Korean Journal of Microbiology (미생물학회지)

The Microbiological Society of Korea (한국미생물학회)
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Current Cronobacter spp. Researches on Prevalence, Control, and Detection

Cronobacter spp. 의 오염, 제어, 검출에 관한 최신 연구동향

  • 송광영 (건국대학교 KU 식품안전연구소) ;
  • 천정환 (건국대학교 KU 식품안전연구소) ;
  • 김현숙 (캘리포니아 대학교(UC DAVIS) 영양학과) ;
  • 서건호 (건국대학교 KU 식품안전연구소)
  • Received : 2012.11.12
  • Accepted : 2012.11.28
  • Published : 2012.12.31
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Abstract

Cronobacter spp. (formerly Enterobacter sakazakii), a Gram-negative bacillus, is a rare cause of meningitis and central nervous system infections. In England, the first case infected by this organism occurred in 1958. By July 2008, approximately 120 documented cases of Cronobacter spp. infection and at least 27 deaths have been identified from all around the world in the published literature and in reports submitted by public health sectors. In 2007, it was proposed by European organizations that the original taxonomy of E. sakazakii would be revised, to consist of five new species moved to a new genus, and identified as "Cronobacter". E. sakazakii has thus now been reclassified as 6 separate species in the new genus, Cronobacter, gen. nov., within the Enterobacteriaceae family. The new species are presently Cronobacter sakazakii, C. turicensis, C. malonaticus, C. muytjensii, and C. dublinensis; the sixth species is identified simply as genomospecies I, as currently including only two representative strains. The objectives of this review are to provide insight on (1) the classification and taxonomy of Cronobacter spp., (2) its clinical etiology and pathogenicity, (3) prequency of Cronobacter spp. in different categories of ready-to-eat food other than infant formula, (4) methods for detecting, isolating and typing Cronobacter spp., and (5) recent research trends for detecting Cronobacter spp.

Keywords

References

  1. Almeida, C., Azevedo, N.F., Iversen, C., Fanning, S., Keevil, C.W., and Vieira, M.J. 2009. Development and application of a novel peptide nucleic acid probe for the specific detection of Cronobacter genomospecies (Enterobacter sakazakii) in powdered infant formula. Appl. Environ. Microbiol. 75, 2925-2930. https://doi.org/10.1128/AEM.02470-08
  2. Byun, M.W. and Lee, J.W. 2003. Application of irradiation technology for food safety and security. Food Sci. Ind. 36, 25-41.
  3. Chen, Y., Hammack, T.S., Song, K.Y., and Lampel, K.A. 2009. Evaluation of a revised U.S. Food and Drug Administration method for the detection and isolation of Enterobacter sakazakii in powdered infant formula: precollaborative study. J. AOAC Int. 92, 862-872.
  4. Chen, Y., Song, K.Y., Brown, E.W., and Lampel, K.A. 2010. Development of an improved protocol for the isolation and detection of Enterobacter sakazakii (Cronobacter) from powdered infant formula. J. Food Prot. 73, 1016-1022. https://doi.org/10.4315/0362-028X-73.6.1016
  5. Choi, B.K., Park, S.Y., Ha, S.D., Kum, J.S., Lee, H.Y., and Park, J.D. 2007. Effect of drying methods of rice flour on growth properties of Bacillus cereus and Enterobacter sakazakii. Korean J. Food Sci. Technol. 39, 295-298.
  6. Choi, J.W., Kim, Y.J., Lee, J.K., Kim, Y.H., Kwon, K.S., Hwang, I.G., and Oh, S.W. 2008. Multiple confirmation and RAPD-genotyping of Enterobacter sakazakii isolated from Sunsik. Korean J. Food Sci. Technol. 40, 101-105.
  7. Choi, M.S., Cheigh, C.I., Jeong, E.A., Shin, J.K., Park, J.Y., Song, K.B., Park, J.H., Kwon, K.S., and Chung, M.S. 2009. Inactivation of Enterobacter sakazakii inoculated on formulated infant foods by intense pulsed light treatment. Food Sci. Biotechnol. 18, 1537-1540.
  8. Chon, J.W., Song, K.Y., Hyeon, J.Y., and Seo, K.H. 2012. Isolation and characterization of cronobacter from desiccated foods in Korea. J. Food Sci. 77, M354-M358. https://doi.org/10.1111/j.1750-3841.2012.02750.x
  9. Chon, J.W., Song, K.Y., Kim. S.Y., Hyeon, J.Y., Kim, Y.G., Hwang, I.G., Kwak, H.S., and Seo, K.H. 2011. Comparison of real-time PCR and conventional culture method for detection of Cronobacter spp. in powdered foods. Korean J. Microbiol. 47, 1-5.
  10. Chun, H.Y., Kim, J.Y., Kim, H.J., and Song, K.B. 2009. Effects of UV-C irradiation on the quality of Sunsik and Misutkaru during storage. J. Food Sci. Nutr. 14, 226-232. https://doi.org/10.3746/jfn.2009.14.3.226
  11. Commission Regulation (EC). 2007. No 1441/2007 of 5 December 2007 amending regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs. 2007. Official Journal of the European Union. L 322/12 -29.
  12. El-Sharoud, W.M., O'Brien, S., Negredo, C., Iversen, C., Fanning, S., and Healy, B. 2009. Characterization of Cronobacter recovered from dried milk and related products. BMC Microbiol. 9, 24. https://doi.org/10.1186/1471-2180-9-24
  13. Farmer, J.J. III. 1995. Enterobacteriaceae: introduction and identification. Manual of Clinical Microbiology, pp. 438-449. In Murray, P.R., Barron, E.J., Pfaller, M.A., Tenover, F.C., and Yolken, R.H. (6th ed) ASM Press Inc., Washington, D.C., USA.
  14. Farmer, J.J. III. 1999. Enterobacteriaceae: introduction and identification. Manual of Clinical Microbiology (7th ed), pp. 442- 458. In Murray, P.R., Barron, E.J., Pfaller, M.A., Tenover, F.C., and Yolken, R.H. (eds.) ASM Press Inc., Washington, D.C., USA.
  15. Farmer, J.J. III., Asbury, M.A., Hickman, F.W., and Brenner, D.J. 1980. Enterobacteriaceae Study Group (USA): Enterobacter sakazakii: a new species of "Enterobacteriaceae" isolated from clinical specimens. Int. J. Syst. Bacteriol. 30, 569-584 https://doi.org/10.1099/00207713-30-3-569
  16. Farmer, J.J. III. and Kelly, M.T. 1992. Enterobacteriaceae. Manual of Clinical Microbiology, pp. 360-383. In Balows, A. (ed.). ASM Press Inc., Washington, D.C., USA.
  17. Food and Agriculture Organizaqtion/World Health Organizatgion. 2004. Joint FAO/WHO workshop on Enterobacter sakazakii and other microorganisms in powdered infant formula. Available from: hppt://www.who.int/foodsafety/publications/feb. 2004/en/print.html. Accessed Dec. 20, 2011.
  18. Gurtler, J.B., Kornacki, J.L., and Beuchat, L.R. 2005. Enterobacter sakazakii: A coliform of increased concern to infant health. Int. J. Food Microbiol. 104, 1-34. https://doi.org/10.1016/j.ijfoodmicro.2005.02.013
  19. Gyeongji-do Research Institute of Health & Environment (GIHE). 2008. Isolation and inactivation of Enterobacter sakazakii from humans foods and related raw materials. Available from: http://gihe.gg.go.kr/ main.do. Accessed on Dec. 25, 2010.
  20. Hwang, J.Y., Lee, J.Y., and Park, J.H. 2008. Microbiological quality and potential pathogen monitoring for powdered infant formulas from the local market. Korean J. Food Sci. Ani. Resour. 28, 555-561. https://doi.org/10.5851/kosfa.2008.28.5.555
  21. Hyeon, J.Y., Park, C., Choi, I.S., Holt, P.S., and Seo, K.H. 2010. Development of multiplex real-time PCR with Internal amplification control for simultaneous detection of Salmonella and Cronobacter in powdered infant formula. Int'l J. Food Microbiol. 144, 177-181. https://doi.org/10.1016/j.ijfoodmicro.2010.09.022
  22. Iversen, C. and Forsythe, S.J. 2003. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 11, 443-454.
  23. Iversen, C., Lancashire, L., Waddington, M., Forsythe, S., and Ball, G. 2006a. Identification of Enterobacter sakazakii from closely related species: The use of artificial neural networks in the analysis of biochemical and 16S rRNA data. BMC Microbiol. 6, 28. https://doi.org/10.1186/1471-2180-6-28
  24. Iversen, C., Lehner, A., Mullane, N., Bidlas, E., Cleenwerck, I., Marugg, J., Fanning, S., Stephan, R., and Joosten, H. 2007a. The taxonomy of Enterobacter sakazakii proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov. Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies 1. BMC Evol. Biol. 7, 64. https://doi.org/10.1186/1471-2148-7-64
  25. Iversen, C., Lehner, A., Mullane, N., Marugg, J., Fanning, S., Stephan, R., and Joosten, H. 2007b. Identification of "Cronobacter" spp. (Enterobacter sakazakii). J. Clin. Microbiol. 45, 3814-3816. https://doi.org/10.1128/JCM.01026-07
  26. Iversen, C., Mullane, N., McCardell, B., Tall, B.D., Lehner, A., Fanning, S., Stephan, R., and 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. System Evol. Microbiol. 58, 1442-1447. https://doi.org/10.1099/ijs.0.65577-0
  27. Iversen, C., Waddington, M., Farmer, J.J. III., and Forsythe, S. 2006b. The biochemical differentiation of Enterobacter sakazakii genotypes. BMC Microbiol. 6, 94. https://doi.org/10.1186/1471-2180-6-94
  28. Iversen, C., Waddington, M., On, S.L., and Forsythe, S. 2004. Identification and phylogeny of Enterobacter sakazakii relative to Enterobacter and Citrobacter species. J. Clin. Microbiol. 42, 5368- 5370. https://doi.org/10.1128/JCM.42.11.5368-5370.2004
  29. Jin, Y.Y., Ku, K.J., Park, J.Y., Park, J.H., Chung, M.S., Kwon, K.S., Chung, K.S., Won, M.S., and Song, K.B. 2008. Comparison on inactivation of Enterobacter sakazakii, Salmonella typhimurium and Bacillus cereus inoculated on infant formula during storage by Gamma irradiation. Food Sci. Biotechnol. 17, 861-864.
  30. Joker, R.N., Norholm, T., and Siboni, K.E. 1965. A case of neonatal meningitis caused by a yellow Enterobacter. Danish Med. Bull. 12, 128-130.
  31. Jung, M.K. and Park, J.H. 2006. Prevalence and thermal stability of Enterobacter sakazakii from unprocessed ready-to-eat agricultural products and powdered infant formulas. Food Sci. Biotechnol. 15, 152-157.
  32. Kandhai, M.C., Reij, M.W., van Puyvelde, K., Guillaume-Gentil, O., Beumer, R.R., and van Schothorst, M. 2004. A new protocol for the detection of Enterobacter sakazakii applied to environmental samples. J. Food Prot. 67, 1267-1270. https://doi.org/10.4315/0362-028X-67.6.1267
  33. Kang, E.S., Nam, Y.S., and Hong, K.W. 2007. Rapid detection of Enterobacter sakazakii using TaqMan Real-Time PCR assay. J. Microbiol. Biotechnol. 17, 516-519.
  34. Kim, S.C. 2008. Bacteriological monitoring of radiology room apparatus in the department of radiological technology and contamination on hands of radiological technologists. J. Radiological Sci. Technol. 31, 329-336.
  35. Kim, J.B., Cho, S.H., Park, Y.B., Lee, J.B., Kim, J.C., Lee, B.K., Lee, H.K., and Chae, H.S. 2008b. Surveillance of stool samples for the presence of Enterobacter sakazakii among Korean people. Yonsei Med. J. 49, 1017-1022. https://doi.org/10.3349/ymj.2008.49.6.1017
  36. Kim, H.J., Koo, M., and Oh, S.W. 2010. Performance comparison of 3 different isolation media of Cronobacter sakazakii. J. Korean Soc. Food Sci. Nutr. 39, 764-768. https://doi.org/10.3746/jkfn.2010.39.5.764
  37. Kim, S.A., Lee, Y.M., Oh, S.W., Gwak, H.S., Hwang, I.G., Kang, D.H., Woo, G.J., and Rhee, M.S. 2009. Biofilm formation and low pH viability of Cronobacter spp. (Enterobacter sakazakii) isolated from powdered infant formula and infant foods in Korea. Korean J. Food Sci. Ani. Resour. 29, 702-708. https://doi.org/10.5851/kosfa.2009.29.6.702
  38. Kim, S.H. and Park, J.H. 2007. Thermal resistance and inactivation of Enterobacter sakazakii isolates during rehydration of powdered infant formula. J. Microbiol. Biotechnol. 17, 364-368.
  39. Kim, J.B., Park, Y.B., Lee, M.J., Kim, K.C., Huh, J.W., Kim, D.H., Lee, J.B., Kim, J.C., Choi, J.H., and Oh, D.H. 2008a. Effect of hot water and microwave heating on the inactivation of Enterobacter sakazakii in reconstituted powdered infant formula and Sunsik. J. Fd. Hyg. Safety 23, 157-162.
  40. Kim, H.K., Ryu, J.H., and Beuchat, L.R. 2007. Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm. Appl. Environ. Microbiol. 73, 1256-1265. https://doi.org/10.1128/AEM.01766-06
  41. Kuzina, L.V., Peloquin, J.J., Vacek, D.C., and Miller, T.A. 2001. Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Curr. Microbiol. 42, 290-294.
  42. Lai, K.K. 2001. Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine 80, 113-122. https://doi.org/10.1097/00005792-200103000-00004
  43. Lampel, K.A. and Chen, Y. 2009. Method for the isolation and detection of Enterobacter sakazakii (Cronobacter) from powdered infant formula. Int. J. Food Microbiol. 136, 179-184. https://doi.org/10.1016/j.ijfoodmicro.2009.08.016
  44. Lee, J.W., Oh, S.H., Byun, E.B., Kim, J.H., Kim, J.H., Woon, J.H., and Byun, M.W. 2007. Inactivation of Enterobacter sakazakii of dehydrated infant formula by gamma-irradiation. Radiat. Phys. Chem. 76, 1858-1861. https://doi.org/10.1016/j.radphyschem.2007.02.105
  45. Lee, J.W., Oh, S.H., Kim, J.H., Yook, H.S., and Byun, M.W. 2006. Gamma radiation sensitivity of Enterobacter sakazakii in dehydrated powdered infant formula. J. Food Prot. 69, 1434-1437. https://doi.org/10.4315/0362-028X-69.6.1434
  46. Lee, E.J. and Park, J.H. 2008. Inactivation activity of bronze alloy Yugi for reduction of cross-contamination of food-borne pathogen in food processing. J. Fd. Hyg. Safety 23, 309-313.
  47. Lee, E.J. and Park, J.H. 2010. Biocontrol of isolated Cronobacter spp. (Enterobacter sakazakii) by heat, sanitizer, and antibiotic. Korean J. Food Sci. Ani. Resour. 30, 479-486. https://doi.org/10.5851/kosfa.2010.30.3.479
  48. Lee, E.J., Ryu, T.H., and Park, J.H. 2009. Tolerance of Korean Cronobacter spp. (Enterobacter sakazakii) isolates to dessication. Korean J. Food Sci. Technol. 41, 681-686.
  49. Lehner, A., Tasara, T., and Stephan, R. 2004. 16S rRNA gene based analysis of Enterobacter sakazakii strains from different sources and development of a PCR assay for identification. BMC Microbiol. 4, 43. https://doi.org/10.1186/1471-2180-4-43
  50. Mange, J.P., Stephan, R., Borel, N., Wild, P., Kim, K.S., Pospischil, A., and Lehner, A. 2006. Adhesive properties of Enterobacter sakazakii to human epithelial and brain microvascular endothelial cells. BMC Microbiol. 6, 58. https://doi.org/10.1186/1471-2180-6-58
  51. Moon, J.H., Lee, H.O., Shim, J.Y., Kim, I.H., Shin, H.S., Won, S.I., Paik, M.K., Shin, H.S., and Om, A.S. 2008. Study on the amendment of standard regulations of food additives and contaminants for infant formulas in Korea. J. Korean Soc. Food Sci. Nutr. 37, 1214-1221. https://doi.org/10.3746/jkfn.2008.37.9.1214
  52. Mullane, N., Healy, B., Meade, J., Whyte, P., Wall, P.G., and Fanning, S. 2008. Dissemination of Cronobacter spp. (Enterobacter sakazakii) in a powdered milk protein manufacturing facility. Appl. Environ. Microbiol. 74, 5913-5917. https://doi.org/10.1128/AEM.00745-08
  53. Muytjens, H.L. and Kollee, L.A.A. 1990. Enterobacter sakazakii meningitis in neonates: causative role of formula. Pediatr. Infect. Dis. J. 9, 372-373. https://doi.org/10.1097/00006454-199005000-00016
  54. Muytjens, H.L., van der Ros-van de Repe, J., and van Druten, H.A.M. 1984. Enzymatic profiles of Enterobacter sakazakii and related species with special reference to the alpha glucosidase reaction and reproducibility of the test system. J. Clin. Microbiol. 20, 684-686.
  55. Park, S., Shukla, S., Kim, Y., Oh, S., Hun Kim, S., and Kim, M. 2012. Development of sandwich enzyme-linked immunosorbent assay for the detection of Cronobacter muytjensii (formerly called Enterobacter sakazakii). Microbiol. Immunol. 56, 472-479. https://doi.org/10.1111/j.1348-0421.2012.00466.x
  56. Park, J.H., Yoon, S.S., and Park, Y.S. 2008. Growth inhibitory activity of Enterococcus faecium isolated from bovine intestinal tract against Enterobacter sakazakii. Korean J. Food Sci. Ani. Resour. 28, 99-104. https://doi.org/10.5851/kosfa.2008.28.1.99
  57. Pearce, L.E., Smythe, B.W., Crawford, R.A., Oakley, E., Hathaway, S.C., and Shepherd, J.M. 2012. Pasteurization of milk: the heat inactivation kinetics of milk-borne dairy pathogens under commercial-type conditions of turbulent flow. J Dairy Sci. 95, 20-35. https://doi.org/10.3168/jds.2011-4556
  58. Raghav, M. and Aggarwal, P.K. 2007. Purification and characterization of Enterobacter sakazakii enterotoxin. Can. J. Microbiol. 53, 750- 755. https://doi.org/10.1139/W07-037
  59. Richards, G.M., Gurtler, J.B., and Beuchat, L.R. 2005. Survival and growth of Enterobacter sakazakii in infant rice cereal reconstituted with water, milk, liquid infant formula, or apple juice. J. Appl. Microbiol. 99, 844-850. https://doi.org/10.1111/j.1365-2672.2005.02656.x
  60. Seo, K.H. and Brackett, R.E. 2005. Rapid, specific detection of Enterobacter sakazakii in infant formula using a real-time PCR assay. J. Food Prot. 68, 59-63. https://doi.org/10.4315/0362-028X-68.1.59
  61. Seo, K.Y., Heo, S.K., Bae, D.H., Oh, D.H., and Ha, S.D. 2008. Growth characteristics of Enterobacter sakazakii used to develop a predictive model. Food Sci. Biotechnol. 17, 642-650.
  62. Song, K.Y., Hyeon, J.Y., Shin, H.C., Park, C.K., Choi, I.S., and Seo, K.H. 2008. Evaluation of a chromogenic medium supplemented with glucose for detecting Enterobacter sakazakii. J. Microbiol. Biotechnol. 18, 579-584.
  63. Teramoto, S., Tanabe, Y., Okano, E., Nagashima. T., Kobayashi, M., and Etoh, Y. 2010. A first fatal neonatal case of Enterobacter sakazakii infection in Japan. Pediatr. Int. 52, 312-313. https://doi.org/10.1111/j.1442-200X.2010.03030.x
  64. United States Food and Drug Administration (US FDA). 2002. Isolation and enumeration of Enterobacter sakazakii from dehydrated powdered infant formula. Available at: http://www.cfsan.fda.gov/ -dms/inf- ltr3.html. Accessed Dec. 27, 2010.
  65. United States Food and Drug Administration (US FDA). 2011. Investigation of Cronobacter Bacteria Illness in Infants. Washington DC, USA Food and Drug Administration. http://www.fda.gov/NewsEvents/ PublicHealthFocus/ucm285401.htm. Accessed Mar. 15, 2012.
  66. United States Food and Drug Administration (US FDA). 2012. Bacteriological Analytical Manual Chapter 29 Cronobacter. Washington DC, USA Food and Drug Administration. http://www.fda.gov/Food/ScienceResearch/ LaboratoryMethods/ BacteriologicalAnalyticalManualBAM/ucm289378.htm. Accessed Jun. 1, 2012.
  67. Urmenyi, A.M.C. and Franklin, A.W. 1961. Neonatal death from pigmented coliform infection. Lancet 1, 313-315.
  68. Wang, X., Zhu, C.Q., Xu, X.L., and Zhou, G.H. 2012. Real-time PCR with internal amplification control for the detection of Cronobacter spp. (Enterobacter sakazakii) in food samples. Food Control. 25, 144 -149. https://doi.org/10.1016/j.foodcont.2011.10.037
  69. Yoo, M.K., Oh, S., and Kim, S.S. 2005. Isolation and genotyping of Enterobacter sakazakii from powdered infant formula manufactured in Korea. Food Sci. Biotechnol. 14, 875-877.
  70. Yoon, Y.H., Byun, M.W., Kim, W.J., Kwon, J.H., and Lee, J.W. 2010. Current status of food irradiation technology on quarantine of agricultural commodities. Food Sci. Ind. 42, 19-26.
  71. Yu, J.H. 2009. Development of a rapid and miniaturize method for estimation of Cronobacter spp. in reconstituted infant formula. Master's Degree thesis, Korea Univ., Seoul.

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