Rats and their helminth parasites: Potential zoonosis threats of land use change in the northeastern sub-watersheds of Mount Makiling, Laguna, Philippines

Rodents have an important place in many food webs, but they are also well-known agricultural and residential pests. For species that are synanthropic, their close association with human habitation could pose threats to public health due to zoonotic transmission. Many of these rodents are carriers of pathogens such as bacteria, viruses, and parasites (Gravinatti et al., 2020; Mihalca et al., 2012), and the spread of rodents into human habitats and vice versa can lead to an increase in spillover risk (Ecke et al., 2022). Studies have shown that rats from different ecosystems in Southeast Asia may serve as reservoirs of some zoonotic helminth species (Chaisiri et al., 2015; Fagir & El-Rayah, 2009; Mohd Zain et al., 2012; Sumangali et al., 2012).

In the Philippines, Rattus tanezumi (Asian house rat), Rattus argentiventer (ricefield rat), Rattus exulans (Polynesian rat), and Rattus norvegicus (brown rat) are known to occur in agroeco-systems and have been recognized as pests of crops such as rice and sugarcane (Stuart et al., 2008). Numerous parasitic infections have also been recorded in rodents collected in the Philippines, such as echinostomiasis, paragonimiasis, capillariasis, schistosomiasis, and angiostrongyliasis (Castillo & Paller, 2018; Eduardo, 1991; Estaño, 2023; Estaño et al., 2020; Estopa & Estopa, 2016). Consequently, there could be a potential effect on the dynamics of pathogen transmission associated with rats and their changing environments. Rodent species that are known to be disease reservoirs are more abundant in anthropogenically modified habitats (Mendoza et al., 2020), and the spread of rodent-borne disease due to land use change is likely to increase in the future (García-Peña et al., 2021). In the Philippines, urban land conversion is expected to grow continuously (Johnson et al., 2021; Mishra et al., 2021), and, in Mount Makiling specifically, built-up areas have already increased by 117 % between 1992 and 2015 (Soriano et al., 2019).

Unfortunately, there are limited studies in the country investigating rat-borne pathogens, particularly endoparasites, and their distribution in rat host populations in relation to host occurrence in different land use types. This study aimed to determine the distribution of rats and their helminth parasites in the changing landscape of Mt. Makiling. With the dearth of epidemiological data on many zoonotic pathogens, there is a need to do more reliable surveillance and elucidate how land use change can influence the risk of disease transmission.

Prior to the conduct of study, the Institutional Animal Care and Use Committee (IACUC) of the University of the Philippines Los Baños approved the experimental protocol with assigned protocol number IBS-201701.

This study records three (3) rat species and 11 helminth parasite species in the northeastern sub-watersheds of Mount Makiling, Laguna, Philippines. The presence of R. tanezumi in all land use categories may suggest that R. tanezumi can act as a bridge species, carrying parasites across different habitats (Estaño et al., 2020). R. norvegicus is opportunistic and highly adaptive to a wide range of conditions, enabling them to inhabit and survive in human-modified habitats successfully (Estaño, 2023). R. exulans is a significant agricultural pest in many parts of Southeast Asia, and it is reported to destroy farm crops such as coconut, palm, rice, sweet potatoes, and maize (Wood & Singleton, 2015). Moreover, this study revealed that rats from residential areas have higher prevalence rates of helminth parasites (Table 1), but rats from agricultural and agroforest sites reported helminth parasites with more complex life cycles that require intermediate hosts. In particular, lowlands or irrigated rice fields are the preferred habitats of helminth parasites, such as Angiostrongylus cantonensis and Echinostoma ilocanum, which require gastropods as intermediate hosts.

This study revealed an overall prevalence of A. cantonensis in rats at 18.33 %. This parasite is a leading cause of human eosinophilic meningitis and infects a wide range of animal hosts, including snails, which plays a significant role in zoonotic transmission (Hochberg et al., 2007). The highest prevalence rate was significantly observed in agricultural and agroforest areas but low in residential areas. Estaño et al. (2020) also reported the same trend due to intermediate host snails abundant in rice fields and swamps. Studies in the Philippines by Tujan et al. (2016) and Castillo & Paller (2018) also reported R. tanezumi and R. norvegicus to be 100 % co-infected with A. cantonensis in Nueva Ecija, Philippines, a notable rice-growing province. Meanwhile, Estaño (2023) recently reported the infection of this helminth parasite in R. tanezumi and R. norvegicus collected in agricultural areas in the Southern Philippines.

C. hepatica was also recovered in this study with an overall prevalence of 23.88 % and was found highest in R. norvegicus at 12.46 % collected in residential sites and lowest at 6.7 % in R. exulans collected in agricultural site. C. hepatica is a zoonotic parasite, and human infection is primarily due to unsanitary practices, poor hygiene, and an abundance of rats. Urbanization in residential areas increases the amount of garbage produced, which favors the proliferation of these rats (Mohd Zain et al., 2012). Transmission in humans occurs via ingestion of embryonated eggs commonly found in the environment (Horiuchi et al., 2013). A higher incidence in children was reported, which may be due to soil-hand mouth practice (Fuehrer et al., 2011; Juncker-Voss et al., 2000; Ochi et al., 2017; Wang et al., 2011). Quilla and Paller (2020) further reported the histopathological effects of the parasites in rat liver collected from Mt. Makiling and adjacent areas. No human infection has been reported in the Philippines, but this could be due to misdiagnosis or unreported cases.

Rats in this study were also found infected with four cestode species, namely, H. diminuta, H. nana, T. pisiformis, and S. fasciolaris. All cestodes were found to be present in agricultural, agroforest, and residential areas except for T. pisiformis, which was observed only in rats from residential areas. H. nana showed the highest prevalence, which could be attributed to the ability of the parasite to be transmitted and complete its life cycle even without the presence of an intermediate host, like insects. This parasite is commonly found in tropical and subtropical areas (Gitonga et al., 2016; Iliev et al., 2017). Interestingly, these two species of H. diminuta and H. nana are zoonotic, causing hymenolepiasis. Infection of other mammalian hosts is acquired by ingesting an intermediate host, like insects carrying the larvae. Likewise, human infections occur by accidental ingestion of infected intermediate hosts in pre-cooked cereals or other food items. Direct ingestion from the environment via oral exploration can also cause infection in children. Mild to moderate infection may be asymptomatic; however, heavy infection may cause dizziness, anorexia, abdominal distress, and diarrhea (Chaisiri et al., 2015; Hancke & Suarez, 2015; Rohela et al., 2012).

On the other hand, E. ilocanum was only recovered in agricultural areas with a 4.4 % prevalence rate. E. ilocanum is an intestinal parasitic fluke in mammals and birds and has an indirect life cycle with aquatic snails as intermediate hosts. Among them, Gyraulos and Hippeutis are the first intermediate hosts, while Pila, Viviparus, Vivipara, Thiara, Planorbis, and Lymnaea act as second intermediate hosts in the Philippines (Chaisiri et al., 2015; Eduardo, 1991). The occurrence of E. ilocanum in rats in agricultural habitats might be due to the presence of intermediate host snails of the parasite (Paller et al., 2019). The lower prevalence of this parasite can be attributed to its life cycle requiring an intermediate host, unlike that of other helminth parasites with direct life cycles, which may have higher chances of dispersion. This parasite can cause Echinostomiasis in humans, infecting the intestine and bile duct (Belizario et al., 2007). Regarding distribution, E. ilocanum is common in South Korea and Southeast Asia, especially in the Philippines. Infection in humans was reported in Southern parts of the Philippines (Eduardo, 1991). Infection of this parasite in wild murid rodents was also recorded in the Indo-Chinese Peninsula, where Echinostoma malanayum and E. ilocanum were recovered (Chaisiri et al., 2015). The presence of infection of E. ilocanum poses a threat to public health, especially in agricultural communities.

Among the parasites recovered, N. brasiliensis showed the highest prevalence and was found in all habitats. High prevalence among rats in different habitats was expected since the transmission is direct and does not require an intermediate host (Gomez Villa-fañe et al., 2008; Paramasvaran et al., 2009). Moreover, N. brasiliensis infection can cause lung damage by disrupting the alveolar architecture due to parasite migration and can result in pulmonary emphysema (Marsland et al., 2008; Hoeve et al., 2009). S. ratti (10.56 %), on the other hand, is also known to cause strongyloidiasis in humans, resulting in coughing, nausea, vomiting, abdominal pain, and weight loss; however, it is usually asymptomatic. Other parasites recorded were Rictularia sp. (1.11 %) and T. muris (7.2 %), which were not zoonotic.

Results on the multiple helminth co-infections in rats reveal some evidence of greater parasite species richness and cases of co-infections in residential habitats similar to previous reports (Chaisiri et al., 2010). The higher number of co-infection cases can be attributed to a greater host density in residential areas as well as the host-susceptibility of R. norvegicus to helminth parasites (Bordes et al., 2011; Morand et al., 2015). With greater host density in residential areas, there is a greater chance of transmission of generalist parasite species within the same host species population. Multiple papers, however, have reported contradicting results but have noted the possible impact of rodent assemblages and community structure in the habitat sampled (Hurtado et al., 2021; Palmeirim et al., 2014;Werner et al., 2020).

This study also attempted to associate the occurrence of parasites with the morphometric characteristics of the hosts. Results revealed a positive correlation between the rat host body size and parasite infection. This could be age-related, so older hosts are more exposed to environmental parasite transmission. Larger hosts can support higher parasite biomass (Poulin & George-Nascimento, 2007) and are also more susceptible because of active behavior related to foraging (Winternitz et al., 2012). Heavier hosts are also more likely to engage in breeding activities, exposing them to chronic infections (Perrin et al., 1996; Schwanz, 2008).

With regards to sex, the prevalence between male and female rats was not significantly different. Although both sexes are susceptible to infections, studies reported that males were more active and had a more extensive home range than females, making them more likely to get infected. This distribution requires male rats to forage more, having higher chances of encountering infective stages of parasites in the environment (Heaney et al., 1999; Soliman et al., 2001; Tew & Macdonald, 1994). Ferrari et al. (2007) mentioned that male rats, especially older males, harbor a substantial portion of parasites in a host population, releasing disproportionately more infective stages into the environment than females. Furthermore, males and females can constitute different environments for parasites. Factors like sex hormones, immune-competence, mobility, body size, home range, and dispersal rates differ between sexes, rendering male and female hosts different habitats for parasites. In addition, it was observed that in agricultural areas and agroforest settings, male rats tend to travel to alternative habitats, whereas breeding females continue to forage in rice fields in order to meet the nutritional requirements needed to raise litter (Estaño et al., 2020). In some cases, male and female rats harbor different parasite loads due to differences in spatial behavior. It is interesting to note that there was no significant difference in infection rates of rats during wet and dry seasons. The climate conditions do not quite vary in tropical countries, and infective stages of parasites are likely to be present in the environment throughout the year.

Infected rats that harbored infection were found primarily in agro-forest and agricultural areas. This could be attributed to the presence and broader distribution of the parasites' intermediate hosts. For instance, A. cantonensis and E. ilocanum require mollusks as intermediate hosts, which abound in agricultural and agroforest areas. However, the increasing land use change and urbanization in the areas could also lead to changes in the dynamics of host behavior, such as the movement of rats to human settlements. Given the evidence of increased transmission in urban-adapted hosts such as rats, the potential zoonosis risk could pose public health threats. Urbanization can provide favorable eco-epidemiological conditions for rodent-borne pathogens, becoming an emerging risk and a severe threat in these areas.