Evaluation of the antimicrobial effect of a probiotic mixture against Cronobacter sakazakii and Salmonella enterica in infant formulas
Abstract
Cronobacter sakazakii and Salmonella enterica have been implicated in outbreaks causing sepsis and meningitis in infants. Several infection cases have been associated with the consumption of contaminated powdered infant formulae. Besides its role in modulating gut microbiota, the inclusion of probiotics in infant formulae may be useful to counteract pathogen contamination in these products and thus to reduce the risk of infection. The aim of this research was to evaluate the antimicrobial effect of a mixture of the probiotics Lactobacillus rhamnosus and Bifidobacterium infantis against Cronobacter sakazakii and Salmonella enterica in reconstituted follow-on formulae. For that, infant formulae (with or without probiotics) were inoculated with either C. sakazakii or S. enterica and incubated at 30 or 40ºC for 72 hours. Overall, the results showed the presence of probiotics inhibiting the growth of C. sakazakii together with incubation temperature (interaction between both factors). Probiotics were viable throughout the incubation period so that nutrient exhaustion could be ruled out as the mechanism of C. sakazakii inhibition. Thus, the acidification of media observed during the study was hypothesized to be responsible for pathogen growth inhibition. However, since in the case of formulae inoculated with Salmonella the behavior of probiotics and pH values was similar to C. sakazakii, the decrease of pH does not satisfactorily explain such a different behavior. So, it is suggested that the production of specific bacteriocins by probiotics against C. sakazakii but not against Salmonellla could be the underlying inhibitory mechanism. Further studies should be carried out to test this hypothesis.
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References
Al-Holy, M.A., Lin, M., Abu-Ghoush, M.M., Al-Qadiri, H.M., Rasco, B.A., 2009. Thermal Resistance, Survival and Inactivation of Enterobacter Sakazakii (Cronobacter spp.) in Powdered and Reconstituted Infant Formula. J. Food Saf. 29, 287–301. https://doi.org/10.1111/j.1745-4565.2009.00157.x
Al-Nabulsi, A.A., Osaili, T.M., Elabedeen, N.A.Z., Jaradat, Z.W., Shaker, R.R., Kheirallah, K.A., Tarazi, Y.H., Holley, R.A., 2011. Impact of environmental stress desiccation, acidity, alkalinity, heat or cold on antibiotic susceptibility of Cronobacter sakazakii. Int. J. Food Microbiol. 146, 137–143. https://doi.org/10.1016/j.ijfoodmicro.2011.02.013
Bai, Y., Yu, H., Du, G., Fei, S., Shi, C., 2019. Survival and Environmental Stress Resistance of Cronobacter sakazakii Exposed to Vacuum or Air Packaging and Stored at Different Temperatures. Drontiers in Microbiology, 10, 303
Braegger, C., Chmielewska, A., Decsi, T., Kolacek, S., Mihatsch, W., Moreno, L., Pieścik, M., Puntis, J., Shamir, R., Szajewska, H., Turck, D., Van Goudoever, J., 2011. Supplementation of infant formula with probiotics and/or prebiotics: A systematic review and comment by the ESPGHAN committee on nutrition. J. Pediatr. Gastroenterol. Nutr. 52, 238–250. https://doi.org/10.1097/MPG.0b013e3181fb9e80
Campana, R., Federici, S., Ciandrini, E., Manti, A., Baffone, W. 2019. Lactobacillus spp. inhibit the growth of Cronobacter sakazakii ATCC 29544 by altering its membrane integrity. J Food Sci Technol 56, 3962–3967.
Comisión Europea, 2016. REGLAMENTO DELEGADO (UE) 2016/127 DE LA COMISIÓN de 25 de septiembre de 2015. D. Of. la Unión Eur. 1–25. https://doi.org/10.1166/apm.2014.1068
Dancer, G.I., 2009. Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae. Lett. Appl. Microbiol. 10, 173. https://doi.org/10.1111/j.1472-765X.2009.02601.x
Drudy, D., Mullane, N.R., Quinn, T., Wall, P.G., Fanning, S., 2006. Enterobacter sakazakii: An Emerging Pathogen in Powdered Infant Formula. Clin. Infect. Dis. 42, 996–1002. https://doi.org/10.1086/501019
EFSA, 2004. Opinion of the Scientific Panel on Biological Hazards on the request from the Commission related to the microbiological risks in infant formulae and Adopted on 9 th September 2004. EFSA J. 113, 1–35. https://doi.org/10.1016/0368-2048(73)80049-0
FAO/WHO, 2006. Enterobacter sakazakii and Salmonella in powdered infant formula: meeting report. Microbiological Risk Assessment.
Ghassem, M., Babji, A.S., Forsythe, S.J., Norrakiah, A.S., 2011. Growth and survival of Cronobacter species as measured by media performance. Int. Food Res. J. 18, 367–372.
Hayes, M., Barrett, E., Ross, R.P., Fitzgerald, G.F., Hill, C., Stanton, C., 2009. Evaluation of an Antimicrobial Ingredient Prepared from a Lactobacillus acidophilus Casein Fermentate against Enterobacter sakazakii. J. Food Prot. 72, 340–346. https://doi.org/10.1182/blood.V100.1.22
Hayes, M., Ross, R.P., Fitzgerald, G.F., Hill, C., Stanton, C., 2006. Casein-Derived Antimicrobial Peptides Generated by Lactobacillus acidophilus DPC6026. Appl. Environ. Microbiol. 72, 2260–2264. https://doi.org/10.1097/00019501-199501000-00002
Hurrell, E., Kucerova, E., Loughlin, M., Caubilla-Barron, J., Forsythe, S.J., 2009. Biofilm formation on enteral feeding tubes by Cronobacter sakazakii, Salmonella serovars and other Enterobacteriaceae. Int. J. Food Microbiol. 136, 227–231. https://doi.org/10.1016/j.ijfoodmicro.2009.08.007
Iversen, C., Lane, M., Forsythe, S.J., 2004. The growth profile, thermotolerance and biofilm formation of Enterobacter sakazakii grown in infant formula milk. Lett. Appl. Microbiol. 38, 378–382. https://doi.org/10.1111/j.1472-765X.2004.01507.x
Jamwal, A., Sharma, K., Chauhan, R., Bansal, S., Goel, G., 2019. Evaluation of commercial probiotic lactic cultures against biofilm formation by Cronobacter sakazakii. Intest Res.17(2), 192-201
Kandhai, M.C., Reij, M.W., Grognou, C., Van Schothorst, M., Gorris, L.G.M., Zwietering, M.H., 2006. Effects of preculturing conditions on lag time and specific growth rate of Enterobacter sakazakii in reconstituted powdered infant formula. Appl. Environ. Microbiol. 72, 2721–2729. https://doi.org/10.1128/AEM.72.4.2721-2729.2006
Kim, D.H., Jeong, D., Song, K.Y., Kang, I.B., Kim, H., Seo, K.H., 2018. Culture supernatant produced by Lactobacillus kefiri from kefir inhibits the growth of Cronobacter sakazakii. J Dairy Res, 85, 98-103.
Kingsbury, J.M., Thom, K., Soboleva, T., 2019. Effect of Storage Temperature on the Survival of New Zealand Egg-Associated Salmonella Isolates in and on Eggs. J Food Prot. 82 (12), 2161–2168.
Kopp-Hoolihan, L., 2001. Prophylactic and therapeutic uses of probiotics: A review. J. Am. Diet. Assoc. https://doi.org/10.1016/S0002-8223(01)00060-8
Lenati, R.F., O’Connor, D.L., Hébert, K.C., Farber, J.M., Pagotto, F.J., 2008. Growth and survival of Enterobacter sakazakii in human breast milk with and without fortifiers as compared to powdered infant formula. Int. J. Food Microbiol. 122, 171–179. https://doi.org/10.1016/j.ijfoodmicro.2007.11.084
Markowiak, P., Ślizewska, K., 2017. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9. https://doi.org/10.3390/nu9091021
Mishra, C., Lambert, J., 1996. Production of anti-microbial substances by probiotics. Asia Pacific J. Clin. Nat. 5, 20–24.
O’Connor, P.M., Kuniyoshi, T.M., Oliveira, R.P., Hill, C., Ross, R.P., Cotter, P.D., 2020. Antimicrobials for food and feed; a bacteriocin perspective. Current Opinion in Biotechnology, 61:160–167.
Osaili, T.M., Shaker, R.R., Ayyash, M.M., Holley, R.A., 2008. Effect of Bifidobacterium breve on the survival and growth of Enterobacter sakazakii in rehydrated infant milk formula. J. Food Prot. 28, 36–46.
Park, J., Soo-Hwan, K., 2007. Thermal Resistance and Inactivation of Rehydration of Powdered Infant Formula. J. Microbiol. Biotechnol. 17, 364–368.
Salimiyan, R.K., Ghazvini K., Farsiani H., 2019. Clinical and pathogenesis overview of Enterobacter infections. Rev Clin Med. 6(4), 146-154.
Shaker, R.S., Osaili, T.M., Ayyash, M., 2008. Effect of thermophilic lactic acid bacteria on the fate of Enterobacter sakazakii during processing and storage of plain yogurt. J. Food Saf. 170–182. https://doi.org/10.3109/08958378.2012.757400
Simón, M. De, Sabaté, S., Cristina Osanz, A., Bartolomé, R., Dolores Ferrer, M., 2010. Investigación de un caso de infeccin neonatal por Enterobacter sakazakii asociada a un preparado en polvo para lactantes. Enferm. Infecc. Microbiol. Clin. 28, 713–715. https://doi.org/10.1016/j.eimc.2010.04.009
Usera, M.A., Echeita, A., Aladuena, A., Blanco, M.C., Reymundo, R., Prieto, M.I., Tello, O., Cano, R., Herrera, D., Martinez-Navarro, F., 1996. Interregional foodborne salmonellosis outbreak due to powdered infant formula contaminated with lactose-fermenting Salmonella Virchow. Eur. J. Epidemiol. 12, 377–381. https://doi.org/10.1007/BF00145301
WHO/FAO, 2007. Storage and handling of powdered infant formula: guidelines.
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