FITNESS AND PATHOGENICITY OF OUTBREAK CAUSING Salmonella UPON SHORT-TERM EXPOSURE TO GROUNDWATER WITH RESIDUAL ANTIBIOTICS

Year 2019, Volume: 20 Issue: 1, 1 - 8, 15.04.2019

Berat Zeki Haznedaroğlu

https://doi.org/10.23902/trkjnat.435384

Abstract

The changes in survival and
pathogenicity of three Salmonella
enterica subsp. enterica
serotypes upon short term exposure to groundwater with residual antibiotics
have been studied in relationship to overall microbial fitness. A wild type
flagellated Salmonella enterica ser.
Typhimurium outbreak strain, a mutant Salmonella
enterica ser. Typhimurium strain, and a wild type avian disease-causing Salmonella enterica ser. Pullorum strain
were exposed to a range of ionic strength (3-30 mM) groundwater with residual
antibiotics for 6-24 hours. Exposed organisms’ pathogenicity was tested in
vitro exposure to a human epithelial cell line (HEp2). Resistance profiles
against 10 common antibiotics were also tested and compared to unexposed
controls. Results show minor antibiotic resistance changes for S. enterica ser. Typhimurium strains in
response to some antibiotic classes mediated with active efflux pumps. This
trend was not observed for S. enterica ser.
Pullorum, suggesting that resistance found in groundwater exposed organisms
might be strain-dependent. In vitro epithelial cell invasion assays showed
bacterial invasion of HEp2 cells initially decreases with time and increases
after 24 hours. It is concluded that S.
enterica serotypes reaching groundwater environments in the presence of
residual antibiotics may exhibit increased levels of pathogenicity,
strain-dependent resistance to antibiotics, and sustained levels of viability.

Keywords

Salmonella, antibiotic resistance, invasion, groundwater, pathogenicity

References

• 1. Abouzeed, Y.M., Baucheron, S. & Cloeckaert, A. 2008. Ramr mutations involved in efflux-mediated multidrug resistance in Salmonella enterica serovar Typhimurium. Antimicrobial Agents and Chemotherapy, 52 (7): 2428-2434.
• 2. Barber, L.B., Keefe, S.H., LeBlanc, D.R., Bradley, P.M., Chapelle, F.H., Meyer, M.T., Loftin, K.A., Kolpin, D.W. & Rubio, F. 2009. Fate of sulfamethoxazole, 4-nonylphenol, and 17β-estradiol in groundwater contaminated by wastewater treatment plant effluent. Environmental Science & Technology, 43 (13): 4843-4850.
• 3. Barnes, K.K., Kolpin, D.W., Furlong, E.T., Zaugg, S.D., Meyer, M.T. & Barber, L.B. 2008. A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States - i) groundwater. Science of The Total Environment, 402 (2-3): 192-200.
• 4. Bezanson, G.S., Khakhria, R., Duck, D. & Lior, H. 1985. Molecular analysis confirms food source and simultaneous involvement of two distinct but related subgroups of Salmonella typhimurium bacteriophage type 10 in major interprovincial Salmonella outbreak. Applied and Environmental Microbiology, 50 (5): 1279-1284.
• 5. Bolster, C.H., Mills, A.L., Hornberger, G.M. & Herman, J.S. 1999. Spatial distribution of deposited bacteria following miscible displacement experiments in intact cores. Water Resources Research, 35 (6): 1797-1807.
• 6. Bradford, P.A. & Dean, C.R. 2008. Resistance of gram-negative bacilli to antimicrobials, In: Fong, I.W. & Drlica, K. (eds) Antimicrobial resistance and implications for the 21st century, Springer, New York, NY, USA, 135 pp.
• 7. Burnham, C.A.D., Shokoples, S.E. & Tyrrell G.J. 2007. Invasion of Hela cells by group b Streptococcus requires the phosphoinositide-3-kinase signalling pathway and modulates phosphorylation of host-cell akt and glycogen synthase kinase-3. Microbiology, 153 (12): 4240-4252.
• 8. Cebrián, L., Rodríguez, J.C., Escribano, I. & Royo, G. 2005. Characterization of Salmonella spp. mutants with reduced fluoroquinolone susceptibility: Importance of efflux pump mechanisms. Chemotherapy, 51 (1): 40-43.
• 9. Centers for disease control and prevention (CDC) - Salmonella outbreaks. (http://www.cdc.gov/salmonella /outbreaks.html), (Date accessed 10 May 2018).
• 10. Centers for disease control and prevention (CDC). Investigation of outbreak of infections caused by Salmonella typhimurium. (http://www.cdc.gov/salmonella/typhimurium /map.html), (Date accessed 10 May 2018).
• 11. Chopra, I. & Roberts, M. 2001. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 65 (2): 232-260.
• 12. Chu, C., Su, L.H., Chu C.H., Baucheron, S., Cloeckaert, A. & Chiu, C.H. 2005. Resistance to fluoroquinolones linked to gyra and parc mutations and overexpression of acrab efflux pump in Salmonella enterica serotype Choleraesuis. Microbial Drug Resistance, 11 (3): 248-253.
• 13. Clinical and Laboratory Standards Institute (CLSI) / National Committee for Clinical Laboratory, 2003. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, 107 pp.
• 14. Crane, S.R. & Moore, J.A. 1984. Bacterial pollution of groundwater: A review. Water, Air, & Soil Pollution, 22 (1): 67-83.
• 15. Giraud, E., Cloeckaert, A., Kerboeuf, D. & Chaslus-Dancla, E. 2000. Evidence for active efflux as the primary mechanism of resistance to ciprofloxacin in Salmonella enterica serovar Typhimurium. Antimicrobial Agents and Chemotherapy, 44 (5): 1223-1228.
• 16. Hutson, S.H., Barber, N.L., Kenny, J.F., Linsey, K.S., Lumia, D.S. & Maupin, M.A. 2004. Estimated use of water in the United States in 2000, in U.S. Geological Survey Circular. U.S. Geological Survey, Virginia, USA, 52 pp.
• 17. Kumar, A & Schweizer, H.P. 2005. Bacterial resistance to antibiotics: Active efflux and reduced uptake. Advanced Drug Delivery Reviews, 57 (10): 1486-1513.
• 18. Kunihiko Nishino, T.L. & Groisman, E.A. 2006. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Molecular Microbiology, 59 (1): 126-141.
• 19. Lacroix, F.J., Cloeckaert, A., Grépinet, O., Pinault, C., Popoff, M.Y., Waxin, H. & Pardon, P. 1996. Salmonella typhimurium acrb-like gene: Identification and role in resistance to biliary salts and detergents and in murine infection. FEMS Microbiology Letters, 135 (2-3): 161-167.
• 20. Niesel, D.W. & Peterson, J.W. 1987. Calcium enhances Salmonella typhimurium invasion of Hela cells. FEMS Microbiology Letters, 41 (3): 299-304.
• 21. Nikaido, H., Basina, M., Nguyen, V. & Rosenberg, E.Y. 1998. Multidrug efflux pump acrab of Salmonella typhimurium excretes only those beta-lactam antibiotics containing lipophilic side chains. Journal of Bacteriology, 180 (17): 4686-4692.
• 22. Orth, P., Schnappinger, D., Hillen, W., Saenger, W. & Hinrichs, W. 2000. Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nature Structural & Molecular Biology, 7 (3): 215-219.
• 23. Peterson, J.W. & Niesel, D.W. 1988. Enhancement by calcium of the invasiveness of Salmonella for Hela cell monolayers. Reviews of Infectious Diseases, 10(Supplement 2): 319-322.
• 24. Piddock, L.J.V., White, D.G., Gensberg, K., Pumbwe, L. & Griggs, D.J. 2000. Evidence for an efflux pump mediating multiple antibiotic resistance in Salmonella enterica serovar Typhimurium. Antimicrobial Agents and Chemotherapy, 44 (11): 3118-3121.
• 25. Poole, K. 2000. Efflux-mediated resistance to fluoroquinolones in gram-negative bacteria. Antimicrobial Agents and Chemotherapy, 44 (9): 2233-2241.
• 26. Quinn, T., O'Mahony, R., Baird, A.W., Drudy, D., Whyte, P. & Fanning, S. 2006. Multi-drug resistance in Salmonella enterica: Efflux mechanisms and their relationships with the development of chromosomal resistance gene clusters Current Drug Targets, 7 (7): 849-860.
• 27. Roberts, M. 1996. Tetracycline resistance determinants: Mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiology Reviews, 19 (1): 1-24.
• 28. Schmoll, O., Howard, G., Chilton, J. & Chorus, I. 2006. Protecting groundwater for health. IWA Publishing, Cornwall, UK, 698 pp.
• 29. Vugia, D.J., Samuel, M., Farley, M.M., Marcus, R., Shiferaw, B., Shallow, S., Smith, K. & Angulo, F.J. 2004. Invasive salmonella infections in the United States, FoodNet, 1996–1999: Incidence, serotype distribution, and outcome. Clinical Infectious Diseases, 38 (Supplement 3): 149-156.
• 30. Vulliet, E. & Cren-Olivé, C. 2011. Screening of pharmaceuticals and hormones at the regional scale, in surface and groundwaters intended to human consumption. Environmental Pollution, 159 (10): 2929-2934.
• 31. Yamaguchi, A., Kimura, T., Someya, Y. & Sawai, T. 1993. Metal-tetracycline/h+ antiporter of Escherichia coli encoded by transposon tn10. The structural resemblance and functional difference in the role of the duplicated sequence motif between hydrophobic segments 2 and 3 and segments 8 and 9. Journal of Biological Chemistry, 268 (9): 6496-6504.
• 32. Yamaguchi, S., Aizawa, S., Kihara, M., Isomura, M., Jones, C.J. & Macnab, R.M. 1986. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. Journal of Bacteriology, 168 (3): 1172-1179.