Abstract
Dairy or non-dairy based products were explored to determine the prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter spp. The isolation was done as per ISO 22964:2006 on chromogenic media followed by further confirmation by biochemical- and 16S rRNA-based identification. From 219 samples, the chromogenic agar assay and biochemical tests yielded presumptive 45 isolates. Among them, only 36 isolates showed 282 bp band amplified from ITS-G gene confirming as Cronobacter sakazakii. The Cronobacter spp. prevalence was highest in herbs and spices (34 %) while environmental samples had contamination rates of 23 % indicating plants as a possible reservoir of this pathogen. All the isolates were resistant to β-lactam derivatives (68 %), macrolides (88.6 %), and aminoglycosides (79.9 %) but susceptible to phenicoles (31.6 %) and tetracyclines (15 %) derivatives. The results emphasize the screening of plant materials before their incorporation in food matrices.
Similar content being viewed by others
References
Al-Nabulsi AA, Osaili TM, Al-Holy MA, Shaker RR, Ayyash MM, Olaimat AN, Holley RA (2009) Influence of desiccation on the sensitivity of Cronobacter spp. to lactoferrin or nisin in broth and powdered infant formula. Int J Food Microbiol 136:221–226
Barron JC, Forsythe SJ (2007) Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J Food Prot 70:2111–2117
Block C, Peleg O, Minster N (2002) Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur J Clin Microbiol Infect Dis 21:613–616
Brady C, Cleenwerck I, Venter S, Coutinho T, De Vos P (2013) Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter. Syst Appl Microbiol 36:309–319
Butler JF, Garcia-Maruniak A, Meek F (2010) Wild florida house flies (Musca domestica) as carriers of pathogenic bacteria. Fla Entomol 93:218–223
Corti G, Panunzi I, Losco M, Buzzi R (2007) Post-surgical osteomyelitis caused by Enterobacter sakazakii in a healthy young man. J Chemother 19:94
Drudy D, O’Rourke M, Murphy M, Mullane N, O’Mahony R, Kelly L, Fischer M, Sanjaq S, Shannon P, Wall P, O’Mahony M, Whyte P, Fanning S (2006) Characterization of a collection of Enterobacter sakazakii isolates from environmental and food sources. Int J Food Microbiol 110:127–134
Fanjat N, Leclercq A, Joosten H, Robichon D (2007) Comparison of the phenotyping methods ID32 and VITEK 2 compact GN with 16S rDNA gene sequencing for the identification of Enterobacter sakazakii. J Clin Microbiol 45:2048–2050
Forsythe SJ (2005) Enterobacter sakazakii and other bacteria in powdered infant milk formula. J Matern Child Nutr 1:44–50
Friedemann M (2007) Enterobacter sakazakii in food and beverages (other than infant formula and milk powder). Int J Food Microbiol 116:1–10
Girlich D, Poirel L, Leelaporn A, Karim A, Tribuddharat C, Fennewald M et al (2001) Molecular epidemiology of the integron-located VEB-1 extended-spectrum beta-lactamase in nosocomial enterobacterial isolates in Bangkok, Thailand. J Clin Microbiol 39:175–182
Gosney MA, Martin MV, Wright AE (2006) Enterobacter sakazakii in the mouths of stroke patients and its association with aspiration pneumonia. Eur J Intern Med 17:185–188
Hamilton JV, Lehane MJ, Braig HR (2003) Isolation of Enterobacter sakazakii from midgut of Stomoxys calcitrans. Emerg Infect Dis 9:1355–1356
Iversen C, Forsythe SJ (2003) Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci Technol 14:443–454
Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, Fanning S, Stephan R, Joosten H (2007) The taxonomy of Enterobacter sakazakii: proposal of new genus Cronobacter gen. nov., and descriptions of Cronobacter sakazakii comb. nov. Cronobacter sakazakii subsp. Malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., and Cronobacter genomospecies I. BMC Evol Biol 7:64–74
Iversen C, Mullane N, McCardell B (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
Jaradat ZW, Ababneh QO, Saadoun IM, Samara NA, Rashdan AM (2009) Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from infant food, herbs and environmental samples and the subsequent identification and confirmation of the isolates using biochemical, chromogenic and molecular methods. BMC Microbiol 9:225–235
Joseph S, Cetinkaya E, Drahovska H (2011) Cronobacter condimenti sp. nov., isolated from spiced meat and Cronobacter universalis sp. nov., a novel species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water, and food ingredients. Int J Syst Evol Microbiol 62:1277–1283
Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe SJ (2012) Cronobacter condimenti sp nov, isolated from spiced meat and Cronobacter universalis sp nov, a novel species designation for Cronobacter sp genomospecies 1, recovered from a leg infection, water, and food ingredients. Int J Syst Evol Microbiol 62:1277–1283
Kandhai MC, Reij MW, Gorris LG (2004) Occurrence of Enterobacter sakazakii in food production environments and households. The Lancet 363:39–40
Kim K, Jang SS, Kim SK, Park JH, Heu S, Ryu S (2008) Prevalance and genetic diversity of Enterobacter sakazakii in ingredients of infant foods. Int J Food Microbiol 122:196–203
Kothary MH, McCardell BA, Frazar CD (2007) Characterization of the zinc-containing metalloprotease encoded by zpx and development of a species-specific detection method for Enterobacter sakazakii. Appl Environ Microbiol 73:4142–4151
Kuzina LV, Peloquin JJ, Vacek DC (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Curr Microbiol 42:290–294
Lai KK (2001) Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine 80:113–122
Masood N, Jackson E, Moore K et al (2014) Draft genome sequence of “Candidatus Cronobacter colletis” NCTC 14934T, a new species in the genus Cronobacter. Genet Announc 2(3):e00585–e00614
Mullane NR, Iversen C, Healy B (2007) Enterobacter sakazakii an emerging bacterial pathogen with implications for infant health. Minerva Pediatr 59:137–148
Muytjens HL, Zanen HC, Sonderkamp HJ (1983) Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J Clin Microbiol 18:115–120
National Committee for Clinical Laboratory Standards (2003) Performance standards for antimicrobial susceptibility testing, 13th informational supplement, approved standard M100eS13 (M2). National Committee for Clinical Laboratory Standards, Wayne
Nazarowec-White M, Faber JM (1999) Phenotypic and genotyping of food and clinical isolates of Enterobacter sakazakii. J Med Microbiol 48:559–567
Nazarowec-White M, Farber JM (1997) Enterobacter sakazakii: a review. Int J Food Microbiol 34:103–113
Oren A, Garrity GM (2013) List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 63:3931–3934
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 41:35–39
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
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory Manual, II edn. Cold Spring Harbour, New York
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
Stephan R, Van Trappen S, Cleenwerck I (2007) Enterobacter turicensis, sp. nov. and Enterobacter helveticus, sp. nov. isolated from fruit powder. Int J Syst Evol Microbiol 57:820–826
Stock I, Wiedemann B (2002) Natural antibiotic susceptibility of Enterobacter amnigenus, Enterobacter cancerogenus, Enterobacter gergoviae and Enterobacter sakazakii strains. Clin Microbiol Infec 8:564–578
Terragno R, Salve A, Pichel M, Epszteyn S, Brengi S, Binsztein N (2009) Characterization and subtyping of Cronobacter spp. from imported powdered infant formulae in Argentina. Int J Food Microbiol 136:193–197
Van Acker J, de Smet F, Muyldermans G (2001) Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J Clin Microbiol 39:293–297
Acknowledgments
The authors wish to thank Dept. of Science and Technology, Govt. of India and Jaypee University of Information Technology (JUIT), Solan, India for providing financial support and essential facilities required for the research work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Singh, N., Goel, G. & Raghav, M. Prevalence and Characterization of Cronobacter spp. from Various Foods, Medicinal Plants, and Environmental Samples. Curr Microbiol 71, 31–38 (2015). https://doi.org/10.1007/s00284-015-0816-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-015-0816-8