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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2024 Feb 9;48(1):108–116. doi: 10.1007/s12639-024-01649-3

Prevalence of gastrointestinal parasitism in pigs of Tripura, India

Subham Das 1, Soumitra Pandit 1, Ruma Jas 1, Surajit Baidya 1, Subhas Chandra Mandal 1, Apurba Debbarma 2, Subhasis Batabyal 1, Ankan De 3,✉
PMCID: PMC10908662  PMID: 38440748

Abstract

Pigs breeds are an important livestock species mostly reared by economically lower incomesection of people in India. Within North-Eastern (NE) states, pig husbandry is very much popular hence maintain the livelihood of the rural native population. Gastrointentinal (GI) parasitic infectionisone of the major constraint in profitable pig production in this area. In the present study, the GI parasitism was investigated in 388 pigs in the three districts of Tripura, NE State of India. The examination of faecal samples revealed 61.65% overall prevalence of parasitic infestation, precisely6 GI parasitic species; including 4 nematodes and 2 protozoa, while 46.91% were the mixed infections.Metastrongylus spp. (17.53%), Strongyloids spp. (19.33%),Trichuris spp. (15.98%), Coccidia spp. (12.37%), and Balantidium coli (10.82%), were detected, however, Ascaris spp. was the most prevalentrecording 32.47%. The epidemiological factors including: age, sex, season, breed, area and farming system wise when considered as markers of study showed the highest prevalence of GI parasites in grower(6–12 months) stage, female, monsoon season, non-descript breeds, Khowai district and free range farming system, recorded 71.52%, 67.27%, 65.78%, 65.71%, 64.57%, and 69.44%, respectively. Overall, our study provides a baseline data for further investigation and formulation of strategies for control of GI parasitism in pigs in Tripura.

Keywords: Prevalence, GI parasites, Nematodes, Protozoa, Pigs, Tripura

Introduction

In India, swine is one of the important livestock species mostly for people belonging to the economically lower income section (Rahman et al. 2008). Besides providing livelihood security to the rural masses, it also improves the socio-economic status of the tribal population (Naskar and Das 2007). Pigs are efficient feed converting animal besides producing manure for agriculture. Moreover, pork is one of the preferred meats in some of the states especially in the North-eastern (NE) of India. The demand and consumption of pork is increasing due to per capita income, urbanization and changes in life style and food habit (Thakur et al. 2019).

Swine husbandry as back-yard piggeries as well as intensive farming are major parts of the native population life style in most of the NE states of India because of its adaptability to the climatic condition of these states. Moreover, due to some biological advantages like prolificacy, faster growth, short generation interval and dressing percentage. 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, including 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 reduction in pork mat production (Rajkhowa et al. 2016).

Pigs farming system enhance their exposure to a variety of pathogens including gastro intestinal (GI) parasites which cause substantial loss of productivity in terms of inefficient feed conversion, poor growth rate, reduced weight gain, decreased litter size, the condemnation of affected organs after slaughter, and even death in case of heavy infections in pigs (Sowemimo et al. 2012). Moreover, pigs also harbour zoonotic parasite which can act as potential health hazards for humans, such as Trichinella spiralis, Criptosporidium spp. etc. (Pinilla et al. 2021; Lin et al. 2023). The parasites of gastrointestinal tract include protozoa such as coccidia (Cystoisospora sp.and Eimeria sp.) and Entamoeba spp. as well as helminths (Henry & Tokach 1995; Johnson et al. 2008; Matsubayashi et al. 2014, 2015; Sangioni et al. 2017; Midttun et al. 2018). The latter includes, Strongyle-type helminths,Strongyloides spp., Ascaris spp.,Trichuris sp., and Fasciolopsis sp. 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 (Ozvari 2017; Li et al. 2022).

The GI parasite infection in pigs have been reported from several countries including different states in India (Permin et al. 1999; Dutta et al. 2005; Tamboura et al. 2006; Matsubayashi et al. 2009; Lai et al. 2011; Lahaet al. 2014; Krishna Murthy et al. 2016; Dadas et al. 2016; Patra et al. 2020). However, no systematic study on GI Parasitism in pigs has been conducted in Tripuraso 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.

Materials and methods

Selection of place and period of study

The present study was conducted in three districts of Tripura vs West Tripura, Sepahijala and Khowai (Fig. 1.). These areas have a large pigs population comprised of local non-descript breed (Sus domesticus) as well as cross bred pigs (crossing between non-descript breed with exotic breed such as Large White Yorkshire or Landrace) reared mostly by the marginal, small farmers and landless labourers where pig husbandry plays an important role in the economy of the study areas. The prevalence study was carried out for eight calendar months starting from March to October, 2021 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. Summer in Tripura remains as hot and humid with temperature upto 35 °C. Whereas, the monsoon season is characterized by heavy rainfall.

Fig. 1.

Fig. 1

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The geographical map of Tripura, India showing the location of three districts (Khowai, Sepahijala and West Tripura) in which the present prevalence study was conducted

Collection and examination of fecal samples

In the present study, pigs of more than two months of age were considered for collection of fecal samples. Per rectal fecal samples or freshly voided faecal samples were collected from 388 pigs of all age groups from all three districts at monthly interval during study seasons. The pigs were restrained and thoroughly investigated by close inspection. About 10–20 g of feces was randomly collected without 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 five 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 nematodal larvae, cestodal eggs, and/or coccidian oocysts by standard salt flotation technique and for trematode eggs by simple sedimentation technique described by Soulsby (1982). The eggs were identified by their morphological charactersas mentioned by Soulsby (1982).

Statistical analysis

Prevalence was expressed as the percentage. To test the significant association between the different groups, Chi square test was performed ((Abonyi and Njoga 2020). 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 (GI) parasitism in pigs in three districts of Tripura (Khowai, Sepahijala and West 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 gastrointestinal 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 identified spp., there were four (4) nematodes; Ascaris spp., Metastrongylus spp., Strongyloides sp., Trichuris spp. and two protozoa; Coccidia spp and Balantidium coli. In the present study, the highest prevalence was observed for Ascaris spp. (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).

Table 1.

Prevalence of gastrointestinal parasite in pigs of Tripura according different epidemiological factors

Epidemiological factor Number of pigs screened Number of pigs infected Prevalence (%) p value No. (%) positive for GI Parasites Mixed infection
Ascaris
sp.		 Metastrongylus
Sp		 Strongyloides
Sp		 Trichuris sp. Coccidia
Sp		 B coli (%)
Sex
Male 168 91 54.17 0.009*

52

(39.30)

27

(16.07)

27

(16.06)

23

(13.69)

18

(10.71)

14

(8.33)

73

(43.45)
Female 220 148 67.27

74

(33.63)

41

(18.64)

48

(21.82)

39

(17.73)

30

(13.64)

28

(12.73)

109

(49.54)
Breed
Non-descript 175 115 65.71 0.105

56

(32)

29

(16.57)

32

(18.28)

26

(14.86)

21

(12)

17

(9.71)

84

(48)
Cross breed 213 124 58.22

70

(32.86)

39

(18.31)

43

(20.19)

36

(16.9)

27

(12.68)

25

(11.73)

98

(46)
Season
Summer 201 116 57.71 0.103

61

(30.31)

27

(13.43)

37

(18.41)

31

(15.42)

26

(12.94)

23

(11.44)

89

(44.28)
Monsoon 187 123 65.78

65

(34.76)

41

(21.93)

38

(20.32)

31

(16.58)

22

(11.76)

20

(10.70)

93

(49.73)
Farming system
Free range 108 75 69.44 0.073

38

(35.18)

23

(21.29)

24

(22.22)

18

(16.67)

18

(16.67)

13

(12.03)

59

(54.63)
Semi-intensive 168 103 61.31

56

(33.33)

29

(17.26)

34

(20.24)

30

(17.85)

19

(11.31)

16

(9.52)

81

(48.21)
Intensive 112 61 54.46

32

(28.57)

16

(14.28)

17

(15.18)

14

(12.5)

11

(9.82)

13

(11.61)

42

(37.5)
District
Sepahijala 124 73 58.87 0.548

37

(29.83)

19

(15.32)

24

(19.35)

18

(14.51)

16

(12.9)

14

(11.29)

55

(44.34)
Khowai 175 113 64.57

59

(33.71)

32

(18.28)

37

(21.14)

29

(16.57)

21

(12)

18

(10.28)

83

(47.43)
West Tripura 89 53 59.55

30

(33.71)

17

(19.10)

14

(15.73)

15

(16.85)

11

(12.36)

10

(11.23)

44

(49.44)
Age
Piglet (below 6 months) 110 65 59.09 0.002*

35

(31.81)

20

(18.18)

21

(19.09)

18

(16.36)

16

(14.54)

11

(10)

56

(50.90)

Grower

(6–12 months)

 158 113 71.52

59

(37.34)

31

(19.62)

37

(23.42)

29

(18.35)

20

(12.66)

18

(11.39)

81

(51.26)
Adult (Above 12 months) 120 61 50.83

32

(26.67)

17

(14.17)

17

(14.17)

15

(12.5)

12

(10)

13

(10.83)

45

(37.5)
Total 388 239 61.59

126

(32.47)

68

(17.53)

75

(19.33)

62

(15.98)

48

(12.37)

42

(10.82)

182

(46.91)
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* Denotes statistically significant p value (p < 0.05), Chi square statistic.

The GI parasitism constitutes a major impediment to efficient and profitable livestock production (Boes et al. 2000; Joachim et al. 2001). GI parasitism in swine affects performance in terms of efficient 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 such as Nagaland (Rajkhowa et al. 2003), Aizawl, Mizoram (Deka et al. 2005), West Bengal (Dutta et al. 2005), north eastern region of India (Laha et al. 2014) and in Punjab (Kaur et al.2017) as well as in abroad such as Southeast District, Botswana (Nsoso et al. 2000), Netherlands (Eijck and Borgsteede 2005), eastern centre province, Burkina Faso (Tamboura et al. 2006), Grenada, West Indies (Tiwari et al. 2009), Mymensingh, Bangladesh (Dey et al. 2014). The present finding varied from the previous reportsprobably 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 anthelmintic or antiparasitic agents, method of sample collection and analysis, and differences in the number of samples analysed. The overall higher prevalence of Ascaris spp. observed in this study was also reported in other studies; Tamboura 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 in prevalence percentage across the studies may be due to seasonal and geographic variations that favour the proliferation of the helminths'. Perpetual wet unhygienic farm conditions with favourable environmental temperatures can lead to high infection rates with A. suum (Kagira 2010; Obonyo et al. 2012). Hence, each 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).

Among protozoan parasites, the Coccidia sp. (12.37%) was the most identified 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 higher rate of Coccidia infections (Nwafor et al. 2019).

Sex wise prevalence of gastrointestinal parasitism in pigs:gastrointestinal parasitism in pigs

The present study included 168 male and 220 female pigs of different age groups; over than two months of age. The sex wise prevalence of the GI parasites in pigs is presented in Table 1. The overall prevalence of GI parasites was found significantly (p < 0.05) higher in females (67.27%) than male (54.17%) pigs in this study. The highest prevalence was recorded for Ascaris sp., in both sex the prevalence of mixed infection in pigs was also found to be higher in female than in males.

The higher prevalence of GI parasites in female population is in agreement with the earlier study of Tamboura et al. (2006), Obonyo et al. (2012) and Dey et al. (2014). However, higher prevalence of GI parasites in male was recorded by Sowemimoet al. (2012) while no significant differences between sexes was reported by Nsoso et al. (2000) in Botswana. The reason of higher prevalence of infection in the females cannot be explained precisely but factors such as hormonal imbalance, gravidity, parturition, lactation and stress might have led to suppression of immunity leading to predisposition to pathogens (Okita et al 2021). Moreover, higher level of lactation and progesterone hormones also make the female individual more susceptible to any infection (Swai et al. 2010).

Age wise prevalence of gastrointestinal parasitism in pigs:

The prevalence of GI parasites in different age groups of pigs is presented in Table 1. In the present study, significant difference (p < 0.05) was observed in terms of GI parasitic infection among the three age groups of pigs. The highest percentage was recorded 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 studied pigs population. The prevalence of mixed infection was also found to be highest 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-specific herd prevalence of pig GI parasites is a common phenomenon that may be due to different host-parasite interactions, especially immunity to the parasite (Roepstorff and Nansen 1994; Damriyasa and Bauer 2006). The significantly (P < 0.01) higher GI parasites infection in grower and piglets found in this study is in agreement with Chou et al. (2004), Dey et al. (2014) and Sharma et al. (2020).Higher infection in the growers is attributed to their more exposure to the infective stages of each parasite while grazing just after weaning (Adhikari et al. 2021), whereas, the higher prevalence in piglets might be associated with under developed immune status, poor nutrition and lack of exposure to the GI parasites (Sharma et al. 2020). On the contrary, the less prevalence observed in the adult pigs might be due to the resistance developed against re-infections due to repeated exposure (Sharma et al. 2020).

Breed wise prevalance of gastrointestinal parasitism in pigs:

In the present study, 175 non-descript breed (Fig. 2) and 213 cross breed pigs of different age groups were examined. The non-descript breed constitute the indigenous pigs of Tripura (Fig. 2). The crossbred pigs under the study are the pigs originated by crossing the non-descript breed with exotic breeds such as Large White Yorkshire or Landrace. The breed wise prevalence of the GI parasites in pigs is presented in Table 1. The overall prevalence of GI mparasites 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 spp. in both breeds. Moreover, the prevalence of mixed infection was also found to be higher in non-descript breed than in cross breed pigs.

Fig. 2.

Fig. 2

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Photograph of the non-descript pig breed of Tripura

In the present study, the higher prevalence of GI parasitic infections was observed in non-descript is in agreement with the findings of Muraleedharan et al. (1994) in Mysore and Mandya districts of Karnataka and Krishna Murthy et al. (2016) in Tioga region, Karnataka (Reference given in this sentence).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 near water land, forest and bushes which increases the chance of picking up infection (Kabir et al. 2011).

Farming system wise prevalanceof gastrointestinal parasitismin pigs

In the present study, 108animals were reared in free range farming system, 168 animals were in semi-intensive rearing system and 112 of pigs were kept in intensive system. The farming system wise prevalence of the GI parasites in pigs is presented in Table 1. The prevalence of parasitism were found higher in pigs kept in free range system (69.44%), followed by the semi intensive rearing system (61.31%), and lowest 54.46%was in the intensive type of farming. The prevalence of mixed infection was also the highest in free range farming system. Similarly, Ascaris spp. was found to be the most prevalent parasitic species in all three farming systems.

The farming system type was found to play a remarkable role in spreading GI parasite infection. Worm load and variety of helminths 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 (Nwoha RIO and Ekwurike 2011). This is because intensive pig production farms had better management and treatment standards (Lin et al. 2013). On the other hand, in most traditional extensive outdoor management systems, the poor hygienic conditions allowed a higher prevalence, burden and rate of helminths transmission without anthelmintic interventions (Roepstorff and Nansen 1994; Nansen and Roepstorff 1999). Infections were thus likely to be more severe in scavenging pigs when compared to those under intensive system of production (Symeonidou et al. 2020).In the present study, the majority of pigs are reared under 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 parasitism in pigs

The prevalence of parasitism in pigs within different districts of Tripura is presented in Table 1. Among the studied three districts, the highest prevalence of GI parasites in pigs was observed in Khowai district (64.57%), followed by West Tripura (59.55%), and then Sepahijala (58.78%). In all three districts, the highest prevalence was observed for Ascaris spp.Notably, no trematode eggs were detected in all faecal samples collected and examined from all three districts. The high frequency of nematode parasites infections indicated both the favourable environment for the survival and development of pre-infective stages of nematodes, as well as, the limited veterinary care given in this region.

Season wise prevalence of gastrointestinal parasitism in pigs

Season wise prevalence of GI parasites in pigs based on fecal sample examination is presented in Table 1, which was conducted over a period of eight months from March to October, 2021. The highest prevalence of GI parasites was observed in the month of July (68.75%) while lowest in the month of April, recorded 68.75% and 52%, respectively. However, the prevalence of mixed infection was found to be the highest in the month of September (57.5%) while the lowest was recorded in the month of October (40.74%) (Data not shown). The highest prevalence was observed for Ascaris spp. during the all 8 months of the study. Altogether, it was found that the overall prevalence of GI parasites in monsoon season was higher (65.78%) than the summer season (57.71%). Further, the prevalence of all four nematodes was also found to be higher in the monsoon than in the summer season.

The highest prevalence recorded in July which is in agreement with the findings of Das et al. (2020) in Meghalaya. This might be on account of warm and wet climate which is the 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 resulted in the persistent of high environmental humidity which satisfies the optimum requirements needed for the development of nematodale eggs and prolonged survival of developmental stages in the soil, which increases the possibility of pigs infection (Bautista-Garfias et al. 2022). Further, to some extent the pigs' feeding habits are major factors for such high infection rate with nematodes, Ascaris spp. The seasonal pattern of overall nematode infections observed within the investigation was attributable to précised factor which is the presence of both eggs and larvae in the soil throughout the year. Highest Egg per gram (EPG) for GI nematodes in pigs was also reported in rainy season followed by summer season by Sharma et al, (2020). Similarly, the highest prevalence of GI parasites was reported in northern India in small and large rumanants (Sharma et al. 2023). Thus, the rainy and summer seasons were choosen for study of prevalence of GI nematodes in poigs in this study.

Conclusion

The present study reported the prevalence of GI parasites in pigs of Tripura. A considerably high prevalence rate was observed in the study warranting treatment. Infection with both nematodes and protozoa was observed in studied pigs' population. Ascaris sp. was found to be the most prevalent parasitic species in the studied area. The study determinants included the epidemiological effects of: age, sex, season, breed and farming system. The highest prevalence of GI parasites in was recorded in females of grower pigs during monsoon season, which belong to non-descript breeds and free ranging farming system. Further studies are required to assess the actual economic impact of the GI parasites in the study area. Altogether, our study provides a baseline data on the prevalence of GI parasitism in pigs in the three districts of Tripura which would be immensely helpful in formulating control strategies against GI parasitism in the near future.

Acknowledgements

The authors would also like to thank to the Vice-chancellor, West Bengal University of Animal and Fishery Sciences, Kolkata, West Bengal, India, the Dean, F/O- Veterinary and Animal Sciences, West Bengal University of Animal and Fishery Sciences, Kolkata, West Bengal, India and the Principal, College of Veterinary Sciences and Animal Husbandry, R.K.Nagar, West Tripura, Tripura, India for providing all necessary facilities and support to conduct the research work.

Author contributions

SD and AD collected the samples and carried out the laboratory works. SP, RJ, SB, SCM and SB designed and supervised the research work. AD ha analysed the data and wrote the manuscript. All authors revised and approved the manuscript for publication.

Funding

“The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.”

Declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

The Department of veterinary Parasitology, Faculty of Veterinary and Animal Sciences, West Bengal University of Animal and Fishery Sciences, Kolkata, West Bengal, India approved the conducted study.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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