Characterization of the gene encoding the 16S rRNA of Enterobacter sakazakii and development of a species-specific PCR method

International Journal of Food Microbiology

Volumn 116, Issue 2, 2007, Pages 214-220

  Hassan, Abdulwahed Ahmed ^a   Akineden, Ömer ^a   Kress, Claudia ^a   Estuningsih, Sri ^b   Schneider, Elisabeth ^a   Usleber, Ewald ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

Author keywords

16S rRNA; Enterobacter sakazakii; PCR; Powdered infant formula

Indexed keywords

RNA 16S;

AMPLICON; ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATION; CITROBACTER KOSERI; COMPARATIVE STUDY; CONTROLLED STUDY; ENTEROBACTER SAKAZAKII; ENTEROBACTERIACEAE; GENE SEQUENCE; GENETIC TRAIT; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA;

BASE SEQUENCE; CONSUMER PRODUCT SAFETY; DNA, BACTERIAL; ENTEROBACTER SAKAZAKII; FOOD CONTAMINATION; HUMANS; INFANT; INFANT FORMULA; INFANT, NEWBORN; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; VARIATION (GENETICS);

CITROBACTER; ENTEROBACTER SAKAZAKII; ENTEROBACTERIACEAE; SALMONELLA ENTERICA;

EID: 33947573543     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2006.12.011     Document Type: Article

References (50)

1. Adamson D.H., and Rogers J.R. Enterobacter sakazakii meningitis with sepsis. Clinical Microbiology Newsletter 3 (1981) 19-20
2. Anonymous. Enterobacter sakazakii and other microorganisms in powdered infant formula: meeting report. Microbiological Risk Assessment Series vol. 6 (2004). 92 4 156262 5. http://www.who.int/foodsafety/publications/micro/es.pdf Available at: http://www.who.int/foodsafety/publications/micro/es.pdf
3. Anonymous. Opinion of the scientific panel on biological hazards on a request from the commission related to the microbiological risks in infant formula and follow-on formulae. EFSA Journal 113 (2004) 1-35. http://www.efsa.eu.int Available at: http://www.efsa.eu.int
4. Anonymous. Commission regulation (EC) no 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union 48 L338 (2005) 1-26. http://europa.eu.int/eur-lex/lex/JOIndex.do?ihmlang=en Available at: http://europa.eu.int/eur-lex/lex/JOIndex.do?ihmlang=en
5. Bentley R.W., and Leigh J.A. Development of PCR-based hybridization protocol for identification of streptococcal species. Journal of Clinical Microbiology 33 (1995) 1296-1301
6. Bertilsson S., Cavanaugh C.M., and Polz M.F. Sequencing-independent method to generate oligonucleotide probes targeting a variable region in bacterial 16S rRNA by PCR with detachable primers. Applied and Environmental Microbiology 6 (2002) 6077-6086
7. Biering G., Karlsson S., Clark N.C., Jónsdóttir K.E., Lúdvígsson P., and Steingrímsson O. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. Journal of Clinical Microbiology 27 (1989) 2054-2056
8. Block C., Peleg O., Minster N., Bar-Oz B., Simhon A., Arad I., and Shapiro M. Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. European Journal of Clinical Microbiology and Infectious Diseases 21 (2002) 613-616
9. Brenner D.J., and Farmer III J.J. Family I. Enterobacteriaceae. In: Brenner D.J., Krieg N.R., and Staley J.T. (Eds). Bergey's Manual of Systematic Bacteriology, Volume Two: The Proteobacteria Part B: The Gammaproteobacteria (2005), Springer, New York 587-669
10. Burdette J.H., and Santos C. Enterobacter sakazakii brain abscess in the neonate: the importance of neuroradiologic imaging. Pediatric Radiology 30 (2000) 33-34
11. Clark N.C., Hill B.C., O'Hara C.M., Steingrímsson O., and Cooksey R.C. Epidemiologic typing of Enterobacter sakazakii in two neonatal nosocomial outbreaks. Diagnostic Microbiology and Infectious Disease 13 (1990) 467-472
12. Estuningsih S., Kress C., Hassan A.A., Akineden Ö., Schneider E., and Usleber E. Enterobacteriaceae in dehydrated powdered infant formula manufactured in Indonesia and Malaysia. Journal of Food Protection 69 (2006) 3013-3017
13. Farmer III J.J., Asbury M.A., Hickman F.W., Brenner D.J., and and the Enterobacteriaceae Study Group. Enterobacter sakazakii, new species of Enterobacteriaceae isolated from clinical specimens. International Journal of Systematic Bacteriology 30 (1980) 569-584
14. FDA, U. S. Food and Drug Administration. Isolation and Enumeration of Enterobacter sakazakii from Dehydrated Powdered Infant Formula (2002). http://www.cfsan.fda.gov/~comm/mmesakaz.html Available at: http://www.cfsan.fda.gov/~comm/mmesakaz.html
15. Guillaume-Gentil O., Sonnard V., Kandhai M.C., Marugg J.D., and Joosten H. A simple and rapid cultural method for detection of Enterobacter sakazakii in environmental samples. Journal of Food Protection 68 (2005) 64-69
16. Harada H., Oyaizu H., and Ishikawa H. A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora. Journal of General and Applied Microbiology 42 (1996) 17-26
17. Hassan A.A., Abdulmawjood A., Yildirim A.Ö., Fink K., Lämmler C., and Schlenstedt R. Identification of streptococci isolated from various sources by determination of cfb gene and other CAMP-factor genes. Canadian Journal of Microbiology 46 (2000) 946-951
18. Hawkins R.E., Lissner C.R., and Sanford J.P. Enterobacter sakazakii bacteremia in an adult. Southern Medical Journal 84 (1991) 793-795
19. Himelright I., Harris E., Lorch V., and Anderson M. Enterobacter sakazakii infections associated with the use of powdered infant formula - Tennessee, 2001. Journal of American Medical Association 287 (2002) 2204-2205
20. Hoffmann H., Stindl S., Stumpf A., Mehlen A., Monget D., Heesemann J., Schleifer K.H., and Roggenkamp A. Description of Enterobacter ludwigii sp. nov., a novel Enterobacter species of clinical relevance. Systematic and Applied Microbiology 28 (2005) 206-212
21. Iversen C., and Forsythe S.J. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Food Science and Technology 14 (2003) 443-454
22. Iversen C., Druggan P., and Forsythe S.J. A selective differential medium for Enterobacter sakazakii, a preliminary study. International Journal of Food Microbiology 96 (2004) 133-139
23. Iversen C., Dale H., Druggan P., Waddington M., Crawford J., and Forsythe S.J. The Identification of Enterobacter sakazakii Using Partial 16S Sequencing and Biochemical Techniques. 104th ASM General Meeting, New Orleans, LA (2004)
24. Iversen C., Waddington M., On S.L.W., and Forsythe S. Identification and phylogeny of Enterobacter sakazakii relative to Enterobacter and Citrobacter species. Journal of Clinical Microbiology 42 (2004) 5368-5370
25. Kämpfer P., Ruppel S., and Remus R. Enterobacter radicincitans sp. nov., a plant growth promoting species of the family Enterobacteriaceae. Systematic and Applied Microbiology 28 (2005) 213-221
26. 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
27. Kleiman M.B., Allen S.D., Neal P., and Reynolda J. Meningoencephalitis and compartmentalization of the cerebral ventricles caused by Enterobacter sakazakii. Journal of Clinical Microbiology 14 (1981) 352-354
28. Kolbert C.P., and Persing D.H. Ribosomal DNA sequencing as a tool for identification of bacterial pathogens. Current Opinion in Microbiology 2 (1999) 299-305
29. Kress C., Hassan A.A., Akineden Ö., Schneider E., Estuningsih S., Becker H., and Usleber E. Enterobacter sakazakii in Trockenerzeugnissen auf Milchbasis. In: DVG (Ed). Deutsche Veterinärmedizinische Gesellschaft. Arbeitstagung des Arbeitsgebietes Lebensmittelhygiene der Deutschen Veterinärmedizinischen Gesellschaft e.V., 27.-30.09.2005 in Garmisch-Partenkirchen vol. 46 (2005). 3-938026-60-X 190-195
30. Kuhnert P., Capaul S.E., Nicolet J., and Frey J. Phylogenetic positions of Clostridium chauvoei and Clostridium septicum based on 16S rRNA gene sequences. International Journal of Systematic Bacteriology 46 (1996) 1174-1176
31. Lau D.K., and Rotton J.W. Development of a Real Time PCR Method for the Detection of Enterobacter sakazakii (2005). http://www.cfsan.fda.gov/~frf/forum04/C-PO-07.html Available at: http://www.cfsan.fda.gov/~frf/forum04/C-PO-07.html
32. Lehmacher A., and Fiegen M. Nachweis, Typiserung und rechtliche Beurteilung von Enterobacter sakazakii in Säuglingsnahrung. Abstracts 7. Fachsymposium Lebensmittelmikrobiologie der VAAM-Fachgruppe Lebensmittelmikrobiologie in Zusammenarbeit mit der Fachgruppe der DGHM, 6-8 April, Seeon, Germany (2005)
33. Lehner A., Tasara T., and Stephan R. 16S rRNA gene based analysis of Enterobacter sakazakii strains from different sources and development of a PCR assay for identification. BMC Microbiology 4 (2004) 43 10.1186/1471-2180-4-43
34. Lehner A., Nitzsche S., Breeuwer P., Diep B., Thelen K., and Stephan R. Comparison of two chromogenic media and evaluation of two molecular based identification systems for Enterobacter sakazakii detection. BMC Microbiology 6 (2006) 15 10.1186/1471-2180-6-15
35. Leuschner R.G.K., and Bew J. A medium for the presumptive detection of Enterobacter sakazakii in infant formula: interlaboratory study. Journal of AOAC International 87 (2004) 604-613
36. Malorny B., and Wagner M. Detection of Enterobacter sakazakii strains by real-time PCR. Journal of Food Protection 68 (2005) 1623-1627
37. Monroe P.W., and Tift W.L. Bacteremia associated with Enterobacter sakazakii (yellow-pigmented Enterobacter cloacae). Journal of Clinical Microbiology 10 (1979) 850-851
38. Monstein H.J., Kihlstrom E., and Tiveljung A. Detection and identification of bacteria using in-house broad range 16S rRNA gene PCR amplification and genus-specific DNA hybridization probes, located within variable regions of 16S rRNA genes. Acta Pathologica, Microbiologica et Immunologica Scandinavica 104 (1996) 451-458
39. Monstein H., Nikpour-Badr S., and Jonasson J. Rapid molecular identification and subtyping of Helicobacter pylori by pyrosequencing of the 16S rRNA gene variable V1 and V3 regions. FEMS Microbiology Letters 199 (2001) 103-107
40. Muytjens H.L., Zanen H.C., Sonderkamp H.J., Kollee 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
41. 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
42. Nazarowec-White M., and Farber J.M. Phenotypic and genotypic typing of food and clinical isolates of Enterobacter sakazakii. Journal of Medical Microbiology 48 (1999) 559-567
43. Römermann A., Bürk C., Becker H., and Märtlbauer E. Nachweis von Enterobacter sakazakii in Säuglingsnahrung mittels PCR. In: DVG (Ed). Deutsche Veterinärmedizinische Gesellschaft. Arbeitstagung des Arbeitsgebietes "Lebensmittelhygiene" der Deutschen Veterinärmedizinischen Gesellschaft e.V. vom 29.09-02.10.2003 in Garmisch-Partenkirchen vol. 44 (2003). 3-936815-85-2 372-376
44. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. (1989), Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
45. Seo K.H., and Brackett R.E. Rapid, specific detection of Enterobacter sakazakii in infant formula using a real-time PCR assay. Journal of Food Protection 68 (2005) 59-63
46. Tärnberg M., Jakobsson T., Jonasson J., and Forsum U. Identification of randomly selected colonies of lactobacilli from normal vaginal fluid by pyrosequencing of the 16S rRNA gene variable V1 and V3 regions. Acta Pathologica, Microbiologica et Immunologica Scandinavica 110 (2002) 802-810
47. Urmenyi A.M.C., and Franklin A.W. Neonatal death from pigmented coliform infection. Lancet 1 (1961) 313-315
48. 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
49. Weiss C., Becker B., and Holzapfel W. Application and acceptability of three commercial systems for detection of Enterobacter sakazakii in ready-to-eat vegetable salads. Archiv für Lebensmittelhygiene 56 (2005) 34-38
50. Woo P.C., Ng K.H., Lau S.K., Yip K.T., Fung A.M., Leung K.W., Tam D.M., Que T.L., and Yuen K.Y. Usefulness of the MicroSeq 500 16S ribosomal DNA-based bacterial identification system for identification of clinically significant bacterial isolates with ambiguous biochemical profiles. Journal of Clinical Microbiology 41 (2003) 1996-2001