of parasites have detrimental effects on the host which include physiological disturbances, nutritional loss and lesions. These effects impact the host’s health and can lead to secondary infections (Toft & Eberhard, 1998). GI parasites in NHPs can be the major cause of gastro-enteritis, watery diarrhea, hemorrhage, dysentery and extra-intestinal infections such as liver abscess and even death (Akpan et al., 2010).

NHPs are one of the major reservoirs of parasites and can transmit zoonotic diseases due to their close interactions with humans (Dawet et al., 2013). There is a long history of interaction between humans and NHPs which has resulted in a complex web of behavioral, ecological, and epidemiological relationships. The spatial overlap and interactions between humans and NHPs create a shared environment which can result in co-mingling of infectious agents (Fuentes, 2006). It has been found that, particularly for viruses, protozoa and specialist parasites, human-NHP sympatry is positively correlated with parasite species richness (Nunn et al., 2004).

Although pathogenic parasites may be the cause of diseases in the host individuals, nonpathogenic parasites are important as their presence in the host can provide evidence of the fecal-oral transmission route (Sarkari et al., 2016). The transmission route of GI parasites within the human community includes uncooked and unwashed food, contaminated water, poor hygiene, and the fecal-oral route (Omalu et al., 2013). The likelihood of interspecies exchange of GI helminths, such as Ascaris spp., Oesophagostomum spp., Trichuris spp. etc., between NHPs and humans depends in part on the degree and nature of anthropogenic disturbance to NHPs’ habitats (Zanzani et al., 2018; Medkour et al., 2020). Human activities like habitat fragmentation may increase an NHP population’s susceptibility to the risk of infection and in some cases can cause mortality (Chapman et al., 2005). Major contributing factors responsible for parasitic transmission are soil and water pollution by waste food and garbage, especially during the festive and picnic programs, and the occasional open defecation by visitors in the forest areas and nearby water sources (Sapkota et al., 2020).

Assessing parasite prevalence in a species is vital to an understanding of the species’ health status, adaptation to the environment, and potential health risks. Among NHPs, rhesus macaques (Macaca mulatta) and humans share a range of infectious agents including gut parasites (Roberts et al., 2020). Many of the diseases shared by humans and NHPs result from the exchange of parasites through the fecal-oral route, animal bites, nasal secretion, and water-mediated route (Chapman et al., 2005). Therefore, an understanding of the intestinal parasites found in both rhesus macaques and the local the community is an important first step in helping to establish proactive measures to mitigate disease risk.

Nepal has a large population of rhesus macaques living both in the wild as well as near human settlements, especially in the temple areas. In many locations, macaques raid crops from agricultural areas as well as storage facilities. In the temples and shrines, visitors and devotees frequently offer supplemental foods to the macaques (Adhikari et al., 2018). As is the case at many temples and shrines around Nepal, human-macaque interaction is a regular occurrence at the Daunne Devi Temple area in Nawalpur District, Nepal. A recent study of the rhesus macaques in the Daunne Devi Temple area (Kshetri et al., 2023) reported a higher dependence on supplemental food provisioning, and their daily path lengths were shortened when the number of visitors in the temple increased. Such interactions could result in the cross-species transmission of potentially zoonotic parasites. Given the potential health risks associated with parasite infection, the purpose of this study was to identify the prevalence, intensity, richness and associated risk factors of GI helminth parasites in the rhesus macaques and local people of the Daunne Forest area situated in the central mid-hills of Nepal.

The required permission for collection of the macaque fecal samples was obtained from the Department of Forest and Soil Conservation, Ministry of Forest and Environment, Government of Nepal (Permission Number 293/078/079). Human subject participation in the study was voluntary and verbal informed consent was obtained from each participant. Prior to their participation, the detailed purpose and procedures of the study were explained verbally to the participants in Nepali language. The participants were informed that they could end their participation in the study at any time. Additionally, in an effort to help protect participant anonymity no personal identifiers were associated with the samples.

Of the 120 rhesus macaque fecal samples examined, 47 samples were found to be positive for gastro-intestinal helminth parasites (Table 2), for an overall prevalence of 39.2 %. Thirty-seven samples had a parasite richness of 1 and 10 other samples had a richness of 2. The mean GI helminth parasite richness was 1.21 ± 0.41 (SD). Four species of helminth parasites were detected in the rhesus macaques including Strongyloides sp., Ascaris sp., hookworm and Trichuris sp. (Fig. 2). Among the 70 human fecal samples, only 8 (11.4 %) were found to be infected, and only with Ascaris lumbricoides eggs. The eight positive samples included one sample from a caretaker of temple area and remaining were from the local people living around the temple stairway. The Sorenson’s Coefficient of similarity for GI helminth parasites between the rhesus macaques and humans at the generic level was 0.4.

The prevalence of parasites in the macaques during the summer season (41.4 %, 29/70) was higher than in the winter season (36 %, 18/50) but the difference was not statistically significant (χ²=0.361, df=1, P=0.575) (Fig. 3A). Based on the age category, the highest prevalence of GI helminth parasites was recorded in the adult macaques (41.67 %, 40/96) followed by young (30.77 %, 4/13) and infants (27.27 %, 3/11) (Fig. 3B). However, no significant differences were observed in the age-wise prevalence of GI helminth parasites in the rhesus macaques (χ²=1.290, df=1, P=0.581). Among 96 adult monkey samples, 35 were from adult males and 61 were from adult females. Parasitic prevalence rate in the females (52.46 %, 32/61) was higher than in males (22.86 %, 8/35). Significant difference was observed in the parasitic prevalence rate between the male and female macaques (χ²=8.018, df=1, P=0.005).

Fig. 2.

Fig. 3.

This study explored the prevalence of GI helminth parasites in rhesus macaques and local people in Daunne Forest of Nawalpur District in the central mid-hills of Nepal. Four species of parasites were identified in the rhesus macaques including Strongyloides sp., Ascaris sp., hookworm and Trichuris sp. and a single species (Ascaris lumbricoides) was found in the humans. The overall parasite prevalence in the rhesus macaques (39.2 %) was considerably lower than reported for other temple sites in Nepal (Jha et al., 2011; Adhikari & Dhakal 2018; Sapkota et al., 2020). The highest prevalence of Strongyloides sp. (19.17 %) observed in this study was similar to the findings by Arunachalam et al. (2015) who recorded 43 % (26/60) prevalence of Strongyloides sp. in free ranging macaques in Namakkal District of Tamil Nadu, India. Additionally, our findings were similar to those reported by Sapkota et al. (2020) who found a 21.4 % prevalence rate of Strongyloides sp. in urban rhesus macaques at a temple area in Kathmandu Valley. But a higher prevalence of Strongyloides sp. in macaques also has been reported by Mutani et al. (2003), Gillespie et al. (2005) and Malla (2007).

Of the 47 macaque samples with parasite infection, 78.7 % had parasite richness of one parasite; the remaining 21.3 % had a richness of two. Jha et al. (2011) and Sapkota et al. (2020) both reported higher parasitic richness, up to five parasite species in rhesus macaques at temples in the Kathmandu Valley. The parasite intensity and richness are managed in macaques by behavioral strategies like grooming techniques, licking, and consumption of medicinal plants (Dhakal et al., 2018; Hart & Hart, 2018). Parasite infection rates are higher in populations of primates living in fragmented habitats than in continuous, protected forests as the fragmented habitats with human settlements create disturbances, and human and domestic animal interactions increase the chances of transmission (Trejo-Macías et al., 2007). The community forest around Daunne Devi Temple is managed and protected by the local user groups. It has a variety of trees which provide substantial food sources for macaques in additional to other provisioned food supplied by the visitors in and around the temple. The availability of a natural forest and lower household densities (and in turn, reduced anthropogenic disturbance to macaques) may account for the lower parasite load observed in the rhesus macaques of Daunne Forest.

A noticeable difference in the seasonal prevalence of helminth parasites in the rhesus macaques was observed. The higher prevalence of intestinal parasites observed during the summer season compared to winter is consistent with Dhakal et al. (2018) for the rhesus macaques of Chitwan-Annapurna Landscape, and with Pokhrel and Maharjan (2014) for the Assamese macaques of Shivapuri Nagarjun National Park. During warmer weather, it is easier for parasites to reproduce resulting in greater contamination of food and water, and in turn, increased parasite infection (Gonzalez-Moreno et al., 2013).

In addition to the seasonal difference in parasite infection, we also observed a higher parasite prevalence in the adult female macaques compared to the adult males and young. This finding is consistent with a study by Kumar et al. (2018) for bonnet macaques of India but is contrary to results reported by Tabasshum et al. (2018) and Kumar et al. (2019) who noted a higher parasite prevalence in male rhesus and lion-tailed macaques, respectively. The higher parasitic prevalence in adult rhesus macaques as compared to the young might be because of the socially mediated exposure of adult macaques to infective stages of helminth parasites (MacIntosh et al., 2012). A higher parasitic prevalence in females may be attributed to their greater dependence to human provisioned food and higher chances of infection through contaminated foods and water (Sapkota et al., 2020).

Parasite prevalence in the humans (11.4 %) was found to be lower than in the macaques (39.2 %). The reason for this disparity may be related to the increased awareness and education regarding parasite infection, and the availability of modern health facilities (Schurer et al., 2019). Ascaris sp. was the only parasite observed in the humans in this study. It also is the most common intestinal helminth detected in other similar studies with humans (Gyawali, 2012; Shrestha & Maharjan, 2013; Chongbang et al., 2016; Sapkota et al., 2017), and is considered to be transmitted via a fecal-oral route and contamination of soil by macaque feces (Sapkota et al., 2017).

The transmission of parasites between humans and macaques represents a serious one-health concern and deserves increased, long-term surveillance. Although we did not find the presence of shared helminth parasite species between the macaques and humans in this study, the risk of bi-directional transmission exists given the close interaction at the temple site. We strongly recommend further investigation (with larger sample sizes for both the macaques and local people) to more thoroughly assess parasite infection rates and the associated risk of disease transmission.

The prevalence of GI helminth parasites was identified in the rhesus macaques and humans in the Daunne Devi Temple area. The parasite occurrence was higher in the summer than in the winter season. The helminths detected in the rhesus macaques may pose a zoonotic risk to the local community and visitors. A comprehensive study, with a larger sample size of both the humans and non-human primates living in this shared environment, needs to be conducted to ascertain the potential zoonotic risk of enteric parasites.