Czech J. Food Sci., 2011, 29(4):391-399 | DOI: 10.17221/255/2010-CJFS

Isolation of Cronobacter spp. isolates from infant formulas and their survival in the production process of infant formula

Songzhe Fu1, Jianxin Gao1, Ying Liu2, Haiying Chen1
1 Nanchang Center for Disease Control and Prevention, Nanchang, P.R. China
2 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P.R. China

Over a 24-month surveillance, three Cronobacter strains, NC041, NC830, and NC1006, were isolated from 77 powder infant formulas (3.90%). No Cronobacter was detected in liquid milk. The prevalence of Cronobacter in the prefinal product and packaged final product was 3.70% and 4.35%, respectively. The isolated Cronobacter strains were subjected to several lethal challenges including the pH, drying, disinfectant, and simulated infant formulas manufacturing process (SIFMP). The results indicated that they exhibited unusual resistance to the dry stress and disinfectant. In SIFMP, Cronobacter isolates were inoculated into three possible contamination entry points involving the stages prior to heating, drying, and filling, respectively. No Cronobacter could survive the heating. However, a high level (105 CFU/ml) of Cronobacter was detected in the samples after the inoculation at the drying point. Furthermore, the survival of Cronobacter was observed during the storage at 10°C after 7 days. The results support the hypothesis that Cronobacter contamination occurs at the stages of drying and filling, and highlight the need to improve the disinfecting measures in the manufacturing process.

Keywords: Cronobacter; dry stress; powdered infant formula (PIF); contamination sources

Published: August 31, 2011  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Fu S, Gao J, Liu Y, Chen H. Isolation of Cronobacter spp. isolates from infant formulas and their survival in the production process of infant formula. Czech J. Food Sci. 2011;29(4):391-399. doi: 10.17221/255/2010-CJFS.
Download citation

References

  1. Acker van J., de Smet F., Muyldermans G., Bougatef A., Naessens A., Lauwers S. (2001): Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. Journal of Clinical Microbiology, 39: 293-297. Go to original source... Go to PubMed...
  2. Arku B., Mullane N., Fox E., Fanning S., Jordan K. (2008): Enterobacter sakazakii survives spray drying. International Journal of Dairy Technology, 61: 102-108. Go to original source...
  3. Breeuwer P., Lardeau A., Peterz M., Joosten H.M. (2003): Desiccation and heat tolerance of Cronobacter. Journal of Applied Microbiology, 95: 967-973. Go to original source... Go to PubMed...
  4. Chap J., Jacksona P., Siqueirab R., Gasparc N., Quintasc C., Parkd J., Osailie T., Shakere R., Jaradatf Z., Hartantyog S.H.P., Sanig N.A., Estuningsihh S., Forsythea S.J. (2009): International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. International Journal of Food Microbiology, 136: 185-188. Go to original source... Go to PubMed...
  5. Craven H.M., McAuley C.M., Duffy L.L., Fegan N. (2010): Distribution, prevalence and persistence of Cronobacter (Enterobacter sakazakii) in the nonprocessing and processing environments of five milk powder factories. Journal of Applied Microbiology, 109: 1044-1052. Go to original source... Go to PubMed...
  6. El-Sharoud W.M., O'Brien S., Negredo C., Iversen C., Fanning S., Healy B. (2009): Characterization of Cronobacter recovered from dried milk and related products. BMC Microbiology, 9: 24-32. Go to original source... Go to PubMed...
  7. Gosney M.A., Martin M.V., Wright A.E., Gallagher M. (2006): Enterobacter sakazakii in the mouths of stroke patients and its association with aspiration pneumonia. European Journal of Internal Medicine, 17: 185-188. Go to original source... Go to PubMed...
  8. Gurtler J.B., Beuchat L.R. (2005): Performance of media for recovering stressed cells of Enterobacter sakazakii as determined using spiral plating and ecometric techniques. Applied and Environmental Microbiology, 71: 7661-7669. Go to original source... Go to PubMed...
  9. Hein I., Gadzov B., Schoder D., Foissy H., Malorny B., Wagner M. (2009): Temporal and spatial distribution of Cronobacter isolates in a milk powder processing plant determined by pulsed-field gel electrophoresis. Foodborne Pathogen Disease, 6: 225-233. Go to original source... Go to PubMed...
  10. Iversen C., Forsythe S.J. (2003): Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends of Food Science and Technology, 14: 443-454. Go to original source...
  11. Iversen C., Mullane N., McCardell B., Tall B.D., Lehner A., Fanning S., Stephan R., Joosten H. (2008): Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov. and Cronobacter dublinensis subsp. lactaridi subsp. nov. International Journal of Systematic and Evolution Microbiology, 58: 1442-1447. Go to original source... Go to PubMed...
  12. Jaradat Z.W., Ababneh Q.O., Saadoun I.M., Samara N.A., Rashdan A.M. (2009): Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from infant food, herbs and environmental samples and the subsequent identification and confirmation of the isolates using biochemical, chromogenic assays, PCR and 16S rRNA sequencing. BMC Microbiology, 9: 225-235. Go to original source... Go to PubMed...
  13. Kandhai M.C., Reij M.W., Gorris L.G., GuillaumeGentil O., Van Schothorst M. (2004): Occurrence of Enterobacter sakazakii in food production environments and households. Lancet, 363: 39-40. Go to original source... Go to PubMed...
  14. Kim H., Beuchat L.R. (2005): Survival and growth of Enterobacter sakazakii on fresh-cut fruits and vegetables and in unpasteurized juice as affected by storage temperature. Journal of Food Protection, 68: 2541-2552. Go to original source... Go to PubMed...
  15. Kim H., Ryu J.H., Beuchat L.R. (2006): Attachment of and biofilm formation by Enterobacter sakazakii on stainless steel and enteral feeding tubes. Applied and Environmental Microbiology, 72: 5846-5856. Go to original source... Go to PubMed...
  16. Liu Y., Gao Q., Zhang X., Hou Y., Yang J., Huang X. (2006): PCR and oligonucleotide array for detection of Enterobacter sakazakii in infant formula. Molecular Cell Probes, 20: 11-17. Go to original source... Go to PubMed...
  17. Molloy C., Cagney C., Fanning S., Duffy G. (2010): Survival Characteristics of Cronobacter spp. in Model Bovine Gut and in the Environment. Foodborne Pathogens and Disease, 7: 671-675. Go to original source... Go to PubMed...
  18. Molloy C., Cagney C., O'Brien S., Iversen C., Fanning S., Duffy G. (2009): Surveillance and characterisation by pulsed-field gel electrophoresis of Cronobacter spp. in farming and domestic environments, food production animals and retail foods. International Journal of Food Microbiology, 136: 198-203. Go to original source... Go to PubMed...
  19. Mullane N.R., Healy B., Meade J., Whyte P., Wall P.G., Fanning S. (2008): Dissemination of Cronobacter spp. (Enterobacter sakazakii) in a powdered milk protein manufacturing facility. Applied and Environmental Microbiology, 74: 5913-5917. Go to original source... Go to PubMed...
  20. Mullane N.R., Whyte P., Wall P.G., Quinn T., Fanning S. (2007): Application of pulsed-field gel electrophoresis to characterise and trace the prevalence of Enterobacter sakazakii in an infant formula processing facility. International Journal of Food Microbiology, 116: 73-81. Go to original source... Go to PubMed...
  21. Nazarowec-White M., Farber J.M. (1997): Thermal resistance of Enterobacter sakazakii in reconstituted dried-infant formula. Letter of Applied Microbiology, 95: 967-973. Go to original source... Go to PubMed...
  22. Riedel K., Lehner A. (2007): Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics, 7: 1217-1231. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.