PRESENCE OF Cronobacter spp. AND SOME QUALITY CHARACTERISTICS OF THE POWDERED INFANT FORMULA

Year 2019, Volume: 37 Issue: 3, 769 - 777, 01.09.2020

Nazan Tokatlı Demırok , Muhammet Arıcı

Abstract

Cronobacter species are opportunistic food-borne pathogens that can cause severe and sometimes lethal infections (meningitis, bacteraemia, and necrotizing enterocolitis) predominantly in neonates and have been frequently isolated from different environments, plant materials (cereals, herbs and spices), and various foods, including powdered infant formula (PIF). Infants and newborns may infected through contaminated PIF with Cronobacter. The purpose of this study was to determine Cronobacter spp., total mesophilic aerobic bacteria count, coliform bacteria count and evaluate physicochemical properties in infant formula as well. Sixty two PIF samples were collected from different companies. In the studied formulas, Cronobacter spp. was identified in three (4.8%) of all PIF samples. The average total mesophilic aerobic bacteria and coliform bacteria numbers were found as 2.66 log cfu/g and 1.32 log cfu/g, respectively. The total sugar, invert sugar and protein content of PIF examples were found 49.12%, 32.36%, and 11.24%, respectively. In conclusion, this study results showed the prevalence of Cronobacter spp. from PIF and demonstrating a potential risk for infants in Turkey.

Keywords

Powder infant formula, physicochemical and microbiological properties, Cronobacter spp

References

• [1] Adekunte A., Valdramidis VP., Tiwari BK, et al., (2010) Resistance of Cronobacter sakazakii in reconstituted powdered infant formula during ultrasound at controlled temperatures: a quantitative approach on microbial responses”, Int. J. Food Microbiol., 142, 53-59.
• [2] Al-Nabulsi AA., Awaisheh SS., Osaili TM., et al., (2015) Inactivation of Cronobacter sakazakii in reconstituted infant milk formula by plant essential oils, J. Appl. Bot. Food Qual., 88, 97-101.
• [3] Alpsan FA., (2008) Determination of available lysine and lactulose values in infant formulas, MSc Thesis, Graduate School of Natural and Applied Sciences, Ege University, Izmir, Turkey.
• [4] AOAC, (1990) Official Methods of Analysis of Association of Official Analytical Chemists”, 15th Edn., Arlington, VA, Method 960.52.
• [5] Barness LA., Mauer AM., Holliday MA., et al., (1976) Commentary on breast-feeding and infant formulas, including proposed standards for formulas, Pediatrics, 57, 278-285.
• [6] Baumgartner A., Grand M., Liniger M., et al., (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.
• [7] Cemeroglu B., (2007) Gıda Analizleri”, Gıda Teknolojisi Derneği Yayınları, Ankara.
• [8] Chap J., Jackson P., Siqueira R., et al., (2009) International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and other infant foods, Int. J. Food Microbiol., 136, 185-188.
• [9] Codex Alimentarius Commission, “Code of Hygienic Practice for Powdered Formulae for Infants and Young Children” CAC/RCP 66, 2008. http://www.codexalimentarius.net/download/standards/11026/CXP_066e.pdf
• [10] Drudy D., Mullane NR., Quinn T., et al., “Enterobacter sakazakii: An emerging pathogen in powdered infant formula. Clin. Infect. Dis., 42, 996-1002, 2006.
• [11] Estuningsih S., Kress C., Hassan AA., et al., “Enterobacteriaceae in dehydrated powdered infant formula manufactured in Indonesia and Malaysia”, J. Food Protec., 69, 3013-3017, 2006.
• [12] Fang R., Wang Q., Yang B., et al., (2015) Prevalence and subtyping of Cronobacter species in goat milk powder factories in Shaanxi province”, China. J. Dairy Sci., 98, 7552-7559.
• [13] Fauziah T., Norrakiah AS, Uma Priya K., Norizan J., (2008) Detection of Cronobacter (Enterobacter) sakazakii and Enterobacteriaceae in Powdered Infant Formula and Children’s Milk”, In: Proceeding of the Seminar on Food Biotechnology: Perspectives, Challenges and opportunities, 352-360.
• [14] FDA, (1998) Isolation and enumeration of Enterobacter sakazakii from dehydrated powdered infant formula, In: Bacteriological Analytical Manual, 8a ed. RevisionA, United States: Food and Drug Administration.
• [15] Fei P., Jiang Y., Jiang Y., Yuan X, Yang T, Chen J, Wang Z, Kang H., Forsythe SJ., (2017) Prevalence, Molecular characterization, and antibiotic susceptibility of Cronobacter sakazakii ısolates from powdered ınfant formula collected from chinese retail markets, Front. Microbiol., 8, 2026-2034.
• [16] Ferrer E., Alegria A., Fare R., Abellan P., Romero F., (2000) Effects of thermal processing and storage on available lysine and furfural compounds cententa of infant formulas”, J. Agric. Food Chem., 48, 1817-1822.
• [17] Forsythe S., (2014) Powdered infant formula”, In: The microbiological safety of low water activity foods and spices. Springer New York, 177-211.
• [18] Gosney M., (2008) Enterobacter sakazakii bacteraemia with multiple splenic abscesses in a 75-year-old woman: a case report, Age and Ageing, 37, 236–237.
• [19] Guerra-Hernández E., Leon C., García‐Villanova B., Romera JM., (2002) Chemical changes in powdered infant formulas during storage, Int. J. Dairy Technol., 55: 171-176.
• [20] Harouna S., Carraminana JJ., Navarro F., Pérez MD, Calvo M.i Sánchez L., (2015) Antibacterial activity of bovine milk lactoferrin on the emerging foodborne pathogen Cronobacter sakazakii: Effect of media and heat treatment, Food Control, 47, 520-525.
• [21] Healy B., Cooney S., O'Brien S., Iversen C., Whyte P., Nally J., Callanan J., Fanning S., (2010) Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen, Foodborne Pathogens Dis., 7, 339-350.
• [22] Heperkan D., Dalkilic-Kaya G., Juneja VK., (2017) Cronobacter sakazakii in baby foods and baby food ingredients of dairy origin and microbiological profile of positive samples, LWT-Food Sci. Technol., 75, 402-407.
• [23] Hernandez-Ledesma B., Quiros A., Amigo L., Recio I., (2007) Identification of bioactive peptides after digestion of human milk and infant formula with pepsin and pancreatin, Int. Dairy J., 17, 42-49.
• [24] Iversen C., Forsythe S., (2004) Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant formula milk and related products, Food Microbiol., 21, 771–777, 2004.
• [25] Iversen C., Druggan P., Schumacher S., Lehner A., Feer C., Gschwend K., Joosten H., Stephan R., (2008) Development of a novel screening method for the isolation of “Cronobacter” spp. (Enterobacter sakazakii), Appl. Environ. Microbiol., 74, 2550-2553.
• [26] Jaradat ZW., Al Mousa W., Elbetieha A., Al Nabulsi A., Tall BD., (2014) Cronobacter spp.–opportunistic food-borne pathogens. A review of their virulence and environmental-adaptive traits, J. Med. Microbiol., 63, 1023-1037.
• [27] Leuschner RG., Bew, J., (2004) A medium for the presumptive detection of Enterobacter sakazakii in infant formula: interlaboratory study, J. AOAC Int., 87, 604–613.
• [28] Mardaneh J., Dallal MMS., (2017) Study of Cronobacter sakazakii strains isolated from powdered milk infant formula by phenotypic and molecular methods in Iran, Arch. Ped. Infec. Dis., 5, e38867.
• [29] Marshall RT., (1992) Standard Methods for the Exmination of Dairy Products, (16th ed.), American Public Health Association, Washington, DC.
• [30] Minami JI., Soejima T., Yaeshima T., (2012) Direct real-time PCR with ethidium monoazide: a method for the rapid detection of viable Cronobacter sakazakii in powdered infant formula, J. Food Protec., 75, 1572-1579,.
• [31] Mullane NR., Whyte P., Wall PG., et al., “Application of pulsed-field gel electrophoresis to characterise and trace the prevalence of Enterobacter sakazakii in an infant formula processing facility”, Int. J. Food Microbiol., 116, 73-81, 2007.
• [32] Muytjens HL, Roelofs-Willemse H., Jaspar GH., (1988) Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae, J. Clin. Microbiol., 26, 743–746.
• [33] Nazarowec-White M., Farber JM., (1997) Incidence, survival, and growth of Enterobacter sakazakii in infant formula, J. Food Protec., 60, 226–230.
• [34] Pagotto FJ., Abdesselam K., (2013) Cronobacter species, In: Food Microbiology Fundamentals and Frontiers (eds: Doyle MP., Buchanan RL.), ASM Press, 311-337.
• [35] Palcich G., de Moraes Gillio C., Aragon-Alegro LC., Pagotto FJ., Farber JM., Landgraf M., Destro MT., (2009) Enterobacter sakazakii in dried infant formulas and milk kitchens of maternity wards in São Paulo, Brazil, J. Food Protec., 72, 37-42.
• [36] Pan Z., Cui J., Lyu G., Du X, Qin L., Guo Y., Xu B., Cui Z., Zhao C., (2014) Isolation and molecular typing of Cronobacter spp. in commercial powdered infant formula and follow-up formula, Foodborne Pathogens Dis., 11, 456–461.
• [37] Pina-Pérez MC., Rodrigo D., López AM., (2009) Sub-lethal damage in Cronobacter sakazakii subsp. sakazakii cells after different pulsed electric field treatments in infant formula milk, Food Control, 20, 1145-1150.
• [38] Reich F., König R., von Wiese W., Klein G., (2010) Prevalence of Cronobacter spp. in a powdered infant formula processing environment, Int. J. Food Microbiol., 140, 214-217.
• [39] Santos RFS., Silva N., Junqueira VCA., Pereira JL, Moitta GC., Silva IF., (2005) Incidencia de Enterobacter sakazakii em alimentos infantis. In Simposio em Ciencias de Alimentos, SIMPOCAL, 3, Florianopolis, Resumo.
• [40] Torres-Chavolla E., Ramírez-Cerda E., Gutiérrez-Rojo R., (2007) Isolation and identification of Enterobacter sakazakii in infant milk formulas, Foodborne Pathogens Dis., 4, 164-168.
• [41] Xu X., Wu Q., Zhang J., Ye Y., Yang X., Dong X., (2014) Occurrence and characterization of Cronobacter spp. in powdered formula from Chinese retail markets, Foodborne Pathogens Dis., 11, 307–312.
• [42] Xu X., Li C., Wu Q Zhang J., Huang J., Yang G., (2015) Prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter spp. in Chinese ready-to-eat foods, Int. J. Food Microbiol., 204, 17-23.
• [43] Yan QQ., Condell O., Power K., Butler F., Tall BD., Fanning S., (2012) Cronobacter species (formerly known as Enterobacter sakazakii) in powdered infant formula: a review of our current understanding of the biology of this bacterium, J. Appl. Microbiol., 113, 1-15.
• [44] Zhang H., Hou P., Lv H., Chen Y., Li X., Ren Y., Wang M., Tan H., Bi Z., (2017) Surveillance and molecular typing of Cronobacter spp. in commercial powdered infant formula and follow up formula from 2011 to 2013 in Shandong Province, China, J. Sci. Food and Agric., 97, 2141-2146.