Seasonal effect on the prevalence of virulence genes of non-O157 Verotoxic E.coli serogroups in faeces of cattle calves


Abstract views: 102 / PDF downloads: 209

Authors

  • PARUL DUVASU, Mathura, Uttar Pradesh 281 001 India
  • B BIST DUVASU, Mathura, Uttar Pradesh 281 001 India
  • B SHARMA DUVASU, Mathura, Uttar Pradesh 281 001 India
  • A KUMAR ICAR, New Delhi
  • S P SINGH DUVASU, Mathura, Uttar Pradesh 281 001 India
  • U JAIN DUVASU, Mathura, Uttar Pradesh 281 001 India
  • M GOSWAMI DUVASU, Mathura, Uttar Pradesh 281 001 India
  • R P MISHRA DUVASU, Mathura, Uttar Pradesh 281 001 India
  • G BASAK DUVASU, Mathura, Uttar Pradesh 281 001 India

https://doi.org/10.56093/ijans.v93i11.126780

Keywords:

Characterization, STEC, Vero cell cytotoxicity assay (VCA), Vero toxin-producing Escherichia coli, VTEC

Abstract

Calves faecal samples (n=216) were investigated to observe the effect of seasons on the prevalence of serogroups and virulence genes of non-O157 VTEC. A total of 177 (81.94%) E. coli were isolated and 32 (14.81%) were identified as VTEC and serotyping resulted in 13 different non-O157 ‘O’ serogroups. The prevalence of serogroups and their virulence genes was found to be influenced by seasons and highest number were shed in summer (22.22%) followed by rainy (13.88%) and winter season (8.33%), respectively. A higher prevalence of O9 and O11 serogroups (25% each) was observed in summers. Molecular detection of virulence genes revealed the overall prevalence of vt1 to be 37.5%, vt2 43.8%, (vt1+vt2) 18.8%, eaeA 21.9% and hlyA 34.4% genes. Dominance of hlyA 50% was observed in summers, whereas vt1 and vt2 were more prevalent during rain (50% each). The study revealed the link between the occurrence of hlyA gene and O9, O11 serogroups in summers as both the serogroups were hlyA gene bearer. This association might be responsible for more VTEC outbreaks in summers. So, faecal contamination of raw milk seems to pose greater threat of non-O157 VTEC outbreak during hotter and humid months.

Downloads

Download data is not yet available.

References

Aksoy A, Yildirim M, Kacmaz B, Apan T Z and Gocmen J S. 2007. Verotoxin production in strains of Escherichia coli isolated from cattle and sheep, and their resistance to antibodies. Turkish Journal of Veterinary and Animal Science 31: 225–31.

Ali D A, Tesema T S and Belachew Y D. 2021. Molecular detection of pathogenic Escherichia coli strains and their antibiogram associated with risk factors from diarrheic calves in Jimma Ethiopia. Scientifc Reports 11: 14356. DOI: https://doi.org/10.1038/s41598-021-93688-6

Bauer A W, Kirby W M, Sherris J C and Turck M. 1966. Antibiotic susceptibility testing by standard single disk method. American Journal of Clinical Pathology 45: 493–96. DOI: https://doi.org/10.1093/ajcp/45.4_ts.493

Beraldo L G, Borges C A, Maluta R P, Cardozo M V, Rigobelo E C and A´vila F A. 2014. Detection of Shiga toxigenic (STEC) and enteropathogenic (EPEC) Escherichia coli in dairy buffalo. Veterinary Microbiology 170:162–16. DOI: https://doi.org/10.1016/j.vetmic.2014.01.023

Beutin L, Geier D, Zimmermann S, Aleksic S, Gillespie H A and Whittam T S. 1997. Epidemiological relatedness and clonal types of natural populations of Escherichia coli strains producing Shiga toxins in separate populations of cattle and sheep. Applied and Environmental Microbiology 63: 2175–80. DOI: https://doi.org/10.1128/aem.63.6.2175-2180.1997

Bibbal D, Loukiadis E, Kérourédan M, Ferré F, Dilasser F, Peytavin de Garam C, Cartier P, Oswald E, Gay E, Auvray F and Brugère H. 2015. Prevalence of carriage of Shiga toxin- producing Escherichia coli serotypes O157:H7, O26: H11, O103:H2, O111:H8, and O145:H28 among slaughtered adult cattle in France. Applied and Environmental Microbiology 81: 1397–1405. DOI: https://doi.org/10.1128/AEM.03315-14

Blankenship H M, Mosci R E, Phan Q, Fontana J, Rudrik J T and Manning S D. 2020. Genetic diversity of non-o157 shiga toxin-producing Escherichia coli recovered from patients in Michigan and Connecticut. Frontiers in Microbiology 11: 529. DOI: https://doi.org/10.3389/fmicb.2020.00529

Callaway T R, Edrington T S, Loneragan G H, Carr M A and Nisbet D J. 2013. Shiga Toxin Producing Escherichia coli (STEC) ecology in cattle and management based options for reducing faecal shedding. Agriculture Food and Analytical Bacteriology 3: 39–69.

Centers for Disease Control and Prevention (CDC). 2018. National Shiga Toxin-Producing Escherichia coli (STEC) Surveillance Annual Report, 2016. US Department of Health and Human Services, Atlanta, Georgia.

Clinical Laboratory Standard Institute (CLSI). 2012. Performance standard for antimicrobial disk susceptibility tests; approved standard- Eleventh Edition. 32.58.

Cooley M B, Jay-Russell M, Atwill E R, Carychao D, Nguyen K and Quiñones B. 2013. Development of a robust method for isolation of Shiga toxin-positive Escherichia coli (STEC) from fecal, plant, soil and water samples from a leafy greens production region in California. PLoS ONE 8. DOI: https://doi.org/10.1371/journal.pone.0065716

Corogeanu D, Willmes R, Wolke M, Plum G, Utermöhlen O and Krönke M. 2012. Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E. coli O104:H4 from the 2011 German outbreak. BMC Microbiology 12: 160. DOI: https://doi.org/10.1186/1471-2180-12-160

Dargatz D A, Bai J, Lubbers B V, Kopral C A and Anderson G A. 2013. Prevalence of Escherichia coli O-types and Shiga toxin genes in fecal samples from feedlot cattle. Foodborne Pathogen and Disease 10: 392–96. DOI: https://doi.org/10.1089/fpd.2012.1289

Dewsbury D M A, Renter D G, Shridhar, P B, Noll L W, Shi X and Nagaraja T G. 2015. Summer and winter prevalence of Shiga toxin–producing Escherichia coli (STEC) O26, O45, O103, O111, O121, O145, and O157 in feces of feedlot cattle. Foodborne Pathogen and Disease 12: 726–32. DOI: https://doi.org/10.1089/fpd.2015.1987

Edrington T S, Callaway T R, Ives S E, Engler M J, Looper M L, Anderson R C and Nisbet D J. 2006. Seasonal shedding of Escherichia coli O157:H7 in rumiants: A new hypothesis. Foodborne Pathogen and Disease 3: 413–21. DOI: https://doi.org/10.1089/fpd.2006.3.413

Edward P R and Ewing W H. 1972. Identification of Enterobacteriaceae. Burgess Publishing Company, Minnesota. USA.

Fink R C, Popowski J M, Anderson J E, Tran J L, Kalyanikutty S, Crawford G I, DiCostanzo A, Cox R B and Diez-Gonzalez F. 2018. Impact of distillers grain solids (DGS) and seasonality on the prevalence of Escherichia coli O157 at an abattoir in the U. S. Upper Midwest. Journal of Applied Animal Research 46: 237–41. DOI: https://doi.org/10.1080/09712119.2017.1288628

Fernandez D, Rodriguez E M, Arroyo G H, Padola N L and Parma A E. 2009. Seasonal variation of Shiga toxin-encoding genes (stx) and detection of E coli O157 in dairy cattle from Argentina. Journal of Applied Microbiology 106: 1260–67. DOI: https://doi.org/10.1111/j.1365-2672.2008.04088.x

Hoyle D V, Keith M, Williamson H, Macleod K, Mathie H, Handel I, Currie C, Holmes A, Allison L, McLean R, Callaby R, Porphyre T, Tongue SC, Henry M K, Evans J, Gunn G J, Gally D L, Silva N and Chase-Topping M E. 2021. Prevalence and epidemiology of non- O157 Escherichia coli serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle, 2014–2015. Applied and Environmental Microbiology 87: e03142-20. DOI: https://doi.org/10.1128/AEM.03142-20

Hussein H S and Sakuma T. 2005. Prevalence of shiga toxin-producing Escherichia coli in dairy cattle and their products. Journal of Dairy Science 88: 450–65. DOI: https://doi.org/10.3168/jds.S0022-0302(05)72706-5

Islam M Z, Musekiwa A, Islam K, Ahmed S, Chowdhury S and Ahad A. 2014. Regional variation in the prevalence of E. coli O157 in cattle: A meta-analysis and meta-regression. PLoS ONE 9(4): e93299. DOI: https://doi.org/10.1371/journal.pone.0093299

Johnson R P, Clarke R C, Wilson J B, Read S C, Rahn K, Renwick S A, Sandhu, K A, Alves D, Karmali M A, Lior H, McEwen S A, Spika J S and Gyles C L. 1996. Growing concerns and recent outbreaks involving non-O157:H7 serotypes of verotoxigenic Escherichia coli. Journal of Food Protection 59: 1112–22. DOI: https://doi.org/10.4315/0362-028X-59.10.1112

Khan A, Yamasaki S, Sato T, Ramamurthy T, Pal A, Datta S, Chowdhury N R, Das S C, Sikdar A, Tsukamoto T, Bhattacharya S K, Takeda Y and Nair G B. 2002b. Prevalence and genetic profiling of virulence determinants of non-O157 Shiga toxin-producing Escherichia coli isolated from cattle, beef, and humans, Calcutta, India. Emerging Infectious Diseases 8: 54–62. DOI: https://doi.org/10.3201/eid0801.010104

Kobayashi Y and H B I El-Sawy. 2007. Year-round Monitoring of verotoxin-producing Escherichia coli from faeces of dairy cattle. Asian-Australian Journal of Animal Science 20: 789–94. Konowalchuk J, Speirs, J I and Stavric S. 1977. Vero response to a cytotoxin of Escherichia coli. Infection and Immunity 18: 775–79. DOI: https://doi.org/10.1128/iai.18.3.775-779.1977

Lal A, Hales S, French N and Baker M G. 2012. Seasonality in human zoonotic enteric diseases: A systematic review. PLoS ONE 7(4): e31883. DOI: https://doi.org/10.1371/journal.pone.0031883

LeJeune J and Kersting A. 2010. Zoonoses: An occupational hazard for livestock workers and a public health concern for rural communities. Journal of Agricultural Safety and Health 16: 161–79. DOI: https://doi.org/10.13031/2013.32041

Mainga A O, Cenci-Goga B T, Malahlela M N, Tshuma T, Kalake A and Karama M. 2018. Occurrence and characterization of seven major Shiga toxin-producing Escherichia coli serotypes from healthy cattle on cow-calf operations in South Africa. Zoonoses Public Health 65: 777–89. DOI: https://doi.org/10.1111/zph.12491

Momtaz H, Farzan R, Rahimi E, Dehkordi F S and Souod N. 2012. Molecular Characterization of Shiga toxin-producing Escherichia coli isolated from ruminant and donkey raw milk samples and traditional dairy products in Iran. The Scientific World Journal (231342): 13. DOI: https://doi.org/10.1100/2012/231342

Moreira C N, Pereira A, Brod C S, Rodrigues D P, Carvalhal J B and Aleixo J A G. 2003. Shiga toxinproducing Escherichia coli (STEC) isolated from healthy dairy cattle in southern Brazil. Veterinary Microbiology 93: 179–83. DOI: https://doi.org/10.1016/S0378-1135(03)00041-5

Mellor G E, Fegan N, Duffy L L, McMillan K E, Jordan D and Barlow R S. 2016. National survey of Shiga toxin-producing Escherichia coli serotypes O26, O45, O103, O111, O121, O145, and O157 in Australian beef cattle feces. Journal of Food Protection 79: 1868–74. DOI: https://doi.org/10.4315/0362-028X.JFP-15-507

Mir R A, Weppelmann T A, Kang M, Bliss T M, DiLorenzo N, Lamb G C, Ahn S and Jeong K C. 2015. Association between animal age and the prevalence of Shiga toxin-producing Escherichia coli in a cohort of beef cattle. Veterinary Microbiology 175: 325–31. DOI: https://doi.org/10.1016/j.vetmic.2014.12.016

Naumova E N, Jagai, J S, Matyasm B, DeMaria Jr A, MacNeill I B and Griffiths J K. 2007. Seasonality in six enterically transmitted diseases and ambient. Agriculture Food and Analytical Bacteriology 3: 1–2013.

Parul, Bist B, Singh S P, Sharma B, Jain U, Mishra R P and Kumar A. 2021. Virulence charecterization and phylogenetic analysis of non-O157 verotoxin producing Escherichia coli (VTEC) isolated from cattle in India. Indian Journal of Biotechnology 20: 343–54.

Paton J C and Paton A W. 1998. Pathogenesis and diagnosis of Shiga-toxin producing Escherichia coli infections. Clinical Microbiology Reviews 11: 450–79. DOI: https://doi.org/10.1128/CMR.11.3.450

Patricia G, Anne C, Eleanor M N, André C, Kostas D, Paul J M. 2016. Serogroup-specific seasonality of verotoxigenic Escherichia coli Ireland. Emerging Infectious Diseases 22: 4. DOI: https://doi.org/10.3201/eid2204.151160

Padola N L, Sanz M E, Blanco J E, Blanco M, Blanco J, Etcheverrı´a A I, Arroyo G H and Usera M A. 2004. Serotypes and virulence genes of Shigatoxigenic Escherichia coli (STEC) isolates from a feedlot in Argentina. Veterinary Microbiology 100: 3–9. DOI: https://doi.org/10.1016/S0378-1135(03)00127-5

Renter D G, Checkley S L, Campbell J and King R. 2004. Shiga toxin-producing Escherichia coli in the feces of Alberta feedlot cattle. Candian Journal of Veterinary Research 68: 150–53.

Sanjukta R K, Surmani H, Mandakini R K, Milton A A P, Das S, Puro K and Ghatak S. 2019. Characterization of MDR and ESBL-producing E. coli strains from healthy swine herds of north-eastern India. Indian Journal of Animal Sciences 89(6): 625–31. DOI: https://doi.org/10.56093/ijans.v89i6.91104

Scott L, McGee P, Walsh C, Fanning S, Sweeney T, Blanco J, Karczmarczylk M, Early B, Leonard N and Sheridan J J. 2009. Detection of numerous verotoxigenic E. coli serotypes, with multiple antibiotic resistance from cattle faeces and soil. Veterinary Microbiology 134: 288–93. DOI: https://doi.org/10.1016/j.vetmic.2008.08.008

Sheng H, Shringi S, Baker K N K, Minnich S A, Hovde C J and Besser T E. 2016. Standardized Escherichia coli O157:H7 exposure studies in cattle provide evidence that bovine factors do not drive increased summertime colonization. Applied and Environmental Microbiology 82: 964–71. DOI: https://doi.org/10.1128/AEM.02839-15

Smith B A, Fazil A and Lammerding A M. 2012. A risk assessment model for Escherichia coli O157:H7 in ground beef and beef cuts in Canada: Evaluating the effects of interventions. Food Control 29: 364–81. DOI: https://doi.org/10.1016/j.foodcont.2012.03.003

Stacey K F, Parsons D J, Christiansen K H and Burton C H. 2007. Assessing the effect of interventions on the risk of cattle and sheep carrying Escherichia coli O157:H7 to the abattoir using a stochastic model. Preventive Veterinary Medicine 79: 32–45. DOI: https://doi.org/10.1016/j.prevetmed.2006.11.007

Stanford K, Johnson R P, Alexander T W, McAllister T A and Reuter T. 2016. Influence of season and feedlot location on prevalence and virulence factors of seven serogroups of Escherichia coli in feces of western-canadian slaughter cattle. PLoS ONE 11: e0159866. DOI: https://doi.org/10.1371/journal.pone.0159866

Tack D M, Kisselburgh H M, Richardson L C, Geissler A, Griffin P M, Payne D C and Gleason B L. 2021. Shiga toxin- producing Escherichia coli outbreaks in the United States, 2010–2017. Microorganisms 9: 1529. DOI: https://doi.org/10.3390/microorganisms9071529

Thran B H, Hussein H S, Hall M R and Khaiboullina S F. 2001. Shiga toxin-producing Escherichia coli in beef heifers grazing an irrigated pasture. Journal of Food Protection 64: 1613–16. DOI: https://doi.org/10.4315/0362-028X-64.10.1613

U.S. Department of Agriculture F.S.I.S. 2012. Shiga toxin- producing Escherichia coli in certain raw beef products. Federal Register 77: 31975–81.

Van Donkersgoed J, Berg J, Potter A, Hancock D, Besser T and Rice D. 2001. Environmental sources and transmission of Escherichia coli O157 in feedlot cattle. Canadian Veterinary Journal 42: 714–20.

Von Müffling T, Smaijlovic M, Nowak B, Sammet K, Bülte M and Klein G. 2007. Preliminary study of certain serotypes, genetic and antimicrobial resistance profiles of verotoxigenic Escherichia coli (VTEC) isolated in Bosnia and Germany from cattle or pigs and their products. International Journal of Food Microbiology 117: 185–91. DOI: https://doi.org/10.1016/j.ijfoodmicro.2006.08.003

Walsh C, Duffy G, Mahony R O, Fanning S, Blair I S and McDowell D.A. 2006. Antimicrobial resistance in Irish isolates of verocytotoxigenic Escherichia coli (E. coli)— VTEC. International Journal of Food Microbiology 109: 173–78. DOI: https://doi.org/10.1016/j.ijfoodmicro.2006.01.023

Wang L U R, Jokinen C C, Laing C R, Johnson R P, Ziebell K and Gannon V P J. 2018. Multi-year persistence of verotoxigenic Escherichia coli (VTEC) in a closed canadian beef herd: A cohort study frontier in microbiology O157:H7 at a commercial beef abattoir. Journal of Applied Microbiology 95: 256–66. DOI: https://doi.org/10.3389/fmicb.2018.02040

Wani S A, Bhat M A, Samanta I, Nishikawa Y and Buchh A S. 2003. Isolation and characterization of Shiga toxin -producing E. coli (STEC) and enteropathogenic E. coli (EPEC) from calves and lambs with diarrhoea in India. Letter of Applied Microbiology 37: 121–26. DOI: https://doi.org/10.1046/j.1472-765X.2003.01364.x

Wells J G, Shipman L D, Greene K D, Sowers E G, Green J H, Cameron D N, Downes F P and Martin M L. 1991. Isolation of Escherichia coli O157:H7 and other Shiga-like-toxin- producing E. coli from dairy cattle. Journal of Clinical Microbiology 29: 985–89. DOI: https://doi.org/10.1128/jcm.29.5.985-989.1991

World Health Organization & Food and Agriculture Organization of the United Nations. 2018. Shiga toxin-producing Escherichia coli (STEC) and food: Attribution, characterization, and monitoring: report. World Health Organization, Geneva, Switzerland. https://apps.who.int/iris/handle/10665/272871

Yoo B B, Liu V, Juneja V, Huang L and Hwang C A. 2017. Effect of environmental stresses on the survival and cytotoxicity of Shiga toxin-producing Escherichia coli. Food Quality and Safety 1: 139–46. DOI: https://doi.org/10.1093/fqsafe/fyx010

Downloads

Submitted

2022-08-09

Published

2023-10-31

Issue

Section

Articles

How to Cite

PARUL, BIST, B., SHARMA, B., KUMAR, A., SINGH, S. P., JAIN, U., GOSWAMI, M., MISHRA, R. P., & BASAK, G. (2023). Seasonal effect on the prevalence of virulence genes of non-O157 Verotoxic E.coli serogroups in faeces of cattle calves. The Indian Journal of Animal Sciences, 93(11), 1046–1052. https://doi.org/10.56093/ijans.v93i11.126780
Citation