Dried Baby Formula as a Source of Opportunistic Members of Enterobacteriaceae for Infants

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Pubblicato: Jul 5, 2023
Versioni:
2023-07-05 (1)
DOI: https://doi.org/10.12681/jhvms.30211
AS Ibrahim
Cairo University, Faculty of Veterinary Medicine, Department of Food Hygiene and Control, Giza, Egypt
https://orcid.org/0000-0002-4117-2680
M Fouad Saad
Cairo University, Faculty of Veterinary Medicine, Department of Food Hygiene & Control
N Moustafa Hafiz
Cairo University, Faculty of Veterinary Medicine, Department of Food Hygiene & Control
Abstract

For evaluating the prevalence of Enterobacteriaceae in baby formulas, we examined 60 different samples of powdered infant milk formula and milk-cereal based infant formula that is recommended for first-day birth and from 6-month age, respectively, and collected from various supermarkets, shops, and pharmacies. Six (20.0%) and thirteen (43.3%) powdered infant milk formulas and milk-cereal based infant formulas, respectively, were contaminated by different Enterobacteriaceae involved Enterobacter cloacae ssp. cloacae, Pantoea spp., Enterobacter hormaechei, and Raoultella ornithinolytica, which were identified using traditional biochemical tests and the vitek2 compact system. Only five samples of investigating milk-cereal based infant formula type have coliforms count of 4 MPN/g. All species were susceptible to gentamycin, while all were resistant to cephalothin antibiotics. Eventually, 20.0 % of powdered infant milk formula samples were unacceptable referred to Egyptian standards (2072/2006) and most of the comparable international standards. In the study, we proved the contamination of powdered milk baby formula by Enterobacteriaceae, which mainly causes health problems in immature and immunocompromised infants. The dried infant formula factories are more needful for good hygiene and safety systems applications. This study is one of the fewest studies conducted in Egypt to isolate Enterobacteriaceae members from dried foods; especially milk-cereal based infant formula. 

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Biografia autore
N Moustafa Hafiz , Cairo University, Faculty of Veterinary Medicine, Department of Food Hygiene & Control

Professor of Food Hygiene & Control

Riferimenti bibliografici
AbbasA, Ahmad I (2018) First report of neonatal early-onset sepsis
caused by multi-drug-resistant Raoultellaornithinolytica. Infection
: 275–277.
Abbas YA, Radhi GF (2016) Rapididentification of Enterobacter spp.
islated from hospitals in Basrah Province by automated system
(VITEK® 2 COMPACT). Intern J Microbiol, Genetics and Monocular Biology Research 2 (2) : 9-20.
Abdullah Sani N, Hartantyo SHP, Forsythe SJ (2013) Microbiological
assessment and evaluation of rehydration instructions on powdered
infant formulas, follow-up formulas, and infant foods in Malaysia. J.
Dairy Sci 6(1) : 1–8.
Alsharjabi FA, Al-QadasiAM, Al-ShorganiNK (2019) Bacteriological
evaluation of weaning dried foods consumed in Taiz City, Republic
of Yemen. JSaudi SocAgric Sci18 (3) : 302–308.
Al-Timimi BJ (2007) Antimicrobial resistance of bacteria isolated from
powdered infant formulas (PIF). Med J Babylon 4(3-4) :251-262.‏
APHA (2004) Standard methods for the examination of dairy products.
th. Ed. American public health association. Washington D.C.
BarronJC, ForsytheSJ (2007) Dry stress and survival time of Enterobacter
sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J Food Prot70 (9) :2111–2117.
BioMérieuxVitek (2013) Vitek 2 – technology product information manual. Pdf version located with the QC SOPs, a hard copy is available
in the laboratory.
CAC (2008) Codex Alimentarius Commission. Code of hygienic practice
for powdered formulae for infants and young children. CAC/RCP 66-
CLSI (2017) Clinical and Laboratory Standards Institute, performance
standards for antimicrobial susceptibility testing. M100S, twenty seventh ed.USA.
DarbandiF(2010) Parallel comparison of accuracy in vitek2 auto analyzer
and Api 20E/Api20NE microsystems.Thesis is a compulsory part in
the Master of Science with a major in chemical engineering - industrial biotechnology, Boras, Sweden.
Davin-RegliA, Pages, J-M (2015) Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic
treatment. Front Microbiol 6:1-10.
EC (2007) European Commission, Commission Regulation (EC) No
/2007 of 5 December 2007 amending Regulation (EC) No
/2005 on microbiological criteria for foodstuffs. Off J Eur Union
L 322:12–29.
EFSA (2007) European Food Safety Authority, Scientific opinion on BIOHAX panel on the request from the Commission for review of the
opinion on microbiological risks in infant formulae and follow-up
formulae with regard to Enterobacteriaceae as indicators. EFSA
J444: 1–14.
El‐Zamkan MA, MohamedHMA (2018) Molecular detection of Enterobacter spp. and other related species in powdered milk infant formula
and milk powder. J. Food Saf 38 (6) :e12538.
ES (2005) Egyptian Standard, processed cereal-based for foods for infants and children. (ES: 3284/ 2005). Cairo: Egyptian Organization
for Standardization and Quality Control, Ministry of Industry.
ES (2006) Egyptian Standard, Infant Formula. (ES: 2072/ 2006). Cairo:
Egyptian Organization for Standardization and Quality Control, Ministry of Industry.
EstuningsihS, KressC, HassanAA, AkinedenÖ, SchneiderE, UsleberE
(2006) Enterobacteriaceae in Dehydrated Powdered Infant Formula Manufactured in Indonesia and Malaysia. J Food Prot 69 (12) :
–3017.
FAO/WHO (2004) Food Agriculture Organization of the United Nations
and World Health Organization, Enterobacter Sakazakii and Other
Microorganisms in Powdered Infant Formula: Meeting Report. In:
Microbiological Risk Assessment Series, No. 6.
FAO/WHO (2006) Food Agriculture Organization of the United Nations
and World Health Organization, Enterobacter Sakazakii and Salmonellapowdered infant formula. Microbiological Risk Assessment Series, No.10.
FarmerJJI, BoatwrightKD, JandaJM (2007) Enterobacteriaceae: Introduction and identification, chapter 42. 9th ed. Manual of Clinical
Microbiology. Washington, DC: American Society for Microbiology,
–669.
FeiP, ManC, LouB, et al (2015) Genotyping and Source Tracking of
Cronobactersakazakii and C. malonaticus Isolates from Powdered
Infant Formula and an Infant Formula Production Factory in China.
ApplEnviron Microbiol 81 (16) : 5430–5439.
Flores, J, Arvizu, S., Silva, J, et al (2011). Two cases of haemorrhagic diarrhea caused by Cronobactersakazakii in hospitalized nursing infants
associated with the consumption of powdered infant formula. J Food
Prot 74: 2177–2181.
ForsytheSJ (2005) Enterobacter sakazakii and other bacteria in powdered
infant milk formula. Matern. Child Nutr 1 (1), 44–50.
Fricker-FeerC (2012) Identification and further characterization of Enterobacteriaceae and Cronobacter spp. in a milk powder and infant
processing plant (Doctoral dissertation, Ludwig Maximilian University of Munich, Germany).
FSANZ (2016) Food Standards Australia New Zealand, Schedule 27 - Microbiological limits in food, (Accessed 1 March 2016).
Giammanco GM, AleoA, GuidaI, et al (2011) Molecular epidemiological survey of Citrobacter freundii misidentified as Cronobacter spp.
(Enterobacter sakazakii) and Enterobacter hormaechei isolated from
powdered infant milk formula. Foodborne pathog and dis 8 (4) :
–525.
Hafiz NM, Saad MF, Hanafy MH,et al (2016) Detection of Mycobacterium avium subsp. paratuberculosis in raw buffaloe’s milk. Inter J
ChemTech Res 9:123-128.
Ibrahim AS, SaadMF,Hafiz NM (2020) Toxic elements in dried milk and
evaluation of their dietary intake in infant formula. Int J Vet Sci9:563-
Ibrahim AS, Saad, MF, Hafiz NM (2021) Safety and quality aspects of
whole and skimmed milk powders. Acta Sci Pol Technol Aliment 20
(2) : 165–177.
Ibrahim AS, Hafiz NM, Saad MF (2022a) Prevalence of Bacillus cereus
in dairy powders focusing on its toxigenic genes and antimicrobial
resistance. Arch Microbiol 204 (6) : 339.
Ibrahim AS, Saad MF, Hafiz NM (2022b) Prevalence of melamine and
cyanuric acid in powdered dairy products in Egypt. Egypt J of Chem
(1) : 699 – 702.
ISO (2017) International Organization for Standardization. Microbiology
of food and animal feeding stuffs horizontal method for the detection
of Salmonella spp., Geneva, Switzerland. ISO, 6579.
ISO/IDF(2006) Technical Specification: Milk and Milk Products e Detection of Enterobacter Sakazakii. ISO/TS 22964; IDF/RM 210.
Iversen, C, Forsythe S (2004). Isolation of Enterobacter sakazakii and
other Enterobacteriaceae from powdered infant formula milk and related products. Food Microbiol 21 (6) : 771–777.
Jackson EE, Forsythe SJ(2016) Comparative study of Cronobacter identification according to phenotyping methods. BMC Microbiol 16 (1)
: 146-155.
Jackson EE, Parra-FloresJ, Fernandez EscartinE, et al (2015) Reevaluation of a spected Cronobactersakazakii outbreak in Mexico. J Food
Prot1191–1196.
JacobsC, BraunP, HammerP (2011) Reservoir and routes of transmission
of Enterobacter sakazakii (Cronobacter spp.) in a milk powder-producing plant. JDairy Sci 94 (8) :3801–3810.
Jaradat ZW, AbabnehQO, SaadounIM, et al (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 (1) :225-235.
KentR, FitzgeraldG, HillC, et al (2015) Novel approaches to improve the
intrinsic microbiological safety of powdered infant milk formula. Nutrients7(2) :1217–1244.
KimSA, OhSW, LeeYM, et al. (2011) Microbial contamination of food
products consumed by infants and babies in Korea. Lett Appl Microbiol53 (5) :532–538.
MardanehJ, DallalMM (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. IranJ Microbiol5 (3) : 263–267.
Martin C, Ling PR, BlackburnG (2016) Review of infant feeding: key
features of breast milk and infant formula. Nutrients 8 (5) :279.
NCCLS (2002) National Committee for Clinical Laboratory Standards,
Performance standards for antimicrobial susceptibility testing for
bacteria isolated from animals; 12th informational supplement,
M100-S12. Wayne, PA: approved standard 2nd edition.
NesmaHY, NagahMH, HalawaMA, et al (2020). Influence of some hygienic measures on the prevalence of subclinical mastitis in a dairy
farm. Int J Dairy Sci 15: 38-47.
NourI, EldeglaHE, NasefN, et al (2017) Risk factors and clinical outcomes for carbapenem-resistant Gram-negative late-onset sepsis in a
neonatal intensive care unit. J Hosp Infect 97(1) :52–58.
Oteo J, CercenadoE, Vindel A, et al (2013) Outbreak of multidrug-resistant CTX-M-15-producing Enterobacter cloacae in a neonatal intensive care unit. J Med Microbiol 62(4) :571–575.
PaauwA, CaspersMPM, SchurenFHJ, et al (2008) Genomic Diversity
within the Enterobacter cloacae Complex. PLoS ONE 3 (8) : e3018.
Parra-Flores J, AguirreJ, JunejaV, et al (2018) Virulence and antibiotic
resistance profiles of Cronobactersakazakii and Enterobacter spp.
involved in the diarrheic hemorrhagic outbreak in Mexico. Front Microbiol9: 2206.
Sanderson MW, Sargeant JM, RenterDG, et al (2005) Factors associated
with the presence of Coliforms in the feed and water of feedlot cattle.
Appl Environ Microbiol71(10) :6026–6032.
Sayed M(2004) Microbiological quality of baby foods. Assiut Veterin
Med J 50: 72–79.
SchmidM, IversenC, GontiaI, et al (2009) Evidence for a plant-associated
natural habitat for Cronobacter spp. ResMicrobiol 160 (8) :608–614.
Sękowska A (2017) Raoultella spp.- clinical significance, infections and
susceptibility to antibiotics. Folia Microbiol 62(3) : 221–227.
Seng P, Boushab, BM, RomainF, et al (2016) Emerging role of Raoultellaornithinolytica in human infections: a series of cases and review of
the literature. Int JInfect Dis 45:65–71.
Sharma, M., Dogra, B.B., Rabındranath, M, et al (2012) Multidrug Resistant PantoeaAgglomerans in a patient with septic arthritis-a rare
report from India. Int J Microbiol Res 4: 263-265.
Townsend SM, Hurrell E, Caubilla-BarronJ, et al (2008) Characterization
of an extended-spectrum beta-lactamase Enterobacter hormaechei
nosocomial outbreak, and other Enterobacter hormaechei misidentified as Cronobacter (Enterobacter) sakazakii. Microbiology 154 (12)
: 3659–3667.
Whitman WB, DeVosP, ChunJ, et al (2015) Bergey’s Manual of Systematic of Archaea and Bacteria, John Wiley & Sons, Inc., Hoboken, New
Jerse, 1st ed.
WHO (2007) World Health Organization, Safe Preparation, Storage and
Handling of Powdered Infant Formula: Guidelines. Geneva, WHO.
Yahya AA, GhosoonFR (2016) Rapid identification of Enterobacterspp. isolated from hospitals in Basrah Province by automated system (VITEK® 2 Compact). Inter J MicrobiolGenet Monocular Biol
‏2:9-20.Res
YoussifNH, HafizNM,HalawaMA, et al (2020) Impact of subclinical mastitis on milk quality in different seasons. Int J Vet Sci 9:313-316