Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation
Introduction
Neonatal infections believed to have been caused by Cronobacter sakazakii, formerly Enterobacter sakazakii (Iversen et al., 2008), were first reported by Urmenyi and Franklin (1961). Numerous cases have been subsequently described. A book (Farber and Forsythe, 2008) and several reviews (Nazarowec-White and Farber, 1997a, Lai, 2001, Iversen and Forsythe, 2003, Lehner and Stephan, 2004, Gurtler et al., 2005, Bowen and Branden, 2006, Drudy et al., 2006, Mullane et al., 2006, Friedemann, 2007) have summarized information on taxonomy, biochemical characteristics, epidemiology, pathogenicity, clinical etiology, and survival and inactivation characteristics of C. sakazakii in foods and the environment.
Reconstituted powdered infant formula and powdered milk have been the most common vehicles implicated in neonatal C. sakazakii infections. Other unidentified sources of the pathogen were involved in cases of infections in infants, children, and immunocompromised adults having underlying medical conditions (Jimenez and Gimenez, 1982, Pribyl et al., 1985, Hawkins et al., 1991, Emery and Weymouth, 1997, Dennison and Morris, 2002). C. sakazakii infections in these age groups raise concerns about the survival and growth characteristics of the pathogen in foods other than powdered and reconstituted infant formula and milk. C. sakazakii has been isolated from a wide range of foods and beverages (Table 1), thereby posing some level of safety risk to the consumer. Information about how the behavior of C. sakazakii on these foods is affected by conditions to which they are exposed would be meaningful when developing strategies and interventions for its control.
Summarized here is a series of experiments conducted in our laboratories. No attempt is made to review the numerous excellent studies reported internationally. The text evolved from a presentation at an International Meeting on Cronobacter (E. sakazakii) in Dublin, Ireland, 22–23 January 2009 at which we were invited to give an overview of our Cronobacter research. Objectives of our work were to better define the survival and growth characteristics of C. sakazakii upon exposure to environments and conditions mimicking those imposed by processes and practices followed in commercial channels and in food storage and preparation areas in hospitals, day-care centers, and the home.
Section snippets
Recovery of stressed cells
Several differential and selective media have been developed for detecting or enumerating C. sakazakii in clinical, food, and environmental samples (Hsing-Chen and Wu, 1992, Iversen et al., 2004b Leuschner et al., 2004a, Leuschner et al., 2004b, Oh and Kang, 2004). While these media are promising for recovering the pathogen from various sources, their suitabilities for supporting repair of stressed or injured cells and colony development by these cells were not compared. C. sakazakii is known
Survival in powdered infant formula
Differences in composition of infant formulas, coupled with differences in aw and storage temperature, are likely to affect the survival of C. sakazakii in powdered infant formula and other foods. The pathogen is known to survive for at least two years in powdered infant formula at low aw (Edelson-Mammel et al., 2005, Barron and Forsythe, 2007). We undertook a study to determine the effects of aw and storage temperature on the survival characteristics of the pathogen in four commercially
Survival in dry infant cereals
Milled, reconstituted cereals are common weaning foods for infants at the age of 4–6 months. The immune systems in these infants is not fully developed. We and others have described conditions affecting the survival of C. sakazakii in powdered and reconstituted infant formula but not dry or reconstituted infant cereal. Recognizing that other foodborne pathogens, e.g., enterohemorrhagic Escherichia coli O157:H7 (Deng et al., 1998) and toxigenic Bacillus cereus (Jaquette and Beuchat, 1998), can
Attachment and formation of biofilm
Attachment of bacteria and fungi to surfaces may be followed by the production of exopolysaccharide and biofilm formation (Kumar and Anand, 1998). C. sakazakii has been reported to be able to attach to abiotic materials such as silicon, latex, polycarbonate, stainless steel, glass, and polyvinyl chloride and form biofilms (Iversen et al., 2004b, Lehner et al., 2005, Grimm et al., 2008). We examined conditions affecting attachment of and biofilm formation by C. sakazakii on stainless steel and
Survival and growth on produce and in unpasteurized juice
Among the ready-to-eat foods from which C. sakazakii has been isolated are lettuce (Soriano et al., 2001), seed sprouts (Kim et al., 2009), and other vegetables (Geiges et al., 1990, Ottaviani et al., 1992, Leclercq et al., 2002, Weiss et al., 2005). The incidence of foodborne diseases associated with consumption of fresh produce has increased in recent years. The ability of C. sakazakii to grow at temperatures as low as 5.5 °C (Nazarowec-White and Farber, 1997b) raises concern about its
Conclusions
C. sakazakii can be found in a wide range of foods and beverages, many of which are not subjected to treatments or processes that will inactivate the pathogen. Its ability to survive and grow in these products raises concern about safety risks not only to neonates and infants but also to older immunocompromised consumers. The suitability of infant cereals and some types of fresh fruits and vegetables to support luxuriant growth of C. sakazakii is of particular concern. The ability of the
Acknowledgments
Studies involving infant formula and cereal were supported, in part, by a grant from the International Life Sciences Institute – North America (ILSI N.A.). Studies on fresh produce were supported by a grant from the United States Department of Agriculture (USDA). The opinions expressed herein are those of the authors and do not necessarily represent the views of ILSI N.A. or USDA.
References (113)
- et al.
A comparative study between overlay method and selective differential media for recovery of stressed Enterobacter sakazakii cells in infant formula
Food Microbiology
(2008) - et al.
Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula
Journal of Food Protection
(2007) - et al.
Epidemiological typing of Enterobacter sakazakii in two neonatal noscomial outbreaks
Diagnostic Microbiology and Infectious Diseases
(1990) - et al.
Characterization of the microflora of attieke, a fermented cassava product, during traditional small-scale preparation
International Journal of Food Microbiology
(2006) - et al.
Influence of temperature and pH on survival of E. coli O157:H7 in dry foods and growth in reconstituted infant rice cereal
International Journal of Food Microbiology
(1998) - et al.
Formation of B-vitamins by bacteria during the soaking process of soybeans for tempe fermentation
International Journal of Food Microbiology
(1994) - et al.
Survival of Enterobacter sakazakii in a dehydrated powdered infant formula
Journal of Food Protection
(2005) - et al.
Microbial spoilage of tofu (soybean curd)
Journal of Food Protection
(1993) Enterobacter sakazakii in food and beverages (other than infant formula and milk powder)
International Journal of Food Microbiology
(2007)- et al.
Cellulose and extracellular matrix component present in Enterobacter sakazakii biofilms
Journal of Food Protection
(2008)
Growth of Enterobacter sakazakii in reconstituted infant formula as affected by composition and temperature
Journal of Food Protection
Inhibition of growth of Enterobacter sakazakii in reconstituted infant formula by the lactoperoxidase system
Journal of Food Protection
Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature
Journal of Food Protection
Enterobacter sakazakii: a coliform of increased concern to infant health
International Journal of Food Microbiology
Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula
Trends in Food Science and Technology
Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant formula milk and related products
Food Microbiology
A selective differential medium for Enterobacter sakazakii, a preliminary study
International Journal of Food Microbiology
Survival and growth of psychrotrophic Bacillus cereus in dry and reconstituted infant rice cereal
Journal of Food Protection
Septic shock due to Enterobacter sakazakii
Clinical Microbiology Newsletter
Survival and growth of Enterobacter sakazakii on fresh-cut fruits and vegetables and in unpasteurized juices as affected by storage temperature
Journal of Food Protection
Survival of Enterobacter sakazakii on fresh produce as affected by temperature, and effectiveness of sanitizers for its elimination
International Journal of Food Microbiology
Fate of Enterobacter sakazakii attached to or in biofilms on stainless steel upon exposure to various temperatures or relative humidities
Journal of Food Protection
Prevalence and genetic diversity of Enterobacter sakazakii in ingredients and of infant foods
International Journal of Food Microbiology
Microbiological examination of vegetable seed sprouts in Korea
Journal of Food Protection
Evaluation of TaqMan PCR assay for detecting Salmonella in raw meat and shrimp
Journal of Food Protection
Significance of microbial biofilms in the food industry: a review
International Journal of Food Microbiology
Biofilm formation, extra-cellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence
Journal of Food Protection
Growth and survival of Enterobacter sakazakii in human breast milk with and without fortifiers as compared to powdered infant formula
International Journal of Food Microbiology
Survival and growth of Enterobacter sakazakii in infant cereal as affected by composition, reconstitution liquid, and storage temperature
Journal of Food Protection
Survival of Enterobacter sakazakii in infant cereal as affected by composition, water activity, and temperature
Food Microbiology
Mechanisms of biofilm resistance to antimicrobial agents
Trends in Microbiology
Identification of Enterobacteriaceae from washed and unwashed commercial shell eggs
Journal of Food Protection
Microbiological quality of sous and tamarind, traditional drinks consumed in Jordan
Journal of Food Protection
Enterobacter sakazakii: a review
International Journal of Food Microbiology
Incidence, survival, and growth of Enterobacter sakazakii in infant formula
Journal of Food Protection
Azteonam in the treatment of serious infections
American Journal of Medicine
Microbiological analysis of seed sprouts in Norway
International Journal of Food Microbiology
Surface contamination of camel carcasses
Modified most-probably-number technique for the specific determination of Escherichia coli from environmental samples using a fluorogenic method
Journal of Microbiological Methods
Preservation by the lactoperoxidase system (LP-S) of a contaminated infant formula
Letters in Applied Microbiology
Enterobacter sakazakii infection in the newborn
Acta Pediatrics
Use of sanitizers in raw fruit and vegetable processing
Invasive Enterobacter sakazakii disease in infants
Emerging Infectious Diseases
Desiccation and heat tolerance of Enterobacter sakazakii
Journal of Applied Microbiology
Microbiological quality of cowpea paste used to prepare Nigerian akara
Journal of Food Science
Bacteriologic findings in ostrich (Struthio camelus) eggs from farms with reproductive failures
Avian Diseases
Counts, behavior and species of Enterobacteriaceae during manufacture of dry-cured lacon, a Spanish traditional meat product
Alimentaria
Characterization of Enterobacteriaceae isolated from an artisanal Italian ewe's cheese (Pecorino Abruzzese)
Journal of Applied Microbiology
Gram-negative bacteria selective medium to detect post-pasteurization contamination of market milk by using dye reduction test
Korean Journal of Dairy Science
Bacterial populations associated with rice seed in the tropical environment
Phytopathology
Cited by (146)
Sensitive detection of viable Cronobacter sakazakii by bioluminescent reporter phage emitting stable signals with truncated holin
2023, Food Research InternationalModeling the UV-C Inactivation Kinetics and Determination of Fluence Required for Incremental Inactivation of Cronobacter spp.
2022, Journal of Food ProtectionEffect of water activity on the mechanical glass transition and dynamical transition of bacteria
2022, Biophysical Journal