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Annals of Microbiology

, Volume 62, Issue 1, pp 1–5 | Cite as

Enterobacter sakazakii: an emerging foodborne pathogenic bacterium

  • XianFeng Zhou
  • SongZhe Fu
  • JianXin Gao
  • HaiYing Chen
Review

Abstract

Enterobacter sakazakii (Cronobacter spp.) is an emerging pathogen associated with the ingestion of contaminated powdered infant formula (PIF) that causes necrotizing enterocolitis, sepsis, and meningitis in low-birth-weight preterm neonatal infants. The natural habitat of E. sakazakii is unknown, but PIF has been suggested as a possible mode of transmission in neonatal infections. The presence of E. sakazakii is not limited to powdered infant formula, it can also be found in a broad range of foods and in water. In recent years, the International Commission on Microbiological Specifications for Foods has ranked E. sakazakii a “severe hazard for restricted populations.” The present review is mainly focused on environmental stress on E. sakazakii and its antibiotic resistance.

Keywords

Enterobacter sakazakii Powdered infant formula Neonatal infections Environmental stress Antibiotic resistance 

References

  1. Adamson DM, Rogers JR (1981) Enterobacter sakazakii meningitis with sepsis. Clin Microbiol Newsl 3:19–20CrossRefGoogle Scholar
  2. Arseni A, Malamou-Ladas E, Koutsia C, Xanthou M, Trikka E (1987) Outbreak of colonization of neonates with Enterobacter sakazakii. J Hosp Infect 9:143–150PubMedCrossRefGoogle Scholar
  3. Asakura H, Morita-Ishihara T, Yamamoto S, Igimi S (2007) Genetic characterization of thermal tolerance in Enterobacter sakazakii. Microbiol Immunol 51:671–677PubMedGoogle Scholar
  4. Bar-Oz B, Preminger A, Peleg O, Block C, Arad I (2001) Enterobacter sakazakii infections in the newborn. Acta Paediatr 90:356–358PubMedCrossRefGoogle Scholar
  5. Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Richards GM (2009) Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int J Food Microbiol 136:204–213PubMedCrossRefGoogle Scholar
  6. Bhat GK, Anandhi RS, Dhanya VC, Shenoy SM (2009) Urinary tract infection due to Enterobacter sakazakii. Indian J Pathol Microbiol 52:430–431PubMedCrossRefGoogle Scholar
  7. Biering G, Karlsson S, Clark NC, Jónsdóttir KE, Lúdvígsson P, Steingrímsson O (1989) Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J Clin Microbiol 27:2054–2056PubMedGoogle Scholar
  8. Block C, Peleg O, Minster N, Bar-Oz B, Simhon A, Arad I, Shapiro M (2002) Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur J Clin Microbiol Infect Dis 21:613–616PubMedCrossRefGoogle Scholar
  9. Bowen A, Braden CR (2006) Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis 12:1185–1189PubMedCrossRefGoogle Scholar
  10. Burdette JH, Santos C (2000) Enterobacter sakazakii brain abscess in the neotate: The importance of neuroradiologic imaging. Pediatr Radiol 30:33–34PubMedCrossRefGoogle Scholar
  11. Chan KL, Saing H, Yung RW, Yeung YP, Tsoi NS (1994) A study of preantibiotic bacteriology in 125 patients with necrotizing enterocolitis. Acta Paediatr Suppl 396:45–48PubMedCrossRefGoogle Scholar
  12. 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 13:467–472PubMedCrossRefGoogle Scholar
  13. Coignard B, Vaillant V, Vincent JP, Lefleche A, Mariani-Kurkdjian P et al. (2004) Infections severs a Enterobacter sakazakii chez des nouveau-nes ayant consomme une prepartation en poudre pour nourrissons, France. Bull Epidemiol Hebdomadaire. http://www.invs.sante.fr/BEh/2006/02_03/beh_02_03_2006.pdf. Accessed 26 December 2010
  14. Drudy D, Mullane NR, Quinn T, Wall PG, Fanning S (2006) Enterobacter sakazakii: An emerging pathogen in powdered infant formula. Clin Infect Dis 42:996–1002PubMedCrossRefGoogle Scholar
  15. Farmer JJ, Aabury MA, Hickman FW, Brenner DJ (1980) Enterobacter sakazakii: a new species of “Enterobacteriaceae” isolated from clinical specimens. Int J Syst Bacteriol 30:569–584CrossRefGoogle Scholar
  16. Food and Agriculture Organisation (2004) Final report of the FAO/WHO Regional Conference on Food Safety for Asia and the Pacific Annex 6 FAO http://www.fao.org/docrep/meeting/008/ad911e/ad911e06. Accessed 25 December 2010
  17. Gallagher PG, Ball WS (1991) Cerebral infarctions due to CNS infection with Enterobacter sakazakii. Pediatr Radiol 21:135–136PubMedCrossRefGoogle Scholar
  18. Girlich D, Poirel L, Leelaporn A, Karim A, Tribuddharat C, Fennewald M, Nordmann P (2001) Molecular epidemiology of the integron-located VEB-1 extended-spectrum beta-lactamase in nosocomial enterobacterial isolates in Bangkok, Thailand. J Clin Microbiol 39:175–182PubMedCrossRefGoogle Scholar
  19. Grimm M, Stephan R, Iversen C, Manzardo GGG, Rattei T, Riedel K, Ruepp A, Frishman D, Lehner A (2008) Cellulose and extracellular matrix component present in Enterobacter sakazakii biofilms. J Food Prot 71:13–18PubMedGoogle Scholar
  20. Gurtler JB, Beuchat LR (2005) Performance of media for recovering stressed cells of Enterobacter sakazakii as determined using spiral plating and ecometric techniques. Appl Environ Microbiol 71:7661–7669PubMedCrossRefGoogle Scholar
  21. Himelright I, Harris E, Lorch V, Anderson M, Jones T, Craig A, Kuehnert M, Fotster T, Arduino M, Jensen B, Jernigan D (2002) Enterobacter sakazakii infections associated with the use of powdered infant formula-Tenessee, 2001. Morbid Mort Weekly Rep 51:297–300Google Scholar
  22. Hunter CJ, Petrosyan M, Ford HR, Prasadarao NV (2008) Enterobacter sakazakii: An emerging pathogen in infants and neonates. Surg Infect (Larchmt) 9:533–539CrossRefGoogle Scholar
  23. Iversen C, Forsythe S (2004) Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant formula and related products. Food Microbiol 21:771–776CrossRefGoogle Scholar
  24. Iversen C, Lane M, Forsythe SJ (2004) The growth profile, thermotolerance and biofilm formation of Enterobacter sakazakii grow in infant formula milk. Lett Appl Microbiol 38:378–382PubMedCrossRefGoogle Scholar
  25. Johler S, Stephan R, Hartmann I, Kuehner KA, Lehner A (2010) Genes involved in yellow pigmentation of Cronobacter sakazakii ES5 and influence of pigmentation on persistence and growth under environmental stress. Appl Environ Microbiol 76:1053–1061PubMedCrossRefGoogle Scholar
  26. Joker RN, Norholm T, Siboni KF (1965) A case of neonatal meningitis caused by a yellow Enterobacter. Dan Med Bull 12:128–130PubMedGoogle Scholar
  27. Kandhai MC, Reij MW, Gorris LG, Guillaume-Gentil O, van Schothorst M (2004) Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 363:39–40PubMedCrossRefGoogle Scholar
  28. Kim SH, Park JH (2007) Thermal resistance and inactivation of Enterobacter sakazakii isolates during rehydration of powdered infant formula. J Microbiol Biotechnol 17:364–368PubMedGoogle Scholar
  29. Kim KP, Klumpp J, Loessner MJ (2007) Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int J Food Microbiol 115:195–203PubMedCrossRefGoogle Scholar
  30. Kleiman MB, Allen SD, Neal P, Reynolds J (1981) Meningoencephalitis and compartmentalization of the cerebral ventricles caused by Enterobacter sakazakii. J Clin Microbiol 14:352–354PubMedGoogle Scholar
  31. Lai KK (2001) Enterobacter sakazakii infections among neonates, infants, children, and adults: case reports and a review of the literature. Medicine 80:113–122PubMedCrossRefGoogle Scholar
  32. Leclercq A, Wanegue C, Baylac P (2002) Comparison of fecal coliform agar and violet red bile lactose agar for fecal coliform enumeration in foods. Appl Environ Microbiol 68:163–168CrossRefGoogle Scholar
  33. Lecour H, Seara A, Cordeiro J, Miranda M (1989) Treatment of childhood bacterial meningitis. Infection 17:343–346PubMedCrossRefGoogle Scholar
  34. Lee JW, Oh SH, Kim JH, Yook HS, Byun MW (2006) Gamma radiation sensitivity of Enterobacter sakazakii in dehydrated powdered infant formula. J Food Prot 69:1434–1437PubMedGoogle Scholar
  35. Lehner A, Stephan R (2004) Microbiological, epidemiological, and food safety aspects of Enterobacter sakazakii. J Food Prot 67:2850–2857PubMedGoogle Scholar
  36. Lehner A, Riedel K, Eberel L, Breeuwer P, Diep B, Stephan R (2005) Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. J Food Prot 68:2287–2294PubMedGoogle Scholar
  37. Maffei HVL, Nobrega FJ (1975) Gastric pH and microflora of normal and diarrhoeic infants. Gut 16:719–726PubMedCrossRefGoogle Scholar
  38. Monroe PW, Tift WL (1979) Bacteremia associated with Enterobacter sakazakii (yellow pigmented Enterobacter cloacae). J Clin Microbiol 10:850–851PubMedGoogle Scholar
  39. Muytjens HL, Kollee LA (1990) Enterobacter sakazakii meningitis in neonates: causative role of formula? Pediatr Infect Dis J 9:372–373PubMedCrossRefGoogle Scholar
  40. Muytjens HL, Zanen H, Sonderkamp H, Kollee L, Wachsmuth I, Farmer J (1983) Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol 18:115–120PubMedGoogle Scholar
  41. Naqvi SH, Maxwell MA, Dunkle LM (1985) Cefotaxime therapy of neonatal gram-negative bacillary meningitis. Pediatr Infect Dis 4:499–502PubMedCrossRefGoogle Scholar
  42. Nazarowec-White M, Farber J (1997) Enterobacter sakazakii: a review. Int J Food Microbiol 34:103–113PubMedCrossRefGoogle Scholar
  43. 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 9:447–448PubMedCrossRefGoogle Scholar
  44. Ongrádi J (2002) Vaginal infection by Enterobacter sakazakii. Sex Transm Infect 78:467PubMedCrossRefGoogle Scholar
  45. Oonaka K, Furuhata K, Hara M, Fukuyama M (2010) Powder infant formula milk contaminated with Enterobacter sakazakii. Jpn J Infect Dis 63:103–107PubMedGoogle Scholar
  46. Pitout JD, Moland ES, Sanders CC, Thomson KS, Fitzsimmons SR (1997) Beta-lactamases and detection of beta-lactam resistance in Enterobacter spp. Antimicrob Agents Chemother 41:35–39PubMedGoogle Scholar
  47. Postupa R, Aldova E (1984) Enterobacter sakazakii: A Tween 80 esterase-positive representative of the genus Enterobacter isolated from powdered milk specimens. J Hyg Epidemiol Microbiol Immunol 28:435–440PubMedGoogle Scholar
  48. Ray P, Das A, Gautam V, Jain N, Narang A, Sharma M (2007) Enterobacter sakazakii infections: novel phenomenon in india. Indian J Med Microbiol 25:408–410PubMedCrossRefGoogle Scholar
  49. Reina J, Parras F, Gil S, Salva F, Alomar P (1989) Human infections caused by Enterobacter sakazakii. Microbiologic considerations. Enferm Infecc Microbiol Clín 7:147–150PubMedGoogle Scholar
  50. Reis M, Harms D, Scharf J (1994) Multiple cerebral infarcts with resulting multicystic encephalomalacia in a premature infant with Enterobacter sakazakii meningitis. Klin Pädiatr 206:184–186CrossRefGoogle Scholar
  51. Riedel K, Lehner A (2007) Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics 7:1217–1231PubMedCrossRefGoogle Scholar
  52. Schindler PRG, Metz H (1991) Coliform bacteria in drinking water from South Bavaria: Identification by the API 20E-system and resistance patterns. Water Sci Technol 24:81–84Google Scholar
  53. Sethi N, Prakash A (2010) In vitro susceptibility of Enterobacter sakazakii to natural products. J Food Technol 8:150–153CrossRefGoogle Scholar
  54. Shadlia-Matug M, Aidoo KE, Candlish AA, Elgerbi AM (2008) Evaluation of some antibiotics against pathogenic bacteria isolated from infant foods in North Africa. Open Food Sci J 2:95–101CrossRefGoogle Scholar
  55. Shaker RR, Osaili TM, Abu Al-Hassan AS, Ayyash MM, Forsythe SJ (2008) Effect of desiccation, starvation, heat and cold stresses on the thermal resistance of Enterobacter sakazakii in rehydrated infant milk formula. J Food Sci 73:354–359CrossRefGoogle Scholar
  56. Simmons BP, Gelfand MS, Haas M, Metts L, Ferguson J (1989) Enterobacter sakazakii infections in neonates associated with intrinsic contamination of a powdered infant formula. Infect Control Hosp Epidemiol 10:398–401PubMedCrossRefGoogle Scholar
  57. Tekkok IH, Baeesa SS, Higgins MJ, Ventureyra EC (1996) Abscedation of posterior fossa dermoid cysts. Childs Nerv Syst 12:318–322PubMedCrossRefGoogle Scholar
  58. U.S. Food and Drug Administration (2002) Isolation and enumeration of Enterobacter sakazakii from dehydrated infant formula. FDA. http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/ucm114665. Accessed 26 December 2010
  59. Urmenyi AM, Franklin AW (1961) Neonatal death from pigmented coliform infection. Lancet 1:313–315PubMedCrossRefGoogle Scholar
  60. 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 39:293–297PubMedCrossRefGoogle Scholar
  61. Willis J, Robinson JE (1988) Enterobacter sakazakii meningitis in neonates. Pediatr Infect Dis J 7:196–199PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag and the University of Milan 2011

Authors and Affiliations

  • XianFeng Zhou
    • 1
  • SongZhe Fu
    • 1
  • JianXin Gao
    • 1
  • HaiYing Chen
    • 1
    • 2
  1. 1.Nanchang Center for Disease Control and PreventionNanchangChina
  2. 2.Medical College of Nanchang UniversityNanchangChina

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