Abstract
About 120–150 neonatal Cronobacter spp. (Enterobacter sakazakii) infections have been described. An analysis of current case numbers, epidemiological measures and risk factors is warranted. Data of microbiologically confirmed cases, published between 2000 and 2008, have been analysed statistically. More than 100 neonatal Cronobacter infections have been reported in this period. The overall lethality of the 67 invasive infections was 26.9%. The lethality of Cronobacter meningitis, bacteraemia and necrotising enterocolitis (NEC) was calculated to be 41.9% (P < 0.0001), <10% and 19.0% (P < 0.05), respectively. Logistic regression models (P < 0.0001) revealed a higher gestational age at birth and parentage not from Europe as significant factors for a higher reporting probability of neonatal Cronobacter meningitis. Neonates with Cronobacter meningitis not originating from North America have a higher risk for lethal outcome than other neonatal Cronobacter infections (P < 0.0001). Continental differences of risk factors for Cronobacter meningitis and for the lethal outcome of neonatal meningitis should be elucidated. Neonatal Cronobacter infections are mainly associated with the contamination of infant formula and of the relevant cleaning and preparation equipment. Eleven neonatal Cronobacter infections, not caused by contaminated infant formula, have been retrieved. Other environmental sources of infection should be considered. Consistent and sufficiently informative data of invasive neonatal Cronobacter infections should be recorded in a centralized reporting system.
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References
Iversen C, Mullane N, McCardell B, Tall BD, 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. Int J Syst Evol Microbiol 58:1442–1447
FAO/WHO (2006) Enterobacter sakazakii and Salmonella in powdered infant formula: meeting report. Available online at: http://www.fao.org/ag/agn/agns/jemra_riskassessment_enterobacter_en.asp
Mullane NR, Iversen C, Healy B, Walsh C, Whyte P, Wall PG, Quinn T, Fanning S (2007) Enterobacter sakazakii an emerging bacterial pathogen with implications for infant health. Minerva Pediatr 59:137–148
Lai KK (2001) Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine (Baltimore) 80:113–122
Iversen C, Forsythe S (2003) Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci Technol 14:443–454
Gurtler JB, Kornacki JL, Beuchat LR (2005) Enterobacter sakazakii: a coliform of increased concern to infant health. Int J Food Microbiol 104:1–34
Coignard B, Vaillant V, Vincent JP, Lefléche A, Mariani-Kurkdjan P, Bernet C, L´Héritaeau F, Sénénchal H, Grimont P, Bingen E, Desenclos JC (2006) Infections séverès à Enterobacter sakazakii chez des nouveau-nés ayant consommé une préparation en poudre pour nourissons, France, octubre-decembre 2004. Bulletin Epidemiologique Hebdomadaire 2–3:10–13
Himelright I, Harris E, Lorch V, Anderson M, Jones T, Craig A, Kuehnert M, Forster T, Arduino M, Jensen B, Jernigan D (2002) Enterobacter sakazakii infections associated with the use of powdered infant formula—Tennessee, 2001. J Am Med Assoc 287:2204–2205
van Acker 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. J Clin Microbiol 39:293–297
Noriega FR, Kotloff KL, Martin MA, Schwalbe RS (1990) Nosocomial bacteremia caused by Enterobacter sakazakii and Leuconostoc mesenteroides resulting from extrinsic contamination of infant formula. Pediatr Infect Dis J 9:447–449
Marcos M, Iñurrieta A, Soriano A, Martínez JA, Almela M, Marco F, Mensa J (2008) Effect of antimicrobial therapy on mortality in 377 episodes of Enterobacter spp. bacteraemia. J Antimicrob Chemother 62:397–403
Patzer JA, Dzierzanowska D, Turner PJ (2008) Trends in antimicrobial susceptibility of Gram-negative isolates from a paediatric intensive care unit in Warsaw: results from the MYSTIC programme (1997–2007). J Antimicrob Chemother 62:369–375
Kim JB, Cho SH, Park YB, Lee JB, Kim JC, Lee BK, Lee HK, Chae HS (2008) Surveillance of stool samples for the presence of Enterobacter sakazakii among Korean people. Yonsei Med J 49:1017–1022
FAO/WHO (2008) Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formulae: meeting report. Available online at: http://www.fao.org/ag/agn/agns/jemra/Sakazaki_FUF_report.pdf
Stoll BJ, Hansen N, Fanaroff AA, Lemons JA (2004) Enterobacter sakazakii is a rare cause of neonatal septicemia or meningitis in VLBW infants. J Pediatr 144:821–823
Friedemann M (2008) Enterobacter sakazakii in powdered infant formula. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 51:664–674
Palcich G, deMorales-Gillio M, Aragon-Alegro LC, Pagotto FJ, Farber JM, Landgraf M, Destro MT (2009) Enterobacter sakazakii in dried infant formulas and milk kitchens of maternity wards in São Paulo, Brazil. J Food Prot 72:37–42
Gutierrez-Rojo R, Torres-Chavolla E (2007) A rapid polymerase chain reaction assay for Enterobacter sakazakii detection in infant milk formulas. J Rapid Methods Autom Microbiol 15:345–358
Estuningsih S, Kress C, Hassan AA, Akineden O, Schneider E, Usleber E (2006) Enterobacteriaceae in dehydrated powdered infant formula manufactured in Indonesia and Malaysia. J Food Prot 69:3013–3017
Muytjens HL, Roelofs-Willemse H, Jaspar GH (1988) Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J Clin Microbiol 26:743–746
Ray P, Das A, Gautam V, Jain N, Narang A, Sharma M (2007) Enterobacter sakazakii in infants: novel phenomenon in India. Indian J Med Microbiol 25:408–410
Barreira ER, Costa de Souza D, de Freitas Góis P, Fernandes JC (2003) Meningite por Enterobacter sakazakii em recém-nascido: relato de caso. Pediatria (São Paulo) 25:65–70
Bar-Oz B, Preminger A, Peleg O, Block C, Arad I (2001) Enterobacter sakazakii infection in the newborn. Acta Paediatr 90:356–358
Tekkök IH, Higgins MJ, Ventureyra ECG, Baeesa SS (1996) Abscedation of posterior fossa dermoid cysts. Childs Nerv Syst 12:318–322
Arseni A, Malamou-Ladas E, Koutsia C, Xanthou M, Trikka E (1987) Outbreak of colonization of neonates with Enterobacter sakazakii. J Hosp Infect 9:143–150
Gosney MA, Martin MV, Wright AE, Gallagher M (2006) Enterobacter sakazakii in the mouths of stroke patients and its association with aspiration pneumonia. Eur J Intern Med 17:185–188
See KC, Than HA, Tang T (2007) Enterobacter sakazakii bacteraemia with multiple splenic abscesses in a 75-year-old woman: a case report. Age Ageing 36:595–596
Bowen AB, Braden CR (2006) Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis 12:1185–1189
Amsler KM, Davies TA, Shang W, Jacobs MR, Bush K (2008) In vitro activity of ceftobiprole against pathogens from two phase 3 clinical trials of complicated skin and skin structure infections. Antimicrob Agents Chemother 52:3418–3423
Thiesemann R, Walter EU, Füsgen I (2009) Nosocomial urinary tract infections in the geriatric hospital–pathogen spectrum and resistancies. Z Gerontol Geriatr 42:99–107
European Commission (EC) (2005) Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Available online: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:338:0001:0026:EN:PDF
Lichtsinn H, Pritzer M, Hoffler U (1989) A nosocomial outbreak of neonatal infections due to multiple resistant Enterobacter sakazakii. Hygiene + Medizin 14:407–410
FAO/WHO (2008) Call for data: Enterobacter sakazakii in follow-up formulae. Available online at: http://www.fao.org/ag/AGN/agns/files/Call%20for%20data%20follow%20up%20formula.pdf
MOH (2005) E. sakazakii meningitis to become a notifiable disease. Available online at: http://www.moh.govt.nz/moh.nsf/0/D6081BEC1D116521CC256FD90074D556
CDR (1993) Bacteraemia and bacterial meningitis. CDR Wkly 3:1
Health Canada (2002) Health professional advisory. Enterobacter sakazakii infection and powdered infant formulas. Available online at: http://www.hc-sc.gc.ca/fn-an/securit/ill-intox/esakazakii/enterobacter_sakazakii-eng.php
Suijkerbuijk AWM (2005) Gesignaleerd. Infectieziekten Bulletin 16:1–3
Coignard B, Poujol I, Carbonne A, Bernet C, Sénéchal H, Dumartin C, Raclot I, Lepoutre A, Thiolet JM, Bouraoui L, Descenclos JC (2006) Le signalement des infections nosocomiales, France, 2001–2005. Bulletin Épidemiologique Hebdomadaire 51–52:406–410
NOIS (2007) Norsk overvåkingssystem for infeksjoner i sykehustjenesten - registerforskriften: Kodeliste over mikroorganismer. Available online at: http://www.fhi.no/dav/713A687485.pdf
CDR (2004) Bacteraemia 2003 England and Wales and Northern Ireland. Available online at: http://www.hpa.org.uk/cdr/archives/2004/bact_2104.pdf
RASFF (2009) Weekly notifications 8/2009. Available online at: http://ec.europa.eu/food/food/rapidalert/reports/week8-2009_en.pdf
EWRS (2004) Early warning and response system. Home page at: https://ewrs.ecdc.europa.eu/
Muytjens HL, Zanen HC, Sonderkamp HJ, Kollée LA, Wachsmuth IK, Farmer JJ 3rd (1983) Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol 18:115–120
Clark NC, Hill BC, O’Hara CM, Steingrimsson O, Cooksey RC (1990) Epidemiologic typing of Enterobacter sakazakii in two neonatal nosocomial outbreaks. Diagn Microbiol Infect Dis 13:467–472
Nazarowec-White M, Farber JM (1997) Enterobacter sakazakii: a review. Int J Food Microbiol 34:103–113
Codex Alimentarius Commission (CAC) (2008) Code of hygienic practice for powdered formulae for infants and young children. Home page at: http://www.codexalimentarius.net/web/index_en.jsp
European Commission (EC) (2007) Commission Regulation (EC) No 1441/2007 of 5 December 2007 amending Regulation No 2073/2005 on microbiological criteria for foodstuffs. Available online at: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2007:322:0012:0029:EN:PDF
Muytjens HL, Kollée LA (1982) Neonatal meningitis due to Enterobacter sakazakii. Tijdschr Kindergeneeskd 50:110–112
Farmer JJ 3rd, Asbury MA, Hickman FW, Brenner DJ (1980) Enterobacter sakazakii: a new species of “Enterobacteriaceae” isolated from clinical specimens. Int J Syst Bacteriol 30:569–584
Caubilla-Barron J, Hurrell E, Townsend S, Cheetham P, Loc-Carrillo C, Fayet O, Prère MF, Forsythe SJ (2007) 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 45:3979–3985
Burdette JH, Santos C (2000) Enterobacter sakazakii brain abscess in the neonate: the importance of neuroradiologic imaging. Pediatr Radiol 30:33–34
RASFF (2002) Alert notification 2002/190: Enterobacter sakazakii in infant formulae from Germany. Available online at: http://ec.europa.eu/food/food/rapidalert/archive_en.htm
Jarvis C (2005) Fatal Enterobacter sakazakii infection associated with powdered infant formula in a neonatal intensive care unit in New Zealand. Am J Infect Control 33:E19
RASFF (2004) Alert notification 2004/658: Enterobacter sakazakii in infant formula. Available online at: http://ec.europa.eu/food/food/rapidalert/reports/week50-2004_en.pdf
Pavcnik-Arnol M, Hojker S, Derganc M (2007) Lipopolysaccharide-binding protein, lipopolysaccharide, and soluble CD14 in sepsis of critically ill neonates and children. Intensive Care Med 33:1025–1032
Aguirre-Conde A, Pérez-Legorburu A, Echániz-Urcelay I, Hernando-Zaráte Z, Arrate-Zugazabeitia JK (2007) Sepsis neonatal por Enterobacter sakazakii. An Pediatr (Barc) 66:196–197
Mange JP, Stephan R, Borel N, Wild P, Kim KS, Pospischil A, Lehner A (2006) Adhesive properties of Enterobacter sakazakii to human epithelial and brain microvascular endothelial cells. BMC Microbiol 6:58
Major P (2006) Rapid method for detection of DNAse activity of Enterobacter sakazakii. Available online at: http://efrira1.antsz.hu/oeti/elbizt/ATT00010.pdf
RASFF (2007) Alert notification 2007/452: Enterobacter sakazakii (present/10 g) in infant formula from Switzerland via Germany. Available online at: http://ec.europa.eu/food/food/rapidalert/reports/week27-2007_en.pdf
Marler B, Clark B (2008) New Mexican baby death blamed on Enterobacter sakazakii. Available online at: http://enterobactersakazakiiblog.com/2008/12/articles/e-sakazakii-watch/new-mexican-baby-death-blamed-on-e-sakazakii/
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Friedemann, M. Epidemiology of invasive neonatal Cronobacter (Enterobacter sakazakii) infections. Eur J Clin Microbiol Infect Dis 28, 1297–1304 (2009). https://doi.org/10.1007/s10096-009-0779-4
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DOI: https://doi.org/10.1007/s10096-009-0779-4