Copro-prevalence and risk factor assessment of gastrointestinal parasitism in Indian domestic pigs

Internal parasites are the major biological constraints to efficient pig production but they are often overlooked as the clinical symptoms are rarely apparent. In pigs, parasites cause 5 % and 31 %, reduction of the daily feed intake and average daily growth, respectively and an average 17 % higher Feed Conversion Ratio compared to the parasite-free fattening pigs (Ózsvári, 2018). In India, majority of pigs are raised under free range system where they feed upon raw garbage, kitchen waste and faecal matter, making them more prone to parasitic infections (Tiwari et al., 2009). Moreover, the close association between pigs and humans enables cross-infection with a range of zoonotic parasites like Taenia solium, Trichinella spiralis and Toxoplasma gondii, all of which contribute deleteriously to human health. Pigs are infected with wide range of gastrointestinal (GI) parasites with reports from all corners of the world (Permin et al., 1999; Tamboura et al.2006; Lai et al., 2011; Navarro-Gonzalez et al., 2013; Yui et al., 2014;Alynne et al., 2015; Junhui et al., 2015; Kabululu et al., 2015; ) including India (Laha et al., 2014; Dadas et al., 2016; Joute et al., 2016;

Krishna Murthy et al., 2016; Singh et al., 2017; Patra et al., 2019). Age, sex of animal, management practices and geographical location are the major risk factors associated with GI parasites in pigs (Permin et al., 1999; Geresu et al., 2015; Roesel et al., 2017). It is predicted that in next ten years, the total consumption of meat in India will double from its present numbers and hence more emphasis need to be given for the efficient and economical pig husbandry. The growing demand for pork due to the growth of hotel industry and proliferation of fast food chains in the country has prompted farmers in Punjab to go in for pig farming in a big way. In preview of the significance of GI parasites as one of the most important causes of economic losses to pig industry (Roesel et al., 2017) and lack of data from Indian states, it was justified to reassess the prevalence and its associated risk factors from Punjab state.

This study was reviewed and approved by the Dean of Post Graduate studies, Guru Angad Dev Veterinary and Animal Science University (GADVASU), Ludhiana, Punjab, India. More detailed ethical review was not required since no invasive sampling was undertaken.

Prevalence rates in range of 11 – 38 % have been reported in pigsfrom various geographical locations in India (Kumari et al., 2002; Deka et al., 2005; Borthakur et al., 2007; Godara & Sharma 2010; Singh et al., 2017). Kaur et al.,2017 have recorded an overall higher prevalence of 56.5 % in pigs of more than 1year age from Punjab, India. This might be due to the differences in the sampling criteria as they targeted scavenging pigs and had included only a few pigs from organised farms. Similarly, infection of pigs with GI parasites with prevalence rates varying between 13.2 to 96.4 % has been widely reported from all corners of world (Roepstorff & Jorsal 1989; Roepstorff et al., 1998; Tamboura et al ., 2006; Tiwari et al., 2009; Ismail et al., 2010; Lai et al., 2011; Obonyo et al., 2013; Dey et al., 2014; Okorafor et al., 2014; Alynne et al., 2015; Lipendele et al.,2015; Atawalna et al., 2015; Nonga & Paulo, 2015; Junhui et al., 2015; Roesel et al., 2017; Chilundo et al., 2017; Kouam et al., 2018) .The parasite spectrum was similar to that of previous studies from other tropical or subtropical countries (Tamboura et al., 2006; Nissen et al., 2011; Chilundo et al., 2017). Within Punjab state, India, Central plain zone and undulating plain zone have more humid conditions as compared to other zones, thus facilitating survival, development and propagation of the pre-parasitic stages of the GI parasites, hence higher prevalence rates.

Ascaris suum (11.1 %) was recorded as the predominant GI parasite of pigs which is in agreement with the findings of Yadav &Tandon (1989from sub-tropical regions of India. The prevalence rate of Trichuris suis (6.43 %) was low and was similar to the reports from other tropical countries like Ghana (4.6 %) and Zimbabwe (4.2 %), by Permin et al., (1999) and Marufu et al., (2008), respectively. Ismail et al. (2010) from Korea, Giarratana et al. (2012) from Italy and Dey et al. (2014) from Bangladesh reported higher prevalence rate of B. coli as 64.7 %, 36.66 % and 40 %, respectively which is contrary to the findings of the current study (4.5 %).

Variation in prevalence of various species of GI parasites observed in the current study and other regions of the world, suggested that geographical location along with management practices including hygiene and deworming are the major determinants responsible. Nonetheless, not only the macroclimate, but the microclimate of the pens i.e. flooring and drainage facilities provide optimum conditions including moisture and temperature for the propagation and existence of pre-parasitic stages in the contaminated feed and surroundings. In addition to these, differences in the basic biological requirements of the pre-infective developmental stages, transmission characteristics and immunogenicity of the different worm species are the contributors. Availability of clean water, practice of open defecation with easy access of pigs, housing, inadequate feed to the pigs, health status as well as inherent characteristics such as host immunity are the other important determinants.

The result of present study suggested that sex of the pigs did not have direct bearing on the prevalence of GI parasites. Similar observations has been reported by other researchers (Yadav &Tandon, 1989; Tamboura et al., 2006; Kumsa & Kifle, 2014; Okarafor, 2014). The highest intensity of infection with strongyles (EPG) was recorded in growers followed by piglets and adults. This can be ascribed to the fact that growers get exposed to the infective stages while they forage on grasses after weaning. The infection rates in piglets are associated to their immune status, level of pre-exposure and nutritional status while adults develop resistance against re-infections.

A significant (P<0.05) seasonal variation was recorded with highest intensity of infection during rainy season followed by winter with large proportion of animals having moderate infection. This finding can be attributed to the fact that suitable environmental conditions like temperature and humidity during this period for development of preparasitic stages makes maximum availability of infective stages to the host. The infection in the winter season may be ascribed to the reduced immuno-tolerance of animals and long prepatent periods of some of the GI parasites. Similar seasonal variations have been reported by Muraleedharan (2005) and Kagira et al.(2010).

It was found that the factors like unorganised farms, absence of deworming and pigs consuming water from unknown sources significantly increased the odds of infection with GI parasites. This could be credited to the habit of coprophagy and scavenging by the pigs which make them more prone to parasitic infections as pigs reared under unhygienic conditions have free access to garbage and contaminated feed and water. Analogous were the findings of Kagira et al. (2010) who have considered confinement or housing as a protective factor against GI parasitism in Western Kenya. There was less evidence of GI parasites in pigs with effective deworming programmes and better farm hygiene. Similar were the findings of a survey conducted in Nigeria by Weka & Ikeh (2009) who found a negative correlation between the prevalence of intestinal parasites and routine deworming of the pigs. However, this is in contrast to the findings of Roesel et al. (2017) who have reported that administering anthelminthic drugs have no significant impact on the prevalence of GI parasites in pigs.

Cluster analysis of the parasites did not identify any significant clusters in the present data. The three parasitic infections (B. coli, T. suis and mixed infection) were closer to each other as compared to other parasites. There have been earlier reports of chronic diarrhoea associated with Balantidium and Trichuris concurrent infection in canines (Ewing & Bull 1966). However, the importance of this co-occurrence in pigs which although was non-significant, needs to be explored further, especially in diarrhoeic animals.

Thus, our findings revealed that the pigs get infected by wide array of GI parasites. Due to their behaviour of coprophagy, pigs are likely to ingest infective stages from the environment. The unorganised farm management system, water consumption from unknown sources and lack of deworming schedule makes them more prone to the risk of GI parasitism.

Gastrointestinal parasites are prevalent in pigs of Punjab state, India with a prevalence rate of 28.4 % and Ascaris suum as the predominant parasite. Among the various risk factors analysed season, agro-climatic zones and managemental practices had a significant (p<0.05) effect on GI parasitism of pigs. Therefore, managemental practices viz. routine removal of manure and litter from pig pens, anthelmintic treatment during rainy and summer season and the use of disinfectants in the pens can be helpful in effective control of GI parasites of pigs.