Skip to main navigation menu Skip to main content Skip to site footer
ACI Avances en Ciencias e Ingenierías

SECTION B: LIFE SCIENCES

Vol. 14 No. 1 (2022)

Microbiological quality of Powdered milk formula sold in Quito, Ecuador

DOI
https://doi.org/10.18272/aci.v14i1.2269
Submitted
May 7, 2021
Published
2022-03-23

Abstract

Human milk is recognized as the best form of nutrition for infants. However, where breast-feeding is not possible, infant milk formulae are used as breast milk substitutes. These formulae provide infants essential nutrients for their normal growth and development, but pathogenic microbes responsible for serious illness could contaminate them. The purpose of this study was to investigate the microbial quality of powdered formulae sold in Quito A total of 12 powdered infant formula and 12 powdered follow-up formula were collected from markets in Quito in 2019. Microbiological quality of samples was analyzed using conventional culture methods. According to the microbiological criteria specified in the Ecuadorian regulation, all powdered infant formulae comply with the total count of aerobic mesophilic organisms and enterobacteria. However, 6 powered follow-up samples do not comply with the regulation. The isolated bacterial genus in the samples were Klebsiella oxytoca (41.7%), Pantoea agglometans, Citrobacter freundii (25%), Bacillus subtilis (16.7%) and Pseudomonas (8.3%). The isolated bacteria genus in follow-up formula were Bacillus subtilis (75%), Bacillus cereus, Klebsiella oxytoca (25%) and Enterobacter aerogenes (25%), Hafnia alvei (16.7%) Escherichia coli (8,3%) and Pantoea agglomerans in the 8.3% of the samples. Salmonella was not found in any sample. This study indicates the necessity of conducing further microbial contamination research in powdered formula products because they could be a potential source of food contaminants and a risk for infants and babies.

viewed = 1458 times

References

  1. Brahm, P., & Valdés, V. (2017). Beneficios de la lactancia materna y riesgos de no amamantar. Revista Chilena de Pediatría,88(1),15-21. doi: http://dx.doi.org/10.4067/S0370-41062017000100001
  2. Organización Mundial de la Salud. (2017). Metas Mundiales de Nutrición 2025: Documento Normativo Sobre Lactancia Materna [Global Nutrition Targets 2025:
  3. Breastfeeding]. Recuperado de https://bit.ly/3ymq5xq
  4. Freire, W. B., Ramírez-Luzuriaga, M. J., Belmont, P., Mendieta, M. J., Silva-Jaramillo, K., Romero, N., Sáenz, K., Piñeiros, P., Goméz, L. F., & Monge, R. (2014). Tomo I: Encuesta Nacional de Salud y Nutriciòn de La Población de Cero a 59 Años ENSANUT- ECU 2012. Ministerio de Salud Pública/Instituto Nacional de Estadísticas y Censos. Quito-Ecuador.
  5. Organización Mundial de la Salud, & Organización Panamericana de la Salud. (2016). La Lactancia Materna En El Siglo XXI. The Lancet 1-8. Recuperado de https://www.paho.org/hq/dmdocuments/2016/LactanciaMaternaEnSigloXXI- April15.pdf
  6. Serrano, M., Pozo, M., Medina, D., Viteri, J. J., & Lombeida, E. (2019). Boletín Técnico: Encuesta Nacional de Salud y Nutrición, 2018 Indicadores de Salud y Nutrición de La Población Ecuatoriana. Recuperado de https://www.ecuadorencifras.gob.ec/documentos/web-inec/Estadisticas_Sociales/ENSANUT/ENSANUT_2018/Boletin ENSANUT 28_12.pdf
  7. Hernández, V. (2011). Fórmulas Infantiles. Revista Gastrohnup,13(2), 531-536.
  8. Recuperado de http://revgastrohnup.univalle.edu.co/a11v13n2s1/a11v13n2s1art5.pdf
  9. Dalmau Serra, J., Ferrer Lorente, B., & Vitoria Miñana, I. (2015). Lactancia artificial. Pediatría Integral,19(4), 251-259. Recuperado de https://www.pediatriaintegral.es/wp-content/uploads/2015/xix04/03/n4-251-259_Jaime%20Dalmau.pdf
  10. Ferrer Lorent, B., & Dalmau Serra, J. (2005). Fórmulas de continuación y fórmulas de crecimiento. Acta Pediátrica Española, 63, 471-475. Recuperado de https://bit.ly/3DszjvI
  11. Organización Mundial de la Salud, & Organización de las Naciones Unidas para la Alimentación y la Agricultura. (2018). Código de prácticas de higiene para alimentos con bajo contenido de humedad CXC 75-2015. Recuperado de https://bit.ly/3jr5eET
  12. Organización de las Naciones Unidas para la Alimentación y la Agricultura, & Organización Mundial de la Salud. (2017). Norma para alimentos envasados para lactantes y niños CODEX STAN 73-1981. Recuperado de https://bit.ly/3sYnlW7
  13. Organización de las Naciones Unidas para la Alimentación y la Agricultura, & Organización Mundial de Salud. (2008). CAC/RCP 66 - 2008 Código de Prácticas de Higiene Para Los Preparados En Polvo Para Lactantes y Niños Pequeños. Recuperado de https://bit.ly/3BpmDnw
  14. Food and Agriculture Organization of the United Nation, & World Health Organization. (2004). Enterobacter sakazakii and other microorganisms in powdered infant formula.
  15. Recuperado de http://www.fao.org/3/y5502e/y5502e.pdf
  16. Rodríguez-Urrego, J., Herrera-León, S., Echeita-Sarriondia, A., Soler, P., Simon, F., Mateo, S., & Investigation team. (2010). Nationwide Outbreak of Salmonella Serotype Kedougou Associated with Infant Formula, Spain, 2008. Eurosurveillance, 15(22), 1-5. doi: https://doi.org/10.2807/ese.15.22.19582-en
  17. Van Acker, J., De Smet, F., Muyldermans, G., Bougatef, A., Naessens, A., & Lauwers, S. (2001). Outbreak of Necrotizing Enterocolitis Associated with Enterobacter sakazakii in Powdered Milk Formula. Journal of Clinical Microbiology, 39(1), 293-297. doi: https://doi.org/10.1128/JCM.39.1.293-297.2001
  18. Agencia Nacional de Regulación, Control y Vigilancia Sanitaria. (2017b). Normativa Técnica Sanitaria Para Alimentos Procesados. Recuperado de https://www.controlsanitario.gob.ec/wp-content/uploads/downloads/2018/03/ARCSA-
  19. DE-067-2015-GGG_Alimentos-Procesados_incluye-RESOL-019-y-010-2.pdf
  20. Agencia Nacional de Regulación, Control y Vigilancia Sanitaria. (2017a). Arcsa informa sobre fórmulas lácteas infantiles contaminadas con Salmonella. Recuperado de https://bit.ly/3gHlEqW
  21. Agencia Nacional de Regulación, Control y Vigilancia Sanitaria. (2019). Actualización N° 2 | alerta sanitaria sobre lote 2958-004 de producto fórmula infantil Blemil Plus 2 arroz
  22. - 400 g contaminado con Salmonella. Recuperado de https://bit.ly/2XYJB6A
  23. Instituto Ecuatoriano de Normalización. (2013). Norma Técnica Ecuatoriana NTE INEN 707:2013 Preparados de inicio para la alimentación de lactantes. Requisitos. Quito.
  24. Recuperado de https://www.normalizacion.gob.ec/buzon/normas/nte_inen_707-3.pdf
  25. Instituto Ecuatoriano de Normalización. (2010). Norma Técnica Ecuatoriana NTE INEN 2516:2010 Preparados de continuación para la alimentación de lactantes. Requisitos.
  26. Quito. Recuperado de https://www.normalizacion.gob.ec/buzon/normas/2516.pdf
  27. Association of Official Analytical Chemists. (2002). AOAC Official Method 990.12 Aerobic Plate Count in Foods. Recuperado de https://www.agriculture.gov.au/sites/default/files/sitecollectiondocuments/aqis/exporting/meat/elmer3/approved-methods-manual/Aerobic-Plate-Count-TVC-Petrifilm-AOAC-998.12.doc
  28. Association of Official Analytical Chemists. (2006). Official Method 2003.01 Enumeration of Enterobacteriaceae in Selected Foods. Recuperado de https://epraise.com.tw/wp-content/uploads/2024/06/Petrifilm-EB_AOAC-OMA-2003.01.pdf
  29. Tortorello, M. L. (2003). Indicator organisms for safety and quality"”Uses and methods for detection: Minireview. Journal of AOAC INTERNATIONAL, 86(6), 1208-1217. doi: https://doi.org/10.1093/jaoac/86.6.1208
  30. Tallent, S., Knolhoff A., Rhodehamel J., Bennett R., & Harmon S. (2020). BAM Chapter 14: Bacillus cereus | FDA. Recuperado de https://bit.ly/3jtSspc
  31. Tallent, S., Hait J., Bennett R., & Lancette G. (2019). BAM Chapter 12: Staphylococcus aureus | FDA. Recuperado de https://bit.ly/38lqoxU
  32. Merck KGaA. (2010). Microbiology Manual. Darmstadt. Recuperado de http://www.laboquimia.es/pdf_catalogo/MERCK_Manual_de_microbiologia_12a_edicio n.pdf
  33. International Organization for Standardization. (2017). ISO 6579-1:2017 Microbiology of the Food Chain-Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella - Part 1: Detection of Salmonella spp. Recuperado de https://www.triphuc.com/wp-content/uploads/2019/10/ISO-6579-1-2017.pdf
  34. U.S. Food & Drug Administration. (2002). Laboratory methods - Isolation and Enumeration of Enterobacter sakazakii from dehydrated powdered infant formula. Recuperado de https://bit.ly/38mMjEX
  35. Microgen Bioproducts Ltd. (2007). Microgen GnA+B-ID. Recuperado de http://repositorio.puce.edu.ec/bitstream/handle/22000/12143/MICROGEN-GN-ID-MID64-641-65.%5B2%5D.pdf
  36. Aycicek, H., Oguz, U., & Karci, K. (2006). Determination of Total Aerobic and Indicator Bacteria on some raw eaten vegetables from wholesalers in Ankara, Turkey. International Journal of Hygiene and Environmental Health, 209(2), 197-201. doi: https://doi.org/10.1016/j.ijheh.2005.07.006
  37. Parra-Flores, J., Cerda-Leal, F., Contreras, A., Valenzuela-Riffo, N., Rodríguez, A., & Aguirre, J. (2018). Cronobacter sakazakii and microbiological parameters in dairy formulas asociated with a food alert in Chile. Frontiers in Microbiology, 9, 1-9. doi: https://doi.org/10.3389/fmicb.2018.01708
  38. Abdullah Sani, N., Hartantyo, S. H. P., & Forsythe, S. J. (2013). Microbiological assessment and evaluation of rehydration instructions on powdered infant formulas, follow-up formulas, and infant foods in Malaysia. Journal of Dairy Science, 96(1), 1-8. doi: https://doi.org/10.3168/jds.2012-5409
  39. Heperkan, D., Dalkilic-Kaya, G., & Juneja, V. (2016). Cronobacter sakazakii in baby foods and baby food ingredients of dairy origin and microbiological profile of positive samples. LWT - Food Science and Technology, 75, 402-407. doi: https://doi.org/10.1016/j.lwt.2016.09.013
  40. Maçi, R., Bijo, B., Xinxo, A., Shehu, F., & Memoçi, H. (2015). Prevalence of Salmonella spp. in imported powered infant formula (PIF). Albanian Journal of Agricultural Sciences, 14(3), 236-240. Recuperado de https://bit.ly/3ywGnUu
  41. Cahill, S. M., Wachsmuth, I. K., Costarrica, M. L., & Embarek, P. K. B. (2008). Powdered Infant Formula as a Source of Salmonella Infection in Infants. Clinical Infectious Diseases, 46(2), 268-273. doi: https://doi.org/10.1086/524737
  42. Park, J. K., Seok, W. S., Choi, B. J., Kim, H. M., Lim, B. K., Yoon, S. S., Kim, S., Kim,
  43. Y. S., & Park, J. Y. (2004). Salmonella enterica Serovar London Infections Associated with Consumption of Infant Formula. Yonsei Medical Journal, 45(1), 43-48. doi: https://doi.org/10.3349/ymj.2004.45.1.43
  44. Wang, X., Meng, J., Zhang, J., Zhou, T., Zhang, Y., Yang, B., Xi, M., & Xia, X. (2012). Characterization of Staphylococcus aureus Isolated from powdered infant formula milk and infant rice cereal in China. International Journal of Food Microbiology, 153(1-2), 142-147. doi: https://doi.org/10.1016/j.ijfoodmicro.2011.10.030
  45. Lesley, M. B., Ernie, S. R., Kasing, A., & Son, R. (2017). Detection of Bacillus cereus in formula milk and ultra high temperature (UHT) treated milk products. International Food Research Journal, 24(3), 985-989. Recuperado de http://www.ifrj.upm.edu.my/24%20(03)%202017/(12).pdf
  46. Matug, S. M., Aidoo, K. E., & Elgerbi, A. M. (2015). Microbiological examination of infant food and feed formula. Emergent Life Sciences Research, 1(1), 46-51. Recuperado de https://bit.ly/3t8qz9y
  47. Medina, G. A., Loredo A., & Aguilar, N. (2014). Cronobacter sakazakii: Un patógeno emergente transmitido por alimentos. Acta Química Mexicana, 6(12), 24-29. Recuperado de https://bit.ly/3gJhMFZ
  48. European Food Safety Authority. (2013). Scientific opinion on nutrient requirements and dietary intakes of infants and young children in the European Union. EFSA Journal,11(10), 1-103. doi: https://doi.org/10.2903/j.efsa.2013.3408
  49. Pei, X., Yang, S., Zhan, L., Zhu, J., Song, X., Hu, X., Liu, G., Ma, G., Li, N., & Yang, D. (2018). Prevalence of Bacillus cereus in powdered infant and powdered follow-up formula in China. Food Control, 93, 101-105. doi: https://doi.org/10.1016/j.foodcont.2018.05.049
  50. Jianyun, S., Hu, X., Lan, G., & Dong, K. (2017). Investigation on microbial contamination of infant formula powder during production process. Chinese Journal of Food Hygiene, 29(4), 474-477. Recuperado de https://bit.ly/3sXFQJZ
  51. Abbott, S. L., Moler, S., Green, N., Tran, R. K., Wainwright, K., & Janda, J. M. (2011). Clinical and Laboratory Diagnostic Characteristics and Cytotoxigenic Potential of Hafnia alvei and Hafnia paralvei Strains. Journal of Clinical Microbiology, 49(9), 3122-3126. doi: https://doi.org/10.1128/JCM.00866-11
  52. PukanÄíková, L., LipniÄanová, S., KaÄániová, M., Chmelová, D., & OndrejoviÄ, M. (2016). Natural microflora of raw cow milk and their enzymatic spoilage otential. Nova Biotechnologica et Chimica, 15(2), 142-155. doi: https://doi.org/10.1515/nbec-2016-0015
  53. Souza Viana, E., Martino Campos, M. E., Reis Ponce, A., Cuquetto Mantovani, H., & Dantas Vanetti, M. C. (2009). Biofilm formation and acyl homoserine lactone production in Hafnia alvei isolated from raw milk. Biological Research, 42(4), 427-436. doi: http://dx.doi.org/10.4067/S0716-97602009000400004
  54. Sezer, C., Vatansever, L., & Bilge, N. (2015). The microbiological quality of infant milk and follow - on formula. Van Veterinary Journal, 26(1), 31-34. Recuperado de https://dergipark.org.tr/en/download/article-file/217577
  55. Zadoks, R. N., Griffiths, H. M., Munoz, M. A., Ahlstrom, C., Bennett, G. J., Thomas, E., & Schukken, Y. H. (2011). Sources of Klebsiella and Raoultella species on dairy farms: Be careful where you walk. Journal of Dairy Science, 94(2), 1045-1051. doi: https://doi.org/10.3168/jds.2010-3603
  56. Babalola, M., & Adebayo, O. (2016). Detection of Chronobacter sakazakii and other enteropathogenic bacteria from selected brands of commercial powdered foods in Nigeria. British Microbiology Research Journal, 11(4), 1-13. doi: https://doi.org/10.9734/BMRJ/2016/17912
  57. Xiao-hong, X., Ping, H., Lin-lin, W., Da-wei, Y., & Yu-zhong, Z. (2012). Detection and analysis of Enterobacteriaceae and other bacteria in commercial infant formula powder in Lanzhou city. Chinese Journal of Health Laboratory Technology. Recuperado de https://bit.ly/3gFtAZF
  58. Cruz, A. T., Cazacu, A. C., & Allen, C. H. (2007). Pantoea agglomerans , a Plant Pathogen Causing Human Disease. Journal of Clinical Microbiology, 45(6), 1989-1992. doi: https://doi.org/10.1128/JCM.00632-07
  59. Mardaneh, J., & Soltan Dallal, M. M. (2013). Isolation, identification and antimicrobial susceptibility of Pantoea (Enterobacter) agglomerans isolated from consumed powdered infant formula milk (PIF) in NICU ward: first report from Iran. Iranian Journal of Microbiology, 5(3), 263-267. Recuperado de https://bit.ly/3zwBQCN
  60. Carvajal, D. (2013). Estudio de la presencia de Enterobacter sakazakii en fórmulas infantiles en polvo proporcionadas a pacientes lactantes de un hospital público de la ciudad de Guayaquil. Escuela Superior Politécnica del Litoral, Guayaquil. Recuperado de https://bit.ly/3ztyMap
  61. Davin-Regli, A., & Pagès, J. M.. (2015). Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Frontiers in Microbiology, 6(MAY), 1-10. doi: https://doi.org/10.3389/fmicb.2015.00392
  62. Liu, L., Chen, D., Liu, L., Lan, R., Hao, S., Jin, W., Sun, H., Wang, Y., Liang, Y., & Xu,
  63. J. (2018). Genetic Diversity, Multidrug Resistance, and Virulence of Citrobacter freundii From Diarrheal Patients and Healthy Individuals. Frontiers in Cellular and Infection Microbiology, 8(JUL), 1-10. doi: https://doi.org/10.3389/fcimb.2018.00233
  64. Giammanco, G. M., Aleo, A., Guida, I., & Mammina, C. (2011). Molecular Epidemiological Survey of Citrobacter freundii Misidentified as Cronobacter spp. (Enterobacter sakazakii) and Enterobacter hormaechei Isolated from Powdered Infant Milk Formula. Foodborne Pathogens and Disease, 8(4), 517-525. doi: https://doi.org/10.1089/fpd.2010.0719
  65. Ma, X., Zhang, G., Li, G., Wan, Y., Sun, H., Wang, H., & Shi, B. (2018). Biofilm bacterial community transition under water supply quality changes in drinking water distribution systems. Environmental Science: Water Research & Technology, 4(5), 644-653. doi: https://doi.org/10.1039/C8EW00033F
  66. De Jonghe, V., Coorevits, A., Van Hoorde, K., Messens, W., Van Landschoot, A., De Vos, P., & Heyndrickx, M. (2011). Influence of storage conditions on the growth of Pseudomonas species in refrigerated raw milk. Applied and Environmental Microbiology, 77(2), 460-470. doi: https://doi.org/10.1128/AEM.00521-10
  67. Dogan, B., & Boor, K. (2003). Genetic diversity and spoilage potentials among Pseudomonas spp. Isolated from fluid milk products and dairy processing plants. Applied and Environmental Microbiology, 69(1), 130-138. doi: https://doi.org/10.1128/AEM.69.1.130-138.2003
  68. Avellan, F., & Parra, Y. (2019). Aislamiento e identificación de Enterobacter sakazakii en una marca de fórmulas lácteas del mercado local. Universidad de Guayaquil, Guayaquil. Recuperado de https://bit.ly/38pt6Ti
  69. Earl, A. M., Losick, R., & Kolter, R. (2008). Ecology and Genomics of Bacillus Subtilis.
  70. Trends in Microbiology, 16(6), 269-275. doi: https://doi.org/10.1016/j.tim.2008.03.004
  71. U.S. Food & Drug Administration. (2012). BAM Chapter 29: Cronobacter | FDA.
  72. Recuperado de https://bit.ly/3BlsIBu
  73. Kent, R., Fitzgerald, G., Hill, C., Stanton, C., & Ross, P. (2015). Novel approaches to improve the intrinsic microbiological safety of powdered infant milk formula. Nutrients, 7, 1217-1244. doi: https://doi.org/10.3390/nu7021217