The prevalence of intestinal parasite infections in goats from smallholder farms in Northern Thailand

The production of small ruminants is an attractive agricultural enterprise for Thai smallholder farmers because of lower inputs and high reproductive rate compared with cattle and buffalo, and their ability to thrive on native pasture that is unsuitable for crop production (Jittapalapong et al., 2012; Windsor et al., 2018). Sheep and goats are becoming increasingly important in Southeast Asia, particularly in regions with large Islamic populations such as Indonesia, Malaysia, and parts of the Philippines. (Windsor et al., 2018). Moreover, in recent years, demand for goat meat from Thailand and neighboring regions is increasing, particularly from Vietnam and Laos. This provides opportunities for smallholder farmers to increase productivity. In Thailand, goat production is traditionally extensive with low inputs, and subsequently low outputs. Five major small ruminant management systems have been described, including: tethering, free range, semi-free range, intensive, semi-rotational grazing and livestock-tree crop integrat

ed systems (Pralomkarn & Boonsanit, 2012). Free range is the most popular system typically practiced by small farmholders and consist of 10 – 60 animals per herd. It allows sheep and goats to browse alongside road verges, empty paddy fields, ample uncultivated areas and used public lands. In most systems, sheep and goats are herded back to the shelter in the evening and kept in small hutches overnight for protection.

An effective herd health program to maintain the health of livestock and prevent the occurrence of disease is necessary for rearing animals. Veterinary services are poor and knowledge about goat diseases is low or non-existent. An effective health management is only provided in commercial and governmental goat farms. Where investigations have occurred, these have mostly been performed by non-veterinarians, and animals being treated with antibiotics without regard to food safety and antimicrobial residue issues. Several investigations regarding health problems in goat have been conducted in Thailand for many years. Gastrointestinal parasite (GI) burdens are frequently associated with grazing management. Therefore, animals that graze communal pastures, are often at higher risk of exposure.

However, helminthic and protozoal infections have been reported among goats in Thailand (Worasing et al., 2011; Jittapalapong et al., 2012). It has also been found that GI parasitism among ruminants occurred all year round in tropical climates such as Thailand, with higher infection intensities during the rainy season (Jittapalapong et al., 2012). Temperature and humidity are primary factors involved in the development and survival of parasite eggs, larvae, cysts, and oocysts in the environment.

To date, the importance of caprine GI parasitic infections has not been investigated in detail in lower Northern Thailand. But, a comprehensive understanding of endoparasitism is crucial for the sustainable control of parasites that interact with hosts in a specific climate, management system and production environment. Improving goat production in Thailand requires prevalence studies to provide the evidence-basis for the practical approaches that can assist smallholder goat farmers to improve their husbandry and health practices for increasing goat productivity. The specific objectives of this investigation were to estimate the prevalence of GI parasitism of goats on smallholder farms reared under traditional production systems.

Аpprovals for using animals in the current study were obtained from the ethical/IACUC committee at the Naresuan University, Phitsanulok, Thailand (Permit Number: NU-AG620504). The research has been complied with all the relevant national regulations and institutional policies for the care and use of animals.

Characteristics of sampled animals and descriptive data of survey Number of samples and presence of parasites are shown in Table 1. The fecal eggs examination identifies eggs of multiple nematodes, one cestode and protozoan species, including Strongyles, Trichuris spp., Strongyloides spp., Moniezia spp., and coccidian species (presumably one or more Eimeria spp.). Out of 885 fecal samples, 772 (87.2) were positive one or more parasites. Strongyles was the most prevalent species (76.8 %), followed by Eimeria spp. (48.8 %).andtapeworm (Moniezia spp.) (14.2 %). In total, the level of egg count numbers differed, with the mean EPG for Stronglyes and OPG for Eimeria spp. of 799 ± 1348 and 427.6 ± 118, respectively.

Third-stage larvae identified in coprocultures were dominated by Haemonchus contortus (55.84 %). (Table 2). Strongyloides papillosus followed with around 20.53 %. Larvae of S. papillosus and H. contortus were found in all farms, but the other genera made up only a small proportion of third-stage larvae.

Influence of host sex on prevalence

The total prevalence did not vary between sexes (P > 0.05) (Table 3). The number of different helminth species per goat separated by sex is show in Figure 2. In males, 51.7 % (N = 29) had a mixed infection with at least 2 species, while it was 48.5 (N = 856) infemales. Male (48.3 %) infected 2 species more often than females (41.5 %). (Fig. 2).

Fig. 2

Table 3

Prevalence of helminth infections (percentage of infected goats) in male and female goats in Northern Thailand.

Parasitic infection	Male			Female			X2	P
	Total	+	%	Total	+	%
Strongyles	29	24	82.8	856	656	76.6	0.591	0.442
Trichuris spp.	29	0	0	856	4	0.5	0.136	0.712
Nematodirus spp.	29	0	0	856	8	0.9	0.274	0.601
Dicrocoelium dendriticum	29	0	0	856	1	0.1	0.034	0.854
Eimeria spp.	29	15	51.7	856	430	50.2	0.025	0.875
Moniezia spp.	29	3	10.3	856	129	15.1	0.494	0.482
Others (Strongyloides spp.)	29	0	0	856	6	0.7	0.205	0.651

Total: total number of examined animals; +: number of infected animals.

Male goats had higher prevalence (P > 0.05) of strongyles than females. Goats with poor body condition had higher mean EPG and prevalence of strongyles than those with good body condition but the differences were not significant (P > 0.05). Similarly, there were no significant (P > 0.05) associations between area of origin and prevalence and mean EPG of strongyles.

The present study shows high prevalence of helminths and Eimeria in Phitsanulok province, Thailand with a tropical savanna climate. To our knowledge, few studies have reported data regarding the prevalence of endoparasite infection in this area. Therefore, we conducted this study to determine the most prominent species of endoparasite in goats in one of the biggest villages in the rural sector of Phitsanulok, and to clarify the effect of gender on the prevalence of infection. Moreover, knowing the current situation and prevalence of coccidiosis might be beneficial to set an appropriate control strategy and minimize economic losses.

The current findings revealed that the animals were affected by a wide variety of parasites. The findings are useful in identifying areas for improvement and modification of current helminth control strategies, so as to minimize the impact of GI parasites on productivity. The overall GI parasites prevalence of 87.2 % observed in the present study is, however, higher than the prevalence of GI parasites in goats in Laos (73 %) (Windsor et al., 2018), Bangladesh (74.8 %) (Islam et al., 2017) and another study from Thailand (79 %) (Jittapalapong et al., 2012). This difference may be attributed to different sampling sites, seasons, animal breeds, management and agro-climatic conditions. The data, however, is a useful confirmation of concerns that there is a need to control GI parasites in this region.

The types of parasites found in this study included gastrointestinal nematodes, cestodes, trematodes and protozoa. Our observations were similar to those of some other studies conducted in Asia and abroad, which described strongyle infection as a major problem in small ruminants (Zvinorova et al., 2016; Lambertz et al., 2018; Windsor et al., 2018; Sharma, 2020). The proportions of the nematode genera according to L³ larvae in the current study in which H. contortus was the most prevalent, followed by Strongyloides spp. and Cooperia spp. In southern Thailand, however, the widely reported GI parasites of small ruminants include strongyles, Trichuris spp., Strongyloides spp., Capillaria spp., Moniezia spp., and Eimeria spp. (Worasing et al., 2011; Jittapalapong et al., 2012). The range in prevalence of strongyles reported in this study shows that the environmental conditions, particularly in moist conditions are highly suitable for transmission of strongyles. However, the order of prevalence reported by a study in South Africa was Eimeria spp., Trichuris spp., S. papillosus, Moniezia spp., and strongyles (Mpofu et al., 2020); while that of a Laos study was Strongyles, Trichuris spp., Strongyloides spp., Capillaria spp., Moniezia spp., and Eimeria spp. (Windsor et al., 2018). Therefore, it seems obvious that differences in prevalence of worm genera dependent on geographical and climatic factors. Climatic conditions, particularly wet periods, are frequently associated with differences in the prevalence of GI parasitic infections, because free-living infective stages (eggs, larvae and oocysts) survive longer in moist conditions (Waruiru et al., 2000). The rainy season in the study region of the current study is 4 months, which accommodates parasite survival in the environment. Also, previous study suggested that the animals became infected during the short rainy season and that high strongyle-type egg counts were consequently detected during the following dry season (Waruiru et al., 2000). In our study, high infections with Strongyles and Eimeira species could be explained by the environment in which animals were reared, and also by poor animal management. Sheep and goats were reared in mixed crop-livestock systems, where a few numbers of goats were herded together in the same area during the dry and wet seasons. This results in high rates of parasitic infection due to possibilities of re-infection in contaminated pastures. Furthermore, all grazing goats were herded back to housing pens for overnight protection. Poor hygiene management may be a contributory factor to the presence of Stronglyes and Eimeria spp. burdens on smallholder farms. Further parasitological and epidemiological studies are required to more accurately quantify the association of parasitism and disease in Thai small ruminants and enhance the development of more efficacious parasite control management programs. In addition, anthelmintic treatments are commonly used for managing internal parasites of small ruminants in many parts of the world (Windsor et al., 2018) including smallholder systems in Thailand, despite lack of registration of most of these products for goats.

The most prevalent nematodes were Strongyles, with Haemonchus being the most common one. Previous studies on the epidemiology of gastrointestinal helminths have also reported Haemonchus as the most important nematode (Chandrawathani and Nural Aini, 2012; Zvinorova et al., 2016; Windsor et al., 2018). H. contortus constitutes a severe problem for ruminant’s production, it is the most frequent nematode parasite found both, in template and tropical regions (Acevedo-Ramírez et al., 2019). Its higher prevalence could be due to that individual females are capable of producing thousands of eggs per day, which can lead to rapid larval pasture contamination and associated outbreaks of haemonchosis (Roeber et al., 2013). Moreover, the requirement of warm and moist environmental conditions for the free-living stages of H. contortus governs the parasite’s geographical and seasonal distributions (Besier et al., 2016). H. contortus has proven to be remarkably adaptable over a wide range of environments, due to its high biotic potential which allows it to take advantage of short periods which are favourable for the development of its free-living stages, and the survival ability of the relatively vigorous infective third-stage larvae, and specific adaptive mechanisms, such as hypobiosis of the fourth-stage larvae (Besier et al., 2016). There is also ability to develop resistance to anthelmintic drugs of H. contortus is great, which poses a problem in terms of control (Kotze & Prichard, 2016).

Infection by trematodes had the lowest prevalence (0.1 %) among examined animals. This finding was closely related to reported in southern Thailand that 0.79 % of goats were infected by Fasciola spp (Worasing et al., 2011). In Thailand three species are very common, i.e., Fasciola spp., Paramphistomatidae spp. and Eurytrema spp. (Worasing et al., 2011; Jittapalapong et al., 2012). Fasciolosis has been associated with areas having high rainfall and poorly drained soils (Kanyari et al., 2009). Notable that in the study areas are arid or semiarid province and does not seem to be a favorite geographical location for liver fluke and rumen fluke, this could be linked with lower prevalence of trematode parasites compared to other areas in Thailand.

On the other hand, the only cestodes identified through fecal examination in this study were Moniezia spp. The occurrence of this parasite elsewhere in the tropics has been described and is associated with ingestion of oribatid mites infected with cysticercoids of Moniezia spp. (Diop et al., 2015).

The prevalence of Eimeria spp. reported in the current study was lower than that reported in Thailand (Jittapalapong et al., 2012) and Laos (Windsor et al., 2018). In the present survey, no clinical signs of coccidiosis were observed in animals. Therefore, there was no significant difference in the prevalence of Eimeria infection between males and females. Infection with Eimeria is considered to be a risk factor when the infected animals are exposed to any stress condition such as transportation or underfeeding and the associated ailments are likely to perturb the immune system, where Eimeria species could propagate intensively in the intestine and result in outbreak (Chartier & Paraud, 2012).

The results of sex-related prevalence of GI parasites revealed that GI parasites infection occurred with similar frequency in males and females, which can be attributed to the fact that both sexes are kept under similar management systems (Windsor et al., 2018; Mpofu et al., 2020). On the contrary, the significant association between host sex and the prevalence of GI parasites was previously reported to occur more often in females higher than male (Islam et al., 2017; Singh et al., 2017). It is interesting to note that females are assumed to be more heavily infected due to stress and low immune status during pregnancy, parturient paresis and lactation periods (Golo et al., 2017).

In this study, the coproculture also showed that the predominant worm species were H. contortus and S. papillosus, a scenario which has been widely reported in other studies (Futagbi et al., 2015; Singh et al., 2016; Bihaqi et al., 2017; Tan et al., 2017; Lambertz et al., 2018). Although relatively low level of strongloides spp. eggs, S. papillosus was predominant species. This is supported by the evidence that the diagnostic tools for infections are mainly limited to fecal analyses with relatively low accuracy and precision (Zanzani et al., 2014). Regarding Teladorsagia spp./Trichostrongylus spp. and Bonustomum previous reports on this country are not available, while prevalences were low in both species. However, the relationship between EPG and worm intensity depends on characteristics of worm communities (intensity and species richness), which are in relation to host susceptibility to infection (Cabaret & Gasnier, 1998). Thus, female H. contortus excreted ten times more than Teladorsagia circumcincta, and hundred times more than Trichostrongylus spp. (Cabaret & Gasnier, 1998). With the multiple infections found, it is probable that these burdens are contributing to subclinical production losses. Further understanding of host-pathogenic-environmental factors related to endoparasite pathogenesis in small ruminants in Thaialnd is needed, including an evaluation of whether parasite populations vary significantly with season, age, breed and the role of diet in parasite burdens in Thai small ruminants. Also, effective small ruminants internal parasite control depends on an understanding by farmers and their advisors of the risk factors that contribute to endoparasite transmission, then successful implementation of management strategies that can reduce the impact of parasites (Windsor et al., 2018). The majority of strongyles are harmful to their hosts, causing anaemia, gastroenteritis, and decreased growth rates and mortalities. In the current study, the high intensity of strongyles was associated with poor body condition, showing that the parasite could be affecting the productivity of the animals.

This study was consistent with the findings of Biswas et al. (2014) and Admasu & Nurlign (2014), who discovered higher parasite infection in poor body condition animals compared to moderate and good condition hosts. Indeed, malnutrition and other concurrent parasitic infection will result in a weak immune response in the host to the parasites’ infective stage (Watson et al., 1994). Meanwhile, Etter et al. (1999) discovered increasing parasite fecundity in immunocompromised animals. Infection of small ruminants with coccidia and strongyles leads to gastroenteritis, protein-losing enteropathy, poor weight gain, and loss of body condition (Soulsby, 1982; Idika et al., 2012).

In conclusion, based on findings from this study, natural infections with gastrointestinal parasites in goats in Phitsanulok are common. The infection level of GIN based on FEC was moderate to high and involved infections with multi-species. H. contortus and S. papillosus were the predominant species. The parasite burden appear to have a significant impact on the body condition of goats. Anthelminthic treatment programs would likely be beneficial, with the stimulation that drug administration should be overseen to ensure utilization of appropriate drug classes and dosages, to minimize the development of drug resistance among parasite populations.