Thermal tolerance of acid-adapted and ... - Wiley Online Library

Letters in Applied Microbiology 2005, 41, 448–453

doi:10.1111/j.1472-765X.2005.01797.x

Thermal tolerance of acid-adapted and unadapted Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes in cantaloupe juice and watermelon juice M. Sharma, B.B. Adler, M.D. Harrison and L.R. Beuchat Center for Food Safety and Department of Food Science and Technology, University of Georgia, Griffin, GA, USA 2005/0705: received 20 June 2005, revised 29 August 2005 and accepted 30 August 2005

ABSTRACT M . S H A R M A , B . B . A D L E R , M . D . H A R R I S O N A N D L . R . B E U C H A T . 2005.

Aims: A study was performed to determine D values of acid-adapted and unadapted cells of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes in cantaloupe juice and watermelon juice. Methods and Results: Salmonella enterica serotype Poona, S. enterica serotype Saphra, two strains of E. coli O157:H7, and two strains of L. monocytogenes were grown in tryptic soy broth (TSB) and TSB supplemented with 1% glucose for 24 h at 37C. Decimal reduction times (D values) of cells suspended in unpasteurized cantaloupe juice and watermelon juice were determined. Acid-adapted cells of Salmonella and E. coli O157:H7, but not L. monocytogenes, had increased thermal tolerance compared with cells that were not acid-adapted. There was no correlation between soluble solids content of the two types of juice and thermal resistance. Conclusions: Growth of Salmonella and E. coli O157:H7 in cantaloupe juice, watermelon juice, or other acidic milieu, either in preharvest or postharvest environments, may result in cross protection to heat. The pasteurization conditions necessary to achieve elimination of pathogens from these juices would consequently have to be more severe if cells are habituated to acidic environments. Significance and Impact of the Study: Insights from this study provide guidance to developing pasteurization processes to eliminate Salmonella, E. coli O157:H7, and L. monocytogenes in cantaloupe juice and watermelon juice. Keywords: cantaloupe, Escherichia coli O157:H7, juice, Listeria monocytogenes, Salmonella, thermal tolerance, watermelon.

INTRODUCTION Outbreaks of foodborne infections associated with the consumption of fresh fruits and vegetables as well as unpasteurized juices contaminated with pathogenic bacteria have been documented (Harris et al. 2003). Outbreaks of salmonellosis (Centers for Disease Control and Prevention. 1991, 2002; Moehler-Boetani et al. 1999) and Escherichia coli O157:H7 infections (Jackson and Keene 2003) have been Correspondence to: Larry R. Beuchat, Center for Food Safety, University of Georgia, 1109 Experiment Street, Griffin, GA 30223-1797, USA (e-mail: [email protected]).

linked to the consumption of cantaloupes. Watermelons have been implicated in outbreaks of salmonellosis (Blostein 1993; Gaylor et al. 1995) and shigellosis (Fredlund et al. 1987). Pathogens known to be contaminants on the surface of melon rinds (Castillo et al. 2004; Duffy et al. 2005) can be translocated to the edible tissues and juices when melons are cut during preparation (Ukuku and Sapers 2001; Ukuku and Fett 2002). Salmonella can rapidly grow on sliced cantaloupe, watermelon, and honeydew melon (Golden et al. 1993), and in cantaloupe juice (Richards et al. 2004) and watermelon juice (Fernandez Escartin et al. 1989). Escherichia coli O157:H7 has been reported to grow on cantaloupe ª 2005 The Authors Journal compilation ª 2005 The Society for Applied Microbiology

THERMAL TOLERANCE OF PATHOGENS IN JUICE

and watermelon cubes (Del Rosario and Beuchat 1995). Listeria monocytogenes can grow in cantaloupe and watermelon pulp (Penteado and Leita˜o 2004). Elimination of foodborne pathogens that may contaminate tissues and juice of melons is essential for preventing infections that may be associated with consumption of these products. Surface decontamination of melons by treatment with chemical sanitizers (Park and Beuchat 1999) and heat (Annous et al. 2004; Ukuku et al. 2004) has not been fully successful in eliminating pathogens. The potential for contamination of edible tissue and juice of melons with pathogens translocated from the surface of the rind during processing emphasizes the need to apply sanitization and pasteurization technologies that will reduce or eliminate the risk of illness associated with consumption of these products. The US Food and Drug Administration has implemented a HACCP program that focuses on minimizing microbiological safety risks that may be associated with fruit and vegetable juices (Al-Taher and Knutson 2004). One of the interventions to eliminate foodborne pathogens is heat treatment. The use of melon juice in blends of nonpasteurized and pasteurized fruit juices offered for sale to the consumer has increased in recent years. To date, research efforts on the microbiological safety of pasteurization processes for fruit juices have concentrated largely on determining D values (decimal reduction times) for Salmonella, E. coli O157:H7, and L. monocytogenes in apple juice (Ingham and Uljas 1998; Dock et al. 2000; Mak et al. 2001). We undertook a study to determine the D values of these pathogens in cantaloupe juice and watermelon juice as affected by acid adaptation preceding exposure to heat.

MATERIALS AND METHODS Strains used Two serotypes of Salmonella enterica (serotypes Poona 01A3907 and Saphra 97A3312, both isolated from patients with salmonellosis associated with eating cantaloupe), two strains of E. coli O157:H7 (E0139, isolated from venison jerky and SEA-13B88, isolated from a patient infection associated with consumption of apple cider), and two strains of L. monocytogenes [F8369 (serotype 1/2a), isolated from corn and G1091 (serotype 4a), isolated from a patient in a coleslaw-associated outbreak] were used. The two strains of E. coli O157:H7 are known to adapt to acid pH (Ryu and Beuchat 1998; Buchanan and Edelson 1999). Preparation of melon juice Fully ripe cantaloupes (Cucamis melo var. reticulatus) and watermelons (Citrullus lanatus var. lanatus) were purchased

449

at a supermarket in Griffin, GA, USA, washed with tap water for 15 s, and air dried before cutting with a sterile stainless steel knife on a sterile cutting surface. Edible tissue (c. 500 g) was removed, placed in a sterile filtered stomacher bag (Filtra, Fisher Scientific, Pittsburgh, PA, USA) and pummeled for 1 min in a Stomacher 400 laboratory blender (Seward Medical Limited, London, UK). The filtrate was poured into a sterile 250-ml glass bottle and held at 22C for 10 min. The pH of the cantaloupe and watermelon juices was measured using a Basic pH meter (Denver Insturments Inc., Arvada, CO, USA). The soluble solids (Brix) were measured using an Abbe 3L refractometer (Spectronic Instruments, Rochester, NY, USA). This juice was used to prepare suspensions of Salmonella, E. coli O157:H7, and L. monocytogenes for heat inactivation studies described below. Preparation of cells for thermal treatment Cells of all strains were cultured in tryptic soy broth containing no glucose (TSB, initial pH 7Æ2; BBL/Difco, Sparks, MD, USA) and TSB supplemented with glucose (10 g l)1) (TSBG, initial pH 7Æ2) at 37C. Broth (10 ml) was inoculated with c. 10 ll of culture at three consecutive 24-h intervals before measuring the pH and collecting cells from cultures to prepare inocula. Cultures were centrifuged in 15ml conical centrifuge tubes (VWR International, South Plainfield, NJ, USA) at 2000 g for 10 min in a Centra CL2 centrifuge (International Equipment Company, Needham Heights, MA, USA). The supernatant was removed, cells in pellets were resuspended in 10 ml of sterile deionized water, and the suspension was centrifuged at 2000 g for 10 min. The cells were again washed in sterile deionized water and collected by centrifugation. The supernatant was decanted and cells were suspended in 10 ml of cantaloupe juice or watermelon juice prepared as described above. Thermal treatment of inoculated juice Suspensions of each serotype or strain of Salmonella, E. coli O157:H7, and L. monocytogenes in cantaloupe or watermelon juice (50 ll) were dispensed in a sterile glass capillary tube (0Æ8–1Æ10 (ID) · 90 mm, Kimble-Kontes, Vineland, NJ, USA) which had been sealed at one end using a 1-ml syringe equipped with a sterile deflected-point needle (Popper and Sons, Inc., Hyde Park, NJ, USA). The open end of each capillary tube was flame-sealed and the tubes were held in sterile water at 22C for 30 min until immersed in a heated water bath. Juice suspensions of Salmonella Poona and Salmonella Saphra prepared from cells grown in TSB and deposited in sealed capillary tubes were immersed in water at 57C for 0, 1, 2, 3, 4, 5, 6, and 7 min; Salmonella grown in TSBG was

ª 2005 The Authors Journal compilation ª 2005 The Society for Applied Microbiology, Letters in Applied Microbiology, 41, 448–453, doi:10.1111/j.1472-765X.2005.01797.x

450 M . S H A R M A ET AL.

immersed in water at 57C for 0, 1, 2, 3, 4, 5, 6, 8, 10, 12, and 14 min. Tubes containing suspensions of cells of E. coli O157:H7 grown in TSB were immersed in water at 57C for 0, 6, 12, 18, 24, 30, 36, and 42 min; suspensions of E. coli O157:H7 grown in TSBG were immersed in water at 57C for 0, 12, 24, 36, 42, 48, 54, and 60 min. Tubes containing suspensions of L. monocytogenes grown in TSB were immersed in water at 56C or 57C (± 0Æ2C) for 0, 2, 4, 6, 8, 10, 12, and 14 min or 0, 1, 2, 3, 4, 5, 6, and 7 min; respectively; suspensions of L. monocytogenes grown in TSBG were immersed in water 56C or 57C for 0, 2, 4, 6, 8, 10, 12, and 14 min or 0, 1, 2, 3, 4, 5, 6, and 7 min, respectively. At the end of each heating time, capillary tubes were immersed in 70% ethanol at 22C for 15 s, rinsed in sterile deionized water at 22C, placed in 5 ml of sterile 0Æ1% peptone water in a 15-ml conical centrifuge tube, and crushed with a sterile glass rod. The heated suspension was thoroughly mixed with the peptone water before analyzing for numbers of surviving pathogens.

(Knudsen et al. 2001; Yamamoto and Harris 2001). Plates were incubated at 37C for 24 h before colonies were counted.

Microbiological analysis

RESULTS

Populations of Salmonella, E. coli O157:H7, and L. monocytogenes in the mixture of heated melon juice and peptone water were determined by surface plating undiluted samples (0Æ25 ml in quadruplicate or 0Æ1 ml in duplicate) or samples serially diluted in 0Æ1% peptone water (0Æ1 ml in duplicate) on tryptic soy agar (TSA, pH 7Æ3; BBL/Difco) supplemented with 0Æ1% sodium pyruvate (Sigma-Aldrich, St Louis, MO, USA) (TSAP) to enhance the recovery of injured cells

In Table 1 pH values of 24-h cultures of pathogens grown in TSB and TSBG are shown. The pH values and soluble contents of the juices are also listed. These values are typical of those fully mature melons used in the fresh-cut and juice industries. The pH and soluble solids content of cantaloupe juice and watermelon juice in which cells of pathogens were suspended during subsequent thermal treatment are also listed. With the exception of E. coli O157:H7 cultured to

Statistical analysis Populations (log CFU ml)1) of each serotype or strain of pathogen surviving heat treatment were plotted on the y-axis against heating time (min) on the x-axis. The linear regression function in SAS (SAS Institute, Cary, NC, USA) was used to calculate equations for best-fit lines for cells of each serotype or strain grown in TSB and TSBG, and D56C or D57C values for Salmonella, E. coli O157:H7, and L. monocytogenes were determined. Data presented represent results from at least three replicate experiments for each pathogen. Within each strain of pathogen, mean D values were compared using the LSD mean separation test in SAS to determine significant differences (P £ 0Æ05) in heat resistance as affected by culture medium.

Table 1 pH values of tryptic soy broth (TSB) and melon juice, and percent soluble solids (Brix) in cantaloupe juice and watermelon juice* Grown in TSB without glucose

Grown in TSB with 1% glucose

pH

pH

Type of juice

Pathogen

Strain or serotype

TSB

Cantaloupe

Salmonella

Poona 01A3907 Saphra 97A3312 E0139 SEA 13B88 F8369 G1091 Poona 01A3907 Saphra 97A3312 E0139 SEA 13B88 F8369 G1091

a a a a a a a a a a a a

Escherichia coli O157:H7 Listeria monocytogenes Watermelon

Salmonella E. coli O157:H7 L. monocytogenes

6Æ9 6Æ9 6Æ7 6Æ7 6Æ8 6Æ8 6Æ9 6Æ9 6Æ8 6Æ8 6Æ9 6Æ9

Juice ± ± ± ± ± ± ± ± ± ± ± ±

0Æ1 0Æ1 0Æ1 0Æ1 0Æ0 0Æ0 0Æ0 0Æ0 0Æ1 0Æ0 0Æ0 0Æ0

a a a a a a a a a a a a

6Æ3 6Æ3 6Æ3 6Æ3 6Æ3 6Æ3 5Æ4 5Æ3 5Æ2 5Æ2 5Æ3 5Æ3

± ± ± ± ± ± ± ± ± ± ± ±

0Æ2 0Æ2 0Æ2 0Æ2 0Æ2 0Æ2 0Æ0 0Æ0 0Æ0 0Æ0 0Æ0 0Æ0

Soluble solids (%)

TSBG

10Æ4 10Æ4 10Æ4 10Æ4 10Æ4 10Æ4 7Æ9 7Æ9 8Æ0 8Æ0 8Æ0 8Æ0

b b b b b b b b b b b b

± ± ± ± ± ± ± ± ± ± ± ±

1Æ1 1Æ1 1Æ1 1Æ1 1Æ1 1Æ1 0Æ2 0Æ2 0Æ4 0Æ4 0Æ4 0Æ5

4Æ7 4Æ7 4Æ7 4Æ7 4Æ9 4Æ4 4Æ7 4Æ5 4Æ7 4Æ8 4Æ5 4Æ5

± ± ± ± ± ± ± ± ± ± ± ±

Soluble solids (%)

Juice 0Æ1 0Æ1 0Æ0 0Æ0 0Æ4 0Æ1 0Æ0 0Æ0 0Æ1 0Æ1 0Æ0 0Æ0

a a a a a a a a b a a a

6Æ3 6Æ3 6Æ3 6Æ3 6Æ3 6Æ3 5Æ6 5Æ6 5Æ3 5Æ3 5Æ4 5Æ4

± ± ± ± ± ± ± ± ± ± ± ±

0Æ1 0Æ1 0Æ1 0Æ1 0Æ1 0Æ1 0Æ0 0Æ0 0Æ1 0Æ1 0Æ2 0Æ2

8Æ8 8Æ8 8Æ8 8Æ8 8Æ8 8Æ8 10Æ0 10Æ0 11Æ8 11Æ8 12Æ8 12Æ8

± ± ± ± ± ± ± ± ± ± ± ±

0Æ9 0Æ9 0Æ9 0Æ9 0Æ9 0Æ9 0Æ0 0Æ0 1Æ4 1Æ4 1Æ3 1Æ3

*Pathogens grown in tryptic soy broth (TSB) containing no glucose and in TSB supplemented with 1% glucose (TSBG) were suspended in melon juice before heating at 56C or 57C to determine D values. Within the same melon juice, pathogen, and growth medium (TSB and TSBG), mean pH values in the same column that are not followed by the same letter are significantly different (P £ 0Æ05). Within the same row, mean pH values for TSB and TSBG that are not preceded by the same letter are significantly different (P £ 0Æ05). ª 2005 The Authors Journal compilation ª 2005 The Society for Applied Microbiology, Letters in Applied Microbiology, 41, 448–453, doi:10.1111/j.1472-765X.2005.01797.x


451

Table 2 D value of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes in cantaloupe and watermelon juice* D56C (min) Type of juice

Pathogen

Strain or serotype

Cantaloupe

Salmonella

Poona 01A3907 Saphra 97A3312 E0139 SEA 13B88 F8369 G1091 Poona 01A3907 Saphra 97A3312 E0139 SEA 13B88 F8369 G1091

E. coli O157:H7 L. monocytogenes Watermelon

Salmonella E. coli O157:H7 L. monocytogenes

TSB

D57C min) TSBG

TSB a 2Æ7 b 2Æ0 b 8Æ2 b 6Æ2 a 8Æ6 a 12Æ7 b 1Æ8 b 1Æ0 b 9Æ1 b 7Æ9

a 7Æ7 ± 2Æ9 a a 7Æ8 ± 2Æ3 a

TSBG ± ± ± ± ± ± ± ± ± ±

1Æ1 0Æ7 0Æ8 0Æ9 0Æ5 2Æ3 0Æ5 0Æ2 2Æ7 2Æ0

a a a b a a a a a a

a 4Æ6 a 4Æ0 a 14Æ8 a 11Æ5 a 10Æ2 a 6Æ1 a 4Æ9 a 5Æ3 a 23Æ1 a 24Æ9

± ± ± ± ± ± ± ± ± ±

1Æ1 0Æ7 3Æ2 3Æ2 3Æ7 1Æ9 0Æ9 0Æ8 1Æ9 5Æ7

a a a a a a a a a a

a 3Æ9 ± 0Æ9 a b 3Æ4 ± 0Æ9 a

*Pathogens grown in TSB containing no glucose (TSB) or supplemented with 1% glucose (TSBG) were suspended in melon juice and heated at 56C or 57C to determine D values. Within the same type of melon juice and pathogen, D values in the same column that are not followed by the same letter are significantly different (P £ 0Æ05). Within the same row, D values that are not preceded by the same letter are significantly different (P £ 0Æ05).

determine D values in watermelon juice, the pH value of 24h TSB and TSBG cultures was unaffected by the serotype or strain of each pathogen. Without exception, the pH value of 24-h TSBG cultures of all serotypes and strains was significantly lower (P £ 0Æ05) than the pH value of 24-h TSB cultures. Reductions in pH resulting from fermentation of glucose were in the range of 1Æ9–2Æ4 units. There appeared to be no correlation between soluble solids content of the two types of test juices and thermal resistance of pathogens. Table 2 lists D values for Salmonella, E. coli O157:H7, and L. monocytogenes grown in TSB and TSBG and heated in cantaloupe juice and watermelon juice. The large coefficients of variation, in some instances, are attributed in part to potential differences in composition of juices extracted from melons used in replicate trials. With the exception of E. coli O157:H7 grown in TSB and heated in cantaloupe juice, D values of the two test serotypes or strains of each pathogen grown in the same medium and heated in the same juice did not differ significantly (P > 0Æ05). With the exception of Salmonella Poona O1A3907 heated in cantaloupe juice, cells of all strains of Salmonella and E. coli O157:H7 grown in TSBG had significantly higher (P £ 0Æ05) thermal resistance than cells grown in TSB, regardless of the type of juice in which they were heated. In contrast, the thermal resistance of both strains L. monocytogenes in cantaloupe juice and strain F8369 in watermelon juice was unaffected by the composition of the broth in which it had been cultured. Cells of L. monocytogenes G1091 grown in TSB and heated in watermelon juice were significantly (P £ 0Æ05) more tolerant to heat than were

cells grown in TSBG. Apparently, L. monocytogenes is less resistant to heat when suspended in watermelon juice, compared with cantaloupe juice. D57C values for the pathogen in watermelon juice (not shown) were very small and variable; thus only the D56C values are reported. DISCUSSION Studies have shown that acid adaptation can result in increased thermal tolerance of foodborne pathogens in fruit juices. Ryu and Beuchat (1998) reported that the D52C values of acid-adapted cells of E. coli O157:H7 E0139 in apple cider and orange juice are considerably higher those of acid-shocked or control cells. Acid adaptation enhanced the survival of E. coli O157:H7 in mango juice (pH 3Æ2) (HsinYi and Chou 2001). Acid-adapted Salmonella, E. coli O157:H7, and L. monocytogenes have increased thermal tolerance in apple, orange, and white grape juices (Mazzotta 2001); D56C values for acid-adapted Salmonella in apple, orange, and white grape juices were 2Æ28 ± 0Æ36, 4Æ54 ± 1Æ07, and 1Æ60 ± 0Æ58 min, respectively, compared with 1Æ21 ± 0Æ42, 2Æ52 ± 1Æ32, and 1Æ38 ± 0Æ18 min for cells that were not acid adapted. The increase in heat resistance was higher for E. coli O157:H7 and L. monocytogenes than for Salmonella. Ryu and Beuchat (1998) reported that acid adaptation of E. coli O157:H7 resulted in increased D54C values in apple cider and orange juice. The extent of enhanced resistance of acid-adapted pathogens to elevated temperatures varies, depending on physiological age of cells, extent or injury, and the pH, type of acidulant, and composition of the heating medium


452 M . S H A R M A ET AL.

(Sharma et al. 2003). Acid-adapted E. coli O157:H7, for example, is more tolerant to lactic acid than to acetic acid (Ryu and Beuchat 1998), and survival of acid-adapted Salmonella serotype Typhimurium is affected by organic acids and other inhibitors produced during fermentation of milk (Leyer and Johnson 1992). In our study, enhanced thermal tolerance of acid-adapted Salmonella and E. coli O157:H7, compared with tolerance of unadapted cells, in cantaloupe juice and watermelon juice is in general agreement with observations on increased heat tolerance of foodborne pathogens as a result of exposure to acid stress. The lack of enhanced thermal resistance of acid-adapted L. monocytogenes, and in one instance (strain G1091) a reduction in thermal resistance in watermelon juice, is attributed in part to the presence of cells that may have been injured as a result of exposure to the reduced pH of TSBG, thus resulting in reduced tolerance to heat. The extent of injury may have masked any increased tolerance healthy cells may have gained during exposure to a gradual reduction in pH during growth in TSBG. In summary, results provide an indication of the level of heat tolerance of Salmonella, E. coli O157:H7, and L. monocytogenes in cantaloupe juice and watermelon juice. With the exception of Salmonella Poona heated in cantaloupe juice, all serotypes or strains of acid-adapted Salmonella and E. coli O157:H7 had significantly higher (P £ 0Æ05) D values than unadapted cells grown in TSB. In contrast, the thermal resistance of both strains of L. monocytogenes in cantaloupe juice and one strain in watermelon juice was unaffected by the broth in which they were cultured. REFERENCES Al-Taher, F. and Knutson, K. (2004) Overview of the FDA juice HACCP rule. Food Prot Trends 24, 222–238. Annous, B.A., Burke, A. and Sites, J.E. (2004) Surface pasteurization of whole fresh cantaloupes inoculated with Salmonella Poona or Escherichia coli. J Food Prot 67, 1876–1885. Blostein, J. (1993) An outbreak of Salmonella Javiana associated with consumption of watermelon. J Environ Health 56, 29–31. Buchanan, R.L. and Edelson, S.G. (1999) pH-Dependent stationaryphase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants. J Food Prot 62, 211–218. Castillo, A., Mercado, I., Lucia, L.M., Martinez-Ruiz, Y., Ponce de Leon, J., Muraon, E.A. and Acuff, G.R. (2004) Salmonella contamination during production of cantaloupe: a binational study. J Food Prot 67, 713–720. Centers for Disease Control and Prevention. (1991) Multistate outbreaks of Salmonella serotype Poona infections – United States and Canada, 1991. Morbid Mortal Wkly Rep 40, 459–552. Centers for Disease Control and Prevention. (2002) Multistate outbreaks of Salmonella serotype Poona infections associated with eating cantaloupe from Mexico – United States and Canada, 20002002. Morbid Mortal Wkly Rep 51, 1044–1047.

Del Rosario, B.A. and Beuchat, L.R. (1995) Survival and growth of enterohemorrhagic Escherichia coli O157:H7 in cantaloupe and watermelon. J Food Prot 58, 105–107. Dock, L.L., Floros, J.D. and Linton, R.H. (2000) Heat inactivation of Escherichia coli O157:H7 in apple cider containing malic acid, sodium benzoate, and potassium sorbate. J Food Prot 63, 1026–1031. Duffy, W.A., Lucia, L.M., Kells, J.M., Castillo, A., Pillai, S.D. and Acuff, G.R. (2005) Concentrations of Escherichia coli and genetic diversity and antibiotic resistance profiling of Salmonella isolated from irrigation water, packing shed equipment, and fresh produce in Texas. J Food Prot 68, 70–79. Fernandez Escartin, E., Castillo Ayala, A. and Saldana Lozano, J. (1989) Survival and growth of Salmonella and Shigella and sliced fresh fruit. J Food Prot 52, 471–472. Fredlund, H., Ba¨ck, E., Sjo¨berg, L. and To¨rnquist, E. (1987) Watermelon as a vehicle of transmission of shigellosis. Scand J Infect Dis 19, 219–221. Gaylor, G.E., MacCready, R.A., Reardon, J.P. and McKernan, B.F. (1995) An outbreak of salmonellosis traced to watermelon. Public Health Rep 70, 311–313. Golden, D.A., Rhodehamel, E.J. and Kautter, D.A. (1993) Growth of Salmonella spp. in cantaloupe, watermelon, and honeydew melons. J Food Prot 56, 194–196. Harris, L.J., Farber, J.M., Beuchat, L.R., Parish, M.E., Suslow, T.V., Garrett, E.H. and Busta, F.F. (2003) Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Comp Rev Food Sci Food Safety 2(Suppl.), 78–141. Hsin-Yi, C. and Chou, C.-C. (2001) Acid adaptation and temperature effect on the survival of E. coli O157:H7 in acidic fruit juice and lactic fermentated milk product. Int J Food Microbiol 70, 189–195. Ingham, S.C. and Uljas, H.E. (1998) Prior storage conditions influence the destruction of Escherichia coli O157:H7 during heating of apple cider and juice. J Food Prot 61, 390–394. Jackson, L. and Keene, W. (2003) Where’s the beef? The role of crosscontamination in four chain restaurant associated outbreaks of Escherichia coli O157:H7 in the Pacific Northwest. Arch Int Med 160, 2380–2385. Knudsen, D.M., Yamamoto, S.A. and Harris, L.J. (2001) Survival of Salmonella spp. and Escherichia coli O157:H7 on fresh and frozen strawberries. J Food Prot 64, 1483–1488. Leyer, G.J. and Johnson, E.A. (1992) Acid adaptation promotes survival of Salmonella spp. in cheese. Appl Environ Microbiol 58, 2075–2080. Mak, P.P., Ingham, B.H. and Ingham, S.C. (2001) Validation of apple cider pasteurization treatments against Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes. J Food Prot 64, 1679–1689. Mazzotta, A.S. (2001) Thermal inactivation of stationary-phase and acid-adapted Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in fruit juices. J Food Prot 64, 315–320. Moehler-Boetani, W., Reporter, R., Werner, S.B., Abbott, S., Farrar, J., Waterman, S.H. and Virgia, D.J. (1999) An outbreak of Salmonella serogroup Saphra due to cantaloupes from Mexico. J Infect Dis 180, 1361–1364. Park, C.M. and Beuchat, L.R. (1999) Evaluation of sanitizers for killing Escherichia coli O157:H7, Salmonella, and naturally occurring



microflora on cantaloupe, honeydew melons, and asparagus. Dairy Food Environ Sanit 19, 842–847. Penteado, A.L. and Leita˜o, M.F.F. (2004) Growth of Listeria monocytogenes in melon, watermelon and papaya pulps. Int J Food Microbiol 92, 89–94. Richards, G.M., Buck, J.W. and Beuchat, L.R. (2004) Survey of yeasts for antagonistic activity against Salmonella Poona in cantaloupe juice and wounds in rinds coinfected with phytopathogenic molds. J Food Prot 67, 2132–2142. Ryu, J.-H. and Beuchat, L.R. (1998) Influence of acid tolerance responses on survival, growth, and thermal cross-protection of Escherichia coli O157:H7 in acidified media and fruit juices. Int J Food Microbiol 45, 185–193. Sharma, M., Taormina, P.J. and Beuchat, L.R. (2003) Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Sci Technol Res 9, 115–127.

453

Ukuku, D.O. and Fett, W. (2002) Behavior of Listeria monocytogenes inoculated on cantaloupes surfaces and efficacy of washing treatments to reduce transfer from rind to fresh-cut pieces. J Food Prot 65, 924–930. Ukuku, D.O. and Sapers, G.M. (2001) Effect of sanitizer treatments on Salmonella Stanley attached to the surface of cantaloupe and cell transfer to fresh-cut tissues during cutting practices. J Food Prot 64, 1286–1291. Ukuku, D.O., Pilizota, V. and Sapers, G.M. (2004) Effect of hot water and hydrogen peroxide treatments on survival of Salmonella and microbial quality of whole and fresh-cut cantaloupe. J Food Prot 67, 432–437. Yamamoto, S.A. and Harris, L.J. (2001) Phosphate buffer increases recovery of Escherichia coli O157:H7 from apple juice. J Food Prot 64, 1315–1319.
