Journal of Pediatric Gastroenterology & Nutrition:
Letters to the Editor
Division of Neonatology, Institute of Child Health, IRCCS Burlo Garofolo, Trieste, Italy.
As with all foodstuffs, powdered infant formula is not a sterile product (1). In 1988, a study (2) showed that 14% of 141 different milk samples, collected in 35 different countries, was contaminated with Enterobacter sakazakii. Of note, all of the investigated samples fulfilled the Codex Alimentarius criteria (3), which set a value <3 cfu/g of powder as the acceptable number of Escherichia coli.
The Food and Agriculture Organization (FAO) considers the presence of E sakazakii a category “A” risk (4), because the association between bacteria in powdered milk and disease (sepsis, necrotizing enterocolitis, and meningitis) in infants has been proven. Environmental contamination of formula can occur at any stage of milk preparation: from basic formula ingredients (especially starch), to mixing, dehydration, and domestic preparation and handling (4).
To reduce the biologic risk, the World Health Organization (WHO) has issued both guidelines for health workers (5) and a booklet for the public (2007) (6). The WHO suggests following 3 main interventions: to dilute the powdered milk in water at a temperature of at least 70°C to inactivate E sakazakii; to consume milk right after each preparation; and to store reconstituted milk at <5°C. Similar recommendations have been put forward by several national authorities, such as the Department of Health of the United Kingdom (7), the Finnish Food Safety Authority (8), and the European Food Safety Authority (9,10).
Of the 3 WHO recommendations, the first one appears to be controversial. In practice, among parents of formula-fed infants younger than 12 weeks, only 22% seem to use water heated to ≥70°C to dilute powdered milk (11). Thus, one may wonder about the impact of this recommendation in real life. On the one hand, there is little doubt that the previously recommended temperature (50°C) was too close to the optimal growth temperature for E sakazakii (37–39°C) and that a higher temperature was required to inactivate such bacteria (12,13). On the other hand, the use of hot water implies acceptance of some untoward consequences, such as the formation of curds and the loss of some nutrients, mainly vitamins (14). Moreover, some consideration should be given to the risk of burns for households (especially children) due to handling of boiling water several times per day for many months (4). Additionally, it may be worth considering the following: The rate of powder contamination with E sakazakii appears to be decreasing. It used to be 14% in the 1980s, and it is estimated to be as low as 2.4% in more recent studies (15). The actual number of infections in the first year of life, although well documented, is low in comparison with millions of bottles of formula prepared each day in the world. The Centers for Disease Control and Prevention reports 46 cases recorded between 1961 and 2005 (16). The risk of infection because of E sakazakii–contaminated powdered milk is greater in some specific categories, such as premature babies, low birth weight infants, and infants younger than 28 days (16–18). Therefore, 2 distinct situations might be identified: In hospitalized newborns the problem is easily resolved by using commercially available liquid formulas. In infants in the first month of life, the issue is still a matter of debate. At present, there appears to be a discrepancy between the recommendations by FAO/WHO and the ones by the European Society of Pediatric Gastroenterology, Hepatology, and Nutrition (19). According to the European Society of Pediatric Gastroenterology, Hepatology, and Nutrition, water heated to ≥70°C is not required and may be potentially harmful to the nutritional quality of formulas.
In conclusion, before definitive changes in the recommendations on home handling of powdered milk are made, additional studies may be needed to clarify the cost/benefit ratio of the 2 possible options: water heated to 50°C or to ≥70°C. Meanwhile, formula manufacturers should continue to improve the microbiologic quality of their products, and parents should strictly adhere to the 2 widely accepted recommendations by FAO/WHO: to prepare the feed just before consumption and to store reconstituted formula at <5°C.
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. Enterobacter sakazakii: an emerging problem in paediatric nutrition. J Int Med Res 2008; 36:394–399.
2. Muytjens HL, Roelofs-Willemse H, Jaspar GH. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J Clin Microbiol 1988; 26:743–746.
3. Food and Agriculture Organization. 1994. Codex Alimentarius: Code of Hygienic Practice for Foods for Infants and Children
. CAC/RC 21-1979. Food and Agriculture Organization of the United Nations, Rome, Italy.
4. FAO/WHO. Enterobacter sakazakii
in powdered infant formula. Meeting Report. Joint FAO/WHO Technical Meeting on Enterobacter sakazakii
powdered infant formula. Rome, Italy 16–20 Jan 06. FAO/WHO, Microbiological Risk Assessment Series N°10. 2006.
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. Guidelines. Geneva: WHO; 2006.
6. WHO/FAO. How to Prepare Formula for Bottle-feeding at Home. Geneva: WHO; 2007.
7. Guidance for Health Professionals on Safe Preparation, Storage and Handling of Powdered Infant Formula. Food Standards Agency/Department of Health, UK; 2007.
8. Preparation and Handling of Powdered Infant Formula and Special Formula. Finnish Food Safety Authority; 2006.
9. Opinion of the Scientific Panel on Biological Hazards on a request from the commission related to the microbiological risks in infant formulae and follow-on formulae. EFSA J
10. Scientific opinion of BIOHAZ Panel on the request from the Commision for review on microbiological risks in infant formulae and follow-on formulae with regard to enterobacteriaceae as indicators. EFSA J
11. Carletti C, Catteneo A. Home preparation of powdered infant formula: is it safe? Acta Pediatr 2008; 97:1131–1132.
12. Forsythe SJ. Enterobacter sakazakii
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13. Kandhai MC, Grognu C, van Schothorst M, et al
. Effects of preculturing conditions on lag time and specific growth rate of enterobacter sakazakii in reconstituted powdered infant formula. Appl Environ Microbiol 2006; 72:2721–2729.
15. Iversen C, Forsythe S. Isolation of enterobacter sakazakii and other enterobacteriaceae from powdered infant formula milk and related products. Food Microbiol 2004; 21:771–777.
16. Bowen AB, Braden CR. Invasive enterobacter sakazakii disease in infants. Emerg Infect Dis 2006; 12:1185–1189.
17. Caubilla-Barron J, Hurrell E, Tonsend S, et al
. Genotypic and phenotypic analysis of Enterobacter sakazakii
strains from an outbreak resulting in fatalities in a neonatal intensive care unit in France. J Clin Microbiol 2007; 45:3979–3985.
18. Van Acker J, De Smet F, Muyldermans G, et al
. Outbreak of Necrotizing enterocolitis associated with Enterobacter sakazakii
in powdered milk formula. J Clin Microbiol 2001; 39:293–297.
19. Agostoni C, Axelsson I, Goulet O, et al
. Preparation and handling of powdered infant formula: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 2004; 39:320–322.