Distribution, prevalence and persistence of Cronobacter (Enterobacter sakazakii) in the nonprocessing and processing environments of five milk powder factories

Craven, H. M.; McAuley, Catherine M.; Duffy, Lesley L.; Fegan, Narelle

doi:10.1111/j.1365-2672.2010.04733.x

Cited by 71 publications

(53 citation statements)

References 22 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Twelve strains of C. sakazakii that were isolated from PIF collected in 12 countries were shown to be ST4. Fifteen strains which had been isolated from milk-processing factories, including roller dryers, tanker bays, and spray dryers, in Australia and Germany (6,21) were revealed to be ST4. Other nonclinical sources included isolates from weaning food, chocolate (44), and a washing brush (46).…”

Section: Mlst Of the Genusmentioning

confidence: 99%

Diversity of the Cronobacter Genus as Revealed by Multilocus Sequence Typing

et al. 2012

View full text Add to dashboard Cite

Cronobacter (previously known as Enterobacter sakazakii ) is a diverse bacterial genus consisting of seven species: C. sakazakii , C. malonaticus , C. turicensis , C. universalis , C. muytjensii , C. dublinensis , and C. condimenti . In this study, we have used a multilocus sequence typing (MLST) approach employing the alleles of 7 genes ( atpD , fusA , glnS , gltB , gyrB , infB , and ppsA ; total length, 3,036 bp) to investigate the phylogenetic relationship of 325 Cronobacter species isolates. Strains were chosen on the basis of their species, geographic and temporal distribution, source, and clinical outcome. The earliest strain was isolated from milk powder in 1950, and the earliest clinical strain was isolated in 1953. The existence of seven species was supported by MLST. Intraspecific variation ranged from low diversity in C. sakazakii to extensive diversity within some species, such as C. muytjensii and C. dublinensis , including evidence of gene conversion between species. The predominant species from clinical sources was found to be C. sakazakii. C. sakazakii sequence type 4 (ST4) was the predominant sequence type of cerebral spinal fluid isolates from cases of meningitis.

show abstract

Section: Mlst Of the Genusmentioning

confidence: 99%

Diversity of the Cronobacter Genus as Revealed by Multilocus Sequence Typing

et al. 2012

View full text Add to dashboard Cite

show abstract

“…More importantly for neonatal health, Cronobacter spp. have been isolated from powdered infant formula (PIF) and milk powder production factories (11)(12)(13). Consequently, they can cause severe neonatal infections through the ingestion of contaminated PIF, especially in low-birth-weight infants (14,15).…”

mentioning

confidence: 99%

Genotyping and Source Tracking of Cronobacter sakazakii and C. malonaticus Isolates from Powdered Infant Formula and an Infant Formula Production Factory in China

Peng

Man

Lou

et al. 2015

Appl Environ Microbiol

View full text Add to dashboard Cite

dCronobacter spp. (formerly defined as Enterobacter sakazakii) are opportunistic bacterial pathogens of both infants and adults. In this study, we analyzed 70 Cronobacter isolates from powdered infant formula (PIF) and an infant formula production facility in China to determine possible contamination routes. The strains were profiled by multilocus sequence typing (MLST), pulsedfield gel electrophoresis (PFGE), PCR-based O-antigen serotyping, and ompA and rpoB sequence analyses. The isolates were primarily Cronobacter sakazakii (66/70) or Cronobacter malonaticus (4/70). The strains were divided into 38 pulsotypes (PTs) using PFGE and 19 sequence types (STs) by MLST. In contrast, rpoB and ompA sequence analyses divided the strains into 10 overlapping clusters each. PCR serotyping of the 66 C. sakazakii and 4 C. malonaticus strains resulted in the identification of four C. sakazakii serotypes (O1, O2, O4, and O7) and a single C. malonaticus serotype, O2. The dominant C. sakazakii sequence types from PIF and an infant formula production factory in China were C. sakazakii clonal complex 4 (CC4) (n ‫؍‬ 19), ST1 (n ‫؍‬ 14), and ST64 (n ‫؍‬ 11). C. sakazakii CC4 is a clonal lineage strongly associated with neonatal meningitis. In the process of manufacturing PIF, the spray-drying, fluidized-bed-drying, and packing areas were the main areas with Cronobacter contamination. C. sakazakii strains with the same pulsotypes (PT3 and PT2) and sequence types (ST1 and ST64) were isolated both from processing equipment and from the PIF finished product.C ronobacter (formerly defined as Enterobacter sakazakii) is a diverse genus in the family Enterobacteriaceae. These organisms are Gram-negative, motile, facultatively anaerobic, nonspore-forming peritrichous rod-shaped opportunistic bacterial pathogens (1-3). The genus consists of seven species: Cronobacter sakazakii, C. malonaticus, C. turicensis, C. muytjensii, C. dublinensis, C. universalis, and C. condimenti (4). Of these, C. sakazakii has been associated primarily with neonatal infections and C. malonaticus with adult infections (5-7). Cronobacter spp. are adapted to a wide range of environments, such as water, soil, plant material (wheat, rice, herbs, and spices), food production environments, and various food products (8-10). More importantly for neonatal health, Cronobacter spp. have been isolated from powdered infant formula (PIF) and milk powder production factories (11-13). Consequently, they can cause severe neonatal infections through the ingestion of contaminated PIF, especially in low-birth-weight infants (14, 15). Once infected by Cronobacter spp., patients may suffer from fatal necrotizing enterocolitis, septicemia, or meningitis, which can cause severe neurological sequelae, developmental disorders, and even death (16,17).Understanding the genetic diversity of the genus Cronobacter can ensure that accurate detection methods are applied for its detection and control, as well as for reliable microbial source tracking of contaminated foods such as infant formula (16)(...

show abstract

“…Pulsed-field gel electrophoresis (PFGE) is an accepted method for tracking isolates across the food chain, and this approach is generally considered suitable for epidemiological studies (12,(21)(22)(23)(24)(25)(26)(27)(28). A multilocus sequence typing (MLST) scheme for Cronobacter species was developed, which focuses on single nucleotide polymorphisms associated with seven housekeeping genes (including atpD, fusA, glnS, gltB, gyrB, infB, and pps) and identifies their associated alleles (29).…”

mentioning

confidence: 99%

Comparative Genotypic and Phenotypic Analysis of Cronobacter Species Cultured from Four Powdered Infant Formula Production Facilities: Indication of Pathoadaptation along the Food Chain

Yan

Wang

Gangiredla

et al. 2015

Appl Environ Microbiol

View full text Add to dashboard Cite

cCronobacter species are opportunistic pathogens commonly found in the environment. Among the seven Cronobacter species, Cronobacter sakazakii sequence type 4 (ST-4) is predominantly associated with recorded cases of infantile meningitis. This study reports on a 26-month powdered infant formula (PIF) surveillance program in four production facilities located in distinct geographic regions. The objective was to identify the ST(s) in PIF production environments and to investigate the phenotypic features that support their survival. Of all 168 Cronobacter isolates, 133 were recovered from a PIF production environment, 31 were of clinical origin, and 4 were laboratory type strains. Sequence type 1 (n ‫؍‬ 84 isolates; 63.9%) was the dominant type in PIF production environments. The majority of these isolates clustered with an indistinguishable pulsotype and persisted for at least an 18-month period. Moreover, DNA microarray results identified two phylogenetic lineages among ST-4 strains tested. Thereafter, the ST-1 and -4 isolates were phenotypically compared. Differences were noted based on the phenotypes expressed by these isolates. The ST-1 PIF isolates produced stronger biofilms at both 28°C and 37°C, while the ST-4 clinical isolates exhibited greater swimming activity and increased binding to Congo red dye. Given the fact that PIF is a low-moisture environment and that the clinical environment provides for an interaction between the pathogen and its host, these differences may be consistent with a form of pathoadaptation. These findings help to extend our current understanding of the epidemiology and ecology of Cronobacter species in PIF production environments. The epidemiological link between Cronobacter infection in neonates and contaminated powdered infant formula (PIF) has been previously established (4, 5), with C. sakazakii sequence type 4 (ST-4) being linked to cases of meningitis (6). Outbreaks have been associated with contaminated food products and the presence of this bacterium in PIF production environments (5, 7).In order to rapidly and accurately characterize Cronobacter species in PIF and its associated environments, several molecularbased protocols have been developed, which include direct target gene detection and subtyping methods (8-20). Pulsed-field gel electrophoresis (PFGE) is an accepted method for tracking isolates across the food chain, and this approach is generally considered suitable for epidemiological studies (12,(21)(22)(23)(24)(25)(26)(27)(28). A multilocus sequence typing (MLST) scheme for Cronobacter species was developed, which focuses on single nucleotide polymorphisms associated with seven housekeeping genes (including atpD, fusA, glnS, gltB, gyrB, infB, and pps) and identifies their associated alleles (29). This protocol has been used to describe some of the diversity related to the genus (6, 29-31). Both PFGE and MLST have been widely applied to study the genomic diversity of Cronobacter isolated from manufacturing facilities, commercial PIF, and follow-up formula, as we...

show abstract

Distribution, prevalence and persistence of Cronobacter (Enterobacter sakazakii) in the nonprocessing and processing environments of five milk powder factories

Cited by 71 publications

References 22 publications

Diversity of the Cronobacter Genus as Revealed by Multilocus Sequence Typing

Diversity of the Cronobacter Genus as Revealed by Multilocus Sequence Typing

Genotyping and Source Tracking of Cronobacter sakazakii and C. malonaticus Isolates from Powdered Infant Formula and an Infant Formula Production Factory in China

Comparative Genotypic and Phenotypic Analysis of Cronobacter Species Cultured from Four Powdered Infant Formula Production Facilities: Indication of Pathoadaptation along the Food Chain

Contact Info

Product

Resources

About