Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula

International Journal of Food Microbiology

Volumn 115, Issue 2, 2007, Pages 195-203

  Kim, Kwang Pyo ^a   Klumpp, Jochen ^a   Loessner, Martin J ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Bacteriophage; Enterobacter sakazakii; Infant formula; Inhibition

Indexed keywords

ARTICLE; ARTIFICIAL MILK; BACTERIAL GROWTH; BACTERIOPHAGE; BIOLOGICAL PEST CONTROL; CELL ISOLATION; CONTROLLED STUDY; ENTEROBACTER SAKAZAKII; NONHUMAN; SEWAGE; TEMPERATURE; ULTRAVIOLET RADIATION;

BACTERIA; BACTERIOPHAGES; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENTEROBACTER SAKAZAKII; FOOD CONTAMINATION; FOOD MICROBIOLOGY; HUMANS; INFANT; INFANT FORMULA; INFANT, NEWBORN; TEMPERATURE; TIME FACTORS;

BACTERIA (MICROORGANISMS); ENTEROBACTER SAKAZAKII;

EID: 33847609256     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2006.10.029     Document Type: Article

References (40)

1. Adams M.H. Methods of study of bacterial viruses. In: Hershey A.D. (Ed). Bacteriophages (1959), Interscience Publishers Inc., New York 443-457
2. Biering G., Karlsson S., Clark N.C., Jonsdottir K.E., Ludvigsson P., and Steingrimsson O. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. Journal of Clinical Microbiology 27 (1989) 2054-2056
3. Breeuwer P., Lardeau A., Peterz M., and Joosten H.M. Desiccation and heat tolerance of Enterobacter sakazakii. Journal of Applied Microbiology 95 (2003) 967-973
4. Carlton R.M., Noordman W.H., Biswas B., de Meester E.D., and Loessner M.J. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatics analyses, oral toxicity study, and application. Regulatory Toxicology and Pharmacology 43 (2005) 301-312
5. Clark N.C., Hill B.C., O'Hara C.M., Steingrimsson O., and Cooksey R.C. Epidemiologic typing of Enterobacter sakazakii in two neonatal nosocomial outbreaks. Diagnostic Microbiology and Infectious Disease 13 (1990) 467-472
6. Dykes G.A., and Moorhead S.M. Combined antimicrobial effect of nisin and a listeriophage against Listeria monocytogenes in broth but not in buffer or on raw beef. International Journal of Food Microbiology 73 (2002) 71-81
7. Edelson-Mammel S.G., and Buchanan R.L. Thermal inactivation of Enterobacter sakazakii in rehydrated infant formula. Journal of Food Protection 67 (2004) 60-63
8. Ellis D.E., Whitman P.A., and Marshall R.T. Effects of homologous bacteriophage on growth of Pseudomonas fragi WY in milk. Applied Microbiology 25 (1973) 24-25
9. Farmer III J.J., Asbury M.A., Hickman F.W., Brenner D.J., and The Enterobacteriaceae study group. Enterobacter sakazakii: a new species of "Enterobacteriaceae" isolated from clinical specimens. International Journal of Systematic Bacteriology 30 (1980) 569-584
10. Food and Drug Administration. Food additives permitted for direct addition to food for human consumption; bacteriophage preparation. Federal Register 71 (2006) 47729-47732
11. Gonzalez S., Flick G.J., Arritt F.M., Holliman D., and Meadows B. Effect of high-pressure processing on strains of Enterobacter sakazakii. Journal of Food Protection 69 (2006) 935-937
12. Goode D., Allen V.M., and Barrow P.A. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Applied and Environmental Microbiology 69 (2003) 5032-5036
13. Hamilton J.V., Lehane M.J., and Braig H.R. Isolation of Enterobacter sakazakii from midgut of Stomoxys calcitrans. Emerging Infectious Diseases 9 (2003) 1355-1356
14. International Commission on Microbiological Specifications for Foods (ICMSF). Microorganisms in Food 7. Microbiological Testing in Food Safety Management (2002), Kluwer Academic/Plenum Publishers
15. Iversen C., Lane M., and Forsythe S.J. The growth profile, thermotolerance and bilfilm formation of Enterobacter sakazakii grown in infant formula milk. Letters in Applied Microbiology 38 (2004) 378-382
16. Kandhai M.C., Reij M.W., Gorris L.G., Guillaume-Gentil O., and van Schothorst M. Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 363 (2004) 39-40
17. Kandhai M.C., Reij M.W., van Puyvelde K., Guillaume-Gentil O., Beumer R.R., and van Schothorst M. A new protocol for the detection of Enterobacter sakazakii applied to environmental samples. Journal of Food Protection 67 (2004) 1267-1270
18. Kuzina L.V., Peloquin J.J., Vacek D.C., and Miller T.A. Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepa ludens (Diptera: Tephritidae). Current Microbiology 42 (2001) 290-294
19. Lai K.K. Enterobacter sakazakii infections among neonates, infants, children, and adults. Medicine 80 (2001) 113-122
20. Lee J.W., Oh S.H., Kim J.H., Yook H.S., and Byun M.W. Gamma radiation sensitivity of Enterobacter sakazakii in dehydrated powdered infant formula. Journal of Food Protection 69 (2006) 1434-1437
21. Lehner A., Riedel R., Eberl L., Breeuwer P., Diep B., and Stephan R. Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. Journal of Food Protection 68 (2005) 2287-2294
22. Leverentz B., Conway W.S., Alavidze Z., Janisiewicz W.J., Fuchs Y., Camp M.J., Chighladze E., and Sulakvelidze A. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. Journal of Food Protection 64 (2001) 1116-1121
23. Leverentz B., Conway W.S., Camp M.J., Janisiewicz W.J., Abuladze T., Yang M., Saftner R., and Sulakvelidze A. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Applied and Environmental Microbiology 69 (2003) 4519-4526
24. Loessner M.J., Neugirg E., Zink R., and Scherer S. Isolation, classification and molecular characterization of bacteriophages for Enterobacter species. Journal of General Microbiology 139 (1993) 2627-2633
25. Mange J.P., Stephan R., Borel N., Wild P., Kim K.S., Pospichil A., and Lehner A. Adhesive properties of Enterobacter sakazakii to human epithelial and brain endothelial cells. BMC Microbiology 6 (2006) 58
26. Muytjens H.L., and Kollee L.A. Enterobacter sakazakii meningitis in neonates: causative role of formula?. Pediatric Infectious Disease Journal 9 (1990) 372-373
27. Muytjens H.L., Zanen H.C., Sonderkamp H.J., Kollée L.A., Wachsmuth I.K., and Farmer III J.J. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. Journal of Clinical Microbiology 18 (1983) 115-120
28. Muytjens H.L., Roelofs-Willemse H., and Jaspar G.H. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. Journal of Clinical Microbiology 26 (1988) 743-746
29. Nazarowec-White M., and Farber J.M. Incidence, survival and growth of Enterobacter sakazakii in infant formula. Journal of Food Protection 60 (1997) 226-230
30. Nazarowec-White M., and Farber J.M. Thermal resistance of Enterobacter sakazakii in reconstituted dried-infant formula. Letters in Applied Microbiology 24 (1997) 9-13
31. Pagotto F.J., Nazarowec-White M., Bidawid S., and Farber J.M. Enterobacter sakazakii: infectivity and enterotoxin production in vitro and in vivo. Journal of Food Protection 66 (2003) 370-375
32. Postupa R., and Aldova E. Enterobacter sakazakii: a Tween 80 esterase-positive representative of the genus Enterobacter isolated from powdered milk specimens. Journal of Hygiene, Epidemiology, Microbiology and Immunology 28 (1984) 435-440
33. Sambrook J., and Russell D.W. Molecular Cloning: A Laboratory Manual. 3rd edition (2001), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
34. Urmenyi A.M.C., and Franklin A.W. Neonatal death from pigmented coliform infection. Lancet 1 (1961) 313-315
35. van Acker J., de Smet F., Muyldermans G., Bougatef A., Naessens A., and Lauwers S. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. Journal of Clinical Microbiology 39 (2001) 293-297
36. Weir E. Powdered infant formula and fatal infection with Enterobacter sakazakii. Canadian Medical Association Journal 166 (2002) 1570
37. Whichard J.M., Sriranganathan N., and Pierson F.W. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. Journal of Food Protection 66 (2003) 220-225
38. Willis J., and Robinson J.E. Enterobacter sakazakii meningitis in neonates. Pediatric Infectious Disease Journal 7 (1988) 196-199
39. You L., Suthers P.F., and Yin J. Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico. Journal of Bacteriology 184 (2002) 1888-1894
40. Zink R., and Loessner M.J. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Applied and Environmental Microbiology 58 (1992) 296-302