Prevalence of gastrointestinal parasitism in pigs of Tripura, India

Pig is an important livestock species mostly reared by economically weaker section of people. In North-Eastern (NE) states of India, pig husbandry is very much popular and is a main stay to maintain the livelihood of the rural native population. Gastrointentinal (GI) parasitic infection is one of the major constrain in pro�table pig production in this area. In the present study, the GI parasitism in pigs was investigated in the three districts of Tripura, a NE State of India. The examination of fecal samples revealed the overall prevalence of 61.65% with detection of 6 GI parasitic species including 4 nematodes and 2 protozoa. Ascaris sp. was found to be the most prevalent GI parasite in pigs in the study. The age, sex, season, breed, area and farming system wise study showed the highest prevalence of GI parasites in grower pigs, female pigs, monsoon season, non-descript breeds, Khowai district and free ranging farming system, respectively. Overall, our study provides a baseline data for further investigation and formulation of strategies for control of GI parasitism in pigs in Tripura.


Introduction
In India, pig is one of the important livestock species mostly for people belonging to the economically weaker section (Rahman et al. 2008).Besides providing livelihood security to the rural masses it also contributes in improving the socio-economic status of the tribal population and weaker section of the society (Naskar and Das 2007).Pig is an e cient feed converting animal besides producing manure for agriculture.Moreover, pork is one of the preferred meats in some of the states especially in the Northeastern (NE) India.The demand and consumption of pork is increasing due to per capita income, urbanization and changes in life style and changing food habit.
Pig husbandry as back-yard piggery as well as intensive farming is a major part of the livelihood of the native population of most of the NE states of India.Pig is the most valued and popular animal species in this region because of its adaptability to the climatic condition of the NE states.Moreover, due to some biological advantages like proli cacy, faster growth, short generation interval and dressing percentage, the pig plays an important role for increasing meat production in this region.The majority of the people of the state Tripura; a NE state in India; are non-vegetarian and pork is the most liked meat in this state (Kumaresan et al. 2009).However, according to the 20th livestock census, 2019, the total pig population in the country has decreased by 12.03% from previous census.The decreasing trends in pig population have also been observed in the Tripura state.The inbreeding depression, lack of organized health care facilities, occurrence of infectious diseases and poor health management are the major reasons behind this (Rajkhowa et al. 2016).
Pigs are mostly reared in backyard farming system.Thus, they get exposed to a variety of pathogens including various gastro intestinal (GI) parasites.These GI parasites cause substantial loss of productivity in terms of ine cient feed conversion, poor growth rate, reduced weight gain, decreased litter size and the condemnation of affected organs after slaughter in pigs (Sowemimo et al. 2012).GI parasitic infections causes slow growth, reduced litter size and even death in case of heavy infections in pigs.Moreover, pigs also harbour zoonotic parasite which can act as potential health hazards for humans.GI nematodes reduce average daily weight gain by up to 30% in pigs of all ages and affects several organs such as lungs, kidney, muscle and gastrointestinal tract.The parasites of gastrointestinal tract include protozoa such as coccidia (Cystoisospora sp.and Eimeria sp.) and Entamoeba sp. as well as helminths.The latter includes, Strongyle-type helminths, Strongyloides spp., Ascaris sp., Trichuris sp., and Fasciolopsis sp.
The GI parasite infection in pigs have been reported from several countries including different states in India (Permin et al. 1999 Patra et al. 2020).However, no systematic study on GI Parasitism in pigs has been conducted in Tripura so far.Hence, there is a pressing need for undertaking systematic studies on prevalence of GI parasitism in pigs in this state to aid in formulating therapeutic and prophylactic strategies.Therefore, the present study was conducted to explore the prevalence of gastrointestinal parasitism in Pigs of Tripura state.

Selection of place and period of study
The present study was conducted in three districts of Tripura viz.West Tripura, Sepahijala and Khowai.These areas are having large pig population reared mostly by the marginal, small farmers and landless laborers and pig husbandry plays an important role in the economy of the study areas.The prevalence study was carried out for eight calendar months period starting from March to October covering two major seasons i.e., summer and monsoon considering the higher prevalence of GI parasitic infection usually found in these seasons.The summer season and monsoon season spanned from March to June and July to October, respectively.

Collection and examination of fecal samples
In the present study, pigs of more than two months of age were considered for collection of fecal sample.Per rectal faecal samples or freshly voided faecal samples were collected from 388 pigs of all age groups from all three districts at monthly interval.The pigs were restrained and thoroughly investigated by close inspection.About 10-20 g of faecal samples of pigs were randomly collected from the oor of the pens avoiding soil contamination and placed into disposable zip lock plastic covers with proper labelling.After collection, samples were transported to the laboratory and stored in 10% formalin and then processed within ve days of collection for detection of parasitic eggs/ova/cyst/larva using microscope (Soulsby 1982).Each faecal sample was examined qualitatively for the presence of nematode, cestode eggs and coccidian oocysts by standard salt otation technique and for trematode eggs by simple sedimentation technique described by Soulsby 1982.The ova/ eggs were identi ed by their morphological characters as mentioned by Soulsby (1982).

Statistical Analysis
Prevalence was expressed as the percentage.To test the signi cant association between the difference groups, Fisher's exact or Chi square test were performed.The statistical analysis was done at 5% probability level using the Statistical Package for the Social Sciences (SPSS), Version 25 software (SPSS Inc., Chicago, IL, USA).

Results and discussion
The present study was conducted to record the prevalence of gastrointestinal (G.I.) parasitism in pigs in three districts of Tripura.The study was conducted for eight months starting from March to October.The study involved a total number of 388 randomly selected pigs of different age groups.

Overall Prevalence of G.I. parasitism in pigs:
The present study revealed that pigs of Tripura were very much susceptible to GI parasite infection.Out of 388 pigs, 239 (61.59%) were found positive with one or more species of GI parasites.During the study period, pigs were found infected with mainly 6 types of parasites.Among the identi ed parasites, there were four (4) species of nematodes such as Ascaris sp., Metastrongylus sp., Strongyloides sp., Trichuris sp. and two species of protozoa such as Coccidia sp and Balantidium coli.In the present study, highest prevalence was observed for Ascaris sp.(32.67%)Most importantly, out of 388 pigs, 46.91% were found to be infected with more than one species of GI parasites (Table 1).

Sex wise prevalence of gastrointestinal parasites
The present study included 168 male and 220 female pigs of different age groups.The sex wise prevalence of the G.I. parasites in pigs is presented in Table 2.The overall prevalence of G.I. parasites was found signi cantly (p < 0.05) higher in females (67.27%) than male (54.17%) pigs in this study.The highest prevalence recorded for Ascaris sp., in both the male and female animals.The prevalence of mixed infection was also found to be higher in female than in male pigs.

Age wise prevalence of G.I. parasites in pigs
The prevalence of parasites in different age groups of pigs is presented in Table 1.In the present study, signi cant difference (p < 0.05) was observed in terms of GI parasitic infection among the three age groups of pigs. it was found that prevalence of GI parasites in pig were higher in grower pigs (71.52%) followed by piglets (59.09%).However, all the 6 types of GI parasites were detected in all three age groups of pigs.The prevalence of mixed infection was also found to be higher in grower pigs and piglets in comparison to the adults.The highest prevalence was observed for Ascaris sp. in all three age groups.
This uneven age-speci c herd prevalence of pig GI parasite is a common phenomenon that may be due to different host-parasite interactions, especially immunity to the parasite (Roepstorff and Nansen 1994; Higher infection in the growers is attributed to their more exposure to the infective stages of parasite while grazing just after weaning.Whereas, the higher prevalence in piglets is might be associated with under developed immune status, poor nutrition and lack of exposure to the GI parasites.On the contrary, the less prevalence observed in the adult pigs is might be due to the resistance against re-infections (Sharma et al. 2020).

Breed wise prevalance of gastrointestinal parasites of pigs
In the present study, 175 non-descript breed and 213 cross breed pigs of different age groups were examined.The breed wise prevalence of the G.I. parasites in pigs is presented in Table 1.The overall prevalence of G.I. parasites was found slightly lower in cross breed (58.22%) than non-descript (65.71%) pigs, in this study.The highest prevalence was recorded for Ascaris sp. in both the groups.Moreover, the prevalence of mixed infection was also found to be higher in non-descript breed than in cross breed pigs.
In the present study, the higher prevalence of GI parasitic infections was observed in non-descript is in agreement with the ndings of Muraleedharan et al. (1994) in Mysore and Mandya districts of Karnataka and Krishna Murthy et al. (2016) in Shimoga region, Karnataka.The high rate of GI parasite infection observed in non-descript pig breeds in the present study might be due to unhygienic farming practices in the unorganized farms with limited use of anthelmintic (Singh and Rath 2013).Whereas, the cross-breed pigs are mostly reared in organized farms and given utmost care with better animal husbandry practices.Furthermore, the non-descript breeds are reared completely in extensive system and are allowed to graze near water land, forest and bushes which increases the chance of picking up infection (Kabir et al. 2011).

Farming System wise Prevalance:
In the present study, 108 animals were reared in free range rearing farming system, 168 animals were in semi-intensive rearing system and 112 numbers of pigs were kept in intensive system.The farming system wise prevalence of the G.I. parasites in pigs is presented in Table 1.The prevalence of G.I. parasites were found higher in pigs kept in free range system (69.44%) of farming followed by semi intensive (61.31%) rearing system and lowest in intensive (54.46%) type of farming.The prevalence of mixed infection was also highest in free range farming system.However, Ascaris sp. was found to be the most prevalent parasitic species in all three farming systems.
The farming system plays a remarkable role in spreading GI parasite infection.Worm load and variety of helminthes species mostly depends on the type of swine production system.In the highly intensive production systems, the infection levels are usually low and involve only few species.This is because intensive pig farms have better management and treatment standards (Lin et al. 2013).On the other hand, in most traditional extensive outdoor management systems, the poor hygienic conditions allow a higher prevalence, burden and rate of helminth transmission without anthelmintic interventions (Roepstorff and Nansen 1994;Nansen and Roepstorff 1999).Infections are thus likely to be more severe in scavenging pigs, compared to those in intensive system of production.In present study, the majority of pigs are reared in traditional free ranging outdoors system.This might be the reason behind the observed higher prevalence of GI parasites.Rearing pigs in free range system and their free access to potentially contaminated areas is a vital risk for persistence of parasitic infection (Chawhan et al. 2014;Kaur et al. 2017).

Area wise prevalence of gastrointestinal parasites of pigs
The prevalence of G.I. parasites in pigs in different districts of Tripura is presented in Table 1.Among the three districts of Tripura, highest prevalence of GI parasites in pigs was observed in Khowai district (64.57%) followed by West Tripura (59.55%) and Sepahijala (58.78%).In all three districts, the highest prevalence was observed for Ascaris sp.Notably, no trematode eggs were detected in fecal samples collected from all three districts in this study.The high frequency of nematode parasite infections in the pigs is an indication of both a favourable environment for the survival and development of pre-infective stages of nematodes and the limited veterinary care of these animals in this region.

Season wise prevalence of gastrointestinal of pigs
Season wise prevalence of G.I. parasites in pigs based on feacal sample examination is presented in Table 2.The present study was conducted over a period of eight months from March to October.The highest prevalence of GI parasites was observed in the month of July (68.75%) and that of lowest in the month of April (52%).However, the prevalence of mixed infection was found to be highest in the month of September (57.5%) and lowest in the month of October (40.74%) (Data not shown).The highest prevalence was observed for Ascaris sp. in all 8 months under this study.Altogether, it was found that the overall prevalence of G.I. parasite in monsoon season was higher (65.78%) than the summer (57.71%).Further, the prevalence of all four nematodes was also found to be higher in the monsoon season than in the summer.
The highest prevalence recorded in the month July which is in agreement with the ndings of Das et al. (2020) in Meghalaya.This might be on account of warm and wet climate which is most congenial for the majority of nematode parasites (Rogers 1962).The moist weather in the rainy season favours the development of the pre-parasitic stages of the nematodes (Yadav and Tandon 1989).The high rainfall in the study area coupled with the very short dry season results in the persistent high humidity in the environment which satis es the optimum requirements needed for the development of nematode eggs and, also ensures a prolonged survival of eggs and larvae in the soil, increases the possibility of host infection.Further, to some extent the feeding habit of pigs is also one of the factors for such a high infection rate of nematodes, Ascaris sp.The seasonal pattern of overall nematode infections observed in the investigation is attributable to one factor, the presence of both eggs and larvae in the soil throughout the year.

Table 1
(Soulsby 1982l.(2006)testinalparasite in pigs of Tripura according to farming system, districts, age and parasitic species Eijck and Borgsteede 2005; Tamboura et al. 2006; Tiwari et al. 2009, Dey et al. 2014; Laha et al. 2014;Kaur et al. 2017).The present nding varied from the previous reports probably because of geographical and climatic conditions, variation in pig breeds, variation in farm management practices, the nutritional and health status of the pigs, consciousness of farmers about the use of anthelmintics or antiparasitic agents, method of sample collection and analysis, and differences in the number of samples analyzed.The overall higher prevalence of Ascaris sp.observed in this study was also reported in other studies byTamboura et al. (2006)in Burkina Faso, Dey et al. (2014) in Bangladesh, Nsoso et al. (2000) in Botswana and Laha et al. (2014) in NE India.However, difference is prevalence percentage across the studies may be due to seasonal and geographic variations that favor the proliferation of the helminthes.Perpetual wet unhygienic farm conditions with favourable environmental temperatures can lead to high infection rates with A. suum(Kagira 2010; Obonyo et al. 2012) Moreover, the female is capable of laying more than 200,000 eggs per day(Soulsby 1982).The eggs have thick, tough shells that protect the developing larvae.These eggs can withstand adverse weather conditions and some chemicals, and they may remain viable and infective for extended periods(Roepstorff and Nansen 1998).
(Nsoso et al. 2000)oachim et al. 2001)impediment to e cient and pro table livestock production(Boes et al. 2000;Joachim et al. 2001).GI parasitism in swine affects performance in terms of e cient feed conversion, poor growth rate, reduced weight gain and the condemnation of affected organs after slaughter(Nsoso et al. 2000).The prevalence of GI parasitism in pigs have also been reported from different parts of India and abroad(Nsoso et al. 2000; Rajkhowa et al. 2003; Deka et al. 2005; Dutta et al. 2005; Among protozoan parasites, the Coccidia sp.(12.37%) was the most identi ed parasite which is in agreement with Tiwari et al. (2009), Dey et al. (2014) and Eijck and Borgsteede (2005).Poor management and unsanitary conditions in the pig farms on most of the farms surveyed could have accounted for the high rate of Coccidia infection (Nwafor et al. 2019).

Table 2
Prevalence of gastrointestinal parasites in pig of Tripura according to various epidemiological factors (Swai et al. 20100)12) signi cant p value (p < 0.05), Fishers' exact test The higher prevalence of GI parasites in female population is in agreement with the earlier study ofTamboura et al. (2006),Obonyo et al. (2012)andDey et al. (2014).However, higher prevalence of GI parasites in male was recorded bySowemimo et al. (2012)and no signi cant different between sexes was reported byNsoso et al. (2000)in Botswana.The reason of higher prevalence of infection in the females cannot be explained exactly but factors such as hormonal imbalance, gravidity, parturition, lactation and stress might have lead to suppression of immunity leading to predisposition to pathogens.Moreover, higher level of lactation and progesterone hormones also make the female individual more susceptible to any infection(Swai et al. 2010).