Skip to main content
Download PDF

A survey of gastrointestinal helminth infestation in smallholder backyard pigs and the first molecular identification of the two zoonotic helminths Ascaris suum and Trichuris suis in Myanmar

BMC Veterinary Research volume 20, Article number: 139 (2024) Cite this article

Abstract

Background

Parasitic infestations have a substantial economic impact on pig production. This study aimed to investigate the gastrointestinal (GI) helminths in pigs and to molecularly characterise two important nematodes, Ascaris and Trichuris species.

Materials and methods

A total of 500 pig faecal samples were collected from small holder backyard pig farms in five townships within Nay Pyi Taw, Myanmar. Microscopic examination was conducted to estimate the prevalence of GI helminth infestation in the pigs. DNA extraction and PCR were performed on faecal samples that were morphologically positive for Ascaris and Trichuris eggs. Molecular analysis was then conducted to characterise A. suum and T. suis, the most common and zoonotic helminths.

Results

According to microscopic examination, 69.2% (346/500) were positive for GI helminth eggs. The GI helminth species observed were A. suum, Strongyle, Strongyloides spp., T. suis, Metastrongylus spp., Hyostrongylus spp., Fasciolopsis spp., Paragonimus spp., and Schistosoma spp., with occurrences of 34.8%, 29.6%, 21.4%, 20.0%, 4.0%, 1.6%, 1.0%, 1.0%, and 0.4%, respectively. Mixed infections of GI helminths were noted in 31.0% of the samples. Overall, sampled pigs excreted mostly low levels (< 100 EPG) or moderate levels (> 100–500 EPG) of GI helminth eggs. The highest mean EPG for each parasite species was noted in A. suum. The presence of A. suum and T. suis was confirmed molecularly. The sequences of the internal transcribed spacer 1 (ITS1) region of A. suum showed high similarity with previously reported sequences. Likewise, the sequences of T. suis exhibited high similarity with the sequences reported from humans and pigs. Age was noted as an associated factor (P < 0.05) for GI helminth infection status.

Conclusions

In this report, A. suum and T. suis were molecularly identified for the first time in Myanmar. It is important to extend the information among the farmers to be aware of the necessity of preventing zoonotic parasites by practicing regular deworming, proper use of anthelmintics and maintaining hygienic conditions in their pig farms.

Peer Review reports

Background

Pig productivity is under threat due to a wide range of pig diseases. Infectious diseases have a substantial economic impact on pig production because they can reduce productivity and reproduction, as well as increase morbidity and mortality [1]. Parasites are frequently reported as the cause of diseases in pigs, particularly in tropical regions. Among parasitic diseases, gastrointestinal (GI) parasites are responsible for substantial loss of productivity in pigs in terms of inefficient feed conversion, poor growth rate, intestinal malabsorption, reduced weight gain, decreased litter size delayed or incomplete immunity subsequent to vaccinations, negative effects on meat quality and the condemnation of affected organs after slaughter [2]. Additionally, several swine parasites can be transmitted from pigs to humans, posing a significant hazard for the producer [3].

The most common helminth infestations in humans and pigs around the world are caused by nematode worms of the genera Ascaris and Trichuris [4]. Some parasites, such as Ascaris suum and Trichuris suis, are widespread in pigs and can infect both humans and pigs [4, 5]. The worms that infect pigs and humans are morphologically similar and difficult to distinguish due to a lack of distinct characteristics [5]. Infection with A. suum may result in production losses due to altered carcass composition, lower weight gain, and liver condemnation [6]. Furthermore, the level of natural worm cross-transmission between pig and human hosts is unknown; nevertheless, experimental cross-infections have proven that A. suum can infect humans, and human zoonotic cases have been reported [5, 7, 8]. Infection with T. suis (whipworm) in pigs can result in anorexia and bloody diarrhoea in growing pigs, which can lead to economic losses [9]. Because of the similarities among Trichuris species, morphological differentiation is very difficult. Moreover, the degree of natural Trichuris cross-transmission between people and pigs is unknown [5]. Although adult worms rarely persist, investigations on experimental infection have shown that human whipworm T. trichiura can establish in pigs, whereas patent T. suis infection has been noted in humans [5]. Because species discrimination by egg morphology is challenging, the development of molecular approaches for species identification and diversity evaluation is extremely beneficial [10]. Several molecular markers have been used for the identification of Ascaris and Trichuris spp., such as nucleotide sequences of internal transcribed spacers 1 and 2 (ITS1 and ITS2) [11, 12].

The pig population in Myanmar in 2021 was estimated to be approximately 6.8 million [13]. Approximately 86% of the Myanmar population resides in rural areas and is involved in agro-livestock production and agro-industrial work. Most pig farmers in Myanmar prefer backyard farming due to its simplicity and low cost, generally with intensive or semi-intense methods [14]. Even though pig production in Myanmar contributes to farmers maintaining a sustainable livelihood, there are many challenges to maintaining productivity, profitability and sustainability. One of these challenges is parasitic infestation. Although our recent study demonstrated the occurrence of Cystoisospora infection in pigs in Myanmar [15], data on helminth infestation are very limited. Therefore, this study aimed to investigate the GI helminths in pigs and to molecularly characterize two important nematodes, Ascaris and Trichuris species, in the Nay Pyi Taw area, Myanmar.

Results

Parasite detection rate

The overall occurrence of GI helminth infestation among pigs was 69.2% (346/500). The helminth species observed were A. suum, Strongyle, Strongyloides spp., T. suis, Metastrongylus spp., Hyostrongylus spp., Fasciolopsis spp., Paragonimus spp., and Schistosoma spp. (Fig. S1 and Table 1). Overall, 31.0% of examined pigs were found to be infested with more than one GI helminth species. The occurrence of GI helminths was found to be the lowest (52.0%) in Lewe township and the highest (85.0%) in Pyinmana township. The mean eggs per gram of faeces (EPGs) for A. suum, Strongyle spp., Strongyloides spp. and T. suis were 172.7, 40.4, 27.8 and 20.5, respectively, and the mean EPGs of overall helminth species were 307.0, 214.4, 225.9, 496.7, and 63.0 in Zay Yar Thi Ri, Tatkon, Pyinmana, Pobba Thi Ri and Lewe Townships, respectively (Fig. 1).

Table 1 Occurrence of GI helminth infestation in pigs in Nay Pyi Taw area (n = 500)
Full size table
Fig. 1
figure 1

EPG of the most common GI helminth species (Ascaris sp., Strongyle, Trichuris sp. and Strongyloides spp.) observed in five townships

Full size image

Distribution of GI helminth infestation among age groups, feeding systems, animal housing floors, hygiene conditions and associated factors

The mean EPG was 261.4 (ranging from 16.7 to 13,800) for overall helminth infestation in this study. The mean EPG (Mean ± SD) values in age groups were 1031 ± 2,023 (Median = 225) in weaners, 429 ± 1177 (Median = 90) in growers and 646 ± 1862 (Median = 143) in adults. Among the age groups, the weaner group showed the highest EPG when compared to the other age groups (P < 0.05) (Fig. 2). Although not significantly different, the highest intensity of helminth infection was found in pigs fed local feed (827 ± 1,946 EPG and median = 150), followed by pigs fed mixed feed (573 ± 1640 EPG and median = 1,640) and pigs fed commercial feed (306 ± 264 EPG and median = 330). In this study, a higher intensity of helminth infestation was found in farms with ground floors (799 ± 1,525 EPG and median = 150), and a lower intensity was found in farms with concrete floors (643 ± 1,836 EPG and median = 120). Furthermore, a higher intensity of helminth infestation was found in farms with no hygiene practices (799 ± 1,525 EPG and median = 150) than in farms with hygiene practices (643 ± 1,836 EPG and median = 120) (Fig. S2). According to the chi-square test, age was identified as the only factor associated (P < 0.05) with the occurrence of GI helminth infestations in pigs in this study (P = 0.026, χ2 = 7.306). Breed, anthelmintic treatment, floor type, feed type and hygienic condition of the farm were not associated with the occurrence of GI helminth infestations.

Fig. 2
figure 2

The intensity of helminth infestation (EPG) was higher (P < 0.05) in weaners than in growers and adults. The top and bottom horizontal lines of the boxplots represent the first and third quartiles of the data range, respectively. The medians are shown by middle horizontal lines, and the data range is shown by vertical lines, with outliers plotted as points. The notches of each boxplot are approximate 95% confidence intervals of medians

Full size image

Molecular identification of Ascaris suum and Trichuris suis

PCR was performed on 15 samples from each of the A. suum- and T. suis-positive samples by microscopic examination. Sequencing was performed on three samples with a targeted size of ~ 515 bp for the A suum-specific ITS1 PCR products. The obtained nucleotide sequences were all clustered together with A. suum sequences available in the database (Fig. 3), with being 99.6 to 100% identical to A. suum from pigs in Japan (AB576592, AB571302 and AB110022), China (HQ721825) and Thailand (MF358944), and one from humans in Lao PDR (MF358943). Three samples were used for sequencing of the T. suis-specific ITS2 PCR products with a targeted size of ~ 635 bp. The obtained nucleotide sequences were all clustered together with T. suis sequences available in the database (Fig. 4), showing 100% identity to the sequences of T. suis from pigs in Egypt (MN967779) and 99.5%, 99.1%, and 98.7% identities to T. suis sequences from pigs in China (MG656441, AM993015 and AM993007), Uganda (JN181800), and Spain (AJ249966), respectively (Table 2).

Fig. 3
figure 3

The phylogenetic relationship of partial ITS1 sequences of Ascaris suum detected in this study and reference sequences. The phylogenetic tree was constructed by the maximum likelihood method based on the Tamura-Nei model. The bold taxa represent the sequences obtained from the current study. The GenBank accession number of each sequence is given. Bootstrap values were computed independently for the purposes of 1000 replicates

Full size image
Fig. 4
figure 4

The phylogenetic relationship of partial ITS2 sequences of Trichuris suis detected in this study and reference sequences. The phylogenetic tree was constructed by the maximum likelihood method based on the Tamura-Nei model. The bold taxa represent the sequences obtained from the current study. The GenBank accession number of each sequence is given. Bootstrap values were computed independently for the purposes of 1000 replicates

Full size image
Table 2 Identification of ITS1 sequences of Ascaris suum or ITS2 sequences of Trichuris suis isolates from pigs in Myanmar using the NCBI BLAST search
Full size table

Discussion

Pigs are frequently affected by helminth parasites worldwide in all types of production systems. The findings of this study were the first to reveal the occurrence of GI helminths in pigs in Myanmar as well as the molecular identification of pig helminths. This study found a higher occurrence of 62.9% compared to 56.95% in Rajasthan district, India [16], and 37.5% in Aizawl district of Mizoram, India [17]. The differences in the infection rates were attributed to factors such as breed, geographical condition, climate, hygiene and faecal examination techniques [18]. The higher occurrence could be attributed to the fact that all of the farms enrolled in this study were smallholder farms with poor hygienic conditions. Many investigations stated that the spread of intestinal helminths in pigs raised using traditional systems was due to poor hygiene, poor nutrition and inadequate anthelmintic interventions [19, 20].

Among the helminths observed in this study, A. suum was the dominant species, with an occurrence of 34.8% and the highest mean EPG of 173. Although the prevalence varies greatly with the environment and production system, A. suum is the most or second most common intestinal species in farmed pigs globally [6). The higher prevalence of Ascaris sp. was also investigated in Denmark (88%) [21], the Netherlands (72.7%) [22], Nagaland, India (65.5%) [23], Vietnam (51%) [24], Nepal (45.0%) [25], South Africa (44.5%) [26], Burkina Faso (40%) [18], and China (36.7%) [27]. A lower prevalence was reported in India (11.1–33.3%) [28, 29], Kenya (28.7%) [19], and Rwanda (10.6%) [30].

According to Băieş et al. [31], A. suum is the most common endoparasite of swine in most countries and is one of the most economically important parasites. Thus, the highest occurrence of Ascaris observed in this study should be considered for worm control, although the sampled pigs were apparently healthy. Moreover, the zoonotic potential of Ascaris should also be considered because its occurrence (34.8%) in the present study was high. Among the ten helminth species observed, Strongyloides spp., Trichuris sp., Fasciolopsis spp., and Schistosoma spp. are zoonotic helminths with occurrences of 21.4%, 20%, 1%, and 1%, respectively. Therefore, it is crucial to manage the smallholder pig farms in the Nay Pyi Taw area to lessen the impact of helminth infestations by practicing proper deworming strategies.

Strongyle was observed as the second most prevalent nematode, with 29.6% occurrence. It was lower than the reports from Uganda, 89% [32], Kenya, 75% [33], Tanzania, 52% [34], Brazil, 46.6% [35] and Nepal, 32% [25], while lower than the findings from Ghana, 11% [36] and India, 11.10% [28]. Strongyloides spp. was observed in 21.4% of samples. Higher prevalence rates were reported from Bangladesh, 29.1% [20], Kenya, 26.6% [33], and Nepal, 23% [25], and lower prevalence rates were described from Indonesia, 19% [37], Tanzania, 15% [34] and India, 12.74% [38].

The 20.0% occurrence of T. suis noted in this study was in agreement with the report from Indonesia, 20.0% [37]. This occurrence was lower than the findings from Kenya, 78.0% [33], South Africa, 50.6% [26], the Netherlands, 37.5% [22], Nepal, 30% [25], India, 27.84% [28] and Japan, 24.8% [39] and higher than the findings from India, 17.3% [40] and Uganda, 17% [32]. The other observed helminths, Metastrongylus spp., Hyostrongylus spp., and Paragonimus spp. were found to have lower infection rates, with occurrence rates of 4.0%, 1.6%, and 1.0%, respectively.

According to the statistical analysis, the occurrence of GI helminth infestation was found to be associated with swine age in this study. Pigs < 3 months of age had an increased risk of infestation when compared to older pigs. The other hypothesized factors, breed, anthelmintic treatment, floor type, feed type and hygienic condition of pig farm, appeared to have no association with GI helminth infestation in this study. For the age factor in this study, a higher infestation rate was noted in younger pigs. Immunity to GI helminths might develop in older pigs and thus could be a reason for the higher occurrence in younger pigs. Foster and Elsheikha [41] also pointed out that the lower prevalence of GI parasites in adult pigs could be due to the enhanced resistance and susceptibility to reinfection governed by increased immunological memory.

In the studied townships, the GI helminths’ occurrences were different with the minimum (52.0%) in Lewe Township and maximum (85.0%) in Pyinmana Township. However, farm management practices, such as deworming, hygienic conditions, feed type and floor type, were not much different among the townships. The significant association (P < 0.05) could be explained by the fact that sampling in Pyinmana Township was conducted at the end of May when the rainy season starts in Myanmar. In the remaining four townships, sampling was performed in the months of December and January. Parasitic worm eggs and larval development prefer a moist environment, and thus, the parasitic contamination rate increased in pigs and the environment. In accordance with this fact, it could be considered that the highest occurrence was noted in Pyinmana Township.

Overall, sampled pigs excreted mostly low levels (< 100 EPG) and moderate levels (> 100–500 EPG) of GI helminths. Thus, it is clear that the sampled pigs seemed to be normal in clinical appearance without showing any abnormalities due to harbouring moderate levels of GI helminth infestations. However, de Araújo et al. [42] suggested that subclinical infections are important and can be frequent, resulting in loss of appetite, low weight gain, and reduced feed conversion in affected animals.

The eggs of most common worms that infect pigs and humans (A. suum and T. suis) are morphologically similar to other species of the same genera and thus the ITS1 and ITS2 sequences have frequently been used for distinguishing closely related species [43]. In this investigation, we identified and examined the sequences of the ITS1 region of A. suum and the ITS2 region of T. suis and compared them to previously published sequences of those infecting humans and pigs from various regions. Sequence analysis of A. suum identified from humans and pigs revealed that the isolates belong to the same clade as the sequences documented in Asian countries and Brazil. Additionally, sequences of T. suis identified from pigs and T. trichiura from humans also belong to the same clade. These findings suggest that humans and pig-derived A. suum exhibit genetic similarities with sequences reported from Asian countries and that T. suis likewise shares genetic similarities between humans and pigs. Therefore, this finding supported the findings of Sadaow et al. [44], who assumed that zoonotic cross-transmission of Ascaris roundworm between pigs and humans might exist in Thailand, Lao PDR, and Myanmar. Although the utilization of ITS1 and ITS2 sequences is beneficial in distinguishing between parasite species [11], their resolution power is comparatively lower than that of other genome-wide identification techniques.

Conclusion

The overall GI parasite infestation rate in pigs was 69.2%, with 31.0% mixed infections, and five species of zoonotic helminths were found in the present study. Furthermore, age was a major factor related to GI helminth infestation in smallholder backyard pigs in the Nay Pyi Taw area. The two zoonotic helminths, A. suum and T. suis, were molecularly identified for the first time. It is important to extend the information among the farmers to be aware of the importance of prevention of zoonotic parasites for public health by practicing regular deworming, proper use of anthelmintics and keeping hygienic conditions in their pig farms.

Methods

Sample size and sample collection

The study area, sample size and sampling period were reported in our previous study [15]. In brief, a cross-sectional study was conducted in five townships within Nay Pyi Taw, located between latitude 19° 45′ N and longitude 96° 06′ E, between December 2020 and May 2021. Samples were collected mostly in suburban and rural areas within townships, which were home to a large number of pig farms. A total of 500 fresh faecal samples were obtained, with 100 samples from each township. Upper parts of freshly dropped faeces on the ground of individual pigs were collected, placed into individual zip lock bags, labelled, put in an ice box, and brought to the Laboratory of Department of Pharmacology and Parasitology, University of Veterinary Science. During sampling, information regarding the age, sex, breed, type of feed, floor type and hygienic condition of the pig farm, as well as anthelmintic usage, were all recorded. The pig breeds included local and DYL (a cross breed of Duroc, Yorkshire, and Landrace). According to Esrony et al. [45], animals were classified as weaners (5–12 weeks), growers (> 12 weeks to 24 weeks), and adults (> 24 weeks).

Laboratory analysis for parasite eggs

The samples were examined for helminth parasites in the laboratory using the faecal flotation and sedimentation methods as described by Zajac and Conboy [46]. On the basis of morphological characteristics described by Taylor et al. [47], parasite species were identified. The McMaster egg counting method was used to calculate the number of eggs per gram (EPG) of faeces [46].

DNA extraction and PCR

DNA extraction was performed on faecal samples that were positive for A. suum or T. suis eggs by fecal examination. According to the manufacturer’s instructions, DNA was extracted using the Power Fecal DNA Isolation kit (MO BIO Laboratories, USA). The extracted DNA samples were eluted in 200 μl elution buffer and kept at -80 °C. A NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, MA, USA) was used to determine the DNA concentration. To amplify the ITS1 region of A. suum, a primer set consisting of the forward primer F2662 (5'-GCAAAAGTCGTAACAAGGT-3') and the reverse primer R3214 (5'- CTGCAATTCGCACTATTTATCG-3') was employed [11]. For the amplification of the ITS2 region of T. suis, a primer set of the forward primer ITS2_tt_F2 (5'-GCTCGTAGGTCGTTGAAG-3') and the reverse primer ITS2_tt_R2_new1 (5'-GGGCAGCTTCCGTACT-3') was used [12]. Thermal cycling began with denaturation at 94 °C for 1 min, then 40 cycles at 98 °C for 10 s, 52 °C (for A. suum) and 54 °C (for T. suis) for 15 s, 68 °C for 1 min, and a final extension at 68 °C for 5 min. DNA samples from previously collected A. suum and T. suis specimens were used as positive controls, with molecular grade deionised water serving as negative controls. PCR products were examined using 2% Tris–acetate-EDTA (TAE) agarose gel electrophoresis after staining with RedSafe Nucleic Acid Staining Solution (iNtRON Biotechnology Inc., Seongnam, Korea).

Sequencing and phylogenetic analysis

Following the manufacturer's instructions, DNA fragments obtained from the PCR were excised from the gel and purified using a NucleoSpin® Gel and PCR Clean-up Kit (MACHEREY–NAGEL, Düren, Germany) and submitted for direct sequencing on an Applied Biosystems 3130 Genetic Analyzer with a BigDye v3.1 Terminator cycle sequencing kit (Applied Biosystems, Inc., Carlsbad, CA, USA). ATGC version 7 (GENETYX Corporation, Tokyo, Japan) was used for multiple sequence alignment. The phylogenetic analysis was conducted using the maximum likelihood (ML) method in MEGA X with Tamura-Nei model [48]. The bootstrap analysis was performed with 1000 replicates per tree. The obtained sequences (OQ825946-OQ825951) were compared to those in the NCBI nucleotide database (http://www.ncbi.nlm.nih.gov/nuccore/).

Statistical analysis

All data were entered into Microsoft Excel 2013 and analysed using the Statistical Package for Social Science (SPSS) version 20.0. The association between the occurrence of GI helminths and the hypothesized factors of age, sex, breed of pigs, anthelmintic treatment, floor type, feed type, and hygienic condition of the pig farm was analysed using a Pearson’s Chi-square test at the P < 0.05 level of significance. The boxplots were explored by the ggplot package using the R language platform [49, 50].

Availability of data and materials

No datasets were generated or analysed during the current study.

References

  1. Alarcon P, Rushton J, Nathues H, Wieland B. Economic efficiency analysis of different strategies to control post-weaning multi-systemic wasting syndrome and porcine circovirus type 2 subclinical infection in 3-weekly batch system farms. Prev Vet Med. 2013;110:103–18.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sowemimo O, Asaolu S, Adegoke F, Ayanniyi O. Epidemiological survey of gastrointestinal parasites of pigs in Ibadan. Southwest Nigeria J Public Health Epidemiol. 2012;4:294–8.

    Article  Google Scholar 

  3. Ismail HA, Jeon HK, Yu YM, Do C, Lee YH. Intestinal parasite infections in pigs and beef cattle in rural areas of Chungcheongnam-do. Korea Korean J Parasitol. 2010;48:347–9.

    Article  PubMed  Google Scholar 

  4. Holland C, Boes J. Distribution and predisposition: people and pigs. In: Holland CV, Kennedy MW, editors. The geohelminths: Ascaris, Trichuris and hookworm. World class parasite. Boston: Kluwer Academic Publishers; 2002. p. 1–24 vol. 2.

    Chapter  Google Scholar 

  5. Nejsum P, Betson M, Bendall RP, Thamsborg SM, Stothard JR. Assessing the zoonotic potential of Ascaris suum and Trichuris suis: looking to the future from an analysis of the past. J Helminthol. 2012;86:148–55.

    Article  CAS  PubMed  Google Scholar 

  6. Thamsborg SM, Nejsum P, Mejer H. Impact of Ascaris suum in livestock. In: Holland C, editor. Ascaris the neglected parasite. London: Academic Press; 2013.

    Google Scholar 

  7. Betson M, Nejsum P, Stothard JR. From the twig tips to the deeper branches: new insights into evolutionary history and phylogeography of Ascaris. In: Holland C, editor. Ascaris the neglected parasite. London: Academic Press; 2013.

    Google Scholar 

  8. Miller LA, Colby K, Manning SE, Hoenig D, McEvoy E, Montgomery S, Mathison B, de Almeida M, Bishop H, Dasilva A, Sears S. Ascariasis in humans and pigs on small-scale farms, Maine, USA, 2010–2013. Emerg Infect Dis. 2015;21:332–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Li YZ, Hernandez AD, Major S, Carr R. Occurrence of intestinal parasites and its impact on growth performance and carcass traits of pigs raised under near-organic conditions. Front Vet Sci. 2022;9:911561.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Dolezalova J, Obornik M, Hajduskova E, Jirku M, Petrzelkova KJ, Bolechova P, Cutillas C, Callejon R, Jozef J, Berankova Z, Modry D. How many species of whipworms do we share? Whipworms from man and other primates form two phylogenetic lineages. Folia Parasitol (Praha). 2015;2015(62):063.

    Google Scholar 

  11. Ishiwata K, Shinohara A, Yagi K, Horii Y, Tsuchiya K, Nawa Y. Identification of tissue-embedded ascarid larvae by ribosomal DNA sequencing. Parasitol Res. 2004;92:50–2.

    Article  PubMed  Google Scholar 

  12. Phosuk I, Sanpool O, Thanchomnang T, Sadaow L, Rodpai R, Anamnart W, Janwan P, Wijit A, Laymanivong S, Pa Aung WP, Intapan PM, Maleewong W. Molecular identification of Trichuris suis and Trichuris trichiura eggs in human populations from Thailand, Lao PDR, and Myanmar. Am J Trop Med Hyg. 2018;98:39–44.

    Article  PubMed  Google Scholar 

  13. FAOSTAT: https://www.fao.org/faostat/en/#data. Accessed 20 Apr 2023.

  14. Thaw YN, Khaing TA, Linn KS, Wai SS, Htun LL, Bawm S. The first seroepidemiological study on Toxoplasma gondii in backyard pigs in Myanmar. Parasite Epidemiol Control. 2021;14:e00216.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Bawm S, Chel HM, Khaing Y, Hmoon MM, Thein SS, Win SY, Soe NC, Thaw YN, Hayashi N, Win MM, Htun LL, Nonaka N, Katakura K, Nakao R. The strong influence of management factors on coccidian infections in smallholder pig farms and the first molecular identification of Cystoisospora suis in Myanmar. Parasite. 2022;29:1.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Yadav S, Gupta A, Choudhary P, Pilania PK, Joshi SP. Prevalence of gastrointestinal helminths and assessment of associated risk factors in pigs from Rajasthan districts. India J Entomol Zool Stud. 2021;9:1418–23.

    Google Scholar 

  17. Borthakur SK, Rahmani S, Sarma K. Prevalence of gastrointestinal helminths in pigs in Aizawl. J Vet Parasitol. 2007;21:173–4.

    Google Scholar 

  18. Tamboura HH, Banga-Mboko H, Maes D, Youssao I, Traore A, Bayala B, Dembele MA. Prevalence of common gastro-intestinal nematode parasites in scavenging pigs of different ages and sexes in Eastern Centre Province. Burkina Faso Onderstepoort J Vet Res. 2006;73:53–60.

    CAS  PubMed  Google Scholar 

  19. Nganga CJ, Karanja DN, Mutune MN. The prevalence of gastrointestinal helminth infections in pigs in Kenya. Trop Anim Health Prod. 2008;40:331–4.

    Article  CAS  PubMed  Google Scholar 

  20. Dey TR, Dey AR, Begum N, Akther S, Barmon BC. Prevalence of endo parasites of pig at Mymensingh. Bangladesh J Agric Vet Sci. 2014;7:31–8.

    Google Scholar 

  21. Roepstorff A, Jorsal SE. Prevalence of helminth infections in swine in Denmark. Vet Parasitol. 1989;33:231–9.

    Article  CAS  PubMed  Google Scholar 

  22. Eijck IA, Borgsteede FH. A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in the Netherlands. Vet Res Commun. 2005;29:407–14.

    Article  CAS  PubMed  Google Scholar 

  23. Laha R, Das M, Goswami A, Sailo B, Sharma BK, Gangmei D, Puii LH, Patra MK, Das RK, Sharma A, Ngullie E. Prevalence of gastrointestinal parasitic infections in pigs of north eastern region of India. Indian J Hill Farming. 2014;27:64–7.

    Google Scholar 

  24. Yoshihara S, Hung NP, Hung NH, Loc CB. Helminths and helminthiosis of pigs in the Mekong Delta, Vietnam with special reference to Ascariosis and Fasciolopsis buski infection. JARQ. 1999;33:193–9.

    Google Scholar 

  25. Adhikari RB, Dhakal MA, Thapa S, Ghimire TR. Gastrointestinal parasites of indigenous pigs (Sus domesticus) in south-central Nepal. Vet Med Sci. 2021;7:1820–30.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nwafor IC, Roberts H, Fourie P. Prevalence of gastrointestinal helminths and parasites in smallholder pigs reared in the central Free State Province. Onderstepoort J Vet Res. 2019;86:e1–8.

    Article  PubMed  Google Scholar 

  27. Boes J, Willingham AL 3rd, Fuhui S, Xuguang H, Eriksen L, Nansen P, Stewart TB. Prevalence and distribution of pig helminths in the Dongting Lake Region (Hunan Province) of the People’s Republic of China. J Helminthol. 2000;74:45–52.

    Article  CAS  PubMed  Google Scholar 

  28. Patra G, Al-Abodi HR, Sahara A, Ghosh S, Borthakur SK, Polley S, Behera P, Deka A. Prevalence of parasitic fauna of pigs in North-Eastern region of India. Biol Rhythm Res. 2019;51:1298–315.

    Article  Google Scholar 

  29. Sharma D, Singh NK, Singh H, Rath SS. Copro-prevalence and risk factor assessment of gastrointestinal parasitism in Indian domestic pigs. Helminthologia. 2020;57:28–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tumusiime M, Ntampaka P, Niragire F, Sindikubwabo T, Habineza F. Prevalence of swine gastrointestinal parasites in Nyagatare District Rwanda. J Parasitol Res. 2020;2020:8814136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Băieş MH, Boros Z, Gherman CM, Spînu M, Mathe A, Pataky S, Lefkaditis M, Cozma V. Prevalence of swine gastrointestinal parasites in two free-range farms from Nord-west region of Romania. Pathogens. 2022;11(9):954.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nissen S, Poulsen IH, Nejsum P, Olsen A, Roepstorff A, Rubaire-Akiiki C, Thamsborg SM. Prevalence of gastrointestinal nematodes in growing pigs in Kabale District in Uganda. Trop Anim Health Prod. 2011;43:567–72.

    Article  PubMed  Google Scholar 

  33. Obonyo FO, Maingi N, Githigia SM, Nganga CJ. Farming practices and risk factors for transmission of helminths of free range pigs in Homabay District, Kenya. Livest Res Rural Dev. 2013;25:36.

  34. Nonga HE, Paulo N. Prevalence and intensity of gastrointestinal parasites in slaughter pigs at Sanawari slaughter slab in Arusha, Tanzania. Livest Res Rural Dev. 2015;27:10.

  35. Barbosa AS, Bastos OM, Dib LV, Siqueira MPD, Cardozo ML, Ferreira LC, Chaves WT, Fonseca ABM, Uchôa C, Amendoeira MRR. Gastrointestinal parasites of swine raised in different management systems in the State of Rio de Janeiro. Brazil Pesqui Vet Bras. 2015;35:941–6.

    Article  Google Scholar 

  36. Atawalna J, Attoh-Kotoku V, Folitse R, Amenakpor C. Prevalence of gastrointestinal parasites among pigs in the Ejisu Municipality of Ghana. Sch J Agric Vet Sci. 2016;3:33–6.

    Google Scholar 

  37. Widisuputri NKA, Suwanti LT, Plumeriastuti H. A Survey for zoonotic and other gastrointestinal parasites in pig in Bali Province. Indonesia Indonesian J Trop Infect Dis. 2020;8:54–65.

    Google Scholar 

  38. Petersen HH, Jianmin W, Katakam KK, Mejer H, Thamsborg SM, Dalsgaard A, Olsen A, Enemark HL. Cryptosporidium and Giardia in Danish organic pig farms: Seasonal and age- related variation in prevalence, infection intensity and species/genotypes. Vet Parasitol. 2015;214:29–39.

    Article  PubMed  Google Scholar 

  39. Matsubayashi M, Kita T, Narushima T, Kimata I, Tani H, Sasai K, Baba E. Coprological survey of parasitic infections in pigs and cattle in slaughterhouse in Osaka. Japan J Vet Med Sci. 2009;71:1079–83.

    Article  PubMed  Google Scholar 

  40. Krishna Murthy CM, Ananda KJ, Adeppa J, Satheesha MG. Studies on gastrointestinal parasites of pigs in Shimoga region of Karnataka. J Parasit Dis. 2016;40:885–9.

    Article  CAS  PubMed  Google Scholar 

  41. Foster N, Elsheikha HM. The immune response to parasitic helminths of veterinary importance and its potential manipulation for future vaccine control strategies. Parasitol Res. 2012;110:1587–99.

    Article  PubMed  Google Scholar 

  42. de Araújo HG, da Silva JT, Álvares FBV, Ferreira LC, Azevedo SS, Vilela VLR. Prevalence and risk factors associated with swine gastrointestinal nematodes and coccidia in the semi-arid region of northeastern Brazil. Trop Anim Health Prod. 2020;52:379–85.

    Article  PubMed  Google Scholar 

  43. Callejón R, Nadler S, De Rojas M, Zurita A, Petrášová J, Cutillas C. Molecular characterization and phylogeny of whipworm nematodes inferred from DNA sequences of cox1 mtDNA and 18S rDNA. Parasitol Res. 2013;112:3933–49.

    Article  PubMed  Google Scholar 

  44. Sadaow L, Sanpool O, Phosuk I, Rodpai R, Thanchomnang T, Wijit A, Anamnart W, Laymanivong S, Aung WPP, Janwan P, Maleewong W, Intapan PM. Molecular identification of Ascaris lumbricoides and Ascaris suum recovered from humans and pigs in Thailand, Lao PDR, and Myanmar. Parasitol Res. 2018;117:2427–36.

    Article  PubMed  Google Scholar 

  45. Esrony K, Kambarage DM, Mtambo MMA, Muhairwa AP, Kusiluka LJM. Intestinal protozoan parasites of pigs reared under different management systems in Morogoro. Tanzania J Appl Anim Res. 1996;10:25–31.

    Article  Google Scholar 

  46. Zajac AM, Comboy GA. Fecal examination for the diagnosis of parasitism. In: Veterinary Clinical Parasitology. 8th ed. Oxford: Willey Blackwell Science Ltd; 2012. p. 22–9.

    Google Scholar 

  47. Taylor MA, Coop RL, Wall RL. Parasites of dogs. In: Veterinary Parasitology. 4th ed. Oxford: Blackwell Publishing; 2016. p. 599–659.

    Google Scholar 

  48. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wickham H. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag; 2016.

    Book  Google Scholar 

  50. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2020. https://www.R-project.org/.

Download references

Acknowledgements

We would like to express our gratitude to the Township Officers and Deputy Officers of LBVD, as well as farm owners, for their assistance in collecting samples. We also thank the final-year DVM students of the graduation thesis group (2020) from UVS, Myanmar, for helping with sample collection.

Funding

This study was partly supported by a research grant (2020–2021) from the Ministry of Agriculture, Livestock and Irrigation, Myanmar.

Author information

Author notes

  1. Saw Bawm, Lat Lat Htun and Hla Myet Chel contributed equally to this work.

Authors and Affiliations

  1. Department of Pharmacology and Parasitology, University of Veterinary Science, Yezin, Nay Pyi Taw, 15013, Myanmar

    Saw Bawm, Lat Lat Htun, Hla Myet Chel, Myint Myint Hmoon, Su Su Thein, Shwe Yee Win, Nyein Chan Soe & Yu Nandi Thaw

  2. Department of Livestock and Aquaculture Research, Yezin, Nay Pyi Taw, 15013, Myanmar

    Saw Bawm

  3. Department of International Relations and Information Technology, University of Veterinary Science, Yezin, Nay Pyi Taw, 15013, Myanmar

    Yadanar Khaing

  4. Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, 060-0818, Japan

    Naoki Hayashi, Nariaki Nonaka, Ken Katakura & Ryo Nakao

  5. Rector Office, University of Veterinary Science, Yezin, Nay Pyi Taw 15013, Myanmar

    Mar Mar Win

Authors
  1. Saw Bawm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lat Lat Htun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hla Myet Chel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yadanar Khaing
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Myint Myint Hmoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Su Su Thein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shwe Yee Win
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nyein Chan Soe
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yu Nandi Thaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Naoki Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mar Mar Win
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nariaki Nonaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ken Katakura
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Ryo Nakao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, SB, LLH, and HMC; methodology, SB, LLH, HMC, MMH, and RN; software, SB, RN and NH; validation, SB, LLH, HMC, MMH, RN, and KK; formal analysis, SB, LLH, HMC, MMH and NH; investigation SB, LLH, HMC, MMH, YK, SST, SYW, NCS, YNT; resources, SB and LLH; data curation, SB, LLH, HMC, and RN; writing-original draft preparation, SB, LLH, and HMC; writing-review and editing, MMW, RN, NN, and KK; visualization, SB; supervision, LLH, RN and KK; funding acquisition, SB, and LLH. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Saw Bawm.

Ethics declarations

Ethics approval and consent to participate

The study was reviewed and approved by the Ethics Review Committee, University of Veterinary Science, Ministry of Agriculture, Livestock and Irrigation, Myanmar (Approval number: ERC/Recom/2020(7) issued on 28 February 2020). The relevant pig farms were informed of the implementation of this study, and consent was obtained from the owner for the participation of the animal in the study. The pig’s faecal samples were provided following owner consent. All methods were performed in accordance with relevant guidelines and regulations.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Supplementary Information

Additional file 1: Fig. S1. 

(A-I). Eggs of Ascaris suum (A), Oesophagostomum spp. (B), Strongyloides spp. (C), Trichuris suis (D), Metastrongylus spp. (E), Hyostrongylus spp. (F), Fasciolopsis spp. (G), Paragonimus spp. (H), and Schistosoma spp. (I) detected in this study.

Additional file 2:

Fig. S2. (A), (B) and (C). Intensity of helminth infestation (EPG) was lower in pigs fed with commercial feed than local and mixed feed (A), higher in pigs reared on ground floor (B) and farms with no hygienic practices (C). The top and bottom horizontal lines of the boxplots represent the first and third quartiles of the data range, respectively, the medians are shown by middle horizontal lines, and the data range is shown by vertical lines, with outliers plotted as points. The notches of each boxplot are approximate 95% confidence intervals of medians.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bawm, S., Htun, L.L., Chel, H.M. et al. A survey of gastrointestinal helminth infestation in smallholder backyard pigs and the first molecular identification of the two zoonotic helminths Ascaris suum and Trichuris suis in Myanmar. BMC Vet Res 20, 139 (2024). https://doi.org/10.1186/s12917-024-03998-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-024-03998-w

Keywords

BMC Veterinary Research

ISSN: 1746-6148

Contact us