Bovine Escherichia coli Mastitis and Effects on Milk Microbiota

Abstract

Escherichia coli is a microorganism that is found in the normal intestinal microbiota of humans and warm-blooded animals, causing intestinal or extra-intestinal infections. Many pathogenic E. coli strains can cause diarrhea, septicemia, neonatal meningitis, mastitis, urogenital system infections and various intra-abdominal, lung, soft tissue and skin infections in pets. Determining the genotypic and phenotypic characteristics of Escherichia coli strains isolated from animals is very important for the prevention of infections caused by E. coli. In recent years, a new animal pathotype mammary pathogenic E. coli (MPEC), which causes mammary gland infections in animals has been included in the extraintestinal pathogenic E. coli group. The fact that approximately %25-%35 of the use of antimicrobials in the treatment of Gram-negative agents is unsuccessful indicates that the use of correct diagnostic tools should take place in routine before etiological diagnosis. Profiles in bovine milk with mastitis suggest that clinical mastitis is associated with dysbacteriosis and that the microbial community in an intact mammary gland helps prevent intramammary infection. In this review, the change in bacterial diversity of milk microbiota due to antimicrobial use in E. coli-induced mastitis cases is discussed together with current studies.

Keywords

• Escherichia coli
• Mastitis
• Microbiota

References

1. Al Humam, N. A. (2016). Special biochemical profiles of Escherichia coli strains isolated from humans and camels by the VITEK 2 automated system in Al-Ahsa, Saudi Arabia. African Journal of Microbiology Research, 10(22), 783-790. 10.5897/AJMR2016.8047
2. Blount, Z.D. (2015). The unexhausted potential of E. coli. Elife, 4:e05826. 10.7554/eLife.05826
3. Blum, S.E., Heller, E.D., Sela, S., Elad, D., Edery, N., Leitner, G. (2015). Genomic and phenomic study of mammary pathogenic Escherichia coli. PLoS One, 10(9), 1-24. 10.1371/journal.pone.0136387
4. Brenner, D.J., Garrity, G.M., Krieg, N.R., Staley, J.T., Boone, D.R., Vos, P., Goodfellow, M., Rainey, F.A., Schleifer, K.H. (Eds.). (2005). Bergey's manual of systematic bacteriology: The gammaproteobacteria Springer. https://doi.org/10.1007/0-387-28022-7
5. Burvenich, C., Van Merris, V., Mehrzad, J., Diez-Fraile, A., Duchateau, L. (2003). Severity of E. coli mastitis is mainly determined by cow factors. Veterinary Research, 34(5), 521-564. 10.1051/vetres:2003023
6. Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and Simple Determination of the Escherichia coli Phylogenetic Group. Applied and Environmental Microbiology, 66, 4555 - 4558. 10.1128/aem.66.10.4555-4558.2000
7. Clermont, O., Christenson, J.K., Denamur, E., Gordon, D.M. (2013). The Clermont Escherichia coli phylo-typing method revised: improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, 5(1), 58-65. 10.1111/1758-2229.12019
8. Clermont, O., Dixit, O.V.A., Vangchhia, B., Condamine, B., Dion, S., Bridier-Nahmias, A., Denamur, E., Gordon, D. (2019). Characterization and rapid identification of phylogroup G in Escherichia coli, a lineage with high virulence and antibiotic resistance potential. Environmental Microbiology, 21(8):3107-3117. 10.1111/1462-2920.14713

9. DebRoy, C., Roberts, E., & Fratamico, P. M. (2011). Detection of O antigens in Escherichia coli. Animal Health Research Reviews, 12(2), 169-185. 10.1017/S1466252311000193
10. Fernández, L., Langa, S., Martín, V., Maldonado, A., Jiménez, E., Martín, R., Rodríguez, J. M. (2013). The human milk microbiota: origin and potential roles in health and disease. Pharmacological Research, 69(1), 1-10. 10.1016/j.phrs.2012.09.001
11. Ganda, E.K., Bisinotto, R.S., Lima, S.F., Kronauer, K., Decter, D.H., Oikonomou, G., Schukken, Y., Bicalho, R.C. (2016). Longitudinal metagenomic profiling of bovine milk to assess the impact of intramammary treatment using a third-generation cephalosporin. Scientific Reports, 6(1), 1-13. 10.1038/srep37565
12. Ganda, E.K., Gaeta, N., Sipka, A., Pomeroy, B., Oikonomou, G., Schukken, Y.H., Bicalho, R.C. (2017). Normal milk microbiome is reestablished following experimental infection with Escherichia coli independent of intramammary antibiotic treatment with a third-generation cephalosporin in bovines. Microbiome, 5(1), 1-17. 10.1186/s40168-017-0291-5
13. Gomes, T.A., Elias, W.P., Scaletsky, I.C., Guth, B.E., Rodrigues, J.F., Piazza, R.M., Ferreira, L.C., Martinez, M.B. (2016). Diarrheagenic Escherichia coli. Brazilian Journal of Microbiology, 47, 3-30. 10.1016/j.bjm.2016.10.015
14. İzgür, M., Diker, K.S., Yardımcı, H., Esendal, Ö., Akan, M., Aydın, N., J. Paracıklıoğlu (Eds.). (2006). Veteriner mikrobiyoloji: Enterobakteri infeksiyonları. İlke-Emek Yayınları.
15. Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T., Ishii, S. (2017). Environmental Escherichia coli: ecology and public health implications-a review. Journal of Applied Microbiology, 123(3): 570-581. 10.1111/jam.13468
16. Lima, S.F., Bicalho, M. L. D. S., Bicalho, R. C. (2018). Evaluation of milk sample fractions for characterization of milk microbiota from healthy and clinical mastitis cows. PLoS One, 13(3), 1-21. 10.1371/journal.pone.0193671
17. Liu, X., Thungrat, K., Boothe, D.M. (2015). Multilocus sequence typing and virulence profiles in uropathogenic Escherichia coli isolated from cats in the United States. PloS one, 10(11), e0143335. 10.1371/journal.pone.0143335
18. Müştak, H.K., Torun, E., Kaya, İ.B., Kaya, E. E., Diker, Ş., Anadol, E., Günaydın, E. (2013). Wistar ırkı ratlardan izole edilen Escherichia coli’lerin filogenetik analizi. Etlik Veteriner Mikrobiyoloji Dergisi, 24(2), 60-63. Oikonomou, G., Bicalho, M. L., Meira, E., Rossi, R. E., Foditsch, C., Machado, V. S., Teixeria, A.G.V., Santisteban, C., Schukken, Y.H., Bicalho, R. C. (2014). Microbiota of cow’s milk; distinguishing healthy, sub - clinically and clinically diseased quarters. PloS one, 9(1), 1-10. 10.1371/journal.pone.0085904
19. Oliveira, L., Ruegg, P. L. (2014). Treatments of clinical mastitis occurring in cows on 51 large dairy herds in Wisconsin. Journal of Dairy Science, 97(9), 5426-5436. 10.3168/jds.2013-7756
20. Porcellato, D., Meisal, R., Bombelli, A., Narvhus, J.A. (2020). A core microbiota dominates a rich microbial diversity in the bovine udder and may indicate presence of dysbiosis. Scientific Reports, 10(1), 1-14. 10.1038/s41598-020-77054-6
21. Prahlad, J., Rao, B.J., Vinay, P.T., Mallinath, K.C., Kharate, A., Suryakanth, P., Paramesh, N.B., Revappayya, M. (2018). Influence of Age, Sex and Season on the Occurrence of Escherichia coli O157: H7 in Sheep and Goats of Hyderabad-Karnataka Region, India. International Journal of Current Microbiology and Applied Sciences, 7(6), 2896-2904. 10.20546/ijcmas.2018.706.341
22. Scheutz, F., Strockbine, N.A. (2015). Escherichia. In M. Trujillo, S. Dedysh, P. DeVos, B. Hedlund, P. Kämpfer, F. Rainey, W.B. Whitman (Eds.), Bergey's Manual of Systematics of Archaea and Bacteria (pp. 1-49). John Wiley & Sons. https://doi.org/10.1002/9781118960608
23. Schukken, Y.H., Hertl, J., Bar, D., Bennett, G.J., González, R.N., Rauch, B.J., Santisteban, C., Schulte, H.F., Tauer, L., Welcome, Y.T., Gröhn, Y.T. (2009). Effects of repeated gram-positive and gram-negative clinical mastitis episodes on milk yield loss in Holstein dairy cows. Journal of dairy science, 92(7), 3091-3105. 10.3168/jds.2008-1557.
24. Vasquez, A. K., Ganda, E. K., Capel, M. B., Eicker, S., Virkler, P. D., Bicalho, R. C., & Nydam, D. V. (2019). The microbiome of Escherichia coli and culture-negative nonsevere clinical mastitis: Characterization and associations with linear score and milk production. Journal of Dairy Science, 102(1), 578-594. 10.3168/jds.2018-15062
25. Vigil, P.D., Alteri, C.J., Mobley, H.L. (2011). Identification of in vivo-induced antigens including an RTX family exoprotein required for uropathogenic Escherichia coli virulence. Infection and immunity, 79(6), 2335-2344. 10.1128/IAI.00110- 11