Pathogens and Indicator Organisms in Powdered Infant Formula

  • International Commission on Microbiological Specifications for Foods (ICMSF)


As defined by Codex Alimentarius (CAC 1981), infant formulae are breast-milk substitutes specially manufactured to satisfy, by themselves, the nutritional requirements of infants during the first months of life up to the introduction of appropriate complementary feeding. The international standard for powdered infant formula and formulae for special medical purpose has been established by Codex Alimentarius in 1981. It has since then been continuously reviewed to take into account the results of new medical research. Definitions as well the age group for which these products are intended may vary depending on the countries. In the case of Europe, for example, infant formulae are intended for infants up to 6 months of age, while follow-up formulae are designed for infants from 6–12 months (EC 2006). In the case of the United States, however, no differences are made and infant formulae are intended for infants from birth up to 12 months.


  1. AFSSA (Agence Française de Sécurité Sanitaire des Aliments). (2005). Handling recommendations for the preparation, handling and storage of feeding bottles. Accessed 1 Jan 2015.
  2. Aguirre-Conde, A., Perez-Legorburu, A., Echaniz-Urcelay, L., Hernando-Zarate, Z., & Arrate-Zugazabeitia, J. K. (2007). Sepsis neonatal por Enterobacter sakazakii. Anales Pediatria, 66, 196–197.CrossRefGoogle Scholar
  3. Belal, M., Al-Mariri, A., Hallab, L., & Hamad, I. (2013). Detection of Cronobacter spp. (formerly Enterobacter sakazakii) from medicinal plants and spices in Syria. Journal of Infection in Developing Countries, 7, 82–89.CrossRefPubMedGoogle Scholar
  4. Broge, T., & Lee, A. (2013). A case of Cronobacter (Enterobacter sakazakii) bacteremia in a breastfed infant. Journal of the Paediatric Infectious Diseases Society, 2(4), e1–e2. Scholar
  5. Brouard, C., Espié, E., Weill, F. X., Kérouanton, A., Brisabois, A., Forgue, A. M., Vaillant, V., & de Valk, H. (2007). Two consecutive large outbreaks of Salmonella enterica serotype Agona infections in infants linked to the consumption of powdered infant formula. The Pediatric Infectious Disease Journal, 26, 148–152.CrossRefPubMedGoogle Scholar
  6. Buchanan, R. L., & Oni, R. (2012). Use of microbiological indicators for assessing hygiene controls for the manufacture of powdered infant formula. Journal of Food Protection, 75, 989–997.CrossRefPubMedGoogle Scholar
  7. CAC (Codex Alimentarius Commission). (1981). Standard for infant formula and formulas for special medical purpose intended for infants. Codex-Stan (pp. 72–1981). Geneva: Rome.Google Scholar
  8. CAC (Codex Alimentarius Commission). (2008). Code of hygienic practice for powdered formulae for infants and young children. CAC/RCP 66–2008.Google Scholar
  9. Cahill, S. M., Wachsmuth, I. K., Costarrica Mde, L., & Ben Embarek, P. K. (2008). Powdered infant formula as a source of Salmonella infection in infants. Clinical Infectious Diseases, 46, 268–273.CrossRefPubMedGoogle Scholar
  10. Calamusa, G., Valenti, R. M., Guida, I., & Mammina, C. (2009). A survey on knowledge and self-reported formula handling practices of parents and child care workers in Palermo, Italy. BMC Pediatrics, 9, 75–81.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carletti, C., & Cattaneo, A. (2008). Home preparation in powdered infant formula: Is it safe. Acta Paediatrica, 97, 1131–1132.CrossRefPubMedGoogle Scholar
  12. CDC (Center for Disease Control and Prevention). (2011). FDA and CDC update: Investigation of Cronobacter bacteria illness in infants. Accessed Nov 2013. Accessed 1 Jan 2016.
  13. China. (2010). Ministry of Health, P.R.China GB 10675–2010, National food safety standard, Infant formula.Google Scholar
  14. Cordier, J. L. (2008). Production of powdered infant formulae and microbiological control measures. In J. M. Farber & S. J. Forsythe (Eds.), Enterobacter sakazakii (pp. 145–185). Washington, DC: ASM Press.CrossRefGoogle Scholar
  15. Dancer, G. I., Mah, J. H., Rhee, M. S., Hwang, I. G., & Kang, D. H. (2009). Resistance of Enterobacter sakazakii (Cronobacter spp.) to environmental stresses. Journal of Applied Microbiology, 107, 1606–1614.CrossRefPubMedGoogle Scholar
  16. Dewanti-Hariyadi, R., Gitapratiwi, D., Meutia, Y. R., Estuningsish, S., Hendrastuti-Hidayat, S., & Nurjanah, S. (2010). Isolation of Enterobacter sakazakii (Cronobacter spp.) from powdered infant formula and other dry foods obtained from Bogor area, Indonesia. In Proceedings of the seminar – Current issues and challenges in food safety: A science based approach for food safety management (pp. 281–286).Google Scholar
  17. Dümen, E. (2010). Cronobacter sakazakii (Enterobacter sakazakii): Only an infant problem? Kafkas Univ Vet Fak Derg, 16, S171–S178.Google Scholar
  18. Dumm, M., Peel, L., Jones, A., Hunter, C., Kendall-Harris, M., Boltwood, C., Hunt, C., & Valentine, C. (2010). Technician training reduces formula preparation errors. Infant, Child and Adolescent Nutrition, 2, 258–260.CrossRefGoogle Scholar
  19. EC (European Commission). (2005). Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union L338/1–26.Google Scholar
  20. EC (European Commission). (2006). Commission Directive 2006/141/EC of 22 December 2006 on infant formulae and follow-on formulae and amending Directive 1999/21/EC. Official Journal of the European Union L401/1–33.Google Scholar
  21. EC (European Commission). (2007). Commission Regulation (EC) No. 1441/2007 of 5 December 2007 amending Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. Official Journal of the European Union, L322/12–29.Google Scholar
  22. Edelson-Mammel, S. G., Porteous, M. K., & Buchanan, R. L. (2005). Survival of Enterobacter sakazakii in a dehydrated powdered infant formula. Journal of Food Protection, 68, 1900–1902.CrossRefPubMedGoogle Scholar
  23. EFSA (European Food Safety Agency). (2007). Opinion of the Scientific Panel on biological hazards (BIOHAZ) on the request for review of the opinion on microbiological risks in infant formulae and follow-on formulae with regard to Enterobactericeae as indicators. EFSA Journal, 444, 1–14.Google Scholar
  24. FAO/WHO. (2004). Enterobacter sakazakii and other microorganisms in powdered infant formula: Meeting report. Microbiological risk assessment series 6. Accessed 18 Nov 2013.
  25. FAO/WHO. (2006). Enterobacter sakazakii and Salmonella in powdered infant formula: Meeting report. Microbiological risk assessment series 10. Accessed 18 Nov 2013.
  26. FAO/WHO. (2008a). Enterobacter sakazakii (Cronobacter spp.) in follow-up formula: Meeting report. Microbiological risk assessment series 15. Accessed 18 Nov 2013.
  27. ICMSF (International Commision on Microbiological Specifications for Foods). (2011). Microorganisms in foods, volume 8: Use of data for assessing process control and product acceptance. New York: Springer Science and Business Media LLC.CrossRefGoogle Scholar
  28. Jason, J. (2012). Prevention of invasive Cronobacter infections in young infants fed powdered infant formulas. Paediatrician, 130, e1076–e1084.Google Scholar
  29. Jongenburger, I., Reij, M. W., Boer, E. P. J., Gorris, L. G. M., & Zwietering, M. H. (2011). Actual distribution of Cronobacter spp. in industrial batches of powdered infant formula and consequences for performance of sampling strategies. International Journal of Food Microbiology, 151, 62–69.CrossRefPubMedGoogle Scholar
  30. Jourdan, N., Le Hello, S., Delmas, G., Clouzeau, J., Manteau, C., Désaubliaux, B., Chagnon, F., Thierry-Bled, F., Demare, N., Weill, F. X., & de Valk, H. (2008). Nationwide outbreak of Salmonella enterica serotype Give infections in infants in France, linked to infant milk formula. EuroSurveillence, 13, 2–4.Google Scholar
  31. Kandhai, M. C., Reij, M. W., Gorris, L. G., Guillaume-Gentil, O., & van Schothorst, M. (2004). Occurrence of Enterobacter sakazakii in food production environments and households. Lancet, 363, 39–40.CrossRefPubMedGoogle Scholar
  32. Kent, G. (2014). Global infant formula: Monitoring and regulating the impacts to protect human health. International Breastfeeding Journal, 10, 6.CrossRefGoogle Scholar
  33. Kilonzo-Nthenge, A., Rotich, E., Godwin, S., Nahashon, S., & Chen, F. (2012). Prevalence and antimicrobial resistance of Cronobacter sakazakii isolated from domestic kitchens in middle Tennessee, United States. Journal of Food Protection, 75, 1512–1517.CrossRefPubMedGoogle Scholar
  34. Kozlica, J., Claudet, A. L., Solomon, D., Dunn, J. R., & Carpenter, L. R. (2010). Waterborne outbreak of Salmonella I4,[5],12:i:-. Foodborne Pathogens and Disease 7, 1431–1433.Google Scholar
  35. Lai, K. K. (2001). Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine, 80, 113–122.CrossRefPubMedGoogle Scholar
  36. Norberg, S., Stanton, C., Ross, R. P., Hill, C., Fitzgerald, G. F., & Cotter, P. (2012). Cronobacter spp. in powdered infant formula. Journal of Food Protection, 75, 607–620.CrossRefPubMedGoogle Scholar
  37. Pagotto, F. J., Nazarowec-White, M., Bidwid, S., & Farber, J. M. (2003). Enterobacter sakazakii: Infectivity and enterotoxin production in vitro and in vivo. Journal of Food Protection, 66, 370–375.CrossRefPubMedGoogle Scholar
  38. Palcich, G., de Moraes-Gillio, C., Aragon-Alegro, L. C., Pagotto, F. J., Farber, J. M., Landgraf, M., & Destro, M. T. (2009). Enterobacter sakazakii in dried infant formulas and milk kitchens of maternity wards in São Paulo, Brazil. Journal of Food Protection, 72, 37–42.CrossRefPubMedGoogle Scholar
  39. Putthana, V., Marounek, M., Brenova, N., Mrazek, J., & Lukesova, D. (2012). Isolation and characterization of Cronobacter spp. from environmental food resources. Agricultura Tropica et Subtropica, 45, 5–11.CrossRefGoogle Scholar
  40. Ray, P., Das, A., Gautam, V., Jain, N., Narrang, A., & Sharma, M. (2007). Enterobacter sakazakii in infants: Novel phenomenon in India. Indian Journal of Medical Microbiology, 25, 408–410.CrossRefPubMedGoogle Scholar
  41. Redmond, E. C., Griffith, C. J., & Riley, S. (2009). Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health. Perspectives in Public Health, 129, 85–94.CrossRefPubMedGoogle Scholar
  42. Reij, M. W., Jongenburger, I., Gkogka, E., Gorris, L. G. M., & Zwietering, M. H. (2009). Perspective on the risk to infants in the Netherlands associated with Cronobacter spp. occurring in powdered infant formula. International Journal of Food Microbiology, 136, 232–237.CrossRefPubMedGoogle Scholar
  43. Renfrew, M. J., McLaughlin, M., & McFadden, A. (2008). Cleaning and sterilization of infant feeding equipment: A systematic review. Public Health Nutrition, 11, 1188–1199.CrossRefPubMedGoogle Scholar
  44. Rodríguez-Urrego, J., Herrera-León, S., Echeita-Sarriondia, A., Soler, P., Simon, F., Mateo, S., & Team, I. (2010). Nationwide outbreak of Salmonella serotype Kedougou associated with infant formula, Spain, 2008. EuroSurveillence, 15, 6–10.Google Scholar
  45. Savage, N., Walker, R., & Steele, J. (2008). Enterobacter sakazakii: A case of coincidental infantile sepsis. Laboratoriums Medizin, 39, 658–660.Google Scholar
  46. Siqueira-Santos, R. F., da Silva, N., Amstalden-Junqueira, V. C., Kajsik, M., Forsythe, S., & Pereira, J. L. (2013). Screening for Cronobacter spp. in powdered and reconstituted infant formulas and from equipment used in formula preparation in maternity hospitals. Annals of Nutrition & Metabolism, 63, 211–214.CrossRefGoogle Scholar
  47. Teramoto, S., Tanabe, Y., Okano, E., Nagashima, T., Kobayashi, M., & Etoh, Y. (2010). A first fatal neonatal case of Enterobacer sakazakii. Pediatrics International, 52, 312–313.CrossRefPubMedGoogle Scholar
  48. Turck, D. (2012). Safety aspects in preparation and handling of infant food. Annals of Nutrition & Metabolism, 60, 211–214.CrossRefGoogle Scholar
  49. Turcovsky, J., Kunikova, K., Drahovska, H., & Kaclikova, E. (2011). Biochemical and molecular characterization of Cronobacter spp. (formerly Enterobacter sakazakii) isolated from foods. Antonie Van Leeuwenhoek, 99, 257–269.CrossRefPubMedGoogle Scholar
  50. Usera, M. A., Echeita, A., Aladueña, 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. European Journal of Epidemiology, 12, 377–381.CrossRefPubMedGoogle Scholar
  51. Usera, M. A., Rodriguez, A., Echeita, A., & Cano, R. (1998). Multiple analysis of a foodborne outbreak caused by infant formula contaminated by an atypical Salmonella virchow strain. European Journal of Clinical Microbiology & Infectious Diseases, 17, 551–555.Google Scholar
  52. Vanegas, M. C., Rugeles, L. C., & Martinez, A. J. (2009). Aislamiento e identificación de Enterobacter sakazakii en lactarios de Bogotá, D.C. Infection, 13, 36–42.CrossRefGoogle Scholar
  53. Walsh, D., Molloy, C., Iversen, C., Carroll, J., Cagney, C., Fanning, S., & Duffy, G. (2011). Survival characteristics of environmental and clinically derived strains of Cronobacter sakazakii in infant milk formula (IMF) and ingredients. Journal of Applied Microbiology, 110, 697–703.CrossRefPubMedGoogle Scholar
  54. WHO/FAO (World Health Organization/Food and Agriculture Organization). (2007). Safe preparation, storage and handling of powdered infant formula - Guidelines. Accessed 1 Jan 2016.

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • International Commission on Microbiological Specifications for Foods (ICMSF)
    • 1
  1. 1.Robert L. Buchanan, editorial committee chairRiverside Corporate Park CSIRONorth RydeAustralia

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