Contamination, persistence and dissemination of Cronobacter during the production of powdered infant formula in China in 2016
Main Article Content
Keywords
biofilm, Cronobacter, PFGE, powdered infant formula
Abstract
A total of 620 samples collected from two factories in China producing powdered infant formula (PIF) between July and November 2016 were analyzed for Cronobacter. Antimicrobial susceptibility, pulsed-field gel electrophoresis (PFGE), and biofilm formation of Cronobacter were carried out. The results showed that 2.26% samples were positive for Cronobacter among the 33 isolates that were identified. All Cronobacter isolates were susceptible to 12 antimicrobial agents tested except one isolate which showed intermediate resistance to Chloramphenicol. PFGE analysis showed that nine clusters comprising the 33 isolates were identified, among which C8, C4, and C5 were the predominant types. All 33 isolates were capable of forming biofilm, and particularly, C. malonaticus isolates showed a good biofilm-forming ability at both 28°C and 37°C. The results illustrated that it is necessary for PIF manufactures to develop control measures for reducing Cronobacter contamination and its associated foodborne illness among infants.
References
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Choi, Y., Kim, S., Hwang, H., Kim, K.P. and Ryu, S., 2014. Plasmid-encoded mcp is involved in virulence, motility, and biofilm formation of Cronobacter sakazakii ATCC 29544. Infection and Immunity 83: 197–204. 10.1128/iai.02633-14
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Drapala, K.P., Mulvihill, D.M. and O’Mahony, J.A., 2018. Improving the oxidative stability of model whey protein hydrolysate—based infant formula emulsions with lecithin. International Journal of Dairy Technology 71: 966–974. 10.1111/1471-0307.12538
Fei, P., Man, C., Lou, B., Forsythe, S.J., Chai, Y., Li, R., et al., 2015. Genotyping and source tracking of Cronobacter sakazakii and C. malonaticus isolates from powdered infant formula and an infant formula production factory in china. Applied and Environmental Microbiology 81: 5430–5439. 10.1128/AEM.01390-15
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Forsythe, S.J., 2018. Updates on the Cronobacter Genus. Annual Review of Food Science and Technology 9: 23–44. 10.1146/annurev-food-030117-012246
Friedemann, M., 2008. Enterobacter sakazakii in powdered infant formula. Bundesgesundheitsbla 51: 664–674. 10.1007/s00103-008-0543-4
Gan, X., Bai, L., Yan, S., Wang, J., Wang, W., Li, Z., et al., 2015. Drug resistant analysis of Cronobacter isolated from infant foods in 2012–2014 in China. Journal of Food Safety and Food Quality 6: 3491–3496.
Gan, X., Dong, Y., Yan, S., Hu, Y., Séamus, F., Wang, J., et al., 2018. Contamination and characterization of multiple pathogens in powdered formula at retail collected between 2014 and 2015 in China. Food Control 87: 40–45. 10.1016/j.foodcont.2017.12.014
GB4789.40, 2016. Cronobacter. National Food Safety Standard Food Microbiological Examination. China.
Gu, M., Han, W. and Yang, J., 2008. Study on antibiotic resistance of Enterobacter sakazakii isolated from imported dairy product. Journal of Inspection Quarterly 21: 14–16. 10.3969/j.issn.1674-5354.2008.01.005
Gurtler, J.B. and Beuchat, L.R., 2007. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. Journal of Food Protection 70: 1579. 10.1016/j.jfoodeng.2006.05.001
Henry, M. and Fouladkhah, A., 2019. Outbreak history, biofilm formation, and preventive measures for control of Cronobacter sakazakii in infant formula and infant care settings. Microorganisms 7: 77. 10.3390/microorganisms7030077
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Jaradat, Z.W., Al, M.W., Elbetieha, A., Al, N.A. and Tall, B.D., 2014. Cronobacter spp.-opportunistic foodborne pathogens. A review of their virulence and environmental-adaptive traits. Journal of Medical Microbiology 63: 1023–1037. 10.1099/jmm.0.073742-0
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Lee, Y.D., Park, J.H. and Chang, H.I., 2012. Detection, antibiotic susceptibility and biofilm formation of Cronobacter spp. from various foods in Korea. Food Control 24: 225–230. 10.1016/j.foodcont.2011.09.023
Lehner, A., Fricker-Feer, C. and Stephan, R., 2012. Identification of the recently described Cronobacter condiment by an rpoB-gene-based PCR system. Journal of Medical Microbiology 61: 1034–1035. 10.1099/jmm.0.042903-0
Ling, N., Li, C., Zhang, J., Wu, Q., Zeng, H., He, W., et al., 2018. Prevalence and molecular and antimicrobial characteristics of Cronobacter spp. isolated from raw vegetables in China. Frontiers in Microbiology 9: 1149. 10.3389/fmicb.2018.01149
Liu, Y., Gao, Q., Zhang, X., Hou, Y., Yang, J. and Huang, X., 2006. PCR and oligonucleotide array for detection of Enterobacter sakazakii in infant formula. Molecular and Cellular Probes 20: 11–17. 10.1016/j.mcp.2005.08.004
Martins, M., Mccusker, M.P., Mccabe, E.M., O’Leary, D., Duffy, G. and Séamus, F., 2013. Evidence of metabolic switching and implications for food safety from the phenome(s) of Salmonella enterica serovar typhimurium dt104 cultured at selected points across the pork production food chain. Applied and Environmental Microbiology 79: 5437–5449. 10.1128/AEM.01041-13
Pei, X., Guo, Y., Xu, J. and Liu, X., 2007. Antibiotic susceptibility of Enterobacter sakazakii isolated from powdered formula for infant and young children. Journal of Hygiene Research 36: 63–65. 10.1016/S1672-6529(07)60007-9
Pires, R.P.S., Cappato, L.P., Guimares, J.T., Rocha, R.S. and Cruz, A.G., 2020. Ohmic heating for infant formula processing: evaluating the effect of different voltage gradient. Journal of Food Engineering 280: 109989. 10.1016/j.jfoodeng.2020.109989
Römling, U. and Balsalobre, C., 2012. Biofilm infections, their resilience to therapy and innovative treatment strategies. Journal of Internal Medicine 272: 541–561. 10.1111/joim.12004
Stoop, B., Lehner, A., Iversen, C., Fanning, S. and Stephan, R., 2009. Development and evaluation of rpob based pcr systems to differentiate the six proposed species within the genus Cronobacter. International Journal of Food Microbiology 136: 165–168. 10.1016/j.ijfoodmicro.2009.04.023
Tutar, E., Akinci, S.K. and Akyol, I., 2018. Development and application of a new multiplex real-time pcr assay for simultaneous identification of brucella melitensis, Cronobacter sakazakii and Listeria monocytogenes in raw milk and cheese. International Journal of Dairy Technology 71: 629–636. 10.1111/1471-0307.12500
Ueda, S., 2017. The effects of temperature on the growth and heat resistance of Cronobacter spp.. Biocontrol Science 22: 125–129. 10.4265/bio.22.125
Yan, Q., Wang, J., Gangiredla, J., Cao, Y., Martins, M., Gopinath, G.R., et al., 2015. Comparative genotypic and phenotypic analysis of Cronobacter species cultured from four powdered infant formula production facilities: indication of pathoadaptation along the food chain. Applied and Environmental Microbiology 81: 4388–4402. 10.1128/AEM.00359-15
Chenu, J.W. and Cox, J.M., 2009. Cronobacter (‘Enterbacter sakazakii’): current status and future prospects. Letters in Applied Microbiology 49: 153–159. 10.1111/j.1472-765X.2009.02651.x
Choi, Y., Kim, S., Hwang, H., Kim, K.P. and Ryu, S., 2014. Plasmid-encoded mcp is involved in virulence, motility, and biofilm formation of Cronobacter sakazakii ATCC 29544. Infection and Immunity 83: 197–204. 10.1128/iai.02633-14
CLSI M100S, 2016. Performance Standards for Antimicrobial Susceptibility Testing, 26th Edition. Clinical and Laboratory Standards Institute.
Dancer, G.I., Mah, J.H., Rhee, M.S., Hwang, I.G. and Kang, D.H., 2009. Resistance of Enterbacter sakazakii (Cronobacter spp.) to environmental stresses. Journal of Applied Microbiology 107: 1606–1614. 10.1111/j.1365-2672.2009.04347.x
Drapala, K.P., Mulvihill, D.M. and O’Mahony, J.A., 2018. Improving the oxidative stability of model whey protein hydrolysate—based infant formula emulsions with lecithin. International Journal of Dairy Technology 71: 966–974. 10.1111/1471-0307.12538
Fei, P., Man, C., Lou, B., Forsythe, S.J., Chai, Y., Li, R., et al., 2015. Genotyping and source tracking of Cronobacter sakazakii and C. malonaticus isolates from powdered infant formula and an infant formula production factory in china. Applied and Environmental Microbiology 81: 5430–5439. 10.1128/AEM.01390-15
Fei, P., Jiang, Y., Jiang, Y., Yuan, X., Yang, T., Chen, J., et al., 2017. Prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter sakazakii isolates from powdered infant formula collected from Chinese retail markets. Frontiers in Microbiology 8: 2026. 10.3389/fmicb.2017.02026
Forsythe, S.J., 2018. Updates on the Cronobacter Genus. Annual Review of Food Science and Technology 9: 23–44. 10.1146/annurev-food-030117-012246
Friedemann, M., 2008. Enterobacter sakazakii in powdered infant formula. Bundesgesundheitsbla 51: 664–674. 10.1007/s00103-008-0543-4
Gan, X., Bai, L., Yan, S., Wang, J., Wang, W., Li, Z., et al., 2015. Drug resistant analysis of Cronobacter isolated from infant foods in 2012–2014 in China. Journal of Food Safety and Food Quality 6: 3491–3496.
Gan, X., Dong, Y., Yan, S., Hu, Y., Séamus, F., Wang, J., et al., 2018. Contamination and characterization of multiple pathogens in powdered formula at retail collected between 2014 and 2015 in China. Food Control 87: 40–45. 10.1016/j.foodcont.2017.12.014
GB4789.40, 2016. Cronobacter. National Food Safety Standard Food Microbiological Examination. China.
Gu, M., Han, W. and Yang, J., 2008. Study on antibiotic resistance of Enterobacter sakazakii isolated from imported dairy product. Journal of Inspection Quarterly 21: 14–16. 10.3969/j.issn.1674-5354.2008.01.005
Gurtler, J.B. and Beuchat, L.R., 2007. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. Journal of Food Protection 70: 1579. 10.1016/j.jfoodeng.2006.05.001
Henry, M. and Fouladkhah, A., 2019. Outbreak history, biofilm formation, and preventive measures for control of Cronobacter sakazakii in infant formula and infant care settings. Microorganisms 7: 77. 10.3390/microorganisms7030077
Iversen, C., Lane, M. and Forsythe, S.J., 2004. The growth profile, thermotolerance and biofilm formation of Enterbacter sakazakii grown in infant formula milk. Letters in Applied Microbiology 38: 378–382. 10.1111/j.1472-765X.2004.01507.x
Jaradat, Z.W., Al, M.W., Elbetieha, A., Al, N.A. and Tall, B.D., 2014. Cronobacter spp.-opportunistic foodborne pathogens. A review of their virulence and environmental-adaptive traits. Journal of Medical Microbiology 63: 1023–1037. 10.1099/jmm.0.073742-0
Kalyantanda, G., Shumyak, L. and Archibald, L.K., 2015. Cronobacter species contamination of powdered infant formula and the implications for neonatal health. Frontiers in Pediatrics 3: 56. 10.3389/fped.2015.00056
Lee, Y.D., Park, J.H. and Chang, H.I., 2012. Detection, antibiotic susceptibility and biofilm formation of Cronobacter spp. from various foods in Korea. Food Control 24: 225–230. 10.1016/j.foodcont.2011.09.023
Lehner, A., Fricker-Feer, C. and Stephan, R., 2012. Identification of the recently described Cronobacter condiment by an rpoB-gene-based PCR system. Journal of Medical Microbiology 61: 1034–1035. 10.1099/jmm.0.042903-0
Ling, N., Li, C., Zhang, J., Wu, Q., Zeng, H., He, W., et al., 2018. Prevalence and molecular and antimicrobial characteristics of Cronobacter spp. isolated from raw vegetables in China. Frontiers in Microbiology 9: 1149. 10.3389/fmicb.2018.01149
Liu, Y., Gao, Q., Zhang, X., Hou, Y., Yang, J. and Huang, X., 2006. PCR and oligonucleotide array for detection of Enterobacter sakazakii in infant formula. Molecular and Cellular Probes 20: 11–17. 10.1016/j.mcp.2005.08.004
Martins, M., Mccusker, M.P., Mccabe, E.M., O’Leary, D., Duffy, G. and Séamus, F., 2013. Evidence of metabolic switching and implications for food safety from the phenome(s) of Salmonella enterica serovar typhimurium dt104 cultured at selected points across the pork production food chain. Applied and Environmental Microbiology 79: 5437–5449. 10.1128/AEM.01041-13
Pei, X., Guo, Y., Xu, J. and Liu, X., 2007. Antibiotic susceptibility of Enterobacter sakazakii isolated from powdered formula for infant and young children. Journal of Hygiene Research 36: 63–65. 10.1016/S1672-6529(07)60007-9
Pires, R.P.S., Cappato, L.P., Guimares, J.T., Rocha, R.S. and Cruz, A.G., 2020. Ohmic heating for infant formula processing: evaluating the effect of different voltage gradient. Journal of Food Engineering 280: 109989. 10.1016/j.jfoodeng.2020.109989
Römling, U. and Balsalobre, C., 2012. Biofilm infections, their resilience to therapy and innovative treatment strategies. Journal of Internal Medicine 272: 541–561. 10.1111/joim.12004
Stoop, B., Lehner, A., Iversen, C., Fanning, S. and Stephan, R., 2009. Development and evaluation of rpob based pcr systems to differentiate the six proposed species within the genus Cronobacter. International Journal of Food Microbiology 136: 165–168. 10.1016/j.ijfoodmicro.2009.04.023
Tutar, E., Akinci, S.K. and Akyol, I., 2018. Development and application of a new multiplex real-time pcr assay for simultaneous identification of brucella melitensis, Cronobacter sakazakii and Listeria monocytogenes in raw milk and cheese. International Journal of Dairy Technology 71: 629–636. 10.1111/1471-0307.12500
Ueda, S., 2017. The effects of temperature on the growth and heat resistance of Cronobacter spp.. Biocontrol Science 22: 125–129. 10.4265/bio.22.125
Yan, Q., Wang, J., Gangiredla, J., Cao, Y., Martins, M., Gopinath, G.R., et al., 2015. Comparative genotypic and phenotypic analysis of Cronobacter species cultured from four powdered infant formula production facilities: indication of pathoadaptation along the food chain. Applied and Environmental Microbiology 81: 4388–4402. 10.1128/AEM.00359-15
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Feb 15, 2021
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