exherichia parte 2
TRANSCRIPT
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 1/12
International Journal of Food Microbiology 45 (1998) 173–184
Influence of temperature and pH on survival of Escherichia coli
O157:H7 in dry foods and growth in reconstituted infant rice cereal
*Yun Deng, Jee-Hoon Ryu, Larry R. Beuchat
Center for Food Safety and Quality Enhancement , Department of Food Science and Technology, University of Georgia,
1109 Experiment Street , Griffin, GA 30223 -1797, USA
Received 9 June 1998; received in revised form 4 September 1998; accepted 21 September 1998
Abstract
Factors affecting the ability of Escherichia coli O157:H7 to survive in foods with a less than required for growth havew
not been fully defined. This study was undertaken to determine the ability of E . coli O157:H7 to survive in a commercial dry
infant rice cereal as affected by a (0.3560.04, 0.5260.03 and 0.7360.03), pH (4.0 and 6.8), and temperature (5, 25, 35w
and 458C), and in nine other reduced-a foods. Death of E . coli O157:H7 in cereal was enhanced with increased temperaturew
and decreased pH during a 16- to 24-week storage period. Survival was enhanced at pH 6.8 compared to pH 4.0 in cereal at
a 0.3460.04 during initial storage at 5 and 258C. The effect of temperature (8, 15, 21 and 308C) on survival and growth of w
acid-adapted cells of E . coli O157:H7 inoculated into cereal reconstituted with milk or apple juice at two inoculum levels(8.2–12.3 cfu/ml and 82–123 cfu/ml of slurry) was also studied. Growth occurred in cereal reconstituted with milk at all
test temperatures and in cereal reconstituted with apple juice at 15, 21 and 308C. Populations increased by . 1 log cfu/ml10
within 3–6 h at 21 and 308C. Acid-adapted and unadapted cells had similar growth patterns. The effects of temperature and
acid adaptation on survival of E . coli O157:H7 in nine commercial foods and food ingredients with pH 4.07–6.49 and aw
0.17–0.82 were determined. The pathogen survived in these foods for various lengths of time, depending the storage
temperature, with an order of survival of 58C. 218C. 378C. Survival appeared to be enhanced in foods with highest pH,
and acid-adapted cells retained higher viability than unadapted cells in only two of the nine test foods. Of particular
importance is the ability of E . coli O157:H7 to survive well in dry foods with a wide range in a and pH, particularly atw
refrigeration temperature. © 1998 Elsevier Science B.V. All rights reserved.
Keywords: Escherichia coli O157:H7; Dry foods; Water activity; Infant food
1. Introduction was first recognized as an important pathogen in the
early 1980s. The pathogen is known to cause
Escherichia coli O157:H7 has been associated hemolytic uremic syndrome, hemorrhagic colitis
with several outbreaks of foodborne disease since it cystitis, balanitis and thrombotic thrombocytopenic
purpura, especially in young children (Doyle et al.,* 1997). Although the major vehicle for E . coliCorresponding author. Tel.: 1 1-770-412-4740; Fax: 1 1-
770-229-3216; E-mail: [email protected] O157:H7 transmission is undercooked ground beef,
0168-1605/ 98/ $ – see front matter © 1998 Elsevier Science B.V. All rights reserved.
P I I : S 0 1 6 8 - 1 60 5 ( 9 8 ) 0 0 1 6 1 - 5
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 2/12
174 Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184
other vehicles are chicken and lamb (Abdul-Raouf et ments by exposure to conditions similar to those in
al., 1996), raw milk (Ansay and Kaspar, 1997), and foods, then monitoring their survival and growth
pasteurized milk (Upton and Coia, 1994). Outbreaks characteristics, would provide valuable information
of infections have been associated with foods such as useful in predicting their behavior in food systems.
yogurt (Morgan et al., 1993), apple cider (Besser et Little is known about the survival of E . colial., 1993), deer jerky (Keene et al., 1997), and O157:H7 in dry foods or growth in reconstituted
salami (Centers of Disease Control and Prevention, infant foods. The study reported here was undertaken
1995). to determine the combined effects of a , pH andw
A study to determine carriage of E . coli O157:H7 temperature on the survival of E . coli O157:H7 in a
by persons living on dairy farms revealed elevated commercial dry infant rice cereal, and to determine
antibody titers against surface antigen of E . coli the effects of temperature and acid adaptation on
O157:H7 (Doyle et al., 1997). Outbreaks of E . coli survival and growth of the pathogen in cereal
O157:H7 infection have occurred in day-care centers reconstituted with milk or apple juice. In addition,
and nursing homes via person-to-person transmis- the effects of acid adaptation of E . coli O157:H7
sion, direct fecal–oral transmission, and cross-con- cells on their survival in commercial foods with and
tamination of foods, (Griffin and Tauxe, 1991). A food ingredients with reduced a
and pH werew
child infected with E . coli O157:H7 in a day care determined.
center-associated outbreak continued to excrete the
pathogen for 62 days (Doyle et al., 1997). The
pathogen has been detected in feces from a healthy2. Materials and methods
person (Rambach et al., 1997), which agrees with the
observation that infected animals may be asympto-2.1. Strains studied
matic (Cray and Moon, 1995). If these carriers work
in a day-care center, it is possible that cross-contami-Five strains of E . coli O157:H7 were used. Strain
nation of foods might occur, putting infants andE09 was isolated from an outbreak of infection
young children in danger.associated with ground beef, strains F500 and 932
Extensive studies have been done to determine
were isolated from human feces, strain 933 wasgrowth and survival characteristics of Salmonella isolated from beef, and strain 944 was isolated from(Foster and Hall, 1990) and enterohemorrhagic E .
salami.coli O157:H7 (Zhao et al., 1993; Leyer et al., 1995)
in acidic foods. Salmonella typhimurium has been
reported to be able to adapt to acid environments, 2.2. Preparation of media
thus greatly enhancing survival in low pH and other
harsh environments (Leyer and Johnson, 1992, 1997; Tryptic soy agar (TSA, pH 7.260.05, Difco,
Leyer et al., 1995). However, in these studies, acid Detroit, MI, USA), tryptic soy broth (TSB, pH
adaptation was achieved by adding HCl rather than 7.360.05, Difco), and sorbitol MacConkey agar
organic acids to cell suspensions to reduce the pH to (SMA, pH 7.0, Unipath-Oxoid, Hampshire, UK)
5.0–5.8. In natural food environments, bacteria are were prepared as specified by the manufacturers.
more often exposed to organic acids either produced Modified sorbitol MacConkey agar (MSMA, pH 7.0)by fermentation or added for the purpose of enhanc- was prepared by adding 4-methyl umbelliferyl-b-D-
ing sensory characteristics or preservation. Changes glucoronide (MUG, 0.2 g/ l) to SMA before heat
in pH are usually gradual. The remarkable ability of sterilization. Molten (47–508C) sterilized MSMA E . coli O157:H7 to tolerate acid environments was poured into petri dishes and held no more than
(Conner and Kotrola, 1995; Buchanan and Edelson, four days at 58C until used. Modified TSB (mTSB)
1996; Rowbury, 1997) has been demonstrated in a was prepared by combining (per liter of deionized
range of fermented and acidified foods (Hathcox et water) 30 g of TSB powder, 1.5 g of bile salts No. 3
al., 1995; Leyer et al., 1995; Miller and Kaspar, (Difco), 1.5 g of K HPO , 10 g of casamino acids2 4
1994; Zhao and Doyle, 1994; Zhao et al., 1993). (Difco), and 10 mg of acriflavin–HCl (Sigma, St.
Adapting E . coli O157:H7 cells to acidic environ- Louis, MO, USA). A stock solution (10 mg/ ml) of
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 3/12
Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184 175
acriflavin was added (10 ml/ l) before sterilization at The pH of an aqueous slurry of the acidified cereal
1218C for 15 min. was 4.0, whereas the pH of the control cereal was
TSB supplemented with 1% glucose (TSBG) was 6.8. Dry cereal at each pH was deposited in
prepared by adding 10 g of glucose (Sigma) to 1 l of aluminum pans, placed over saturated solutions of
TSB. Both TSB and TSBG were dispensed into potassium acetate, magnesium nitrate, or potassiumeither 1503 16 mm screw-capped tubes (10 ml) or chloride, and held at 218C until desired a values
w
250-ml Erlenneyer flasks (100 ml) and autoclaved at were reached. The a of cereal was measured usingw
1218C for 15 min. Broths were stored at 58C for up an Aqualab CX2 instrument (Decagon Devices,
to four days until used. Pullman, WA, USA). Cereal (5 g) at each a / pHw
combination was placed in polypropylene vials and2.3. Preparation of inocula 50 ml of E . coli O157:H7 inoculum was added. An
additional 5 g of cereal was then added to each vial
Stock cultures of E . coli O157:H7 maintained on before caps were secured.
TSA (TSA containing 1.5% agar) slants at 58C were
transferred to 10 ml of TSB and incubated at 378C. 2.4.1. Enumeration of E . coli in dry cereal
Three consecutive 24-h loop transfers were made Populations of E . coli
O157:H7 in inoculatedbefore inoculating into 100 ml of TSB or TSBG. cereal were determined after incubation times rang-
Cultures incubated at 378C for 24 h were used to ing from 1 to 24 weeks. The content (10 g) of each
prepare inocula for use in the rice cereal study, vial was combined with 90 ml of sterile 0.1%
whereas 18-h cultures were used in studies involving peptone, pummeled in a stomacher for 15 s, and
survival and growth in infant rice cereal reconstituted surface plated in quadruplicate (0.25-ml samples) or
with milk or apple juice, and survival in low- and serially diluted in sterile 0.1% peptone and plated in
intermediate-a foods. duplicate (0.1-ml samples) on MSMA. Presumptivew
E . coli O157:H7 colonies were counted after in-2.3.1. Enumeration of E . coli O157: H 7 in inocula cubating plates at 378C for 48 h. Two or three
Cultures (24 h) of each strain of E . coli O157:H7 colonies from each sample were confirmed by ag-
were centrifuged for 15 min at 2100 g at 248C. The glutination using a latex agglutination test kit (Un-
supernatant was decanted and cell pellets were ipath-Oxoid) and by biochemical tests using the´resuspended in 25 ml of sterile 0.05 M potassium API-20E miniatured diagnostic kit (bio Merieux
phosphate buffer (pH 7.4). Populations of each strain Vitek, Hazelwood, MO, USA).
were determined by serially (1:10) diluting cell In cereal samples predicted to contain low popula-
suspensions in sterile 0.1% peptone water and sur- tions of E . coli O157:H7, the content of each vial
face plating (0.1 ml) duplicate samples on TSA and was combined with 90 ml of mTSB broth as well as
MSMA to confirm purity. Colonies were counted plated on MSMA. This mixture was incubated for
after incubation at 378C for 24 h. Cell suspensions 18–24 h at 378C, then streaked on MSMA, and again
were combined at ratios resulting in an inoculum incubated for 24 h at 378C. Plates were examined for
containing approximately equal populations of cells the presence of presumptive E . coli O157:H7
of each strain. colonies, which were subsequently subjected to latex
agglutination and biochemical tests for confirmation.2.4. Survival of E . coli O157: H 7 in dry rice
cereal 2.5. Growth and survival in reconstituted cereal
The combined effects of a , pH and temperature The ability of E . coli O157:H7 to grow in aw
on survival of E . coli O157:H7 in a commercial dry commercial infant rice food reconstituted with milk
infant rice cereal were determined. Dry cereal (a or apple juice as affected by temperature wasw
0.35) was placed in aluminum pans and further dried determined. Unadapted (control) and acid-adapted
in a forced-air oven at 508C for 18–20 h. Part of the cells were used as inocula.
cereal (3600 g) was combined with 75.6 g of Pasteurized milk (2% fat) purchased at a local
powdered citric acid, followed by thorough mixing. supermarket was adjusted to 218C within 1 h of
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 4/12
176 Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184
removal from refrigeration. Pasteurized apple juice mixture of either acid-adapted or control cell in-
was stored at 218C until used. Milk or apple juice oculum of E . coli O157:H7 was deposited on the
was added to dry rice cereal at a ratio of 6:1 (ml:g), surface of the sample. An additional 5 g of food was
based upon the cereal manufacturer’s recommenda- then added to each tube before caps were secured.
tion for reconstitution, and mixed with a sterile Sealed tubes were stored at 5, 21 and 378C.spatula. Cereal (200 g) reconstituted with 1200 ml of Populations of E . coli O157:H7 in the nine test
milk or apple juice at 218C was inoculated with 1 ml foods were monitored over a 12-week period. At
or 10 ml of a diluted mixed-strain suspension of E . each sampling time, the entire 10-g sample wascoli O157:H7 to give two population levels (0.91 placed into a stomacher bag with 90 ml of mTSB,
and 1.91 log cfu/ ml of slurry for acid-adapted pummeled for 1 min, and surface plated in quad-10
cells; 1.09 and 2.09 log cfu / ml for control cells) ruplicate (0.25 ml) or serially diluted in sterile 0.1%10
and stirred for 1 min. Samples (40 ml) of reconsti- peptone and plated in duplicate (0.1 ml) on MSMA.
tuted cereal were then deposited into sterile jars, Colonies were counted after incubating plates for 48
sealed, and immediately placed in incubators at 8, h at 378C. The remaining portion of the food slurry
15, 21 or 308C. was incubated at 378C for 18–24 h, then streaked
Reconstituted cereal was analyzed for populations into MSMA plates and incubated 24 h at 378C beforeof E . coli O157:H7 after 0, 3, 6, 9, 12, 24, 48 and 72 examining for the presence of E . coli O157:H7
h of storage. After shaking containers vigorously by colonies.
hand for 15 s, samples (1.0 ml) were surface plated Populations of aerobic mesophilic microorganisms
in quadruplicate (0.25 ml) or serially diluted in in nine test foods (Table 1) subsequently inoculated
sterile 0.1% peptone and surface plated in duplicate with E . coli O157:H7 were also determined. Samples
(0.1 ml) on MSMA. Colonies were counted after 48 (10 g) were combined with 90 ml of sterile 0.1%
h of incubation at 378C. The remaining portions of peptone water, pummeled for 1 min, and surface
samples were combined with 90 ml of sterile mTSB, plated (0.1 ml in duplicate) on plate count agar
incubated at 378C for 24 h, and streaked on mSMA (Difco). Plates were incubated at 308C f o r 4 8 h
to determine the presence of E . coli O157:H7. before colonies were counted.
2.6. Survival in foods with low and intermediate 2.7. Statistical analysisaw
Three replicates of each experiment were done.
Inocula were prepared as described for reconsti- All data were analyzed using the general linear
tuted cereal studies. Each test food (5 g) (Table 1) model of the Statistical Analysis System (SAS)
was placed in a sterile tube and 50 ml of a five-strain procedure. Duncan’s multiple range test was used to
Table 1
The pH, population of aerobic mesophilic microorganisms, and a of foods and food ingredients (listed in ascending order of initial a )w w
inoculated with E . coli O157:H7 and stored at 58C for up to 12 weeks
Aerobic
Food / mesophiles Storage time (weeks)
ingredient pH (cfu / 10 g) 0 1 2 3 5 8 12
Almond paste 5.93 , 1 0.82 0.82 0.81 0.82 0.82 0.81 0.83
Apple powder (unsulfured) 4.07 , 1 0.16 0.20 0.19 0.23 0.18 0.20 0.19
Apple powder (sulfured) 4.63 , 1 0.17 0.20 0.18 0.23 0.18 0.18 0.18
Buttermilk powder 6.49 22 0.21 0.26 0.27 0.30 0.35 0.37 0.38
Cheddar cheese seasoning 1 5.27 52 0.21 0.22 0.23 0.22 0.21 0.23 0.24
Cheddar cheese seasoning 2 5.62 44 0.32 0.31 0.32 0.36 0.31 0.34 0.33
Fig paste 4.25 370 0.70 0.68 0.69 0.69 0.70 0.70 0.70
Powdered chicken 6.43 , 1 0.37 0.35 0.35 0.36 0.34 0.39 0.38
Sour cream powder 5.26 10 0.29 0.31 0.31 0.31 0.30 0.31 0.31
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 5/12
Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184 177
determine if significant differences ( p# 0.05) ex- acidity on Salmonella newport and Staphylococcus
isted between populations detected in dry cereal at aureus in foods with reduced a was also noted byw
different a . The least significant difference test was Christian and Stewart (1973).w
used to determine if significant differences ( p# Death of E . coli O157:H7 was enhanced by an
0.05) existed between populations in dry cereal at increase in temperature, regardless of other testdifferent pH and between populations of acid- parameters. After one, five and 11 weeks of incuba-
adapted and non-adapted (control) cells detected in tion at 45, 35 and 258C, respectively, E . coli
dry foods. O157:H7 populations were below levels detectable
(, 10 cfu/g) by direct plating. The pathogen was
not detected in cereal stored at 458C for three weeks,
3. Results and discussion regardless of a or pH. Others have observed that E .w
coli O157:H7, at a given a , survives better inw
3.1. Survival in dry cereal salami (Clavero and Beuchat, 1996; Faith et al.,
1998a), pepperoni (Faith et al., 1998b), and bovine
The a of the infant rice cereal purchased at a feces (Wang et al., 1997) stored at refrigerationw
local supermarket ranged from 0.35 to 0.40. After temperatures compared to ambient temperatures.drying in a forced air oven, the cereal (a 0.18) was Calicioglu et al. (1997) observed that E . coliw
adjusted to desired a . The three a ranges O157:H7 inoculated into sausage incubated at 4 orw w
(0.3560.04, 0.5260.03 and 0.7360.03 ) of cereals 258C could be detected by enrichment after one
subsequently inoculated with E . coli O157:H7 were week. Some cells may have been injured by high
thus achieved via a water absorption process. E . coli temperature, low a and / or low pH, and entered aw
O157:H7 was not detected in uninoculated dry or viable but non-culturable state. These observations
equilibrated cereal. The addition of citric acid to underscore the importance of enrichment to detect
cereal (pH 6.7560.05) reduced the pH to 4.060.05. injured and low numbers of E . coli O157:H7 cells in
Results of studies to determine survival of E . coli foods that impose stress environments.
O157:H7 in cereal at six combinations of a and pHw
stored for up to 24 weeks at four storage tempera- 3.2. Growth and survival in reconstituted cereal
tures are shown in Table 2. The initial populations of E . coli O157:H7 were 6.31 and 6.10 log cfu / g in Populations of aerobic microorganisms in dry rice
10
inoculated cereal at pH 6.8 and 4.0, respectively. cereal, milk, and apple juice are listed in Table 3.
These populations were selected to simulate a situa- The population of aerobic mesophilic microorga-
tion where cross-contamination of cereal might occur nisms in pasteurized milk is similar to that reported
in the home or day-care center due to improper by Wang et al. (1997). E . coli O157:H7 was not
hygienic practices. The number of E . coli O157:H7 detected in dry cereal, pasteurized milk, or apple
in cereal subjected to all a , pH, and temperature juice.w
conditions decreased at least 1 log within one week Survival and growth characteristics of E . coli
of storage. At a given sampling time and storage O157:H7 in rice cereal reconstituted with milk or
temperature, survival of significantly higher popula- apple juice and held at 8, 15, 21 or 308C were
tions of E . coli O157:H7 was observed in cereal at determined. There were differences in pH values of higher a . This phenomenon was most evident the 18-h cultures of acid-adapted (TSBG, 4.860.2)
w
during the initial stage of storage at lower tempera- and unadapted (TSB, 6.260.1) cells used as inocula.
tures. This is in contrast to observations reported by Shown in Table 4 are populations of E . coli
Christian and Stewart (1973) and Juven et al. (1984) O157:H7 in reconstituted cereal inoculated with
that salmonellae survived better in dry foods as the acid-adapted (TSBG) [8.2 (0.91 log ) cfu/ ml] or10
a was decreased. control (TSB) [12.3 (1.09 log ) cfu /ml] cells. Tablew 10
Survival of E . coli O157:H7 was enhanced at pH 5 shows in reconstituted cereal inoculated with
6.8 compared to pH 4.0 in cereal at a 0.3560.04 higher populations of acid-adapted [82 (1.92 log )w 10
during storage for one week at 5 and 258C, and in cfu/ ml] and unadapted [123 (2.09 log ) cfu/ ml].10
cereal at all test a held at 358C. The lethal effect of Initial populations were determined by plating cellsw
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 6/12
Table 2
Population of E . coli O157:H7 in rice cereal as affected by a , pH, temperature and storage timew
aStorage Population (log cfu/g)10
temperature 1 week 2 weeks 3 weeks 4 weeks 5 weeks 7 weeks 8 weeks 9 weeks
b b(8C) a pH Log E Log E Log E Log E Log E Log E Log E Log Ew 10 10 10 10 10 10 10 10
5 0.356
0.04 6.8 b 3.93 a a 3.96 a b 3.55 c 2.88 a 4.0 c 3.46 b b 3.31 b b 3.40 c 3.27 c 3.06 a
0.5260.03 6.8 b 4.47 a a 4.55 b b 3.90 b 3.37 a
4.0 b 4.20 a a 4.81 a b 3.81 b 3.60 b 3.60 a
0.7360.03 6.8 a 5.07 a a 4.65 a a 4.70 a 4.52 a
4.0 a 4.77 a a 4.49 a a 4.39 a 4.68 a 4.41 a
25 0.3560.04 6.8 a 4.24 a b 3.11 a b 2.77 a b 2.44 a b 1.12 a
4.0 c 2.78 b b 2.20 b b 2.79 a b 2.03 a b 1.12 a
0.5260.03 6.8 b 3.30 a b 3.14 a b 2.78 a b 2.81 , 1.00 1
4.0 b 3.20 a b 2.16 b c 1.43 b , 1.00 b 1 , 1.00 1
0.7360.03 6.8 a 5.36 a a 5.04 a a 3.93 a a 3.80 a a 2.94
4.0 a 4.20 b a 3.77 b a 3.75 a a 3.28 b , 1.00 1
35 0.3560.04 6.8 b 3.12 a b 1.87 a , 1.00 1 1.52 1 , 1.00 1 , 1.00 1 , 1.00
4. 0 b 1 .70 b , 1.00 a 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00
0.5260.03 6.8 b 3.22 a , 1.00 1 , 1.00 1 , 1.12 1 , 1.00 1 , 1.00 2 , 1.00
4.0 b 2 .34 b , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 2 , 1.00
0.7360.03 6.8 a 4.58 a a 3.88 1.17 a , 1.00 1 , 1.00 1 , 1.00 2 , 1.00
4.0 a 3 .56 b , 1.00 1 1.67 a , 1.00 1 , 1.00 2 , 1.00 2 , 1.00
45 0.3560.04 6.8 , 1.00 , 1.00 2 , 1.00 2 , 1.00 2
4.0 , 1.00 1 , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
0.5260.03 6.8 , 1.00 , 1.00 2 , 1.00 2 , 1.00 2
4.0 , 1.00 1 , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
0.7360.03 6.8 , 1.00 , 1.00 2 , 1.00 2 , 1.00 2
4.0 , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
aLog cfu/ g dry cereal. Initial population (0 week) was 6.31 log cfu/ g of cereal at pH 6.8 and 6.10 log cfu/ g cereal at pH 4.0.Values
10 10 10
the same temperature, a and storage time) are significantly different ( p# 0.05). Values not preceded by the same letter, (within the saw
significantly different ( p# 0.05).b
Enriched in mTSB, 1 indicates E . coli O157:H7; 2 indicates E . coli O157:H7 was not detected.
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 7/12
Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184 179
Table 3 been associated with E . coli O157:H7 infectionThe pH and populations of aerobic mesophilic microorganisms in (Besser et al., 1993). The use of apple juice contami-dry cereal, milk and apple juice, and in cereal reconstituted with
nated with the pathogen to reconstitute infant ricemilk and apple juice
cereal may result in high populations within a shortItem pH Aerobic mesophiles
time.Rice cereal (dry) 6.8 , 10 cfu/g A previous study in our laboratory showed thatMilk 6.7 45 cfu / ml Bacillus cereus did not grow in infant rice cerealApple juice 3.8 , 1 cfu/ml
reconstituted with apple juice (Jaquette and Beuchat,Cereal reconstituted with milk 6.7 , 10 cfu/ml
1998). In the study reported here, E . coli O157:H7Cereal reconstituted with apple juice 4.6 , 10 cfu/ml
grew at 15, 21 and 308C, though at different rates. In
cereal reconstituted with apple juice and inoculated
on TSA and calculating log cfu / ml of reconstituted with 8.2–12.3 cfu of E . coli O157:H7 per ml (Table10
cereal. The number of viable E . coli O157:H7 cells 4), populations exceeded 1 log cfu / ml within 9, 2410
decreased within the first 3 h after inoculation, then and 72 h at 30, 21 and 158C, respectively.8
increased with time when cereal reconstituted with Populations of E . coli O157:H7 exceeding 10
milk was stored at 15, 21 or 308C, regardless of the cfu/ ml of cereal reconstituted with apple juiceinoculum population. caused no detectable change in color or aroma.
Acid-adapted and unadapted cells grew similarly However, this population in cereal reconstituted with
at the same temperature in cereal reconstituted with milk resulted in a sour aroma. Abdul-Raouf et al.
milk or apple juice. Unpasteurized apple juice has (1993) reported that the visual appearance of raw
Table 4
Populations of E . coli O157:H7 recovered from reconstituted rice cereal inoculated with acid-adapted (TSBG) cells [8.2 (0.91 log )10
cfu/ml] and unadapted (TSB) cells [12.3 (1.09 log ) cfu/ ml]10
aStorage Population (log cfu /ml)10
Reconstituted temperature Cell 3 h 6 h 9 h 12 h 24 h 48 h 72 h
bliquid (8C) type Log E Log E Log E Log E Log E Log E Log E 10 10 10 10 10 10 10
Milk 8 TSBG 0.93 a 1 0.54 1 , 0 1 , 0 1 0.30 a 1 , 0 1 , 0 1
TSB 0.40 b 1 , 0 1 , 0 1 , 0 1 0.65 a 1 0.54 1 0.18 1
15 TSBG 0.70 a 1 0.81 a 1 0.90 a 1 1.41 a 1 3.97 a 5.82 a 8.59 a
TSB 0.80 a 1 0.74 a 1 0.98 a 1 1.22 b 1 2.84 a 5.86 a 7.34 a
21 TSBG 0.30 a 1 1.41 a 1 2.05 a 1 3.18 a 6.48 a 8.44 a 8.67 a
TSB 0.88 a 1 1.31 a 1 1.67 a 1 2.51 a 5.76 a 8.73 a 8.08 a
30 TSBG 0.48 b 1 2.65 q 1 4.04 a 5.50 b 8.41 a 8.68 a 8.59 a
TSB 1.00 a 1 2.42 a 1 4.02 a 5.77 a 8.35 a 8.47 a 8.44 a
Apple juice 8 TSBG 0.65 1 0.65 a 1 0.18 a 1 , 0 1 0.70 a 1 , 0 1 , 0 1c
TSB , 0 1 1.02 a 1 0.48 a 1 0.18 1 0.18 a 1 , 0 1 0.18 1
15 TSBG , 0 1 0.30 a 1 0.40 a 1 0.30 a 1 , 0 1 0.93 a 1 1.41 a 1
TSB 0.48 1 0.81 a 1 0.40 a 1 0.00 a 1 , 0 1 1.00 a 1 1.65 a 1
21 TSBG 0.81 a 1 , 0 1 , 0 1 0.88 a 1 1.82 a 1 3.80 a 1 5.30 a
TSB 0.40 a 1 0.18 1 , 0 1 0.65 a 1 1.76 a 1 3.96 a 1 4.76 a
30 TSBG , 0 1 0.30 a 1 1.11 a 1 2.17 a 1 4.41 a 1 6.77 b 8.25 a
TSB , 0 1 0.48 a 1 1.40 a 1 2.20 a 1 4.78 a 1 7.13 a 8.22 a
aValues not followed by the same letter (within the same reconstitution fluid, temperature and storage time) are significantly different
( p# 0.05).b
Indicates the presence of E . coli O157:H7 detected by enrichment in mTSB.c, 1 cfu/ml.
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 8/12
180 Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184
Table 5
Populations of E . coli O157:H7 recovered from reconstituted rice cereal inoculated with acid-adapted (TSBG) cells [82 (1.91 log ) cfu / ml]10
and unadapted (TSB) cells [123 (2.09 log ) cfu/ ml]10
aStorage Population ( log cfu / ml)
10
Reconstituted temp. Cell 3 h 6 h 9 h 12 h 24 h 48 h 72 hb
liquid (8C) type Log E Log E Log E Log E Log E Log E Log E 10 10 10 10 10 10 10
Milk 8 TSBG 1.26 a 1 1.41 a 1 1.10 b 1 1.24 b 1 0.98 b 1 0.90 a 1 0.78 a 1
TSB 1.44 a 1 1.35 a 1 1.45 a 1 1.41 a 1 1.32 a 1 1.19 a 1 0.88 a 1
15 TSBG 1.41 a 1 1.26 b 1 1.57 b 1 2.01 a 1 3.87 a 6.61 a 7.90 a
TSB 1.27 a 1 1.62 a 1 1.78 a 1 2.20 a 1 3.74 a 7.10 a 8.31 a
21 TSBG 1.35 a 1 1.89 b 1 2.44 a 3.41 a 5.63 a 8.81 a 8.90 a
TSB 1.57 a 1 2.11 a 1 2.69 a 3.62 a 6.70 a 8.69 a 8.96 a
30 TSBG 1.60 a 1 2.03 b 4.67 a 5.44 a 8.62 a 8.89 a 8.78 a
TSB 1.59 a 1 3.32 a 4.95 a 6.56 a 8.50 a 8.69 a 8.49 a
Apple juice 8 TSBG 1.36 a 1 1.24 a 1 1.51 a 1 1.31 a 1 1.16 a 1 1.15 a 1 0.81 a 1TSB 1.23 a 1 1.54 a 1 1.45 a 1 1.24 a 1 0.90 a 1 1.00 a 1 0.54 a 1
15 TSBG 1.41 a 1 1.13 a 1 1.37 a 1 1.34 a 1 1.08 a 1 1.45 b 1 2.06 a 1
TSB 1.13 a 1 1.29 a 1 1.45 a 1 1.37 a 1 1.04 a 1 1.98 a 1 2.84 a 1
21 TSBG 1.18 a 1 1.26 a 1 1.20 a 1 1.45 b 1 2.58 a 1 4.43 a 1 5.81 a
TSB 1.18 a 1 1.27 a 1 1.27 a 1 1.73 a 1 2.90 a 1 5.02 a 1 6.22 a
30 TSBG 1.52 a 1 1.76 a 1 1.88 b 1 2.81 b 1 5.08 a 1 6.62 a 8.18 a
TSB 1.36 b 1 1.85 a 1 2.24 a 1 3.25 a 1 6.10 a 1 8.13 a 8.22 a
aValues not followed by the same letter (within the same reconstitution fluid, temperature and storage time) are significantly different
( p# 0.05).b
Indicates the presence of E . coli O157:H7 detected by enrichment in mTSB.
vegetables was not influenced substantially by pathogen grew at 15, 21 and 308C, and survived for
growth of E . coli O157:H7. 72 h at 88C in cereal reconstituted with apple juice.
Populations of E . coli O157:H7 in reconstituted This further confirms observations that E . coli
cereal initially inoculated with 1.91 or 2.09 log O157:H7 has a high tolerance to the acidic (pH 4.6)10
cfu/ ml of acid-adapted or unadapted cells, respec- conditions.
tively, are shown in Table 5. In cereal reconstituted
with milk, the population of E . coli O157:H7 3.3. Survival of E . coli O157: H 7 in low- and
increased at all incubation temperatures except 88C intermediate-a foodsw
as occurred with cereal inoculated with the lower
inoculum (Table 4). At 88C, the population slowly Survival of acid-adapted and unadapted E . coli
declined during 72 h of incubation. As with cereal O157:H7 cells inoculated into nine low- andinoculated lower numbers of E . coli O157:H7, intermediate-a foods and stored at 5, 21 and 378C
w
growth of the higher inoculum occurred at 15, 21 for up to 12 weeks was determined. Populations of
and 308C. The lag phase of growth in cereal with the aerobic mesophilic microorganisms, pH and a of w
higher inoculum was shorter than the lag phase in foods and food ingredients are shown in Table 1.
cereal containing the lower inoculum. Cereal recon- The pH of test foods ranged from 4.07 to 6.49 and
stituted with apple juice did not change in color and the a ranged from 0.16 to 0.82.w
aroma. At a given storage time, increased storage Shown in Table 6 are the populations of acid-
temperature enhanced the growth of E . coli adapted and unadapted E . coli O157:H7 cells in test
O157:H7, with no marked differences in growth foods as affected by storage temperature. Initial (0
rates of acid-adapted and unadapted cells. The week) populations were determined by plating the
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 9/12
Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184 181
Table 6
Populations of E . coli O157:H7 (log cfu/ ml) in foods and ingredients as affected by cell type (acid-adapted, grown in TSBG; unadapted,10
grown in TSB), temperature and time
aStorage Population (log cfu /g)10
Food/ temperature Cell 1 week 2 weeks 3 weeks 5 weeks 8 weeks 12 weeks 19 weeks
bingredient (8C) type Log E Log E Log E Log E Log E Log E Log E 10 10 10 10 10 10 10
Almond paste 5 TSBG 4.15 b 3.99 b 4.26 b 4.32 a 4.00 a 3.83 a
TSB 4.34 a 4.20 a 4.40 a 4.42 a 3.98 a 3.76 a
21 TSBG 3.20 b 2.16 a 1 2.18 a 1 , 1.00 1 , 1.00 1 , 1.00 2
TSB 3.58 a 2.33 a 1 2.15 a 1 , 1.00 1 , 1.00 1 , 1.00 2
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
Apple powder 5 TSBG 3.89 a 3.83 a 3.90 a 3.71 b 3.25 a 2.51 a
(unsulfured) TSB 3.48 b 3.40 a 3.85 a 4.03 a 3.18 a 2.39 b
21 TSBG 2.88 a 1.78 a 1 2.22 a 1 1.30 a 1 , 1.00 1 , 1.00 1TSB 2.59 b 1.85 a 1 2.32 a 1 1.18 a 1 , 1.00 1 , 1.00 1
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
Apple powder 5 TSBG 3.34 a 3.37 a 3.92 a 3.86 b 3.42 b 2.90 b
(sulfured) TSB 3.65 b 3.65 a 3.86 a 4.41 a 4.08 a 3.68 a
21 TSBG 3.35 a 2.15 a 2.81 a 1 1.65 a 1 1.60 a 1 , 1.00 1
TSB 3.12 b 2.49 a 3.18 a 1 1.98 a 1 2.52 a 1 1.30
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
Buttermilk powder 5 TSBG 3.83 a 4.33 a 4.13 a 4.48 a 4.00 a 3.58 aTSB 4.20 a 3.81 b 4.50 a 3.99 b 3.54 b 4.00 a
21 TSBG 3.88 a 2.77 a 1 2.37 a 1 2.57 a 1 1.88 a 1 , 1.00 1
TSB 3.60 a 2.53 a 1 2.33 a 2.54 a 1 1.54 a 1 , 1.00 1
37 TSBG 1.60 a 1 , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB 1.48 a 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 2
Cheddar cheese 5 TSBG 4.27 a 4.11 a 4.18 a 3.88 a 4.25 a 3.13 a
seasoning 1 TSB 3.80 b 3.34 b 3.50 b 3.55 b 3.09 b 2.46 a
21 TSBG 3.16 a 2.52 a 1 2.37 a 1 1.88 1 , 1.00 1 , 1.00 1
TSB 2.62 b 1.60 b 1 1.95 b 1 , 1.00 1 , 1.00 1 , 1.00 1
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
Cheddar cheese 5 TSBG 4.51 a 4.00 a 3.69 a 3.49 a 3.05 a 2.18 a
seasoning 2 TSB 3.45 b 3.11 b 3.33 b 2.90 b 2.18 b 1.15 b
21 TSBG 2.41 a 1.48 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1
TSB 1.48 b , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1
37 TSBG , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 10/12
182 Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184
Table 6. Continued
aStorage Population (log cfu /g)10
Food/ temperature Cell 1 week 2 weeks 3 weeks 5 weeks 8 weeks 12 weeks 19 weeks
bingredient (8C) type Log E Log E Log E Log E Log E Log E Log E 10 10 10 10 10 10 10
Fig paste 5 TSBG 4.11 a 3.45 b 2.82 a , 1.00 2 , 1.00 2 , 1.00 2
TSB 4.23 a 3.67 a 3.01 a , 1.00 2 , 1.00 2 , 1.00 2
21 TSBG , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
Powdered chicken 5 TSBG 4.21 a 4.24 a 4.37 a 4.29 a 3.97 a 4.10 a
TSB 4.33 a 4.20 a 4.19 a 4.25 a 4.16 a 3.55 a
21 TSBG 3.46 a 3.00 a 1 2.99 a 1 2.98 a 1 1.78 b 1 , 1.00 1
TSB 3.57 a 3.02 a 1 3.01 a 1 2.66 a 1 2.51 a 1 , 1.00 1
37 TSBG , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 2 , 1.00 2
TSB 1.48 1 , 1.00 1 , 1.00 1 , 1.00 1 , 1.00 2 , 1.00 2
Sour cream 5 TSBG 4.20 a 3.99 a 3.69 b 3.48 b 2.16 b 2.26 b
powder TSB 4.45 a 3.80 b 4.43 a 4.18 a 3.66 a 2.94 a
21 TSBG 2.34 b 2.65 a 1 , 1.00 a 1 , 1.00 1 , 1.00 1 , 1.00 2
TSB 3.26 a 2.32 b 1 2.29 a 1 1.18 1 , 1.00 1 , 1.00 2
37 TSBG , 1.00 2 , 1.00 2 , 1.00 2 , 1.00 2
TSB , 1.00 1 , 1.00 2 , 1.00 2 , 1.00 2
aValues not followed by the letter (within the same food and storage temperature) are significantly different ( p# 0.05). Initial populations of
acid-adapted and unadapted cells were 5.48 and 5.71 log cfu/ g, respectively, in almond paste, Cheddar cheese seasonings and apple10
powder, and 5.60 and 5.83 log cfu/ g, respectively, in fig paste, chicken powder, sour cream powder and buttermilk powder.10
b Enrichment in mTSB: 1 indicates presence of E . coli O157:H7; 2 indicates that E . coli O157:H7 was not detected.
inoculum on TSA and then calculating cfu/ g of exception of fig paste, in which E . coli O157:H7
food. The initial populations of acid-adapted and survived three weeks but not eight weeks, the
unadapted cells were 5.48 and 5.71 log cfu/ g, pathogen maintained high viability for 19 weeks.10
respectively, in almond paste, Cheddar cheese Death in fig paste is attributed to stress conditions
seasonings, and apple powders, and 5.60 and 5.83 imposed by low pH and a relatively high a at whichw
log cfu / g, respectively, in fig paste, chicken pow- metabolic activity of cells would not be minimized.10
der, sour cream powder, and buttermilk powder. Numbers of E . coli O157:H7 recovered from sul-
With the exceptions of buttermilk powder and pow- fured and unsulfured apple powder did not differ
dered chicken, E . coli O157:H7 was not detected in significantly.
foods stored at 378C for two weeks. The pathogen Various types and amounts of solute in test foodssurvived in the latter foods for at least eight and five may influence survival of E . coli O157:H7. The type
weeks, respectively. Of the nine products tested, of solute is known to influence minimum a atw
buttermilk powder and chicken powder had the which E . coli O157:H7 will grow (Buchanan and
highest pH values (Table 1), suggesting that acid Bagi, 1997), and may also influence the rate of
environments adversely affected viability. The same inactivation at a values less than required forw
trend was noted for rice cereal (Table 2). At 218C, E . growth. Our observation that E . coli O157:H7 sur-
coli O157:H7 survived for less than two weeks in fig vives better in reduced-a foods at refrigerationw
paste, eight weeks but not 12 weeks in almond paste temperature agrees with observations on its behavior
and sour cream powder, and at least 12 weeks in all in dry rice cereal and reports by Clavero and Beuchat
other foods. When storage was at 58C, with the (1996) indicating that survival was better in salami
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 11/12
Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184 183
as a simple means of evaluating the acid tolerance of at 58C than at 208C or 308C and Zhao and Doylestationary-phase cells. Appl. Environ. Microbiol. 62, 4009–(1994) that E . coli O157:H7 survived in mayonnaise4013.
for 34 to 55 days at 58C and for 8 to 21 days at 208C.Buchanan, R.L., Bagi, L.K., 1997. Effect of water activity and
Acid-adapted cells consistently retained higher humectant identity on the growth kinetics of Escherichia coli
viability than control cells in Cheddar cheese season- O157:H7. Food Microbiol. 14, 413–423.Calicioglu, M., Faith, N.G., Buege, D.R., Luchansky, J.B., 1997.ings stored at 5 and 218C. This suggests that acid
Viability of Escherichia coli O157:H7 in fermented semidryadaptation, at least adaptation to lactic acid, resultedlow-temperature-cooked beef summer sausage. J. Food Prot.
from growth in TSBG, rendering cells more tolerant60, 1158–1162.
to lactic acid presumed to be present in these dairy Clavero, M.R.S., Beuchat, L.R., 1996. Survival of Escherichia
products. In a previous study (Deng et al., 1998) we coli O157:H7 in broth and processed salami as influenced by
pH, water activity, and temperature and suitability of mediaobserved that enhanced acid tolerance of acid-for its recovery. Appl. Environ. Microbiol. 62, 2735–2740.adapted E . coli O157:H7 cells was influenced by
Centers of Disease Control and Prevention 1995. Escherichia colistrain, type of acidulant used to induce acid adapta-
O157:H7 outbreak linked to commercially distributed dry-tion, and the nature of secondary stresses. Studies by cured salami-Washington and California. Morbid. Mortal.
Arnold and Kaspar ( 1995) and Miller and Kaspar Weekly Rep. 44, 157–160.
Christian, J.H.B., Stewart, B.J., 1973. Survival of Staphylococcus
(1994) have shown that sustained acid tolerance of aureus and Salmonella newport in dried foods, as influence by E . coli O157:H7 depends on phase of growth andwater activity and oxygen. In: Hobbs, B.C., Christian, J.H.B.
starvation, not on adaptation. Survival of the patho-(Eds.), The Microbiological Safety of Foods. Academic Press,
gen is undoubtedly influenced by these and many London, pp. 107–118.
other physiological and environmental factors that Conner, D.E., Kotrola, J.S., 1995. Growth and survival of Es-
cherichia coli O157:H7 under acidic conditions. Appl. En-must be considered when predicting the behavior of viron. Microbiol. 61, 382–385. E . coli O157:H7 in low- and intermediate-a foods.
w Cray, W.C., Moon, H.W., 1995. Experimental infection of calves
and adult cattle with Escherichia coli O157:H7. Appl. En-
viron. Microbiol. 61, 1586–1590.
Acknowledgements Deng, Y., Ryu, J., Beuchat, L.R., 1998. Tolerance of acid-adapted
and non-adapted Escherichia coli O157:H7 to reduced pH as
affected by type of acidulant. J. Appl. Microbiol. accepted forThe authors wish to thank Dr. Rocelle Clavero,
publication.Ms. Brenda Nail, and Ms. Kimberly Hortz for their Doyle, M.P., Zhao, T., Meng, J., Zhao, T., 1997. Escherichia colitechnical assistance. O157:H7. In: Doyle, M.P., Beuchat, L.R., Montville, T.J.
(Eds.), Food Microbiology – Fundamentals and Frontiers.
American Society of Microbiology Press, Washington, DC,
Ch. 10, pp. 171–191.ReferencesFaith, N.G., Parniere, N., Larson, T., Lorang, T.D., Kaspar, C.W.,
Luchansky, J.B., 1998. Viability of Escherichia coli in salamiAbdul-Raouf, U.M., Ammar, M.S., Beuchat, L.R., 1996. Isolation following conditioning of batter fermentation and drying of
of Escherichia coli O157:H7 from some Egyptian foods. Int. sticks, and storage of slices. J. Food Prot. 61, 377–382.J. Food Microbiol. 29, 423–426. Faith, N.G., Wierzba, R.K., Ihnot, A.M., Roering, A.M., Lorang,
Abdul-Raouf, U.M., Beuchat, L.R., Ammar, M.S., 1993. Survival T.D., Kaspar, C.W., Luchansky, J.B., 1998. Survival of Es-and growth of Escherichia coli O157:H7 on salad vegetables. cherichia coli O157:H7 in full- and reduced-fat pepperoniAppl. Environ. Microbiol. 59, 1999–2006. after manufacture of sticks, storage of slices at 48C or 218C
Ansay, S.E., Kaspar, C.W., 1997. Survey of retail cheeses, dairy under air and vacuum, and baking of slices on frozen pizza atprocessing environments and raw milk for Escherichia coli 135, 191 and 2468C. J. Food Prot. 61, 383–389.O157:H7. Lett. Appl. Microbiol. 25, 131–134. Foster, J.W., Hall, H.K., 1990. Adaptive acidification tolerance
Arnold, K.W., Kaspar, C.W., 1995. Starvation- and stationary response of Salmonella typhimurium. J. Bacteriol. 172, 771–phase-induced acid tolerance in Escherichia coli O157:H7. 778.Appl. Environ. Microbiol. 61, 2037–2039. Griffin, P.M., Tauxe, R.V., 1991. The epidemiology of infections
Besser, R.E., Lett, S.M., Weber, J.T., Doyle, M.P., Barrett, T.J., caused by Escherichia coli O157:H7, other enterohemorrhagicWells, J.G., Griffin, P.M., 1993. An outbreak of diarrhea and E . coli and the associated hemolytic uremic syndrome. Epi-hemolytic uremic syndrome from Escherichia coli O157:H7 in demiol. Rev. 13, 60–98.fresh pressed apple cider. J. Am. Med. Assoc. 269, 2217– Hathcox, A.K., Beuchat, L.R., Doyle, M.P., 1995. Death of 2220. enterhemorrhagic Escherichia coli O157:H7 in real and re-
Buchanan, R.L., Edelson, S.G., 1996. Culturing enterohemor- duced-calorie mayonnaise as influenced by initial populationrhagic Escherichia coli in the presence and absence of glucose and temperature of storage. J. Food Prot. 61, 4172–4177.
8/11/2019 Exherichia Parte 2
http://slidepdf.com/reader/full/exherichia-parte-2 12/12
184 Y . Deng et al. / International Journal of Food Microbiology 45 (1998) 173 –184
Jaquette, C.B., Beuchat, L.R., 1998. Survival and growth of coli O157:H7 infections associated with the consumption of
psychrotrophic Bacillus cereus in dry and reconstituted infant yoghurt. Epidemiol. Infect. 111, 181–187.
rice cereal. J. Food Prot. accepted for publication. Rambach, A., Mariani-Kurdjian, P., Bingen, E., Bettelheim, K.A.,Keene, W.E., Sakie, E., Kok, J., Rice, D.H., Hancock, D.D., Balan, 1997. Detection of a biochemically atypical urease-producing
V.K., Zhao, T., Doyle, M.P., 1997. An outbreak of Escherichia shiga-like toxin-producing strain of Escherichia coli O157:H7
coli O157:H7 infections traced to jerky made from deer meat. from faecal culture of a healthy person by means of theJ. Am. Med. Assoc. 277, 1229–1231. chromogenic medium CHROMagar O157. Suppl. J. Appl.
Juven, B.J., Cox, N.A., Bailey, J.S., Thomson, J.E., Charles, O.W., Microbiol. 83, 14.Shutze, J.V., 1984. Survival of Salmonella in dry food and Rowbury, R.J., 1997. More chaos on the microbiology front: thefeed. J. Food Prot. 47, 445–448. E . coli O157 outbreaks. Sci. Prog. 80, 3–4.
Leyer, G.J., Johnson, E.A., 1992. Acid adaptation promotesUpton, P., Coia, J.E., 1994. Outbreak of Escherichia coli O157
survival of Salmonella spp. in cheese. Appl. Environ. Mi-infection associated with pasteurized milk supply. Lancet 344,
crobiol. 58, 2075–2080.1015–1015.
Leyer, G.J., Johnson, E.A., 1997. Acid adaptation sensitizesWang, G., Zhao, T., Doyle, M.P., 1997. Survival and growth of Salmonella typhimurium to hypochlorous acid. Appl. Environ.
Escherichia coli O157:H7 in unpasteurized and pasteurizedMicrobiol. 63, 461–467.milk. J. Food Prot. 60, 610–613.Leyer, G.J., Wang, L., Johnson, E.A., 1995. Acid adaptation of
Zhao, T., Doyle, M.P., 1994. Fate of enterohemorrhagic Es- Escherichia coli O157:H7 increases survival in acidic foods.cherichia coli O157:H7 in commercial mayonnaise. J. FoodAppl. Environ. Microbiol. 61, 3752–3755.
Prot. 57, 780–783.Miller, L.G., Kaspar, C.W., 1994. Escherichia coli O157:H7 acid
tolerance and survival in apple cider. J. Food Prot. 57, 460– Zhao, T., Doyle, M.P., Besser, R.E., 1993. Fate of enterohemor-
464. rhagic Escherichia coli O157:H7 in apple cider with and
Morgan, D., Nawman, C.P., Hutchinson, D.N., Walkes, A.M., without preservatives. Appl. Environ. Microbiol. 59, 2526–
Rowe, B., Maijd, F., 1993. Verotoxin-producing Escherichia 2530.