Prevalence and molecular characterization of Cronobacter species in Egyptian table eggs and egg-based desserts; special insight on Cronobacter sakazakii
Main Article Content
Keywords
Cronobacter spp, C. sakazakii, desserts, eggs, PCR, 16S rRNA sequencing
Abstract
The occurrence of Cronobacter spp. was investigated in table eggs and egg-based desserts obtained from retail stores. Cronobacter was isolated from 57 out of 180 (31.7%) (95% Confidence Interval [CI]: 26–43%) examined samples of eggs and egg-based desserts. The prevalence of Cronobacter spp. was significantly higher in farm eggs (67%) (P < 0.05) than in Balady eggs (23%), cream cake (27%) and small-scale ice cream (27%). Cronobacter (C.) sakazakii and C. muytjensii were the predominant isolates obtained in the present study. All C. sakazakii isolates were molecularly confirmed with higher incidence in small-scale ice cream (62.5%).
References
Abou Elkhair, E., Salama, A., Radwan, H., Khalafallah, A., Arafa, H. 2014. Bacteriological quality of packaged ice cream in Gaza city, Palestine. J Nutr Food Sci. 2(3): 68–73. 10.11648/j.jfns.20140203.14
Aksu, F., Altunatmaz, S.S., Issa, G., Aksoy, A., Aksu, H. 2019. Prevalence of Cronobacter spp. in various foodstuffs and identification by multiplex PCR. Food Sci Technol (Campinas). 39 (3): 729–734. 10.1590/fst.06818
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J Mol Biol. 215: 403–410. 10.1016/s0022-2836(05)80360-2
Amer, M.M. and Mekky, H.M. 2019. Cronobacter sakazakii (Enterobacter sakazakii). Int J Pharm Biol Sci. 6(4): 4–14.
Bai, Y., Yu, H., Guo, D., Fei, S. and Shi, C. 2019. Survival and environmental stress resistance of Cronobacter sakazakii exposed to vacuum or air packaging and stored at different temperatures. Front Microbiol. 10: 303. 10.3389/fmicb.2019.00303
Baumgartner, A., Grand, M., Liniger, M. and Iversen, C. 2009. Detection and frequency of Cronobacter spp. (Enterobacter sakazakii) in different categories of ready-to-eat foods other than infant formula. Int J Food Microbiol. 136: 189–192. 10.1016/j.ijfoodmicro.2009.04.009
Berhilevych, O. and Kasianchuk, V. 2017. Identification of Cronobacter spp. (Enterobacter sakazakii) from raw milk and environmental samples of dairy farms. East Eur J Enterp Technol. 6: 4–10.
Beuchat, L.R., Kim, H., Gurtler, J.B., Lin, L.C., Ryu, J.H. and Richards, G.M. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int J Food Microbiol. 136: 204–213. 10.1016/j.ijfoodmicro.2009.02.029
Das, S.K., Kumar, S.H., Nayak, B.B. and Lekshmi, M. 2021. Isolation and identification of Cronobacter spp. from fish and shellfish sold in retail markets. Curr Microbiol. 78: 1973–1980. 10.1007/s00284-021-02447-3
European Food Safety Authority i (EFSA). 2014. Scientific opinion on the public health risks of table eggs due to deterioration and development of pathogens. EFSA J. 12: 3782. 10.2903/j.efsa.2014.3782
El-Gamal, M.S., Eldairouty, R., Okda, A., Salah, S.H. and El-Shamy, S.M. 2013. Incidence and interrelation of Cronobacter sakazakii and other foodborne bacteria in some milk products and infant formula milks in Cairo and Giza area. World Appl Sci J. 26: 1129–1141. 10.5829/idosi.wasj.2013.26.09.13542
Food and Agriculture Organization/World Health Organization (FAO/WHO). 2008. Enterobacter sakazakii (Cronobacter spp.) in powdered followup formulae: meeting report. In: Micro-biological Risk Assessment Series No. 15. Rome. 84 pp.
Galiş, A.M., Marcq, C., Marlier, D., Portetelle, D., Van, I., Beckers, Y. and Théwis, A. 2013. Control of salmonella contamination of shell eggs—preharvest and postharvest methods: a review. Compr Rev Food Sci Food Safe. 12: 155–182. 10.1111/1541-4337.12007
Gurtler, J.B. and Beuchat, L.R. 2007. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. J Food Prot. 70: 1579–1586. 10.4315/0362-028x-70.7.1579
Hassan, M.K., Afify, M.A. and Aly, M.M. 2004. Genetic resistance of Egyptian chickens to infectious bursal disease and Newcastle disease. Trop Anim Health Prod. 36: 1–9. 10.1023/b:trop.0000009524.47913.d4
Hayman, M.M., Edelson-Mammel, S.G., Carter, P.J., Chen, Y.I., Metz, M., Sheehan, J.F., Tall, B.D., Thompson, C.J. and Smoot, L.A. 2020. Prevalence of Cronobacter spp., and salmonella in milk powder manufacturing facilities in the United States. J Food Prot. 83: 1685–1692. 10.4315/jfp-20-047
Hochel, I., Růžičková, H., Krásný, L. and Demnerová, K. 2012. Occurrence of Cronobacter spp. in retail foods. J Appl Microbiol. 112: 1257–1265. 10.1111/j.1365-2672.2012.05292.x
Holý, O. and Forsythe, S. 2014. Cronobacter spp. as emerging causes of healthcare-associated infection. J Hosp Infect. 86: 169–177. 10.1016/j.jhin.2013.09.011
Iversen, C., Lehner, A., Mullane, N., Bidlas, E., Cleenwerck, I., Marugg, J., Fanning, S., Stephan, R. and Joosten H. 2007. 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. 10.1186/1471-2148-7-64
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 genomo species 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. 10.1099/ijs.0.65577-0
Jaradat, Z.W., Ababneh, Q.O., Saadoun, I.M., Samara, N.A. and Rashdan, A.M. 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 assays, PCR and 16S rRNA sequencing. BMC Microbiol. 9: 225. 10.1186/1471-2180-9-225
Joseph, S., Cetinkaya, E., Drahovska, H., Levican, A., Figueras, M.J. and Forsythe, S.J. 2012. Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. Int J Syst Evol Microbiol. 62: 1277–1283. 10.1099/ijs.0.032292-0
Kandhai, M.C., Heuvelink, A.E., Reij, M.W., Beumer, R.R., Dijk, R., van Tilburg, J.J.H.C., van Schothorst, M. and Gorris, L.G.M. 2010. A study into the occurrence of Cronobacter spp. in the Netherlands between 2001 and 2005. Food Control. 21: 1127–1136. 10.1016/j.foodcont.2010.01.007
Kim, H., Ryu, J. and Beuchat, L. 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. 10.1128/AEM.01766-06
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. 10.1186/1471-2180-4-43
Ling, N., Li, C., Zhang, J., Wu, Q., Zeng, H., He, W., Ye, Y., Wang, J., Ding, Y., Chen, M., Xue, L., Ye, Q. and Guo, W. 2018. Prevalence and molecular and antimicrobial characteristics of Cronobacter spp. isolated from raw vegetables in China. Front Microbiol. 9: 1149. 10.3389/fmicb.2018.01149
Lu, Y., Chen, Y., Lu, X.A., Lv, J., Man, C.X., Chai, Y.L. and Jiang, Y.J. 2013. Comparison of methods for the microbiological identification and typing of Cronobacter species in infant formula. J Dairy Sci. 97: 632–641. 10.3168/jds.2013–7147
Mathews, S., Ngoma, L., Gashe, B. and Mpuchane, S. 2013. General microbiological quality of ice cream and ice pop sold in Gaborone, Botswana. Stud Ethno Med. 7: 217–226. 10.1080/09735070.2013.11886463
Moustafa, Sh. M. 2021. Incidence of Cronobacter species in milk and some dairy products. PhD thesis, Assiut University, Assiut, Egypt.
Mullane, N., O’Gaora, P., Nally, J.E., Iversen, C., Whyte, P., Wall, P.G. and Fanning, S. 2008. Molecular analysis of the Enterobacter sakazakii O-antigen gene locus. Appl Environ Microbiol. 74: 3783–3794. 10.1128/AEM.02302-07
Oh, S., Chen, P. and Kang, D. 2007. Biofilm formation by Enterobacter sakazakii grown in artificial broth and infant milk formula on plastic surface. J Rapid Methods Autom Microbiol. 15: 311–319. 10.1111/j.1745-4581.2007.00103.x
Pienaar, A.C., Coetzee, L. and Bragg, R.R. 1995. A rapid method to determine bacterial contamination on hatching eggs. 2. Correlation of the optical-density measurements after incubation to bacterial counts on hatching eggs. Onderstepoort J Vet Res. 62: 25–33.
Saad, N.M. and Ewida, R.M. 2018. Incidence of Cronobacter sakazakii in dairy-based desserts. J Adv Vet Res. 8(2): 16–18. Retrieved from https://advetresearch.com/index.php/AVR/article/view/288
Siriken, B., Çadirci, Ö., Inat, G. and Pamuk, S. 2009. Microbiological examination of meatball, cream cake and Turkish delight (Lokum). J Anim Vet Adv. 8: 2049–2054.
Vanderzant, C. and Splittstoesser, D.F. 1992. Compendium of methods for the microbiological examination of foods, 3rd edition. American Public Health Association, Washington DC, pp. 423–431.
Warke, R., Kamat, A., Kamat, M. and Thomas, P. 2000. Incidence of pathogenic psychrotrophs in ice creams sold in some retail outlets in Mumbai, India. Food Control. 11: 77–83. 10.1016/S0956-7135(99)00027-4
World Health Organization/Food and Agriculture Organization (WHO/FAO). 2008. Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formula: meeting report. WHO, Rome, Italy.
Yörük, N. 2019. Determination of the presence of Cronobacter sakazakii, Listeria monocytogenes, Salmonella spp., and Enteroba-ctericeae count in ice creams and infant formulas. Adv Food Sci. 41: 54–60.
Aksu, F., Altunatmaz, S.S., Issa, G., Aksoy, A., Aksu, H. 2019. Prevalence of Cronobacter spp. in various foodstuffs and identification by multiplex PCR. Food Sci Technol (Campinas). 39 (3): 729–734. 10.1590/fst.06818
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J Mol Biol. 215: 403–410. 10.1016/s0022-2836(05)80360-2
Amer, M.M. and Mekky, H.M. 2019. Cronobacter sakazakii (Enterobacter sakazakii). Int J Pharm Biol Sci. 6(4): 4–14.
Bai, Y., Yu, H., Guo, D., Fei, S. and Shi, C. 2019. Survival and environmental stress resistance of Cronobacter sakazakii exposed to vacuum or air packaging and stored at different temperatures. Front Microbiol. 10: 303. 10.3389/fmicb.2019.00303
Baumgartner, A., Grand, M., Liniger, M. and Iversen, C. 2009. Detection and frequency of Cronobacter spp. (Enterobacter sakazakii) in different categories of ready-to-eat foods other than infant formula. Int J Food Microbiol. 136: 189–192. 10.1016/j.ijfoodmicro.2009.04.009
Berhilevych, O. and Kasianchuk, V. 2017. Identification of Cronobacter spp. (Enterobacter sakazakii) from raw milk and environmental samples of dairy farms. East Eur J Enterp Technol. 6: 4–10.
Beuchat, L.R., Kim, H., Gurtler, J.B., Lin, L.C., Ryu, J.H. and Richards, G.M. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int J Food Microbiol. 136: 204–213. 10.1016/j.ijfoodmicro.2009.02.029
Das, S.K., Kumar, S.H., Nayak, B.B. and Lekshmi, M. 2021. Isolation and identification of Cronobacter spp. from fish and shellfish sold in retail markets. Curr Microbiol. 78: 1973–1980. 10.1007/s00284-021-02447-3
European Food Safety Authority i (EFSA). 2014. Scientific opinion on the public health risks of table eggs due to deterioration and development of pathogens. EFSA J. 12: 3782. 10.2903/j.efsa.2014.3782
El-Gamal, M.S., Eldairouty, R., Okda, A., Salah, S.H. and El-Shamy, S.M. 2013. Incidence and interrelation of Cronobacter sakazakii and other foodborne bacteria in some milk products and infant formula milks in Cairo and Giza area. World Appl Sci J. 26: 1129–1141. 10.5829/idosi.wasj.2013.26.09.13542
Food and Agriculture Organization/World Health Organization (FAO/WHO). 2008. Enterobacter sakazakii (Cronobacter spp.) in powdered followup formulae: meeting report. In: Micro-biological Risk Assessment Series No. 15. Rome. 84 pp.
Galiş, A.M., Marcq, C., Marlier, D., Portetelle, D., Van, I., Beckers, Y. and Théwis, A. 2013. Control of salmonella contamination of shell eggs—preharvest and postharvest methods: a review. Compr Rev Food Sci Food Safe. 12: 155–182. 10.1111/1541-4337.12007
Gurtler, J.B. and Beuchat, L.R. 2007. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. J Food Prot. 70: 1579–1586. 10.4315/0362-028x-70.7.1579
Hassan, M.K., Afify, M.A. and Aly, M.M. 2004. Genetic resistance of Egyptian chickens to infectious bursal disease and Newcastle disease. Trop Anim Health Prod. 36: 1–9. 10.1023/b:trop.0000009524.47913.d4
Hayman, M.M., Edelson-Mammel, S.G., Carter, P.J., Chen, Y.I., Metz, M., Sheehan, J.F., Tall, B.D., Thompson, C.J. and Smoot, L.A. 2020. Prevalence of Cronobacter spp., and salmonella in milk powder manufacturing facilities in the United States. J Food Prot. 83: 1685–1692. 10.4315/jfp-20-047
Hochel, I., Růžičková, H., Krásný, L. and Demnerová, K. 2012. Occurrence of Cronobacter spp. in retail foods. J Appl Microbiol. 112: 1257–1265. 10.1111/j.1365-2672.2012.05292.x
Holý, O. and Forsythe, S. 2014. Cronobacter spp. as emerging causes of healthcare-associated infection. J Hosp Infect. 86: 169–177. 10.1016/j.jhin.2013.09.011
Iversen, C., Lehner, A., Mullane, N., Bidlas, E., Cleenwerck, I., Marugg, J., Fanning, S., Stephan, R. and Joosten H. 2007. 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. 10.1186/1471-2148-7-64
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 genomo species 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. 10.1099/ijs.0.65577-0
Jaradat, Z.W., Ababneh, Q.O., Saadoun, I.M., Samara, N.A. and Rashdan, A.M. 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 assays, PCR and 16S rRNA sequencing. BMC Microbiol. 9: 225. 10.1186/1471-2180-9-225
Joseph, S., Cetinkaya, E., Drahovska, H., Levican, A., Figueras, M.J. and Forsythe, S.J. 2012. Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water and food ingredients. Int J Syst Evol Microbiol. 62: 1277–1283. 10.1099/ijs.0.032292-0
Kandhai, M.C., Heuvelink, A.E., Reij, M.W., Beumer, R.R., Dijk, R., van Tilburg, J.J.H.C., van Schothorst, M. and Gorris, L.G.M. 2010. A study into the occurrence of Cronobacter spp. in the Netherlands between 2001 and 2005. Food Control. 21: 1127–1136. 10.1016/j.foodcont.2010.01.007
Kim, H., Ryu, J. and Beuchat, L. 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. 10.1128/AEM.01766-06
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. 10.1186/1471-2180-4-43
Ling, N., Li, C., Zhang, J., Wu, Q., Zeng, H., He, W., Ye, Y., Wang, J., Ding, Y., Chen, M., Xue, L., Ye, Q. and Guo, W. 2018. Prevalence and molecular and antimicrobial characteristics of Cronobacter spp. isolated from raw vegetables in China. Front Microbiol. 9: 1149. 10.3389/fmicb.2018.01149
Lu, Y., Chen, Y., Lu, X.A., Lv, J., Man, C.X., Chai, Y.L. and Jiang, Y.J. 2013. Comparison of methods for the microbiological identification and typing of Cronobacter species in infant formula. J Dairy Sci. 97: 632–641. 10.3168/jds.2013–7147
Mathews, S., Ngoma, L., Gashe, B. and Mpuchane, S. 2013. General microbiological quality of ice cream and ice pop sold in Gaborone, Botswana. Stud Ethno Med. 7: 217–226. 10.1080/09735070.2013.11886463
Moustafa, Sh. M. 2021. Incidence of Cronobacter species in milk and some dairy products. PhD thesis, Assiut University, Assiut, Egypt.
Mullane, N., O’Gaora, P., Nally, J.E., Iversen, C., Whyte, P., Wall, P.G. and Fanning, S. 2008. Molecular analysis of the Enterobacter sakazakii O-antigen gene locus. Appl Environ Microbiol. 74: 3783–3794. 10.1128/AEM.02302-07
Oh, S., Chen, P. and Kang, D. 2007. Biofilm formation by Enterobacter sakazakii grown in artificial broth and infant milk formula on plastic surface. J Rapid Methods Autom Microbiol. 15: 311–319. 10.1111/j.1745-4581.2007.00103.x
Pienaar, A.C., Coetzee, L. and Bragg, R.R. 1995. A rapid method to determine bacterial contamination on hatching eggs. 2. Correlation of the optical-density measurements after incubation to bacterial counts on hatching eggs. Onderstepoort J Vet Res. 62: 25–33.
Saad, N.M. and Ewida, R.M. 2018. Incidence of Cronobacter sakazakii in dairy-based desserts. J Adv Vet Res. 8(2): 16–18. Retrieved from https://advetresearch.com/index.php/AVR/article/view/288
Siriken, B., Çadirci, Ö., Inat, G. and Pamuk, S. 2009. Microbiological examination of meatball, cream cake and Turkish delight (Lokum). J Anim Vet Adv. 8: 2049–2054.
Vanderzant, C. and Splittstoesser, D.F. 1992. Compendium of methods for the microbiological examination of foods, 3rd edition. American Public Health Association, Washington DC, pp. 423–431.
Warke, R., Kamat, A., Kamat, M. and Thomas, P. 2000. Incidence of pathogenic psychrotrophs in ice creams sold in some retail outlets in Mumbai, India. Food Control. 11: 77–83. 10.1016/S0956-7135(99)00027-4
World Health Organization/Food and Agriculture Organization (WHO/FAO). 2008. Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formula: meeting report. WHO, Rome, Italy.
Yörük, N. 2019. Determination of the presence of Cronobacter sakazakii, Listeria monocytogenes, Salmonella spp., and Enteroba-ctericeae count in ice creams and infant formulas. Adv Food Sci. 41: 54–60.
Article Sidebar
Published
Oct 8, 2023
Article Details
How to Cite
M. Kamal, S., Maharik, N. M., Valero, A., & Faried, A. M. (2023). Prevalence and molecular characterization of Cronobacter species in Egyptian table eggs and egg-based desserts; special insight on Cronobacter sakazakii. Italian Journal of Food Science, 35(4), 50-57. https://doi.org/10.15586/ijfs.v35i4.2384
Section
Paper
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright Agreement with Authors
Before publication, after the acceptance of the manuscript, Authors have to sign a Publication Agreement with "Italian Journal of Food Science", granting and assigning to "Italian Journal of Food Science" the perpetual right to distribute the work free of charge by any means and in any parts of the world, including the communication to the public through the journal website.
License for Published Contents
http://creativecommons.org/licenses/by-nc-nd/4.0/
How to Cite
M. Kamal, S., Maharik, N. M., Valero, A., & Faried, A. M. (2023). Prevalence and molecular characterization of Cronobacter species in Egyptian table eggs and egg-based desserts; special insight on Cronobacter sakazakii. Italian Journal of Food Science, 35(4), 50-57. https://doi.org/10.15586/ijfs.v35i4.2384