Open Access
Research (Published online: 09-02-2019)
6. Coinfection of diarrheagenic bacterial and viral pathogens in piglets of Northeast region of India
Hosterson Kylla, Tapan K. Dutta, Parimal Roychoudhury and Prasant K. Subudhi
Veterinary World, 12(2): 224-230

Hosterson Kylla: Department of A.H and Veterinary, Disease Investigation Office, Meghalaya, Shillong, India.
Tapan K. Dutta: Department of Veterinary Microbiology, Central Agricultural University, Aizawl, Mizoram, India.
Parimal Roychoudhury: Department of Veterinary Microbiology, Central Agricultural University, Aizawl, Mizoram, India.
Prasant K. Subudhi: Department of Veterinary Microbiology, Central Agricultural University, Aizawl, Mizoram, India.

doi: 10.14202/vetworld.2019.224-230

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Article history: Received: 15-10-2018, Accepted: 26-12-2018, Published online: 09-02-2019

Corresponding author: Hosterson Kylla


Citation: Kylla H, Dutta TK, Roychoudhury P, Subudhi PK (2019) Coinfection of diarrheagenic bacterial and viral pathogens in piglets of Northeast region of India, Veterinary World, 12(2): 224-230.

Aim: This study aimed to study the prevalence of the coinfection of enteric bacterial and viral pathogens, namely Escherichia coli, Salmonella, Rotavirus, and Picobirnavirus from fecal samples of pre-weaned piglets in Northeast region of India.

Materials and Methods: A total of 457 fresh fecal samples were collected from piglets under 9 weeks old during 2013-2015 from organized (n=225) and unorganized (n=232) farms of Manipur, Meghalaya, Mizoram, and Nagaland. Samples were collected from diarrheic (n =339) and non-diarrheic (n=118) piglets including local indigenous (n=130) and crossbreed (n=327) piglets in different seasons during the study period. The samples were processed for the isolation of E. coli and Salmonella and detection of their putative virulence genes by polymerase chain reaction (PCR). Samples were also processed for the detection of Rotavirus and Picobirnavirus by RNA-polyacrylamide agarose gel electrophoresis and reverse transcriptase-PCR (RT-PCR).

Results: A total of 11 (2.40%) samples were found positive for two or more coinfecting enteric bacterial and viral pathogens. All the 11 positive fecal samples were recovered from diarrheic piglets. Salmonella Typhimurium (enterotoxin, stn gene) and Picobirnavirus genogroup 1 were found to be more frequent as coinfecting agents. Coinfection was recorded higher in unorganized (3.87%) compared to organized farm (0.88%). Again, higher detection was recorded in crossbreed (2.75%) than local indigenous piglets (1.53%). The occurrence of coinfection was found to be more common during summer (4.68%) followed by winter (2.27%) season.

Conclusion: The present study highlighted the significance of E. coli, Salmonella, Rotavirus, and Picobirnavirus as important diarrheagenic pathogens causing coinfection in piglets in Northeast region of India. Probably, this is the first systematic study of the coinfection of four important diarrheagenic bacterial and viral agents associated with piglet diarrhea in India.

Keywords: coinfection, Escherichia coli, Picobirnavirus, piglets, Rotavirus, Salmonella.


1. Livestock Census. (2012) Department of Animal Husbandry and Dairying, Ministry of Agriculture. Government of India, New Delhi.

2. Kongsted, H., Stege, H., Toft, N. and Nielsen, J.P. (2014) The effect of new neonatal porcine diarrhea syndrome (NNPDS) on average daily gain and mortality in four Danish pig herds. BMC Vet. Res., 10(1): 90. [Crossref] [PubMed] [PMC]

3. Klein, E.Y., Monteforte, B., Gupta, A., Jiang, W., May, L., Hsieh, Y.H. and Dugas, A. (2016) The frequency of influenza and bacterial coinfection: A systematic review and meta-analysis. Influenza Other Respir. Viruses, 10(5): 394-403. [Crossref] [PubMed] [PMC]

4. Martin-Loeches, I., van Someren Greve, F. and Schultz, M.J. (2017) Bacterial pneumonia as an influenza complication. Curr. Opin. Infect. Dis., 30(2): 201-207. [Crossref] [PubMed]

5. Seppala, O., Karvonen, A., Rellstab, C., Louhi, K.R. and Jokela, J. (2012) Reciprocal interaction matrix reveals complex genetic and dose-dependent specificity among co-infecting parasites. Am. Nat., 180(3): 306-315. [Crossref] [PubMed]

6. Susi, H., Barres, B., Vale, P.F. and Laine, A.L. (2015) Co-infection alters population dynamics of infectious disease. Nat. Commun., 6: 5975. [Crossref] [PubMed] [PMC]

7. O'Ryan, M., Prado, V. and Pickering, L.K. (2005) A millennium update on pediatric diarrheal illness in the developing world. Semin. Pediatr. Infect. Dis., 16(2): 125-136. [Crossref]

8. Cox, F.E. (2001) Concomitant infections, parasites and immune responses. Parasitology, 122: S23-38. [Crossref]

9. Read, A.F. and Taylor, L.H. (2001) The ecology of genetically diverse infections. Science, 292(5519): 1099-1102. [Crossref]

10. Li, X.X. and Zhou, X.N. (2013) Co-infection of tuberculosis and parasitic diseases in humans: A systematic review. Parasit. Vectors, 6(1): 79. [Crossref]

11. Grimprel, E., Rodrigo, C. and Desselberger, U. (2008) Rotavirus disease: Impact of coinfections. Pediatr. Infect. Dis. J., 27(1): S3-S10. [Crossref]

12. Bonkoungou, I.J., Haukka, K., Osterblad, M., Hakanen, A.J., Traore, A.S., Barro, N. and Siitonen, A. (2013) Bacterial and viral etiology of childhood diarrhea in Ouagadougou, Burkina Faso. BMC. Pediatr., 13(1): 36. [Crossref]

13. Bhavnani, D., Goldstick, J.E., Cevallos, W., Trueba, G. and Eisenberg, J.N. (2012) Synergistic effects between Rotavirus and coinfecting pathogens on diarrheal disease: Evidence from a community-based study in northwestern Ecuador. Am. J. Epidemiol., 176(5): 387-395. [Crossref] [PubMed] [PMC]

14. Holland, R.E. (1990) Some infectious causes of diarrhea in young farm animals. Clin. Microbiol. Rev., 3(4): 345-375. [Crossref]

15. Black, R.E., Cousens, S., Johnson, H.L., Lawn, J.E., Rudan, I., Bassani, D.G., Jha, P., Campbell, H., Walker, C.F., Cibulskis, R., Eisele, T., Liu, L. and Mathers, C. (2010) Global, regional, and national causes of child mortality in 2008: A systematic analysis. Lancet, 375(9730): 1969-1987. [Crossref]

16. Das, J.K., Salam, R.A. and Bhutta, Z.A. (2014) Global burden of childhood diarrhea and interventions. Curr. Opin. Infect. Dis., 27(5): 451-458. [Crossref] [PubMed]

17. Snodgrass, D.R., Terzolo, H.R., Campbell, D., Sherwood, I., Menzies, J.D. and Synge, B.A. (1986) Aetiology of diarrhea in young calves. Vet. Rec., 119(2): 31-34. [Crossref]

18. Zimmerman, J.J., Karriker, L.A., Ramirez, A., Schwartz, K.J. and Stevenson, G.W. (2012) Diseases of Swine. 10th ed. Wiley, New York.

19. Ewing, W.H. (1986) Edward and Ewing's Identification of Enterobacteriaceae. 4th ed. Elsevier, New York. p1-536.

20. World Health Organization. (2009) Manual of Rotavirus Detection and Characterization Methods. World Health Organization Manual, Geneva, Switzerland.

21. Herring, A.J., Inglis, N.F., Ojeh, C.K., Snodgrass, D.R. and Menzies, J.D. (1982) Rapid diagnosis of Rotavirus infection by direct detection of viral nucleic acid in silver-stained polyacrylamide gels. J. Clin. Microbiol., 16(3): 473-477. [PubMed] [PMC]

22. Kylla, H. (2015) Detection and Molecular Characterization of Enteric Bacterial and Viral Pathogens of Piglets in North Eastern States (Manipur, Meghalaya, Mizoram and Nagaland) of India. Ph. D Thesis Submitted to the Central Agricultural University, Imphal, Manipur (India).

23. Gabbay, Y.B., Borges, A.A., Oliveria, D.S., Linhares, A.C., Mascarenhas, J.D., Barardi, C.R., Simoes, C.M., Wang, Y., Glass, R.I. and Jiang, B. (2008) Evidence for zoonotic transmission of group C Rotaviruses among children in Belem, Brazil. J. Med. Virol., 80(9): 1666-1674. [Crossref] [PubMed]

24. Kylla, H., Dutta., T.K., Roychoudhury, P., Malik., Y.S., Mandakini, R. and Subudhi, P.K. (2017) Prevalence and molecular characterization of porcine Picobirnavirus in piglets of North East region of India. Trop. Anim. Health. Prod., 49(2): 417-422. [Crossref] [PubMed]

25. Smits, S.L., Poon, L.M.M., Van Leeuwen, M., Lau, P.N., Parera, H.K.K., Peiris, J.S.M., Simon, J.H. and Osterhaus, A.D.M. (2011) Genogroup I and II Picobirnaviruses in respiratory tracts of pigs. Emerg. Infect. Dis., 17(12): 2328-2330. [Crossref] [PubMed] [PMC]

26. Paton, J.C. and Paton, A.W. (1998) Pathogenesis and diagnosis of Shiga-toxin producing Escherichia coli infections. Clin. Microbiol. Rev., 11(3): 450-479. [Crossref]

27. Prager, R., Fruth, A. and Tschape, H. (1995) Salmonella enterotoxin (stn) gene is prevalent among strains of Salmonella Enterica but not among Salmonella Bongori and other Enterobacteriaceae. FEMS Immunol. Med. Microbiol., 12(1): 47-50. [Crossref] [PubMed]

28. Galan, J.E., Ginocchio, C., Costeas, P. (1992) Molecular and functional characterization of the Salmonella gene invA: homology of invA to members of a new protein family. J. Bacteriol., 174(13): 4338-4349. [Crossref]

29. Rahman, H., Prager, R. and Tschape, H. (2000) Occurrence of sef and pef genes among different serovars of Salmonella. Ind. J. Med. Res., 111: 40-42. [PubMed]

30. Mesonero-Escuredo, S., Strutzberg-Minder, K., Casanovas, C. and Segales, J. (2018) Viral and bacterial investigations on the etiology of recurrent pig neonatal diarrhea cases in Spain. Porcine. Health. Manag., 4: 5.

31. Katsuda, K., Kohmoto, M., Kawashima, K. and Tsunemitsu, H. (2006) Frequency of enteropathogen detection in suckling and weaned pigs with diarrhea in Japan. J. Vet. Diagn. Investig., 18(4): 350-354. [Crossref] [PubMed]

32. Zhang, S.X., Zhou, Y.M., Xu, W., Tian, L.G., Chen, J.X., Chen, S.H., Dang, Z.S., Gu, W.P., Yin, J.W., Serrano, E. and Zhou, X.N. (2016) Impact of co-infections with enteric pathogens on children suffering from acute diarrhea in southwest China. Infect. Dis. Poverty, 5(1): 64. [Crossref]

33. Fairbrother, J.M. and Gyles, C.L. (2012) Colibacillosis. In: Zimmerman, J., Karriker, L.A., Ramirez, A., Schwartz, K.J. and Stevenson, G.W. Diseases of Swine. 10th ed. Wiley-Blackwell, Chichester. p723-749.

34. Pedersen, L.J., Malmkvist, J., Kammersgaard, T. and Jorgensen, E. (2013) Avoiding hypothermia in neonatal pigs: Effect of duration of floor heating at different room temperatures. J. Anim. Sci., 91(1): 425-432. [Crossref] [PubMed]

35. Martineau, G.P., Vaillancourt, J.P. and Broes, A. (1995) Principal neonatal diseases. In: Varley, M.A., editor. The Neonatal Pig Development and Survival. CAB International, Wallingford. p239-264.

36. Malik, Y.S., Kumar, N., Sharma, K., Dhama, K., Shabbir, M.Z., Ganesh, B., Kobayashi, N. and Banyai, K. (2014) Epidemiology, phylogeny and evolution of emerging enteric Picobirnaviruses of animal origin and their relationship to human strains. Biomed. Res. Int., 2014: 1-13. [Crossref] [PubMed] [PMC]

37. Banyai, K., Jakab, F., Reuter, G., Bene, J., Melegh, B. and Szucs, G. (2003) Sequence heterogeneity among human Picobirnaviruses detected in a gastroenteritis outbreak. Arch. Virol., 148(1): 2281-2291. [Crossref] [PubMed]

38. Vlasova, A.N., Amimo, J.O. and Saif, L.J. (2017) Porcine Rotaviruses: Epidemiology, immune responses and control strategies. Viruses, 9(3): 48. [Crossref]

39. Theuns, S., Vyt, P., Desmarets, L.M.B., Roukaerts, I.D.M., Heylen, E., Zeller, M., Matthijnssens, J. and Nauwynck, H.J. (2016) Presence and characterization of pig group A and C Rotaviruses in feces of Belgian diarrheic suckling piglets. Virus Res., 213(1): 172-183. [Crossref] [PubMed]

40. Marthaler, D., Homwong, N., Rossow, K., Culhane, M., Goyal, S., Collins, J., Matthijnssens, J. and Ciarlet, M. (2014) Rapid detection and high occurrence of porcine rotavirus A, B, and C by RT-qPCR in diagnostic samples. J. Virol. Methods, 209: 30-34. [Crossref] [PubMed]

41. Kylla, H., Dutta, T.K., Roychoudhury, P., Mandakini, R. and Subudhi, P.K. (2018) Detection and characterization of genogroup 5 Rotavirus associated with piglet diarrhea in the North East region of India. Vet. Arch., 88(4): 453-466. [Crossref]

42. Kim, Y., Chang, K.O., Straw, B. and Saif, L.J. (1999) Characterization of group C Rotaviruses associated with diarrhea outbreak in feeder pigs. J. Clin. Microbiol., 37(5): 1484-1488. [PubMed] [PMC]

43. Martella, V., Banyai, K. and Lorusso, E. (2007) Prevalence of group C Rotaviruses in weaning and post-weaning pigs with enteritis. Vet. Microbiol., 123(1-3): 26-33. [Crossref] [PubMed]

44. Chan, G., Farzan, A., DeLay, J., McEwen, B., Prescott, J.F. and Friendship, R.M. (2013) A retrospective study on the etiological diagnoses of diarrhea in neonatal piglets in Ontario, Canada, between 2001 and 2010. Can. J. Vet. Res., 77(4): 254-260. [PubMed] [PMC]

45. Nataro, J.P. and Kaper, J.B. (1998) Diarrhoeagenic Escherichia coli. Clin. Microbiol. Rev., 11(2): 142-201. [Crossref]

46. Kylla, H., Dutta, T.K. and Kawlni, L. (2017) Prevalence and molecular characterization of shigatoxigenic Escherichia coli in piglets of North East region of India. Int. J. Trop. Dis. Health, 27(2): 1-8. [Crossref]

47. Malkawi, H.I. and Gharaibeh, R. (2004) Rapid and simultaneous identification of two Salmonella Enterica serotypes Enteritidis and Typhimurium from chicken and meat product by multiplex PCR. Biotechnology, 3(1): 44-48. [Crossref]

48. Symonds, E.M., Griffin, D.W. and Breitbart, M. (2009) Eukaryotic viruses in wastewater samples from the United States. Appl. Environ. Microbiol., 75(5): 1402-1409. [Crossref] [PubMed] [PMC]