International Journal of Food Microbiology 116 (2007) 1 10

www.elsevier.com/locate/ijfoodmicro

Review
Enterobacter sakazakii in food and beverages
(other than infant formula and milk powder)
Miriam Friedemann
Bundesinstitut fr Risikobewertung (BfR), Federal Institute for Risk Assessment (BfR), Alt-Marienfelde 17-21, D-12277 Berlin, Germany
Received 31 August 2006; received in revised form 28 December 2006; accepted 29 December 2006

Abstract

The ubiqitous microorganism Enterobacter sakazakii is a rare contaminant of infant formula and may cause severe systemic infection in
neonates. So far, other food is not known to cause E. sakazakii-infections. The scarce information about the ecology of E. sakazakii and the
uncertainty concerning the source of infection in children and adults warrant a summary of the current knowledge about the presence of this
opportunistic microorganism in food other than infant formula. This review systematizes publications on the presence of E. sakazakii in food and
beverages until June 2006. Food other than infant formula has been rarely investigated for the presence of E. sakazakii. Nevertheless, this
microorganism could be isolated from a wide spectrum of food and food ingredients. E. sakazakii was isolated from plant food and food
ingredients like cereal, fruit and vegetables, legume products, herbs and spices as well as from animal food sources like milk, meat and fish and
products made from these foods. The spectrum of E. sakazakii-contaminated food covers both raw and processed food. The kind of processing of
E. sakazakii-contaminated food was not restricted to dry products. Fresh, frozen, ready-to-eat, fermented and cooked food products as well as
beverages and water suitable for the preparation of food, were found to be contaminated by E. sakazakii. Although E. sakazakii-contaminated
food do not have general public health significance, measures for prevention should consider the presence of E. sakazakii in food, food
ingredients, their processing and preparation as possible source of contamination, colonization or infection.
2007 Elsevier B.V. All rights reserved.

Keywords: Enterobacter sakazakii; Animal food; Vegetable food; Drinking water

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2. Materials and methods used in this review of literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. E. sakazakii in food and drink . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3.1. Survival of E. sakazakii in food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3.2. Micro- and molecular-biological methods for detection of E. sakazakii in food . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3. Detection of E. sakazakii in food and drink. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3.1. E. sakazakii in food and beverages of vegetable origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3.2. E. sakazakii in food of animal origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3.3. E. sakazakii in drinking water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
3.4. E. sakazakii in food production and the preparation environment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

Tel.: +49 30 8412 2384; fax: +49 30 8412 2951.

E-mail address: m.friedemann@bfr.bund.de.

0168-1605/$ - see front matter 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijfoodmicro.2006.12.018
2 M. Friedemann / International Journal of Food Microbiology 116 (2007) 110
1. Introduction
Since the first description of the ubiquitous and opportunistic
bacteria Enterobacter sakazakii (E. sakazakii) by Farmer et al.
(1980), clinical, ecological, micro- and molecular-biological
background information have been summarized and reported
more precisely (Lai, 2001; Iversen and Forsythe, 2003; Gurtler
et al., 2005; Drudy et al., 2006a). Dried infant formula was
confirmed as the source of severe systemic neonatal infections
with microbiological and molecular-genetic typing methods
(Clark et al., 1990; Van Acker et al., 2001) and epidemiolog-
icalstatistical methods (Simmons et al., 1989; Van Acker et al.,
2001; Himelright et al., 2002). Recent recalls of infant formula
(RASFF, 2004) as well as cases and outbreaks of severe
neonatal infection with E. sakazakii (EWRS, 2004) show that
even in this present period of great attention being paid to E.
sakazakii, contamination of infant formula with related diseases
could not be eliminated completely. Case-reports of E.
sakazakii-infections in adults are rarely published because of
the less severe nature of the illness in comparison with the high
lethality of E. sakazakii-infections occurring in new-born
infants (Lai, 2001). Oral and intestinal colonization with E.
sakazakii (Farmer et al., 1980; Galili et al., 1995; O'Hara and
Miller, 2003) may be associated with ingestion of contaminated
food. As E. sakazakii is an opportunistic pathogen, the patients'
own colonization flora is the most probable source of infection
under circumstances of immunosuppression and severe under-
lying disease in patients after the neonatal period. General
public health significance, however, has not been attributed to
the occurrence of E. sakazakii in food of plant and animal origin
with the exception of infant formula, especially for pre-term,
low-birth-weight and immunocompromised neonates. The
scarce information about the ecology of E. sakazakii, the
uncertainty concerning the source of infection in children and
adults, and numerous single information so far not considered in
recent reviews warrant a summary of the current knowledge
about the presence of this opportunistic microorganism in food
and beverages other than infant formula. Relevant publications
until June 2006 are reviewed in this paper. Information on E.
sakazakii in food and food ingredients (Iversen and Forsythe,
2003, 2004) from previous publications was supplemented and
systematized. As criteria for systematization, the vegetable or
animal origin of different foods or food products was taken into
consideration, as well as special states and characteristics of
food processing. Additionally, drinking water as an ingredient
of food and drink was included in this review. Food other than
infant formula has been rarely investigated for the presence of
E. sakazakii. Nevertheless, this microorganism could be
isolated from a wide spectrum of food and food ingredients.
E. sakazakii was isolated from plant food and food ingredients
like cereal, fruit and vegetables, legume products, herbs and
spices as well as from animal food sources like milk, meat and
fish and products made from these foods. The spectrum of E.
sakazakii-contaminated food covers both raw and processed
food. The kind of processing of E. sakazakii-contaminated food
was not restricted to dry products. Fresh, frozen, ready-to-eat,
fermented and cooked food products as well as beverages and
water suitable for the preparation of food, were found to be
contaminated by E. sakazakii. Food and food ingredients may
be contaminated with E. sakazakii under conditions of hygiene
mismanagement by contaminated insects (Kuzina et al., 2001;
Hamilton et al., 2003) and rats (Gakuya et al., 2001).
E. sakazakii has been detected in food production as well
as in domestic environments (Breeuwer et al., 2003; Kandhai
et al., 2004; Lehner et al., 2004). Although E. sakazakii-con-
taminated food do not have general public health significance,
measures for prevention should consider the presence of
E. sakazakii in food, food ingredients, their processing and
preparation as possible source of contamination, colonization
or infection.
2. Materials and methods used in this review of literature
PubMed, ISI (Web of Science, CAB Abstracts, Food Science
and Technology Abstracts) and Scopus abstract and citation
databases (ISI, 2006; PubMed, 2006; Scopus, 2006) as well as
the alert systems of big publishers (ASM, Blackwell, Elsevier,
Oxford and Springer) were used for this review with the search
strategy of E. sakazakii in food, described anywhere in the text
and without limitation of time span and language (01 June 2006).
Reference lists of related articles were studied to detect articles
not traced by this search strategy. Further information was
received from epidemiological report systems alerting food
related hazards and risks of illness (RASFF, EWRS, FDA).
Other (incomplete) information sources were laboratories of the
Federal Microbiological Food Monitoring Programme in
Germany. One source of the E. sakazakii-strain from a culture
collection database was included in this report because this
aquatic strain has not been described in previous publications.
Results of E. sakazakii-detection in infant formula and milk
powder were not included in this review.
3. E. sakazakii in food and drink
3.1. Survival of E. sakazakii in food
The ubiquitous microorganism E. sakazakii has been isolated
from a wide spectrum of environmental sources (Farmer et al.,
1985; Drudy et al., 2006b) including water (Farmer et al., 1985),
waste- (Dudley et al., 1980) and thermal spring water (De Los
AngelesMosso et al., 1994), soil (Khan et al., 1998), dust from
households and food production-lines (Kandhai et al., 2004).
E. sakazakii has an unusual surviving ability under dry
conditions (Gurtler et al., 2005), but the thermal tolerance of
E. sakazakii-strains may differ (Edelson-Mammel and Bucha-
nan, 2004). Pasteurization is effective in destroying E. sakazakii
(NazarowecWhite and Farber, 1997; Breeuwer et al., 2003;
Iversen et al., 2004a). Acidification reduced the concentration of
E. sakazakii in different types of infant formula and vegetable-
based food products (Joosten and Lardeau, 2004; Richards et al.,
2005; Coulin et al., 2006). In juices of vegetables, the reduction
of pH after 48 h was correlated with a reduction of the numbers
of E. sakazakii, but with increasing numbers of E. sakazakii in
juices of different fruits (Kim and Beuchat, 2005). The abilities
 M. Friedemann / International Journal of Food Microbiology 116 (2007) 110
of E. sakazakii to produce capsule (Iversen and Forsythe, 2003)
and biofilm (Zogaj et al., 2003; Iversen et al., 2004a; Lehner
et al., 2005) reduce the efficacy of UV-light, high osmotic
pressure, heat, dry conditions, starvation, acids, inhibitory
detergents like sanitisers and antibiotics, phagocytes, anti-
bodies, and bacteriophages (Lehner et al., 2005; Iversen et al.,
2004a). E. sakazakii-strains are able to adhere on surfaces of
materials used in the production, preparation and administra-
tion of food like plastics, silicon, latex, polyvinyl chloride and
polycarbonate (Lehner et al., 2005; Iversen et al., 2004a; Zogaj
et al., 2003), less frequent on glass (Lehner et al., 2005) and
stainless steel (Iversen et al., 2004a). E. sakazakii was cul-
tivated from biofilms of drinking water systems (Bartolucci
et al., 1996; Lee and Kim, 2003; Williams and Braun-Howland,
2003).
3.2. Micro- and molecular-biological methods for detection of
E. sakazakii in food
In comparison with conventional, labour-intensive methods
(Muytjens et al., 1988; Simmons et al., 1989; FDA, 2002), the
recently developed fluoro- and chromogenic, differential,
(selective) media decrease the time for isolation of E. sakazakii
(Iversen et al., 2004; Lehner et al., 2006; Leuschner et al.,
2004; Oh and Kang, 2004, 2005; Restaino et al., 2006). The
phenotypic identification of E. sakazakii with commercial
systems may be inadequate for strains isolated from food
specimens (Weiss et al., 2005; Drudy et al., 2006b). Molecular-
genetic methods revealed that several strains identified as E.
sakazakii by commercial biochemical kits belonged to distinct
species (Iversen et al., 2004b; Drudy et al., 2006b). For
confirmation of E. sakazakii, Restaino et al. (2006) recommend
using more than one differentiation system. Computationally
based methods including biochemical and 16S rDNA-data
improve the reliability and the detection time of identification
(Iversen et al., 2006). (Real-time) PCR methods enable
(quantitative), sensitive, specific, and rapid detection of E.
sakazakii in infant formula (Lehner et al., 2004; Malorny and
Wagner, 2005; Seo and Brackett, 2005; Lehner et al., 2006;
Mohan Nair and Venkitanarayanan, 2006). Very low concentra-
tions b 10 cfu/100 g infant formula, which caused neonatal E.
sakazakii-infections (Simmons et al., 1989; RASFF, 2004),
could be detected within 48 h with new species-specific
oligonucleotide-based techniques (Liu et al., 2005, 2006).
Drudy et al. (2006b) compared E. sakazakii-isolates from
environmental and food sources reliably by random amplifica-
tion of polymorphic DNA (RAPD) analysis.
3.3. Detection of E. sakazakii in food and drink
Only few publications describe the qualitative and quanti-
tative data of E. sakazakii in food. There is no essential need for
special microbiological criteria of E. sakazakii in food other
than infant formula, because E. sakazakii is a ubiquitous
opportunistic microorganism. E. sakazakii will be detected only
in studies with the aim of differentiating Enterobacteriaceae or
specially of tracking E. sakazakii. Iversen and Forsythe (2003)
3
referred in their risk-profile to E. sakazakii-contamination in
food. In 2004, they published a survey about the isolation of E.
sakazakii from a variety of powdered infant formulas, milk
powders and related food products (Iversen and Forsythe,
2004). Drudy et al. (2006b) compared biochemical and
molecular-genetic methods in the investigation of a collection
of European and Australasian E. sakazakii-isolates from
environment and food sources.
3.3.1. E. sakazakii in food and beverages of vegetable origin
E. sakazakii-contaminated vegetarian food and drinks
comprise vegetable, fruit, legumes, cereal, herbs, spices and
other related products (Table 1). E. sakazakii was isolated from
the xylem fluid of lemon rootstocks (Gardner et al., 1982), from
the rhizosphere of wheat (Forlani et al., 1995) and as endophytic
bacteria from the leaves of rice plants (Yang et al., 1999).
Kanivets and Pishchur (2001) detected E. sakazakii in the
bacterial colonization flora of disinfected sugar beet seeds. As
E. sakazakii belongs to the cultivable endophytic and epiphytic
flora of rice (Yang et al., 1999) and soy bean plants (Kuklinsky-
Sobral et al., 2005; Kuklinsky-Sobral et al., 2004), it could be
isolated from related food products (Table 1). Some traditional
cereal-, herb- and legume-based food and beverages were found
to be contaminated with E. sakazakii (Bulgarelli et al., 1988;
Tamura et al., 1995; Gassem, 1999; Mensah et al., 2002;
Nassereddin and Yamani, 2005; Coulin et al., 2006). E.
sakazakii may be part of starter cultures for fermentation of
traditional vegetarian food products (Coulin et al., 2006).
Geiges et al. (1990) and Osterblad et al. (1999) detected E.
sakazakii in mixed salad vegetables and imported, fresh and
deep-frozen vegetables at retail level.
3.3.2. E. sakazakii in food of animal origin
E. sakazakii-contaminated food of animal origin comprise a
variety of meat and meat products from camel, pig, beef and
poultry, and, additionally, eggs, raw milk and different dairy
products and, less frequently, fish (Table 2). E. sakazakii has
been isolated from animals (Farmer et al., 1985; Goullet and
Picard, 1986), especially from birds, lizards, rats and piglets
(Goullet and Picard, 1986; Shyu et al., 1996; Gakuya et al.,
2001; Montgomery et al., 2002). In vertebrates, E. sakazakii is a
member of the normal (animal and human) oral and intestinal
flora (Gakuya et al., 2001; Montgomery et al., 2002; Zogaj
et al., 2003). Salmon et al. (1998) found E. sakazakii among the
isolates from secretions of an infected mammary gland of dairy
heifers. Liu et al. (2005) detected E. sakazakii in feed for pets.
E. sakazakii was isolated from a variety of raw and ready-to-eat
meat (products) (Table 2). Watanabe and Esaki (1994) isolated
E. sakazakii during a complicated curing process of meat
products. E. sakazakii is a histamine forming microorganism in
the ripening process of cheese (Roig-Sagus et al., 2002; Mora-
les et al., 2004). E. sakazakii has been isolated from a cheese
whey substrate (De Haast and Britz, 1986). Lipolytic activity
of an E. sakazakii-strain was demonstrated by Chaves-Lopez
et al. (2006). E. sakazakii has been detected in fresh and
prepared fish (Table 2). Miranda et al. (2003) isolated a
tetracycline-resistant E. sakazakii-strain from a Chilean
4 M. Friedemann / International Journal of Food Microbiology 116 (2007) 110

Table 1 Table 1 (continued )

E. sakazakii in food of vegetable origin
Food (product) Property Origin Reference
Food (product) Property Origin Reference
4. Fruit and vegetables
1. Cereal (products) Mixed salad Sliced, Italy Galli et al.
Green malt (barley) Interim Germany Scheepe- vegetables ready-to-eat (1990)
beer-product Leberkhne and Mixed salad Sliced, Germany Geiges et al.
Wagner (1986) vegetables ready-to-eat (1990)
Khamir (sorghum) Fermented bread Saudi Gassem (Mixed) salad Sliced, Italy Ottaviani et al.
Arabia (1999) vegetables ready-to-eat (1992)
Rice seed Dried product Philippines Cottyn et al. Lettuce Fresh produce Ireland Francis and
(2001) O'Beirne
Sobia (wheat, Fermented Saudi Gassem (1998)
malt flours) beverage Arabia (2002) Vegetables Raw and Finland, The sterblad et al.
Grains, ground Dried products Great Iversen et al. deep-frozen Netherlands, (1999)
maize, ground rice Britain (2004a,b) Italy,
Rice, rice starch, Dried products USA Gurtler et al. Poland,
rice flour (2005) and Hungary,
Richards et al. Portugal
(2005) Mixed salad Sliced, Germany Lack et al.
Flour or meal of corn, Dried products USA Restaino et al. vegetables ready-to-eat (1999)
soy, wheat, rice (2006) Lettuce Fresh produce Spain Soriano et al.
Adult cereal, Dried products USA Restaino et al. (2001)
infant cereal (2006) Courgette Fresh produce, Spain Gray et al.
Grain Dried product South Jung and skin (2001)
Korea Park (2006) Vegetables Fresh produce France Leclercq
et al. (2002)
2. Legume (products) Salad Ready-to-eat Ghana Mensah et al.
Cowpea paste Street food Nigeria Bulgarelli et al. street food (2002)
(1988) Tomato stew Ready-to-eat Ghana Mensah
Soy bean sprouts Fresh produce Germany Geiges et al. (1990) street food et al. (2002)
Tofu (soy) Coagulated USA Fouad and Fufu (pounded Ready-to-eat Ghana Mensah et al.
soy milk Hegeman (1993) cassava with street food (2002)
Tempe (soy) Fermented product Indonesia Denter and plantain or yam)
Bisping (1994) Raw winery Winery South Africa Keyser et al.
Tofu (soy) Coagulated South No et al. (2002) effluent wastewater (2003)
soy milk Korea Fruit-based Dried product Great Iversen et al.
Mung bean sprouts, Fresh produce Norway Robertson et al. infant food Britain (2004)
alfalfa sprouts (2002) Nuts, fruits, almonds, Dried products Great Iversen et al.
Mung bean sprouts Fresh produce Germany Boehme et al. pistachio, coconut Britain (2004)
(2004) a powder, sunflower
Alfalfa sprouts Fresh produce Mexico Cruz et al. seeds, sesame seeds,
(2004) sponge mix,
Pea soup powder Dried product Czech Leuschner et al. vegetable suet
Republic (2004) Fruit powder Dried product Switzerland Lehner et al.
Soy protein, Dried products Great Iversen et al. (2004, 2005)a
beanfeast, lentils Britain (2004a,b) Potato Raw Poland Szafranek et al.
Sous (liquorice) Beverage based Jordan Nassreddin and (2005)a
on dried product, Yamani (2005) Mixed salad Sliced, Germany Weiss et al.
street food vegetables ready-to-eat (2005)
Attik (cassava Fermented, Ivory Coast Coulin et al.
3. Tea, herbs and spices product) dried granules (2006)
Sour tea Fermented China Tamura et al. based
beverage (1995) Vegetables Dried products USA Restaino et al.
Iced tea Dried product USA Zhao et al. (2006)
(1997) Vegetable, laver Unprocessed, South Korea Jung and
Herbal tea (fennel, Dried product Germany Federal (red algae) ready-to-eat Park (2006)
aniseed, caraway) Microbiol- a
Personal communication by the author.
ogical Food b
Institutional communication from the Federal Office of Consumer Protection
Monitoring
and Food Safety (BVL), Berlin (Germany).
Programme
(2003a) b
Herbs and spices Dried products Great Iversen et al.
Britain (2004) freshwater salmon farm with no history of recent antibiotic
Herb containing Dried product Great Iversen et al. use. E. sakazakii has been isolated from smoked sardines after
infant food Britain (2004) 12 weeks of storage after irradiation (Nketsia-Tabiri et al.,
Spices Dried products USA Restaino et al. 2003). E. sakazakii-contaminated food of mixed vegetable and
(2006)
animal or unknown origin are listed in Table 3.
 M. Friedemann / International Journal of Food Microbiology 116 (2007) 110 5

Table 2 Table 2 (continued )

E. sakazakii in food of animal origin
Food Property Origin Reference
Food Property Origin Reference (product)
(product)
4. Fish (products)
1. Meat (products) Fish Fried, ready-to-eat Ghana Mensah et al. (2002)
Sausages France Goullet and Picard (1986) street food
Sausages Cooked, cold cuts Germany Schalch et al. (1994) Sardines Smoked, ready-to-eat Ghana Nketsia-Tabiri
Meat Curing process Japan Watanabe and Esaki et al. (2003)
products (1994) Fish Aquaculture USA Miranda et al. (2003)
Meat Minced Canada Nazarowec-White and and Call et al. (2003)a
Farber (1997) Fish Dried product China Liu et al. (2005)
Meat Raw Japan Kimura et al. (1999) (powder)
products Fish bolus China Liu et al. (2005)
Lacon (pork) Dryrawcured, Spain Castano et al. (2001) a
Personal communication by the author.
surface
Camel Carcasses, directly after Saudi Al-Dugham and
meat preparation Arabia Yassien (2001) 3.3.3. E. sakazakii in drinking water
and stamping Drinking water is used for cleaning and for rinsing off of
Poultry Skin, directly after Sweden Dahlenborg et al.
food and equipment for food preparation, for dilution and
slaughter (2001) a and Lfstrm
et al. (2004)a reconstitution of food or directly as beverage. Oger et al. (1981)
Beef, sausage Minced France Leclercq et al. (2002) and Schindler and Metz (1991) found E. sakazakii in total
meat frequencies of 1.8% (10/564 strains) and 0.4% (1/256 strains)
Poultry Carcasses, directly Argentina Jimenez et al. (2003) investigating central and local drinking water supplies.
after evisceration
Bartolucci et al. (1996), Lee and Kim (2003) and Williams
Gelatine Semifinal extracts Belgium De Clerck et al. (2004)
and Braun-Howland (2003) identified E. sakazakii as bacteria
2. Milk (products) indigenous to the water distribution system during their
Cheese whey South De Haast and Britz investigations for biofilm formation. Even bottled beverages
digester Africa (1986) should not be considered as free of microorganisms, as shown
Milk Republic Choi et al. (1999)
by the results of Schindler (1994) for E. sakazakii-contaminated
of Korea
Bulk tank Raw milk USA Jayarao and Wang
milk (1999) Table 3
Cheese France Leclercq et al. (2002) E. sakazakii in food of mixed vegetable and animal or unknown origin
Cheese Spain Roig-Sagus et al.
(2002) Food (product) Property Origin Reference
Fresh cheese Raw milk-based Spain Morales et al. (2003, Food The Koning et al. (1982)
(ewe) 2004)a Netherlands
Cheese Great Iversen et al. (2004a,b) Powdered food products Dried USA Robison (1984)
products Britain product
Milk (cow) Raw milk France Lafarge et al. (2004) Macaroni Ready- Ghana Mensah et al. (2002)
Milk Switzerland Lehner et al. (2004, to-eat
2005)a street
Milk Raw milk France Ogier et al. (2004) food
Cheese Raw milk-based, France Ogier et al. (2004) Dumpling Frozen Czech Leuschner et al.
(Morbier) semihard Republic (2004)
Cheese China Liu et al. (2005) Rice-based infant food Dried Great Iversen et al.
Cheese Turkey Ozturk and Ercisli product Britain (2004)
(2006)a Baby food Dried Switzerland Lehner et al.
Sodium Dried products USA Restaino et al. (2006) product (2004, 2005) a
caseinate, Milk-based pure with cherry Dried Germany Federal
curd and banana, biscuit-based products Microbiological Food
Cheese Italy Chaves-Lopez et al. pure for infants and Monitoring
(Pecorino (2006) children, semolina milk- Programme (2003b) b
Abruzzese, based pure, infant
ewe) semolina
Protein powder Dried China Liu et al. (2005)
3. Egg (products) product
Eggs Egg albumen and yolk Italy Cabassi et al. (2004) Biscuits Dried China Liu et al. (2005)
(ostrich) product
Eggs Shells, unwashed USA Musgrove et al. (2004) Sweets China Liu et al. (2005)
Eggs USA Gurtler et al. (2005) Food Europe, Drudy et al. (2006b)
Ireland
4. Fish (products) a
Personal communication by the author.
Shellfish Fresh, raw Spain Balebona et al. (1990) b
Results were kindly provided by Dr. Kirschfeld, Institute for Food, Drugs
Shrimps Deep frozen Switzerland Teuber (2001)
and Animal Epizootics (ILAT), Berlin (Germany).
(continued on next page)
6 M. Friedemann / International Journal of Food Microbiology 116 (2007) 110

Table 4 were contaminated with E. sakazakii (Schindler and Metz,

E. sakazakii in water 1990).
Food (product) Origin Reference
Water Great Britain NCTC 9529 (1954) 4. Summary
Drinking water France Leclerc et al. (1981) and Oger
et al. (1981) This review emphasizes the wide spectrum of different kinds
Water USA Farmer et al. (1985)
of food found to be contaminated with E. sakazakii. This
Drinking water USA Camper et al. (1986)
Water Belgium Goullet and Picard (1986) microorganism has been detected in raw or fresh products of
Water France Goullet and Picard (1986) animal and vegetable origin as well as in processed and
Drinking water Germany Schindler and Metz (1991) prepared food such as dried, smoked, frozen, fermented, cooked
Bottled mineral Germany Schindler (1994) or fried products, ready-to-eat and street food. In fresh vegetable
water
food, primary E. sakazakii-contamination may occur intrinsi-
Drinking water Italy Bartolucci et al. (1996)
(biofilm) cally, e.g. endophytically or through contacts with water, soil
Water Great Britain Oliver (1997) and living vectors like insects or small vertebrates. Raw food of
Water France Leclerc et al. (2001) animal origin may be contaminated additionally via the (fecal)
Drinking water Republic of Lee and Kim (2003) microflora of the food-source animal itself. Food may be
(biofilm) Korea
contaminated during the whole food production process. All
Drinking water Great Britain Williams and Braun-Howland (2003)
(biofilm) untreated raw materials for food and drink, as well as other
Water USA Cruz et al. (2004) environmental sources (water, soil, dust), are potential con-
taminants in the food production process. In processed and
prepared food contamination may occur through primary
bottled mineral water. Sources of E. sakazakii-contaminated contamination of the raw materials or through secondary
(drinking) water are shown in Table 4. contamination during food processing and preparation. Regard-
ing the ubiquitousness of E. sakazakii in inanimate (water, soil,
3.4. E. sakazakii in food production and the preparation plants) and animate environment (animals, man) it is not
environment surprising, that E. sakazakii was detected in a wide spectrum of
food and food products of animal and vegetable origin.
In addition to primary contaminated food ingredients, E. Altogether, E. sakazakii is not very frequent in food. Hygiene
sakazakii-contaminated water from environmental sources mismanagement due to incorrect temperature and time factors
(Alonso et al., 1999; Angles d'Auriac et al., 2000; Emiliani as well as due to the contact transmission of microorganisms via
et al., 2001), drinking water (Schindler and Metz, 1991; Lee hands, insects, small vertebrates and equipment should be
and Kim, 2003), soil (Neelam et al., 1987; Khan et al., 1998; avoided during production, preparation and storage of food and
Espeland and Wetzel, 2001), dust (Kandhai et al., 2004) and drink. E. sakazakii may be associated with food spoilage. But
air-particles (Masaki et al., 2001) should be regarded as the detection of the ubiquitous E. sakazakii in food is not
potential sources for contamination of animal- and plant-based always an indicator for hygiene mismanagement. For persons
food throughout the entire food production chain. In the animal with congenital or acquired immunological deficiency, espe-
production environment, E. sakazakii was isolated from stable cially neonates, elderly and persons with severe underlying
flies (Stomoxys calcitrans) in cattle (Mramba et al., 2006) and diseases, the widespread occurrence of E. sakazakii and other
dairy farms (Buma et al., 1999) and from adults of lesser Enterobacteriaceae in the environment and in food may
mealworm (Alphitobius diaperinus) in a poultry brooder house represent a hazard to health. During the preparation of food
(Chernaki-Leffer et al., 2002). Colonized insects (Kuzina et and beverages for these persons, the rules for special hygiene
al., 2001; Hamilton et al., 2003) and rats (Gakuya et al., 2001) measures during preparation, storage and serving should be
may contribute to contamination of food with E. sakazakii observed. According to the recommendations of the FAO/WHO
under conditions of hygiene mismanagement. Besides the expert meetings in 2004 and 2006 (FAO/WHO, 2004, 2006)
isolation of E. sakazakii from the production environment in this review may contribute to a better understanding of the
the dairy industry, especially in milk powder factories ecology of E. sakazakii and will give some information for the
(Breeuwer et al., 2003; Kandhai et al., 2004; Lehner et al., interpretation of epidemiological data.
2004), Kandhai et al. (2004) detected E. sakazakii in factories
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