Investigation of Cronobacter sakazakii (Enterobacter sakazakii) Presence in Cereal Infant Foods
Main Article Content
Keywords
Cronobacter sakazakii, cereal infant foods, powdered infant formula
Abstract
C. sakazakii is an opportunistic pathogen that may cause serious infections. Infant formulas are frequently reported as the source of infections caused by C. sakazakii. In spite of all of the taken precautions, there are recently published studies related to the isolation of C. sakazakii in formula and small children foods. In this study, we aimed to investigate the presence of C. sakazakii in cereal based infant formulas and complementary foods sold in the markets of Turkish Republic of Northern Cyprus (TRNC). We also aimed to determine the infection risk in these products. This research was carried out between May – December 2017 with the cereal-based continuing formulas and small child complementary foods of the brands offered for sale at T. R. N. C. In a total of 265 samples, including 36 varieties of cereal-based infant formula and 17 varieties of cereal-based infants and small children foods were analysed. Analysis of samples were carried out according to; ISO / TS 22964: 2006 method. C. sakazakii was not detected in any of the study samples. In conclusion, C. sakazakii was not detected in any of the cereal-based foods despite the reported detection of C. sakazakii in most of the microbiological analysis of baby foods in both the world and Turkey.
References
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2. U.S. Food and Drug Administration (FDA): Isolation and Enumeration of Enterobacter sakazakii from Dehydrated Powdered Infant Formula. Accessed: August 2002.
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9. U.S. Food and Drug Administration (FDA): Questions and Answers on Enterobacter sakazakii in powdered infant formula. Version 4, Accessed: 13 February 2004.
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12. European Commission(EU): Commision Regulation(EU) No:365/2010 of 28 April 2010 amending regulation (EC) No:2073/2005 on microbiological criteria for foodstuffs as regards Enterobacteriaceae in pasteurized milk and other pasteurized liquid dairy products and Listeria monocytogenes in food garde sat. L107, 9-11, Accessed:2010.
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14. Centers for Disease Control and Preventation(CDC): Investigation of Cronobacter Infections Among Infants in the United States. 2012A
15. Shaker R, Osaii T, Al-Omary W, Jaradat , Al-Zuby M: Isolation of Enterobacter sakazakii and other Enterobacter sp. From food and food production environments. Food Control, 18:1241-45, 2007.
DOI:10.1016/j.foodcont.2006.07.020
16. Restino L, Frampton EW, Lionberg WC, Becker RJ: A chromogenic plating medium for the isolation and identification of Enterobacter sakazakii from foods, food ingredients and evrironmental sources. Journal of Food Protection, 69: 315-22,2006. DOI: 10.4315/0362-028X-69.2.315
17. Oonaka K, Furuhata K, Hara M, Fukuyama M: Powder infant formula milk contaminated with Enterobacter sakazakii. Japanese Journal of Infection Diseases, 63:103-107, 2010.
18. Aigbekaen BO, Oshama CE: Isolation of Enterobacter sakazakii powdered foods locally consumed in Nigeria. Pakistan Journal of Nutrition, 9(7):659-663, 2010. DOI:10.3923/pjn.2010.659.663
19.Yemis GP: Investigation of Isolation and Development Parameters of Cronobacter sakazakii in Infant Foods (in Turkish: Cronobacter Sakazakii’nin Bebek Mamalarından İzolasyonu ve Gelişme Parametrelerinin İncelenmesi.) Ankara University, PhD Thesis. Ankara /Turkey, Accessed: 2011.
20.Cakmak B: The Existence of Enterobacter sakazakii in Various Infant Foods and Pasteurized Milk Presented on the Market (in Turkish: Piyasada Satışa Sunulan Çeşitli Bebek Mamalarında ve Pastörize Sütlerde Enterobacter sakazakii’nin Varlığı) İstanbul University, PhD Thesis. İstanbul/Turkey, Accessed: 2012.
21.Cetingurbuz B: Prevalence of Enterobacter Sakazakii in Powdered Infant Food and Raw Milk (in Turkish: Hazır Toz Bebek Mamaları ve Çiğ Sütlerde Enterobacter sakazakii’nin Bulunma Sıklığı) Gazi University, MsC.Thesis. Ankara/Turkey, Accessed: 2013.
22. International Organization for Standardization (ISO): ISO/TS 22964 IDF/RM 210: Milk and Milk Products-Detection of Enterobacter sakazakii. 1st ed., ISO Copyright Office, Switzerland, 2006.
23- Muytjens HL, Roelofs-Willemse H, Jaspar GH: Quality of powdered substitutes for breakfast milk with regard to members of the family Enterobacteriaceae. Journal of Clinical Microbiology, 26: 743-746, 1988.
24- Nazarowec-White M, Farber JM: Incidence, survival, and growth of Enterobacter sakazakii in infant formula. Journal of Food Protection, 60; 226–230, 1997.
25. Leuschner RGK, Baird F, Donald B, Cox LJ: Retracted: A medium for the presumptive detection of Enterobacter sakazakii in ifant formula. Food Microbiol, 21: 527-533, 2004.
DOI: 10.1016/j.fm.2003.12.002
26. Iversen C, Forsythe S: Isolation of E. sakazakii and other Enterobacteraceae from powdered formula milk and related products. Journal of Food Microbiol, 21: 771-777, 2004. DOI: 10.1016/j.fm.2004.01.009
27. Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C, Park J: International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. International Journal of Food Microbiology, 136;185-188, 2009.
DOI: 10.1016/j.ijfoodmicro.2009.08.005
28. Kandhai MC, Heuvelink AE, Reij MW, Beumer RR, Dijk R, van Tilburg JJHC, van Schothorst M, Gorris LGM: Study into the occurrence of Cronobacter spp. in the Netherlands between 2001 and 2005. Food Control, 21:1127-1136, 2010.
29. Hoque A, Ahmed T, Shahidullah M, Hossain A, Mannan A, Noor K, Nahar K, Ilias M, Ahmed D: Isolation and molecular identification of Cronobacter spp. from powdered infant formula (PIF) in Bangladesh. Int J Food Microbiol, 142: 375-378, 2010.
DOI: 10.1016/j.ijfoodmicro.2010.07.019
30. Fei P, Man C, Lou B, Forsythe S J, Chai Y, Li R, Niu J, Jiang Y: Genotyping and source tracking of Cronobacter sakazakii and C. malonaticus isolates from powdered infant formula and an infant formula production factory in China. Appl Environ Microbiol, 81: 5430–5439, 2015.
DOI: 10.1128/AEM.01390-15
31. Fei P, Jiang Y, Yuan X, Yang T, Chen J, Wang Z, Kang H, Forstrhe SJ: Prevalence, Molecular Characterization and Antibiotic Susceptibility of Cronobacter sakazakii Isolates from Powedered Infant Formula Collected from Chinese Retail Market. Front Microbiol, 8:2026, 2017.
DOI: 10.3389/fmicb.2017.02026
32- Tokatlı N: Composition of Baby Foods Produced in Different Formulations, Some Microbiological Properties and Determination of Enterobacter sakazakii Presence in Those Foods (in Turkish: Farklı Formülasyonlarda Üretilen Bebek Mamalarının Bileşimi, Bazı Mikrobiyolojik Özellikleri ve Enterobacter sakazakii Varlığının Belirlenmesi) Namık Kemal University, MsC. Thesis Tekirdag/Turkey, Accessed: 2009.
33.Gökmen M., Tekinşen K.K., Gürbüz Ü: Presence of Enterobacter sakazakii in Milk Powder, Whey Powder and White Cheese Produced in Konya. Kafkas Üniv.Vet Fak. Derg, 16(Suppl-A):S163-S166, 2010. DOI:10.9775/kvfd.2010.2801
34. Kaya GD: The Effect of Temperature and Sugar Varieties on Investigation and Development of Enterobacter sakazakii (Cronobacter spp.) in Dairy Products and Infant Foods (in Turkish: Süt Ürünlerinde ve Bebek Mamalarında Enterobacter sakazakii(Cronobacter spp.) Varlığının Araştırılması ve Gelişmesine Sıcaklık ve Şeker Çeşitlerinin Etkisi) İstanbul Technical University, PhD Thesis İstanbul/Turkey, Accessed: 2011.
35. Koluman A:Çeşitli gıdalarda Cronobacter spp., (Enterobacter sakazakii) izolasyon ve identifikasyon) Gida Teknolojileri Elektronik Dergisi, 6:16-19, 2011.
36.Manga M: Investigation of Cronobacter spp. (Enterobacter sakazakii) in Powder Infant Foods and Newborn Nutrition Tubes (in Turkish: Toz Bebek Mamalarında ve Yenidoğan Beslenme Tüplerinde Cronobacter spp.(Enterobacter sakazakii) Araştırılması) İstanbul University, MsC thesis. İstanbul/Turkey, Accessed: 2011.
2. U.S. Food and Drug Administration (FDA): Isolation and Enumeration of Enterobacter sakazakii from Dehydrated Powdered Infant Formula. Accessed: August 2002.
3. Iversen C, Forsythe S.: Risk profile of E. sakazakii, an emergent pathogen associated with infant milk Formula. Trends in Food Sci Tech, 14: 443-451, 2003.
4. Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, Fanning S, Stephan R, Joosten H: 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, 2007. DOI: 10.1186/1471-2148-7-64
5. Bowen AB, Braden CR: Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis, 12:1185-1189, 2006. DOI: 10.3201/eid1208.051509
6. World Health Organization and Food and Agriculture Organization: Enterobacter sakazakii and other microorganisms in powdered infant formula. Meeting report. Microbiological Risk Assessment Series 6. Genowa Switzerland 2004.
7- Holy O, Forsythe S: Cronobacter spp. As emerging causes of healthcare associated infection. J Hosp Infect, 86,169-177, 2014. DOI: 10.1016/j.jhin.2013.09.011
8.Urmenyi AMC, Franklin AW: Neonatal death from pigmented coliform infection. Lancet. 1(7172); 313-5, 1961. DOI: 10.1016/S0140-6736(61)91481-7
9. U.S. Food and Drug Administration (FDA): Questions and Answers on Enterobacter sakazakii in powdered infant formula. Version 4, Accessed: 13 February 2004.
10- Jaradat ZW, Al Mousa W, Elbetieha A, Al Nabulsi A, Tall BD: Cronobacter spp.-opportunistic food borne pathogens. A review of their virulence and environmental adaptive traits. Journal of Medical Microbiology, 63:1023-1037, 2014. DOI: 10.1099/jmm.0.073742-0
11- Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Richards GM: Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. International Journal of Food Microbiology, 136:204-213, 2009. DOI: 10.1016/j.ijfoodmicro.2009.02.029
12. European Commission(EU): Commision Regulation(EU) No:365/2010 of 28 April 2010 amending regulation (EC) No:2073/2005 on microbiological criteria for foodstuffs as regards Enterobacteriaceae in pasteurized milk and other pasteurized liquid dairy products and Listeria monocytogenes in food garde sat. L107, 9-11, Accessed:2010.
13. Turkish Food Codex : Microbiological Criteria Regulation No: 28157, Ankara/Turkey, Accessed: 29 December 2011.
14. Centers for Disease Control and Preventation(CDC): Investigation of Cronobacter Infections Among Infants in the United States. 2012A
15. Shaker R, Osaii T, Al-Omary W, Jaradat , Al-Zuby M: Isolation of Enterobacter sakazakii and other Enterobacter sp. From food and food production environments. Food Control, 18:1241-45, 2007.
DOI:10.1016/j.foodcont.2006.07.020
16. Restino L, Frampton EW, Lionberg WC, Becker RJ: A chromogenic plating medium for the isolation and identification of Enterobacter sakazakii from foods, food ingredients and evrironmental sources. Journal of Food Protection, 69: 315-22,2006. DOI: 10.4315/0362-028X-69.2.315
17. Oonaka K, Furuhata K, Hara M, Fukuyama M: Powder infant formula milk contaminated with Enterobacter sakazakii. Japanese Journal of Infection Diseases, 63:103-107, 2010.
18. Aigbekaen BO, Oshama CE: Isolation of Enterobacter sakazakii powdered foods locally consumed in Nigeria. Pakistan Journal of Nutrition, 9(7):659-663, 2010. DOI:10.3923/pjn.2010.659.663
19.Yemis GP: Investigation of Isolation and Development Parameters of Cronobacter sakazakii in Infant Foods (in Turkish: Cronobacter Sakazakii’nin Bebek Mamalarından İzolasyonu ve Gelişme Parametrelerinin İncelenmesi.) Ankara University, PhD Thesis. Ankara /Turkey, Accessed: 2011.
20.Cakmak B: The Existence of Enterobacter sakazakii in Various Infant Foods and Pasteurized Milk Presented on the Market (in Turkish: Piyasada Satışa Sunulan Çeşitli Bebek Mamalarında ve Pastörize Sütlerde Enterobacter sakazakii’nin Varlığı) İstanbul University, PhD Thesis. İstanbul/Turkey, Accessed: 2012.
21.Cetingurbuz B: Prevalence of Enterobacter Sakazakii in Powdered Infant Food and Raw Milk (in Turkish: Hazır Toz Bebek Mamaları ve Çiğ Sütlerde Enterobacter sakazakii’nin Bulunma Sıklığı) Gazi University, MsC.Thesis. Ankara/Turkey, Accessed: 2013.
22. International Organization for Standardization (ISO): ISO/TS 22964 IDF/RM 210: Milk and Milk Products-Detection of Enterobacter sakazakii. 1st ed., ISO Copyright Office, Switzerland, 2006.
23- Muytjens HL, Roelofs-Willemse H, Jaspar GH: Quality of powdered substitutes for breakfast milk with regard to members of the family Enterobacteriaceae. Journal of Clinical Microbiology, 26: 743-746, 1988.
24- Nazarowec-White M, Farber JM: Incidence, survival, and growth of Enterobacter sakazakii in infant formula. Journal of Food Protection, 60; 226–230, 1997.
25. Leuschner RGK, Baird F, Donald B, Cox LJ: Retracted: A medium for the presumptive detection of Enterobacter sakazakii in ifant formula. Food Microbiol, 21: 527-533, 2004.
DOI: 10.1016/j.fm.2003.12.002
26. Iversen C, Forsythe S: Isolation of E. sakazakii and other Enterobacteraceae from powdered formula milk and related products. Journal of Food Microbiol, 21: 771-777, 2004. DOI: 10.1016/j.fm.2004.01.009
27. Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C, Park J: International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. International Journal of Food Microbiology, 136;185-188, 2009.
DOI: 10.1016/j.ijfoodmicro.2009.08.005
28. Kandhai MC, Heuvelink AE, Reij MW, Beumer RR, Dijk R, van Tilburg JJHC, van Schothorst M, Gorris LGM: Study into the occurrence of Cronobacter spp. in the Netherlands between 2001 and 2005. Food Control, 21:1127-1136, 2010.
29. Hoque A, Ahmed T, Shahidullah M, Hossain A, Mannan A, Noor K, Nahar K, Ilias M, Ahmed D: Isolation and molecular identification of Cronobacter spp. from powdered infant formula (PIF) in Bangladesh. Int J Food Microbiol, 142: 375-378, 2010.
DOI: 10.1016/j.ijfoodmicro.2010.07.019
30. Fei P, Man C, Lou B, Forsythe S J, Chai Y, Li R, Niu J, Jiang Y: Genotyping and source tracking of Cronobacter sakazakii and C. malonaticus isolates from powdered infant formula and an infant formula production factory in China. Appl Environ Microbiol, 81: 5430–5439, 2015.
DOI: 10.1128/AEM.01390-15
31. Fei P, Jiang Y, Yuan X, Yang T, Chen J, Wang Z, Kang H, Forstrhe SJ: Prevalence, Molecular Characterization and Antibiotic Susceptibility of Cronobacter sakazakii Isolates from Powedered Infant Formula Collected from Chinese Retail Market. Front Microbiol, 8:2026, 2017.
DOI: 10.3389/fmicb.2017.02026
32- Tokatlı N: Composition of Baby Foods Produced in Different Formulations, Some Microbiological Properties and Determination of Enterobacter sakazakii Presence in Those Foods (in Turkish: Farklı Formülasyonlarda Üretilen Bebek Mamalarının Bileşimi, Bazı Mikrobiyolojik Özellikleri ve Enterobacter sakazakii Varlığının Belirlenmesi) Namık Kemal University, MsC. Thesis Tekirdag/Turkey, Accessed: 2009.
33.Gökmen M., Tekinşen K.K., Gürbüz Ü: Presence of Enterobacter sakazakii in Milk Powder, Whey Powder and White Cheese Produced in Konya. Kafkas Üniv.Vet Fak. Derg, 16(Suppl-A):S163-S166, 2010. DOI:10.9775/kvfd.2010.2801
34. Kaya GD: The Effect of Temperature and Sugar Varieties on Investigation and Development of Enterobacter sakazakii (Cronobacter spp.) in Dairy Products and Infant Foods (in Turkish: Süt Ürünlerinde ve Bebek Mamalarında Enterobacter sakazakii(Cronobacter spp.) Varlığının Araştırılması ve Gelişmesine Sıcaklık ve Şeker Çeşitlerinin Etkisi) İstanbul Technical University, PhD Thesis İstanbul/Turkey, Accessed: 2011.
35. Koluman A:Çeşitli gıdalarda Cronobacter spp., (Enterobacter sakazakii) izolasyon ve identifikasyon) Gida Teknolojileri Elektronik Dergisi, 6:16-19, 2011.
36.Manga M: Investigation of Cronobacter spp. (Enterobacter sakazakii) in Powder Infant Foods and Newborn Nutrition Tubes (in Turkish: Toz Bebek Mamalarında ve Yenidoğan Beslenme Tüplerinde Cronobacter spp.(Enterobacter sakazakii) Araştırılması) İstanbul University, MsC thesis. İstanbul/Turkey, Accessed: 2011.
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Jun 12, 2020
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Ziver T, Okburan G, Akgül Özer, Saribas S, Kocazeybek B, Kocazeybek B. Investigation of Cronobacter sakazakii (Enterobacter sakazakii) Presence in Cereal Infant Foods. Progr Nutr [Internet]. 2020 Jun. 12 [cited 2024 Jul. 18];22(2):596-602. Available from: https://mattioli1885journals.com/index.php/progressinnutrition/article/view/8907
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How to Cite
1.
Ziver T, Okburan G, Akgül Özer, Saribas S, Kocazeybek B, Kocazeybek B. Investigation of Cronobacter sakazakii (Enterobacter sakazakii) Presence in Cereal Infant Foods. Progr Nutr [Internet]. 2020 Jun. 12 [cited 2024 Jul. 18];22(2):596-602. Available from: https://mattioli1885journals.com/index.php/progressinnutrition/article/view/8907
