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Volume 26, Number 5—May 2020
CME ACTIVITY - Synopsis

Food Safety and Invasive Cronobacter Infections during Early Infancy, 1961–2018

Jonathan Strysko, Jennifer R. CopeComments to Author , Haley Martin, Cheryl Tarr, Kelley Hise, Sarah Collier, and Anna Bowen
Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Main Article

Table 1

Numbers of reported invasive Cronobacter infections among infants, by country, 1961–2018

Country No. cases reported, n = 183 Appendix reference*
Argentina 3 (16)
Australia 1 (10)
Belgium 2 (3,14)
Brazil 8 (11,1719)
Canada 3 (2022)
China 3 (23,24)
Denmark 1 (25)
France 5 (4,15,26)
Germany 1 (27)
Greece 1 (28)
Iceland 3 (6)
India 2 (29)
Israel 4 (12)
Japan 2 (4,13)
Kenya 1 (30)
Netherlands 8 (2)
New Zealand 1 (31)
Philippines 16 (4)
Portugal 1 (32)
Romania 1 (33)
Spain 1 (34)
Switzerland 1 (35)
United Kingdom 35 (1,4)
United States 79 (5,7,8,9,36–48)

*A full list of reviewed manuscripts is provided in the Appendix.

Main Article

References
  1. Bowen  AB, Braden  CR. Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis. 2006;12:11859. DOIPubMedGoogle Scholar
  2. Urmenyi  AM, Franklin  AW. Neonatal death from pigmented coliform infection. Lancet. 1961;1:3135. DOIPubMedGoogle Scholar
  3. Muytjens  HL, Zanen  HC, Sonderkamp  HJ, Kollée  LA, Wachsmuth  IK, Farmer  JJ III. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol. 1983;18:11520. DOIPubMedGoogle Scholar
  4. van Acker  J, de Smet  F, Muyldermans  G, Bougatef  A, Naessens  A, Lauwers  S. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J Clin Microbiol. 2001;39:2937. DOIPubMedGoogle Scholar
  5. Patrick  ME, Mahon  BE, Greene  SA, Rounds  J, Cronquist  A, Wymore  K, et al. Incidence of Cronobacter spp. infections, United States, 2003-2009. Emerg Infect Dis. 2014;20:15203. DOIPubMedGoogle Scholar
  6. Food and Agriculture Organization of the United Nations, World Health Organization. Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae: meeting report. 2008 [cited 2019 Feb 14]. https://www.who.int/foodsafety/publications/micro/MRA_followup.pdf
  7. Forsythe  SJ. Updates on the Cronobacter genus. Annu Rev Food Sci Technol. 2018;9:2344. DOIPubMedGoogle Scholar
  8. Simmons  BP, Gelfand  MS, Haas  M, Metts  L, Ferguson  J. Enterobacter sakazakii infections in neonates associated with intrinsic contamination of a powdered infant formula. Infect Control Hosp Epidemiol. 1989;10:398401. DOIPubMedGoogle Scholar
  9. Biering  G, Karlsson  S, Clark  NC, Jónsdóttir  KE, Lúdvígsson  P, Steingrímsson  O. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J Clin Microbiol. 1989;27:20546. DOIPubMedGoogle Scholar
  10. Noriega  FR, Kotloff  KL, Martin  MA, Schwalbe  RS. Nosocomial bacteremia caused by Enterobacter sakazakiki and Leuconostoc mesenteroides resulting from extrinsic contamination of infant formula. Pediatr Infect Dis J. 1990;9:4479. DOIPubMedGoogle Scholar
  11. Centers for Disease Control and Prevention. From the Centers for Disease Control and Prevention. Enterobacter sakazakii infections associated with the use of powdered infant formula—Tennessee, 2001. JAMA. 2002;287:22045.PubMedGoogle Scholar
  12. Jason  J. Prevention of invasive Cronobacter infections in young infants fed powdered infant formulas. Pediatrics. 2012;130:e107684. DOIPubMedGoogle Scholar
  13. United States Food and Drug Administration Enforcement Story Archives. Center for Food Safety and Applied Nutrition. 2002 [cited 2019 Feb 14]. https://www.fda.gov/iceci/enforcementactions/enforcementstory/enforcementstoryarchive/ucm105959.htm
  14. Food and Agriculture Organization of the United Nations, World Health Organization. Safe preparation, storage and handling of powdered infant formula: guidelines. 2007 [cited 2019 Feb 14]. http://www.who.int/foodsafety/publications/micro/PIF_Bottle_en.pdf
  15. United States Food and Drug Administration. FDA takes final step on infant formula protections. 2014 Jun 9 [cited 2019 Feb 14]. https://www.fda.gov/ForConsumers/ConsumerUpdates/ucm048694.htm
  16. Bowen  A, Wiesenfeld  HC, Kloesz  JL, Pasculle  AW, Nowalk  AJ, Brink  L, et al. Notes from the field: Cronobacter sakazakii infection associated with feeding extrinsically contaminated expressed human milk to a premature infant—Pennsylvania, 2016. MMWR Morb Mortal Wkly Rep. 2017;66:7612. DOIPubMedGoogle Scholar
  17. McMullan  R, Menon  V, Beukers  AG, Jensen  SO, van Hal  SJ, Davis  R. Cronobacter sakazakii infection from expressed breast milk, Australia. Emerg Infect Dis. 2018;24:3934. DOIPubMedGoogle Scholar
  18. Sundararajan  M, Enane  LA, Kidwell  LA, Gentry  R, Danao  S, Bhumbra  S, et al. Notes from the field: Cronobacter sakazakii meningitis in a full-term neonate fed exclusively with breast milk—Indiana, 2018. MMWR Morb Mortal Wkly Rep. 2018;67:12489. DOIPubMedGoogle Scholar
  19. PubMLST: public databases for molecular typing and microbial genome diversity [cited 2019 Feb 14]. https://pubmlst.org
  20. Chaves  CEV, Brandão  MLL, Lacerda  MLGG, Rocha  CABC, Leone de Oliveira  SMDV, Parpinelli  TC, et al. Fatal Cronobacter sakazakii sequence type 494 meningitis in a newborn, Brazil. Emerg Infect Dis. 2018;24:194850. DOIPubMedGoogle Scholar
  21. Muytjens  HL, Zanen  HC, Sonderkamp  HJ, Kollée  LA, Wachsmuth  IK, Farmer  JJ III. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol. 1983;18:11520. DOIPubMedGoogle Scholar
  22. Block  C, Peleg  O, Minster  N, Bar-Oz  B, Simhon  A, Arad  I, et al. Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur J Clin Microbiol Infect Dis. 2002;21:6136. DOIPubMedGoogle Scholar
  23. Teramoto  S, Tanabe  Y, Okano  E, Nagashima  T, Kobayashi  M, Etoh  Y. A first fatal neonatal case of Enterobacter sakazakii infection in Japan. Pediatr Int. 2010;52:3123. DOIPubMedGoogle Scholar
  24. Drudy  D, Mullane  NR, Quinn  T, Wall  PG, Fanning  S. Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin Infect Dis. 2006;42:9961002. DOIPubMedGoogle Scholar
  25. Coignard  B, Vaillant  V, Vincent  JP, Lefleche  A, Mariani-Kurkdjian  P, Bernet  C, et al.. Severe infections of Enterobacter sakazakii in neonates who consumed powdered infant formula, France, October–December 2004 [in French]. Bulletin Epidemiologique Hebdomadaire. 2006;2–3:103.
  26. Farmer  JJ III. My 40-year history with Cronobacter/Enterobacter sakazakii—lessons learned, myths debunked, and recommendations. Front Pediatr. 2015;3:84. DOIPubMedGoogle Scholar
  27. Jongenburger  I, Reij  MW, Boer  EP, Gorris  LG, Zwietering  MH. Actual distribution of Cronobacter spp. in industrial batches of powdered infant formula and consequences for performance of sampling strategies. Int J Food Microbiol. 2011;151:629. DOIPubMedGoogle Scholar
  28. Jaradat  ZW, Al Mousa  W, Elbetieha  A, Al Nabulsi  A, Tall  BD. Cronobacter spp.—opportunistic food-borne pathogens. A review of their virulence and environmental-adaptive traits. J Med Microbiol. 2014;63:102337. DOIPubMedGoogle Scholar
  29. Jones  G, Pardos de la Gandara  M, Herrera-Leon  L, Herrera-Leon  S, Varela Martinez  C, Hureaux-Roy  R, et al. Outbreak of Salmonella enterica serotype Poona in infants linked to persistent Salmonella contamination in an infant formula manufacturing facility, France, August 2018 to February 2019. Euro Surveill. 2019;24. DOIPubMedGoogle Scholar
  30. Rodriguez-Urrego  J, Herrera-Leon  S, Echeita-Sarriondia  A, Soler  P, Simon  F, Mateo  S; Investigation team. Nationwide outbreak of Salmonella serotype Kedougou associated with infant formula, Spain, 2008. Euro Surveill. 2010;15:19582.PubMedGoogle Scholar
  31. Earnest  GS, Reed  LD, Conover  D, Estill  C, Gjessing  C, Gressel  M, et al.; Centers for Disease Control and Prevention. Engineering and public health at CDC. MMWR Suppl. 2006;55:103.PubMedGoogle Scholar
  32. Appleton  J, Laws  R, Russell  CG, Fowler  C, Campbell  KJ, Denney-Wilson  E. Infant formula feeding practices and the role of advice and support: an exploratory qualitative study. BMC Pediatr. 2018;18:12. DOIPubMedGoogle Scholar
  33. Losio  MN, Pavoni  E, Finazzi  G, Agostoni  C, Daminelli  P, Dalzini  E, et al. Preparation of powdered infant formula: could product’s safety be improved? J Pediatr Gastroenterol Nutr. 2018;67:5436. DOIPubMedGoogle Scholar
  34. Iversen  C, Mullane  N, McCardell  B, Tall  BD, Lehner  A, Fanning  S, et al. 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. Int J Syst Evol Microbiol. 2008;58:14427. DOIPubMedGoogle Scholar
  35. Alsonosi  A, Hariri  S, Kajsík  M, Oriešková  M, Hanulík  V, Röderová  M, et al. The speciation and genotyping of Cronobacter isolates from hospitalised patients. Eur J Clin Microbiol Infect Dis. 2015;34:197988. DOIPubMedGoogle Scholar

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Page created: April 15, 2020
Page updated: April 15, 2020
Page reviewed: April 15, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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