Background/Aims:Cronobacter spp. have been identified as being of considerable risk to neonates. The occurrence of organisms in infant formulas is therefore of considerable interest. Methods: The occurrence of Cronobacter spp. in infant feeds (formulas and fortified cow's milk) was determined using most probable number (MPN) analysis, and from formula preparation utensils. Ninety-nine samples were analyzed, of which 42 were unopened cans of powdered infant formula (PIF), 25 reconstituted infant formulas in feeding bottles, 27 utensils used in the preparation of infant formula and 5 samples of fortified cow's milk. Presumptive Cronobacter spp. isolates were identified using the 7 allele multilocus sequence typing (MLST) scheme. Results: C. sakazakii, C. malonaticus and C. muytjensii were recovered from PIF. Although the incidence of Cronobacter in PIF was 29% (12/42), the level was low with an average of 0.54 MPN/100 g. According to MLST profiling, C. sakazakii was the most frequently isolated Cronobacter species, and C. sakazakii ST4 (associated with neonatal meningitis) was recovered from 2/42 PIF samples at 0.51 and 0.92 MPN/100 g. Conclusions:Cronobacter spp. can be isolated from PIF and therefore strict hygienic practices during PIF preparation are important to minimize neonate exposure and reduce the risk of severe infections.

Kucerova E, Joseph S, Forsythe S: Cronobacter: diversity and ubiquity. Qual Ass Safety Foods Crops 2011;3:104-122.
Lai KK: Enterobacter sakazakii infections among neonates, infants, children, and adults: case reports and a review of the literature. Medicine 2001;80:113-122.
Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras M, Forsythe SJ: Cronobacter condimenti sp. nov., isolated from spiced meat and Cronobacter universalis sp. nov., a novel species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. Intl J System Evol Microbiol 2012;62:1277-1283.
Joseph S, Sonbol H, Hariri S, Desai P, McClelland M, Forsythe SJ: Diversity of the Cronobacter genus as revealed by multi locus sequence typing. J Clin Microbiol 2012;50:3031-3039.
Iversen C, Forsythe SJ: Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant formula milk and related products. Food Microbiol 2004;21:771-776.
Communicable Disease Centre: CDC update: investigation of Cronobacter infections among infants in the United States. 2011.
Hariri S, Joseph S, Forsythe SJ: Cronobacter sakazakii ST4 clonal complex strains and neonatal meningitis, United States, 2011. Emerg Infect Dis 2013;19:175-177.
Joseph S, Desai P, Ji Y, Cummings CA, Shih R, Degoricija L, Rico A, Brzoska P, Hamby SE, Masood N, Hariri S, Sonbol H, Chuzhanova N, McClelland M, Furtado MR, Forsythe SJ: Comparative analysis of genome sequences covering the seven Cronobacter species. PLoS ONE 2012;7:e49455.
Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM: Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 2004;68:132-153.
Lacomba R, Salcedo J, Alegria A, Barberá R, Hueso P, Matencio E, et al: Sialic acid (N-acetyl and N-glycolylneuraminic acid) and ganglioside in whey protein concentrates and infant formulae. Intl Dairy J 2011;21:887-895.
Baldwin A, Loughlin M, Caubilla-Barron J, Kucerova E, Manning G, Dowson C, Forsythe SJ: Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. BMC Microbiol 2009;9:223.
Joseph S, Forsythe SJ: Insights into the emergent bacterial pathogen Cronobacter spp., generated by multilocus sequence typing and analysis. Front Microbiol 2012;3:397.
Joseph S, Forsythe SJ: Predominance of Cronobacter sakazakii ST4 in neonatal infections. Emerg Infect Dis 2011;17:1713-1715.
Sonbol H, Joseph S, McAuley C, Craven H, Forsythe SJ: Multilocus sequence typing of Cronobacter spp. from powdered infant formula and milk powder production factories. Intl Dairy J 2013;30:1-7.
Bowen AB, Braden CR: Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis 2006;12:1185-1189.
Simmons BP, Gelfand MS, Haas M, Metts L, Ferguson J: Enterobacter sakazakii infection in neonates associated with intrinsic contamination of a powdered infant formula. Infect Contl Hosp Epidemiol 1989;10:398-401.
van Acker J, de Smet F, Muyldermans G, Bougatef A, Naessens A, Lauwers S: Outbreak of necrotizing enterocolitis associated with Enterobactersakazakii in powdered milk formula. J Clin Microbiol 2001;39:293-297.
Himelright I, Harris E, Lorch V, Anderson M: Enterobacter sakazakii infections associated with the use of powdered infant formula - Tennessee, 2001. MMWR Morb Mortal Wkly Rep 2002;51:298-300.
Gurtler JB, Beuchat LR: Growth of Enterobacter sakazakii in reconstituted infant formula as affected by composition and temperature. J Food Prot 2007;70:2095-2103.
Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Glener M, Richards GM: Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Intl J Food Microbiol 2009;136:204-213.
Osaili T, Forsythe S: Desiccation resistance and persistence of Cronobacter species in infant formula. Intl J Food Microbiol 2009;136:214-220.
Kandhai MC, Reij MW, Gorris LGM, Guillaume-Gentil O, van Schothorst M: Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 2004;363:39-40.
Broge T, Lee A: A case of Cronobacter(Enterobacter sakazakii) bacteremia in a breastfed infant. J Ped Inf Dis Soc 2013, E-pub ahead of print.
Hurrell E, Kucerova E, Loughlin M, Caubilla-Barron J, Hilton A, Armstrong R, Smith C, Grant J, Shoo S, Forsythe S: Neonatal enteral feeding tubes as loci for colonisation by members of the Enterobacteriaceae. BMC Infec Dis 2009;9:146.
Bar-Oz B, Preminger A, Peleg O, Block C, Arad I: Enterobactersakazakii infection in the newborn. Acta Pediatr 2001;90:358.
Block C, Peleg O, Minster N, Bar-Oz B, Simhon A, Arad I, Shapiro M: Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Euro J Clin Microbiol Infect Dis 2002;21:613-616.
Caubilla-Barron J, Hurrell E, Townsend S, Cheetham P, Loc-Carrillo C, Fayet O, Prere M-F, Forsythe SJ: 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.
Palcich G, Gillio CM, Aragon-Alegro LC, Pagotto FJ, Farber JM, Landgraf M, Destro MT: Enterobacter sakazakii in dried infant formulas and milk kitchens of maternity wards in São Paulo, Brazil. J Food Prot 2009;72:37-42.
FAO/WHO: Workshop on Enterobacter sakazakii and other microorganisms in powdered infant formula. 2004.
FAO/WHO: Expert meeting on Enterobacter sakazakii and Salmonella in powdered infant formula. 2006.
FAO/WHO: Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae. Microbiological Risk Assessment Series No. 15. 2008.
Codex Alimentarius Commission (CAC): Report of the thirty-first session of the Codex Alimentarius Commission. Alinorm 08/31/rep.
Codex Alimentarius Commission (CAC): Code of hygienic practice for powdered formulae for infants and young children. CAC/RCP 66-2008.
Mullane NR, Murray J, Drudy D, Prentice N, Whyte P, Wall PG, Parton A, Fanning S: Detection of Enterobacter sakazakii in dried infant milk formula by cationic-magnetic-bead capture. Appl Environ Microbiol 2006;72:6325-6330.
Muytjens HL, Roelofs-Willemse H, Jaspar GHJ: Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J Clin Microbiol 1988;26:743-746.
Edelson-Mammel SG, Forteous MK, Buchanan RL: Survival of Enterobacter sakazakii in dehydrated powdered infant formula. J Food Protect 2005;68:1900-1902.
Oonaka K, Fururata K, Hara M, Fukuyama M: Powder infant formula milk contaminated with Enterobacter sakazakii. J Infect Dis 2010;63:103-107.
Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C, Park J, Osaili T, Shaker R, Jaradat Z, Hartantyo SHP, Sani NA, Eestuningsih S, Forsythe SJ: International survey of Cronobacter sakazakii and other Cronobacter spp. in follow-up formulas and infant foods. Intl J Food Microbiol 2009;136:185-188.
Caubilla-Barron J, Kucerova E, Loughlin M, Forsythe SJ: Bacteriocidal preparation of powdered infant formula. Food Standards Agency. 2009.
Iversen C, Forsythe S: Comparison of media for the isolation of Enterobacter sakazakii. Appl Environ Microbiol 2007;73:48-52.
Townsend SM, Hurrell E, Caubilla-Barron J, Loc-Carrillo C, Forsythe SJ: Characterization of an extended-spectrum beta-lactamase Enterobacter hormaechei nosocomial outbreak, and other Enterobacter hormaechei misidentified as Cronobacter(Enterobacter) sakazakii. Microbiology 2008;154:3659-3667.
Kucerova E, Clifton SW, Xia XQ, Long F, Porwollik S, Fulton L, Fronick C, Minx P, Kyung K, Warren W, Fulton R, Feng D, Wollam A, Shah N, Bhonagiri V, Nash WE, Hallsworth-Pepin K, Wilson RK, McClelland M, Forsythe SJ: Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS ONE 2010;5:e9556.
Cetinkaya E, Joseph S, Ayhan K, Forsythe SJ: Comparison of methods for the microbiological identification and profiling of Cronobacter species from ingredients used in the preparation of infant formula. Mol Cell Probes 2012;27:60-64.
Mullane NR, Whyte P, Wall PG, Quinn T, Fanning S: Application of pulsed-field gel electrophoresis to characterise and trace the prevalence of Enterobacter sakazakii in an infant formula processing facility. Intl J Food Microbiol 2007;116:73-81.
Sun Y, Wang M, Wang Q, Cao B, He X, Li K, Feng L, Wang L: Genetic analysis of the Cronobacter sakazakii O4 to O7 O-antigen gene clusters and development of a PCR assay for identification of all C. sakazakii O serotypes. Appl Environ Microbiol 2012:78; 3966-3974.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.