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Publication #FSHN12-06

Growth, Reduction, and Survival of Bacteria on Tomatoes1

Angela M. Valadez, Keith R. Schneider, and Michelle D. Danyluk2

Fresh-market tomatoes are a popular commodity in homes and food service around the world. In the United States, fresh-market tomatoes are produced in every state, with commercial-scale production in about 20 states (USDA-ERS, 2009). In terms of consumption, the tomato is the nation's fourth most popular fresh-market vegetable behind potatoes, lettuce, and onions (USAD-ERS, 2009). In total, approximately 5 billion pounds of fresh tomatoes are eaten annually in the United States (CDC, 2007). In 2010, Florida produced 45% of the total U.S. value of fresh-market tomatoes behind California, Georgia, Virginia, and Tennessee (FDACS, 2012; USDA-ERS, 2008).

Tomato producers are committed to taking proactive steps to ensure and enhance the safety of the food they produce, in addition to providing consistency in product quality and wholesomeness. Still, the inherent risks of contamination by foodborne pathogens present a challenge to the produce industry and regulators. Since fresh-market tomatoes are intended to be consumed fresh, there is no “kill-step” in the processing that would eliminate pathogens in the event of contamination (Maitland et al., 2011). As such, the concern for tomato safety in the United States will continue to grow as tomato consumption increases. Even with the advancements in food processing and food safety controls employed by tomato growers and packers, the risk for foodborne pathogens, including Salmonella enterica, to be linked to outbreaks of illness associated with tomato consumption still exists.

Fresh-produce handlers and processors have developed hazard analysis and critical control point (HACCP) plans where the critical control points (CCPs) are set in place to help reduce contamination and aid in the prevention of cross-contamination (Hedberg et al., 1999). Currently, however, there exists no technology proven to eliminate bacterial hazards in any fresh-market fruit or vegetable once contamination occurs (Maitland et al., 2011). Many processing methods have been studied, a number of which warrant further examination of their efficacy as the search continues for fail-safe intervention strategies to ensure the safety of fresh-market tomatoes.

This document, therefore, is intended to highlight current tomato safety related studies on the growth, reduction, and survival of bacteria on fresh-market tomatoes. Enclosed are evaluated bacterial studies on natural antimicrobials including carvacrol (oregano), eugenol, β-resorcylic acid, trans-cinnamaldehyde (cinnamon), allyisothiocynail (mustard and horseradish), thymol, and thyme oil; detergents including chlorine dioxide (ClO2), chlorine, carbon dioxide (CO2), hydrogen peroxide (H2O2), sodium hypochlorite, ozone, sodium lauryl sulfate (SDS), tween80, acidified sodium chlorite (ASC), peroxyacetic acid (PAA), and calcinated calcium; and food processing studies including high pressure processing, irradiation, X-ray, and modified atmosphere packaging (MAP). Cross-contamination and shelf-life studies were also evaluated.

The table focuses primarily on three categories:

  1. By tomato shape or variety, including Round, Roma, plum, cherry, grape, vine, unknown red, green mature, mixed green to red, and diced

  2. By tomato composition, including the tomato stem, pulp, seeds, cotyledons, hypocotyls, and leaves

  3. By bacteria, including acid-adapted and non-acid adapted Salmonella spp., Shigella spp., E. coli O157:H7, Listeria monocytogenes, Erwinia carotovora, and Staphylococcus aureus

The intended audience for this document includes tomato processors, researchers, and government officials interested in tomato safety:

  • During evaluation of their current processing and sanitation facilities, tomato processors can use the table as a reference as they seek alternative or adaptable technologies.

  • Researchers can use this table as a guide to innovate future experiments from current literature.

  • Government officials can reference this table as current policies and regulations are evaluated and updated.

Limited studies in tomato sanitation, primarily focusing on salsa preparation and natural antimicrobial usage, are also featured here for home consumers. Overall, this tomato safety review serves as a reference for everyone concerned in the safety of fresh-market tomatoes.

Table 1. 

Tomato shape or variety according to publication

Waxed

Microbe

Time

Decontamination variable(s)

Temp. (°C)

Initial bacterial counts

Reduction or growth achieved; detection (positive or negative)

Parameters

Comments

Reference

Round red

Unknown

S. Typhimurium

S. Newport

S. Javiana

S. Braenderup (CDC)

Dip inoculated for 30 s at ~25°C and then dried overnight

Unspecified time collection points

Compared their lab-model (chicken replica), Pathogen Modeling Program, and ComBase

10

12.5

15

17.5

20

22.5

25

27.5

30

35

106 CFU/ml pre-inoculation

103 to 104 CFU/whole tomatoes

102 CFU/g of cut tomato post-inoculation

Their lab model (chicken replica) was more favorable compared to the other models.

pH 4.0–4.5

Researchers developed a mathematical model to predict the growth rate of Salmonella (102 CFU/g to 108 CFU/g) on cut tomatoes as a function of incubation temp.

Pan and Schaffner, 2010

Roma

Untreated (no washing or oiling)

No

S. Enteritidis ATCC 13076

S. Newport ATCC 6962

S. Typhimurium ATCC 14028

300 µl spot inoculated

(s)

2

4

6

10

ClO2 + sterile tap water (ppm)

(High)

20

10

5

(Low)

0

1

3

5

10

23

7 log CFU/ml

S. enterica

Reduction:

A full minute of contact with ClO2 at 20 and 10 ppm was required to achieve a 5 log reduction of S.enterica on freshly spot-inoculated tomatoes.

Immersing wet-inoculated tomatoes in water (0 ppm ClO2) for 1 min alone reduced S. enterica by ~ 1.2 log CFU/cm2.

On inoculated fruit surfaces, populations decreased>3 log CFU/cm2 during desiccation at 24°C for 24 h. Populations of air-dried Salmonella were not significantly reduced by ClO2 at ≤20 ppm after 1 min.

For each treatment, nine inoculated tomatoes were immersed in 2 liters of ClO2 or water for 20 to 60 s. Relative humidity 40– 50%

The study investigated the sanitizing effects of a ClO2 solution on S. enterica in water, on tomato surfaces, and between tomato loads.

Pao et al., 2007

Roma

Untreated (unwashed or oiled)

No

S. Enteritidis ATCC 13076

S. Newport ATCC 6962

S. Typhimurium ATCC 14028

30 ml of inoculum was distributed evenly over two synthetic polyethylene roller brushes rotating at 85 revolutions per minute.

(s)

10

20

40

60

ClO2 flow rate 5.0 ml/s

NA

Calculated brush contamination of 6.9 log CFU/cm3

Reduction:

Washing with ClO2 at 5 ppm for 10 to 60 s reduced the transfer of Salmonella from revolving brushes to fruit surfaces by 4.5 to 5.0 log cycles.

The presence of ClO2 lowered the Salmonella transfer to runoff by 5.2 to 6.4 log cycles in comparison to using water alone.

 

The study tested the ability of ClO2 at 5 ppm during spray washing of tomatoes to prevent Salmonella transfer from inoculated revolving brushes to fruit and wash runoff. Cross-contamination study.

Pao et al., 2009

Roma

Untreated (unwashed or oiled)

No

S. Enteritidis ATCC 13076

S. Newport ATCC 6962

S. Typhimurium ATCC 14028

Spot inoculated

Up to 60 sec

ClO2 or water spray washing for up to 60 s at either low or high flow rate (5.0 or 9.3 ml/s per fruit, respectively). For wet-inoculum trials, six fruits marked with circles were brushed on inoculated revolving brushes without spraying to obtain cross-contamination for 60 s to simulate newly introduced contaminants.

NA

5.7 log CFU/cm2 on fruit surfaces

Reduction:

Washing with ClO2 at a low flow rate for 10 to 60 s generated a 4.4 to 5.2 log CFU/cm2 reduction of air-dried Salmonella on fruit surfaces.

 

The study tested the ability of ClO2 at 5 ppm during spray washing of tomatoes to prevent Salmonella transfer from fruit surface to uninoculated revolving brushes.

Pao et al., 2009

Roma

(Lycopersicon esculentum)

No

S. Montevideo

S. Javiana

S. Baildon (Purdue University Bacteria Collection)

100ml spot inoculated

Air dry, 1 h

(s)

0

10

30

60

120

180

ClO2 gas (mg/liter)

0

2

5

8

10

25

1.0 x 108 CFU/ml

Reduction:

Range of 1.16 to 5.53 log cfu/cm2.

The greatest reduction at 10 mg/l of ClO2 and 180 s gave a post population 4.87 log cfu/cm2.

Relative humidity 90–95%

ClO2 parameters were then taken from this study that gave the optimal 3, 4, and 5 log reduction to select for optimal treatment conditions. The data 10 mg/l for 180 s gave a >5 log reduction.

Trinetta et al., 2010

Ripe Roma

(Lycopersicon esculentum cv Roma)

Unknown

S. Anatum F4317

S. Stanley H0558

S. Enteritidis PT30

Submerged for 1 min

(h)

0

24

48

72

(kGy )

0.25

0.50

0.75

1.0

1.5

4

8.0 log CFU/ml

Reductions ranged from 3.3 to 4.2 log CFU/g (1.5 kGy).

The irradiation sensitivity of Salmonella did not differ significantly with increasing refrigerated storage time.

A 5-log reduction in dose would be approximately

1.9 to 2.4 kGy.

Cesium-137 at a dose rate of 4.89 kGy/h

The study evaluated the influence of refrigerated storage time on the efficacy of irradiation for removing Salmonella from sliced Roma tomatoes.

Niemira 2011

Roma

(Lycopersicon esculentum)

Unknown

A 3-serotype mixture of:

S. Javiana

S. Montevideo

S. Typhimurium

(ATCC or personal collection)

Spot inoculated

NA

X-ray (# kGy/16 min)

0.1

0.5

0.75

1.0

1.5

22

Three or two strains of each bacterium were mixed with an equal volume to give approximately 107–9 CFU/ml.

Reduction:

~3.7 log CFU/tomato reduction S.enterica was achieved by treatment with 0.75 kGy X-ray, respectively.

More than a 5 log CFU/tomato reduction was achieved at 1.0 or 1.5 kGy X-ray for all tested pathogens.

Relative humidity 55–60%

Inactivation of inoculated Salmonella enterica on whole Roma tomato surfaces.

Mahmoud, 2010

Roma

(Lycopersicon esculentum)

Unknown

A 2-strain mixture of S. flexneri ATCC 9199 and ATCC 12022

Spot inoculated

NA

X-ray (# kGy/16 min)

0.1

0.5

0.75

1.0

1.5

22

Three or two strains of each bacterium were mixed with an equal volume to give approximately 107–9 CFU/ml.

Reduction:

~3.6 log CFU/tomato reduction of S. flexneri was achieved by treatment with 0.75 kGy X-ray, respectively.

More than a 5 log CFU/tomato reduction was achieved at 1.0 or 1.5 kGy X-ray for all tested pathogens.

Relative humidity 55–60%

Inactivation of inoculated Shigella flexneri on whole Roma tomato surfaces.

Mahmoud, 2010

Plum

Wax was washed off with 70% ethanol followed by DI wash

S. Montevideo

S. Poona

S. Newport

S. Baildon

S. Braenderup

S. Saintpaul (University of Georgia – L. Beuchat)

100ml spot inoculated, held to dry for 1 h at 23°C

15 s

1 min

3 min

DI (control)

Chlorine (100 ppm) Carvacrol (0.25 and 0.75%)

Trans-cinnamaldehyde (0.5 and 0.75%)

Eugenol (0.25 and 0.75%)

b-resorcylic acid (0.75 and 1.0 %)

25°C in water bath shaker

108 CFU/ml before inoculation and 107 CFU/ml post inoculation

Reduction:

~2 log CFU/ml for DI

~4 log CFU/ml for Cl

~7 log CFU/ml for Carvacrol (0.25 and 0.75%)

~6 log CFU/ml for Trans-cinnamaldehyde (0.5 and 0.75%)

2.5 log CFU/ml for Eugenol (0.25%)

>6 log CFU/ml (0.75%)

6 log CFU/ml forb-resorcylic acid (0.75 and 1.0 %)

   

Mattson et al., 2010

Cherry

(fresh and uncoated)

Unknown

S. Enteritidis PT4 E10 (Uludag University)

50ml spot inoculated for 1 h at 22°C

50ml was injected into the stem scar with a sterile syringe

50ml was pipetted onto the stem scar

Day at 7°C: 10

Day at 22°C:

20

Air storage

7

22

Before inoculation: 8.3 and 4.3 log CFU/ml

Post inoculation: (high) 7.0 log CFU/tomato; (low) 3.0 log CFU/tomato

Reduction –

Spot inoculated: (High) ~4–5 log CFU/tomato reduction at 7°C and 22°C; (low) ~3 log CFU/tomato reduction

Stem-scar syringe/pipetted: ~1 log CFU/tomato growth at 7 and 22°C

   

Das et al., 2006

Cherry

(fresh and uncoated)

Unknown

S. Enteritidis PT4 E10 (Uludag University)

50ml spot inoculated for 1 h at 22°C

50ml was injected into the stem scar with a sterile syringe

50ml was pipetted onto the stem scar

Day at 7°C:

10

Day at 22°C:

20

Modified atmosphere packaging (LDPE film)

7

22

Before inoculation: 8.3 and 4.3 log CFU/ml

Post inoculation: (high) 7.0 log CFU/tomato (low) 3.0 log CFU/tomato

Reduction –

Spot inoculated: (High) ~5 log CFU/tomato reduction at 7°C and 22°C; (low) ~3 log CFU/tomato reduction

Stem-scar syringe/pipetted: ~1 log CFU/tomato growth at 7 and 22°C

20% O2

80% CO2

 

Das et al., 2006

Cherry

(fresh and uncoated)

Unknown

S. Enteritidis PT4 E10 (Uludag University)

50ml spot inoculated for 1 h at 22°C

50ml was injected into the stem scar with a sterile syringe

50ml was pipetted onto the stem scar

Day at 7°C:

10

Day at 22°C:

20

5% CO2

7

22

Before inoculation: 8.3 and 4.3 log CFU/ml

Post inoculation: (high) 7.0 log CFU/tomato; (low) 3.0 log CFU/tomato

Reduction –

Spot inoculated: (High) ~5 log CFU/tomato reduction at 7°C and 22°C; (low) ~3 log CFU/tomato reduction

Stem-scar syringe/pipetted: ~1 log CFU/tomato growth at 7 and 22°C

   

Das et al., 2006

Cherry

(fresh and uncoated)

Unknown

S. Enteritidis PT4 E10 (Uludag University)

50ml spot inoculated for 1 h at 22°C

20 min

10 mg/l ozone

NA

Before inoculation: 8.3 and 4.3 log CFU/ml

Post inoculation: (high) 7.0 log CFU/tomato

(low) 3.0 log CFU/tomato

Detection:

High/4 h - the cells died completely

High/1 h - the complete death time was 15 min

Low/1 h and 4 h - the complete death time was 5 min

1 h or 4 h attachment time of the cells on tomatoes after inoculation

 

Das et al., 2006

Cherry

(fresh and uncoated)

Unknown

S. Enteritidis PT4 E10 (Uludag University)

50ml spot inoculated for 1 h at 22°C

20 min

5 and 20 mg/l ozone

NA

Before inoculation: 8.3 log CFU/tomato

Post inoculation: 7.0 log CFU/tomato

Reduction:

High/5 mg/1 h - there was a ~4 log CFU/tomato reduction

High/5 mg/4 h - there was a ~2.5 log CFU/tomato reduction

High/20 mg/4h - death at 15 min

High/20 mg/1h - death at 10 min

1 h or 4 h attachment time of the cells on tomatoes after inoculation

 

Das et al., 2006

Cherry

Unknown

S. Typhimurium (ATCC 14028, KCTC 2421, KCTC 2057)

1 ml spot inoculated

10 day storage

10 mg/L

chlorine dioxide (5 min)

5 kJ m-2 UV-C (254 nm) irradiation

Chlorine dioxide + UV-C irradiation

4

5.90 log CFU/g

Reduction:

Chlorine dioxide + UV-C irradiation achieved the most effective among the three treatments, which eliminated detection.

Chlorine dioxide achieved a 2.53 log CFU/g; UV-C irradiation achieved a 2.58 log CFU/g.

   

Song et al., 2011

Cherry

Unknown

E. coli O157:H7 (NCTC 12079)

1 ml spot inoculated

10 day storage

10 mg/L

chlorine dioxide (5 min)

5 kJ m-2 UV-C (254 nm) irradiation

Chlorine dioxide + UV-C irradiation

4

6.21 log CFU/g

Reduction:

Chlorine dioxide + UV-C irradiation achieved the most effective among the three treatments, which eliminated detection.

Chlorine dioxide achieved a 2.26 log CFU/g; UV-C irradiation achieved a 2.65 log CFU/g.

   

Song et al., 2011

Grape

Unknown

S.Typhimurium

S. Kentucky

S. Senftenberg

S. Enteritidis (University of Delaware Culture Collection)

Inocula (25 ml) were deposited on intact surfaces to form a drop and allowed to air dry at 25°C for about 2 h.

5 min

10 min

Chlorine (200 ppm)

thymol (0.2 and 0.4 mg/ml)

thyme oil (2.0 mg/ml)

carvacrol (0.4 mg/ml)

washing solutions

NA

107–8 CFU/ml

Reduction:

Thymol was the most effective among the three natural antimicrobial agents, which achieved >4.1 log CFU/ml reductions of S. enterica serovars Typhimurium, Kentucky, Senftenberg, and Enteritidis on grape tomatoes after a 5-min washing and >4.3 log CFU/ml reductions after a 10-min washing.

A >4.6 log CFU/ml reduction in the S. enterica populations in comparison to control was observed with the use of thymol solutions.

 

Evaluated the antibacterial activities of thymol, carvacrol, and thyme oil compared to chlorine against Salmonella spp. on grape tomatoes during the washing procedure.

Lu and Wu, 2010

Grape

(Lycopersicon esculentum Mill.)

Unknown

S. Poona (Cantaloupe)

S. Stanley H 1256 (Alfalfa sprouts)

S. Baildon (Tomato)

S. Typhimurium DT 104 (Resistant to multiple antibiotics)

S. Montevideo (Tomato) (University of Georgia – M. Harrison)

Spot inoculated 100 µl

At 4°C and 10°C

(d)

0

4

7

10

At 25°C (h)

0

4

7

10

Allyl isothiocyanate (AIT, from mustard and horseradish)

Carvacrol (from oregano)

Cinnamaldehyde (from cinnamon)

5, 10, and 15 µl (equivalent to 41.5, 83.3, and 125 µl/liter of air, respectively) of ≥97% pure carvacrol or ≥98% pure cinnamaldehyde or 1, 2, and 4 µl (equivalent to 8.3, 16.6, and 33.3 µl/liter of air, respectively) of ≥98% pure AIT

4

10

25

Whole grape tomatoes 100 µl 9.0 log CFU/ml placed on 10 separate spots

Reduction:

AIT exhibited the highest antimicrobial activity followed by cinnamaldehyde.

This level of AIT inactivated Salmonella on whole tomatoes to the detection limit of <2 log CFU/tomato at 4 and 10°C in 10 d and by 1.3 log CFU/tomato at 25°C in 10 h.

Overall, greater inactivation occurred at 10 than at 4°C and on the tomato surface than between tomato slice study.

 

The study elucidated the effect of these antimicrobial activity on pathogen inactivation on tomato skin (using whole tomatoes) and on tomato pulp (using sliced tomatoes).

Obaidat and Frank, 2009

Vine-ripened

(Lycopersicon

esculentum Mill., cv Rutgers)

No wax or oil

S. Agona (Alfalfa sprouts)

S. Baildon (Tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

50ml spot inoculated

Dip inoculated in 5 liters for 1 min

50ml spray inoculated for 2 s with thin-layer chromatography reagent sprayer at 22°C for 1 or 24 h

Agitated at 150 rpm for 5 min

Chlorine (200 mg/ml) solution

NA

Spot and spray inocula to each tomato were 7.22 log CFU/tomato.

Dip count could not be determined.

Reduction:

Spot decreased by 0.80 and 2.20 log CFU/ml, respectively, within 1 and 24 h of drying.

Spray-inoculated tomatoes decreased by 1.37 and 4.00 log CFU/ml within the same respective drying times 24 and 1 h.

 

Populations of Salmonella declined substantially between 1 and 24 h of drying; reductions were high on spray-inoculated tomatoes compared with spot-inoculated tomatoes.

Lang et al., 2004

Vine-ripened

Unknown

Shigella exneri (ATCC 12023)

Shigella sonnei (ATCC 25931)

Shigella boydii (ATCC 9207)

2 min

Sodium lauryl sulfate (SLS) 0.1 %

Tween 80 (polysorbate 80) 0.1%

22

40

6 log CFU/ml

Reductions of 1.5 to 4 log CFU/ml were achieved.

 

The study evaluated the efficacies of these detergents in removing Shigella from the surfaces of vine tomatoes at different treatment temps.

Raiden et al., 2003

Vine-ripened

Unknown

A five-strain Salmonella cocktail:

S. Typhimurium (ATCC 14028)

S. Agona (Alfalfa sprouts)

S. Baildon (Lettuce/tomato)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato) (University of Georgia – L. Beuchat)

2 min

0.1 % sodium lauryl sulfate (SLS)

0.1% Tween 80 (polysorbate 80)

22

40

6 log CFU/ml

Reductions of 1.5 to 4 log CFU/ml were achieved.

 

The study evaluated the efficacies of these detergents in removing Salmonella from the surfaces of vine tomatoes at different treatment temps.

Raiden et al., 2003

Firm tomatoes at the light-red stage of ripeness, free of external defects

Unknown

S. Montevideo

G4639 (Tomato)

S. Baildon 61-99 (Tomato) (University of Georgia – L. Beuchat)

Dip inoculated

2 min

200 ppm Cl2

5% H2O2

60

10.13 log CFU/ml

Reduction:

1.34 log CFU/g (Cl2)

1.45 log CFU/g (H2O2)

 

Efficacy of wash treatments in reducing population of Salmonella on dip-inoculated tomatoes.

Sapers and Jones, 2006

Fully ripened (variety not known)

Yes

S. Montevideo G4639 (CDC)

1 ml inoculated on diced

2 min. treatment;

At 5°C

(h)

22

46

96

142

216

At 20°C

(h)

6

22

46

70

96

142

At 30°C

(h)

6

22

46

70

Sodium hypochlorite (0.5%)

5

20

30

~4.5 log CFU/g

S. Montevideo remained essentially constant in tomatoes stored at 5°C for 216 h.

Growth 3 log CFU/g at 30°C and 2 log CFU/g at 20°C

 

Fate of S. Montevideo in chopped ripe tomatoes.

Zhuang et al., 1995

Red, ripened

Unknown

S. Braenderup (Tomato) (CDC)

Whole tomatoes at room temp. (22°C) were spot inoculated (at stem scar) with 0.1 ml of inoculum.

120 s

High pressure processing (MPa)

350

450

550

20

Whole skin: 6.33 log CFU/g

Whole pulp: 5.44 CFU/g

Reduction:

Whole Skin 4.15 log CFU/g reduction

Whole pulp 3.44 log CFU/g reduction

 

To determine the effect of pressure to reduce or eliminate the more pressure-resistant S. enterica tomato outbreak serovar from whole red Round tomatoes.

Maitland et al., 2011

Red, ripened

(Lycopersicon esculentum)

Unknown

S. Montevideo (Tomato) (University of Georgia), resistant to rifampicin

100ml spot inoculated for 90 min at 22°C under 97% RH

(d)

0

0.4

1

4

7

10

NA

22

30

5 log CFU/ fruit before attachment; after attachment, 3.8 log CFU/ fruit

Growth: After 10 days of storage at 30°C, the S. Montevideo population increased to 0.7, 1.0, 1.2, and 2.2 log CFU/ tomato. A similar trend was observed at 22°C, although populations were lower than at 30°C.

Relative humidity (%): 60, 75, 85, 97

 

Iturriaga et al., 2007

Mature, red, ripe, organic tomato

(Lycopersicon esculentum)

Unknown

S. Montevideo (Tomato) (University of Georgia), resistant to rifampicin

100ml drops on the tomato surface near the blossom; stored 22°C for 90 min

(min)

0

90

NA

22

5 and 8 log CFU/100ml

Number is proportional to storage time. The highest percentage of attachment

(6.6%) after 90 min occurred on tomatoes inoculated with the lowest population (4.95 log CFU/tomato).

100% RH

Effect of inoculum population on attachment ofSalmonella on tomatoes.

Iturriaga et al., 2003

Red, ripe

No

Salmonella Enteritidis IFO-3313, SE-1, SE-3, SE-4 (Chicken feces); SE-2 (Bovine feces) (Japan)

100 µl spot inoculated

30 min

Calcinated calcium 0.5% (wt/vol)

200 ppm chlorine water

Sterile distilled water

22

7.36–7.46 log CFU/tomato for Salmonella

Reduction: Treatment with 200 ppm chlorine and calcinated calcium resulted in 2.07 and 7.36 log CFU/tomato .

Antimicrobials were sprayed on.

 

Bari et al., 2002

Lycopersicon esculentum

No

S. Agona (Alfalfa sprouts)

S. Baildon (Tomato)

S. Montevideo (Tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

100ml spot inoculated and air dried 20–22 h at 22°C

(min)

0

6

12

25

ClO2 gas (mg/liter)

1.4

2.7

4.1

22

8 log CFU/tomato

Reduction (log CFU/tomato):

1.11

2.04

4.33

Relative humidity: 34-62%

 

Sy et al., 2005

Hydroponic

(Lycopersicon esculentum)

Unknown

S. Javiana (Tomato)

S. Baildon (Tomato)

S. Montevideo (Tomato)

100ml spot inoculated and air dried 2 h at 22°C

(min)

0

12

ClO2 gas (mg/liter)

0.1

0.3

0.5

22

8–9 log CFU/tomato before drying and 7–8 log CFU/cm2 after drying

Reduction (log CFU/cm2):

~2.5–3.0

~3.0

>5

Relative humidity: 85–90%

 

Bhagat et al., 2010

Hydroponic

(Lycopersicon esculentum)

Unknown

Listeria monocytogenes LCDC 81-861 (Coleslaw/cabbage) and F4244 (Ice cream)

100ml spot inoculated and air dried 2 h at 22°C

(min)

0

12

ClO2 gas (mg/liter)

0

0.1

0.3

0.5

22

8–9 log CFU/tomato before drying and 7–8 log CFU/cm2 after drying

Reduction:

L. monocytogenes ~3.5, ~4.5, >5 log CFU/cm2

Relative humidity: 85–90%

 

Bhagat et al., 2010

Round, unripe, green ‘Florida 47’

No

Cocktail of:

S. Agona

S. Gaminara

S. Michigan

S. Montevideo

S. Poona (University of California –Davis – L. Harris)

Rifampicin resistant

Puncture: 10 µl aliquot inoculum

Shaved, stem scars, and intact surfaces: 100 µl aliquot inoculum

(s)

30

60

120

150 ppm free chlorine, pH 6.5

25

35

At 25°C: 6.52 to 6.77 log CFU/ml

At 30°C:5.77 to 6.49 log CFU/ml

Reductions at 120 s:

At 25°C, Stem 1.86 log CFU/ml, Scrape 1.42 log CFU/ml, Puncture 0.73 log CFU/ml, Intact 6.36 log CFU/ml

At 30°C, Stem 1.0 log CFU/ml, Scrape 0.56 log CFU/l, Puncture 0.71 log CFU/ml, Intact 4.85 log CFU/ml

 

Salmonellarecovery was tested on four surface types: intact, punctures, shaves, and stem scars.

Felkey et al., 2006

Round, unripe, green ‘Florida 47’

No

S. Agona

S. Gaminara

S. Michigan

S. Poona

S. Montevideo

Ten-10 µl aliquot, spot inoculated around blossom scar

(d)

0

1

3

7

11

14

21

28

 

20

30

4.6–5.1 log CFU/ml

Reduction by day 28:

At 20°C/60% RH, 3.1 log CFU/ml

At 20°C/90% RH, 3.2 log CFU/ml

At 30°C/80% RH, 5 log CFU/ml

Relative humidity (%):

60, 80, 90

 

Allen et al., 2005

Lightly waxed, mature green

Unknown

S. Montevideo (Tomato)

S. Michigan (Cantaloupe)

S. Poona (Cantaloupe)

S. Hartford Orange juice

S. Enteritidis (Eggs) (CDC)

Ampicillin resistant, inoculated 50ml near the blossom end of the tomato

Tomatoes were analyzed after storage for (d)

0

1

2

4

7

10

14

NA

20

7.72 log CFU/tomato

Reduction of ~4 log CFU/tomato by day 14

70% RH

Determine the survival characteristics of Salmonella inoculated on tomato surfaces following storage at 20°C.

Guo et al., 2002 JFP

Lightly waxed, mature green

Unknown

S. Montevideo (Tomato)

S. Michigan (Cantaloupe)

S. Poona (Cantaloupe)

S. Hartford Orange juice

S. Enteritidis (Eggs) (CDC)

Ampicillin resistant, inoculated 50ml near the blossom end of the tomato

Tomatoes were analyzed after storage for (d)

0

1

2

4

7

10

14

NA

20

7.77–8.15 CFU/g

Growth of 2.5 log CFU/tomato at 4–10 days

 

Study attachment and infiltration of Salmonella into tomatoes placed on the surface of water-saturated soil inoculated with the pathogen.

Guo et al., 2002 JFP

Mature green

(Lycopersicon esculentum cv Agriset, and Lycopersicon esculentum cv Solimar), stored at RT until ripe

Unknown

S. Montevideo G4639 (CDC)

Rifampicin resistant

25 µl spot inoculated

NA

NA

Room temp.

Four groups of 5 tomatoes each were inoculated on the stem scars with a bacterial population of 4.4 × 103, 5.4 × 104, 6.6 × 105, or 5.0 × 106 CFU in 25 µl

Detection:

1st set, 33–95% detectable on 103–106 CFU

2nd set, 10–45% on 105–106 CFU

3rd set, no detection

 

Bacterial transfer by using a cutting knife from inoculated to uninoculated tomatoes. Bacteria were transferred by using a cutting knife from inoculated to uninoculated tomatoes at high CFU.

Lin and Wei, 1997

Mature green

(Lycopersicon esculentum cv Agriset, and Lycopersicon esculentum cv Solimar), stored at RT until ripe

Unknown

S. Montevideo G4639 (CDC)

Rifampicin resistant

25 µl spot inoculated

NA

NA

Room temp.

25 µl 2.8 × 102, 2.8 × 103, 2.8 × 104 or 2.8 × 105 CFU/ml in butterfield phosphate buffer or tryptic soy broth was placed on the stem scars of 10 tomatoes to yield a final population of 7, 70, 700, or 7,000 CFU.

Detection:

3.8–36% detectable by direct plating for 70–7,000 CFU, no detection for 7 CFU, 4.2–94% detectable after 6 h enrichment for 7–7,000 CFU

 

Determination of the rate of bacterial detection following cutting of inoculated tomatoes: introduction and/or transfer of bacterial contaminants by using a cutting knife could occur at a bacterial population as low as <10 CFU at the stem scar.

Lin and Wei, 1997

Mature green

(Lycopersicon esculentum cv Agriset, and Lycopersicon esculentum cv Solimar), stored at RT until ripe

Unknown

S. Montevideo G4639 (CDC)

Rifampicin resistant

25 µl spot inoculated

NA

NA

Room temp.

Four tomatoes were each inoculated with 6.25 × 103, 6.25 × 104, or 9.5 × 105 CFU in 25 µl at stem scar.

Detection:

At the lower inoculum dose of 6.25 x 103 CFU, S. Montevideo colonies were found to cluster at the stem scar region on TSA-RIF plates.

However, as the inoculum levels were increased, the colonies were found to spread from the stem scar region to the center and bottom of cut tomatoes along the cutting direction of the knife.

 

Bacterial distribution on the cut surface of tomato halves.

Lin and Wei, 1997

Green

(‘Florida 47’ cultivar)

No

S. Agona

S. Gaminara

S. Michigan

S. Montevideo

S. Poona (University of California - Davis – L. Harris)

Rifampicin resistant, spot inoculated

(s)

60

20 treatment and 5 d study

200 ppm chlorine (pH 6.5)

35

30–100 µL of inoculums of 108 to 109 CFU/mL Salmonella cocktail

Reduction of 96.19 – >99.99 % at 120 sec on day 5

 

Effectiveness of 200 ppm chlorine (pH 6.5) treatment on smooth surface, stem scar tissue, and puncture wound of tomatoes.

Yuk et al., 2005

Green

(‘Florida 47’ cultivar)

No

S. Agona

S. Gaminara

S. Michigan

S. Montevideo

S. Poona (University of California - Davis – L. Harris)

Rifampicin resistant

Spot inoculated

(s)

60

20 treatment and 5 d study

1,200 ppm acidified sodium chlorite (ASC; pH 2.5)

35

30-100 µL of inoculums of 108 to 109 CFU/mL Salmonella cocktail

Reduction of 98.05 – >99.99 % at 120 sec on day 5

 

Effectiveness of 1200 ppm acidified sodium chlorite wash on smooth surface, stem scar tissue, and puncture wound of tomatoes.

Yuk et al., 2005

Green

(‘Florida 47’ cultivar)

No

S. Agona

S. Gaminara

S.Michigan

S. Montevideo

S. Poona

(University of California - Davis – L. Harris)

Rifampicin resistant

Spot inoculated

(s)

60

20 treatment and 5 d study

87 ppm peroxyacetic acid (PAA)

35

30–100 µL of inoculums of 108to 109CFU/mL Salmonella cocktail

Reduction of 94.79 – >99.99 % at 120 sec on day 5

 

Effectiveness of 87 ppm peroxyacetic acid treatment on smooth surface, stem scar tissue, and puncture wound of tomatoes.

Yuk et al., 2005

Green

(‘Florida 47’ cultivar)

No

S. Agona

S. Gaminara

S.Michigan

S. Montevideo

S. Poona

(University of California - Davis – L. Harris)

Rifampicin resistant

Spot inoculated

1 h treatment and 5 d study

100 mg chlorine dioxide (ClO2) gas treatment

35

30–100 µL of inoculums of 108to 109CFU/mL Salmonella cocktail

Reduction of 99.35 – >99.99 % at 120 sec on day 5

 

Effectiveness of chlorine dioxide (ClO2) gas treatment on smooth surface, stem scar tissue, and puncture wound of tomatoes.

Yuk et al., 2005

Green

(‘Florida 47’ cultivar)

No

S. Agona

S. Gaminara

S. Michigan

S. Montevideo

S. Poona (University of California - Davis – L. Harris)

Rifampicin resistant

Spot inoculated

NA

200 ppm chlorine (pH 6.5), a 1200 ppm acidified sodium chlorite (ASC; pH 2.5), a chlorine dioxide (ClO2) gas treatment

35

30–100 µL of inoculums of 108 to 109 CFU/mL Salmonella cocktail

Reduction of 99.245 – >99.99 % at 120 sec on day 5

2 min in the chlorine bath (200 ppm, 35°C, pH 6.5) as the initial treatment, followed by a 30 s washing in acidified sodium chlorite (1200 ppm, 35°C, pH 2.5), and then tomatoes were treated with chlorine dioxide gas for 1 hour at room temp. (23°C ± 2°C) in a 22-quart vessel

Effectiveness of combination treatment on smooth surface, stem scar tissue, and puncture wound of tomatoes.

Yuk et al., 2005

Mature green

(Sunny cultivar)

No

S. Montevideo G4639 (CDC)

Batches of tomatoes (18 to 20) were submerged and constantly agitated in the bacterial suspension for 2 min and were then air dried in a laminar flow hood at 22°C for 4 h.

Storage

(d)

1

2

4

7

9

15

18

NA

10

20

30

~1.5 log CFU/cm2

Growth: Pathogen did not change significantly on tomatoes stored at 10°C throughout the 18-day storage period.

Significant increases in the population ofS. Montevideo occurred within 7 days and within 1 day when tomatoes were stored at 20 and 30°C, respectively.

A 3 log CFU/cm2growth at 30C

Relative humidity 45–60%

Fate ofS. Montevideo on tomato surfaces.

Zhuang et al., 1995

Mature green

(Sunny cultivar)

No

S. Montevideo G4639 (CDC)

10 tomatoes were submerged and constantly agitated for 2 min, dried, placed in plastic bags, and stored at 10 or 20°C.

Storage (d) at 10°C

1

3

5

8

At 20°C

(d)

1

3

5

8

18

NA

10

20

~4.5 log CFU/g

Growth:

A significantly higher number of S. Montevideo cells were taken up by core tissue when tomatoes at 25°C were dipped in suspension at 10°C compared with the number of cells taken up by tomatoes dipped in suspensions at 25 or 37°C.

Tomatoes remained essentially constant throughout subsequent storage for 18 days at 10°C. Storage of tomatoes at 20°C resulted in significant increases in the population ofS. Montevideo in core tissues within 3, 5, and 18 days of storage of tomatoes that had been dipped in suspension at 10, 25, and 37°C.

 

Uptake ofS.Montevideo by core tissue. Effect of temp. differential between tomatoes (25°C) and dip suspension (10, 25, or 37°C) on uptake ofS. Montevideo by core tissue, and effect of subsequent storage temp. (10 or 20°C) on survival.

Zhuang et al., 1995

Mature green

(Sunny cultivar)

No

S. Montevideo G4639 (CDC)

Batches (18 to 22) of tomatoes were submerged in the suspension, constantly agitated for 2 min, air dried for 5 h, and stored at 25°C for 18 h.

2-min treatment

Free Cl2 (ppm)

60

110

210

320

NA

~4.95 log CFU/cm2 on surface and unknown in core

Reduction:

Dipping in a solution containing 320 ppm chlorine for 2 min resulted in approximately 1.5 log reduction in the number of viable S. Montevideo on the surfaces of tomatoes.

Concentrations of 110 to 320 ppm significantly reduce the number of viable cells.

 

Efficacy of chlorine for inactivating S. Montevideo.

Zhuang et al., 1995

Freshly-harvested

Unripened (green), and ripened

Unknown

Separately:

S. Javiana 5913 (Chicken feces)

S. Javiana 6027 (Bovine feces)

S. Montevideo (Tomato)

S. Newport (Alfalfa sprouts)

S. Enteritidis (Egg)

S. Hadar (Poultry house)

S. Typhimurium (Pork slaughter line)

S. Dublin (Raw milk)

S. Senftenberg (Alfalfa sprouts)

S. Infantis (Clinical isolate) (University of Guelph Culture Collection)

(d)

7

14

NA

15

25

106 CFU/ml

Growth (internal and external) was promoted at the high incubation temp. (25°C) and high relative humidity (95%), although this was serovar dependent. The growth and persistence of Salmonella introduced on and into ripened (red) tomatoes was serovar dependent. Salmonella serovars Enteritidis, Typhimurium, and Dublin were less adapted to grow in or on intact red tomatoes than were serovars Hadar, Montevideo, or Newport.

Vacuum chamber (operating at 103Pa), 75 or 95% RH

Inoculation of tomato fruit on surface and internally .

Shi et al., 2007

Mature, red, ripe tomato; green tomato; ripened tomatillo (Physalis ixocarpa)

Unknown

S. Montevideo (Tomato) (University of Georgia)

Rifampicin resistant

100ml spot inoculated

90 min

NA

12

22

30

7 log CFU/fruit

Population ranged from 4.0 to 5.4 log CFU/fruit).

Temp. and RH alone did not affect the number of cells attached to the tomato or tomatillo surface.

Both the type of product and interaction of temp. and RH showed a significant effect on the attachment of Salmonella Montevideo to the surface of tomatoes and tomatillos.

Relative humidity (%): 75, 85, 97

Influence of relative humidity, temp., and stage of ripening on attachment of Salmonella to tomatoes and tomatillos.

Iturriaga et al., 2003

Mature green through fully red tomatoes of the Sunny variety

Unknown

S. Montevideo G4639 (CDC)

Rifampicin resistant

25-µl aliquots on the stem scar of each tomato

30 s

1 min

2 min

Free chlorine (ppm) 100

Room temp.

8.09 log CFU/tomato skin circle in DI

3.25 log CFU/tomato skin circle in TSB

Low 3.98 log CFU/stem scar in DI

High 8.09 log CFU/stem scar in DI

Reduction:

After 2 min, 1.09 (DI) to 5.95 (TSB) log CFU/tomato skin circle and Low 1.27 log CFU/stem scar

After 1 min, High 1.66 log CFU/stem scar

 

Efficacy of aqueous chlorine solutions against populations of S. Montevideo located on the surface, wounded areas, or stem scars of tomatoes.

Wei et al., 1995

Mature green through fully red tomatoes of the Sunny variety

Unknown

S. Montevideo G4639 (CDC)

0.5 ml aliquot added

30 s

1 min

2 min

Free chlorine (ppm)

50

75

100

Room temp.

Tryptic soy broth: 3.72, 5.99, 9.07 log CFU/ml

Butterfield buffer: 9.34 log CFU/ml

DI: 9.36 log CFU/ml

Reduction:

After 2 min for TSB, 2.60 (75 ppm), 3.61 (75 ppm), 7.18 (100 ppm) log CFU/ml

Buffer, 8.49 log CFU/ml (100 ppm)

DI, 8.36 log CFU/ml (100 ppm)

 

Efficacy of aqueous chlorine against S. Montevideo populations suspended in distilled water, in growth medium, or on the dried surface of glass beads (a model for cellular attachment or embedding in particulates).

Wei et al., 1995

Mature green through fully red tomatoes of the Sunny variety

Unknown

S. Montevideo G4639 (CDC)

25 µl aliquot added

Growth

(h)

18

24

48

Survival

(d)

1

2

3

7

NA

Growth 25°C

Survival 20°C

25°C

Growth: 9.06 log CFU/ml to 9.48 CFU/ml

Survival: 25 µl of low 4.76, medium 5.76, or high 8.76 log CFU/ml, which dried up to be 3.16, 4.16, and 7.16 log CFU/ml

Growth:

Low ~1.75 log CFU/wounded area growth

Medium ~0.4 log CFU/wounded area

High no growth. Ripeness had no apparent effect on bacterial growth.

Survival, relative humidity: 83 and 72%

Determine the ability of S. Montevideo to grow and/or survive on tomato surfaces, including the unbroken skin, wounded areas, growth cracks, or stem scars.

Wei et al., 1995

Roma

(Lycopersicon esculentum)

Unknown

A 3-strain mixture of E. coli O157:H7 (C7927, EDL933, and 204P)

Spot inoculated

NA

X-ray (# kGy/16 min)

0.1

0.5

0.75

1.0

1.5

22

Three or two strains of each bacterium were mixed with an equal volume to give approximately 107-9 CFU/ml.

Reduction:

~ 4.2 log CFU/tomato reduction of E. coli O157:H7 were achieved by treatment with 0.75 kGy X-ray. More than a 5 log CFU/tomato reduction was achieved at 1.0 or 1.5 kGy X-ray for all tested pathogens.

Relative humidity: 55–60%

Inactivation of inoculated Escherichia coli O157:H7 on whole Roma tomato surfaces.

Mahmoud, 2010

Vine-ripened

(Lycopersicon Esculentum Mill. cv Rutgers)

No

E. coli O157:H7 strains LJH557 (Apple cider), SEA-13B88 (Apple cider), CDC-658 (Cantaloupe), H1730 (Lettuce), and F4546 (Alfalfa sprouts)

50ml spot inoculated or dip inoculated in 5 liters for 1 min or 50ml spray inoculated for 2 sec with thin-layer chromatography reagent sprayer at 22°C for 1 or 24 h

Agitated at 150 rpm for 5 min

Chlorine (200 mg/ml) solution

NA

Spot and spray inocula to each tomato were 7.21, log CFU/ml.

Dip could not be determined.

Reduction:

Spot inoculation was reduced by 1.07 and 3.17 log CFU/ml after drying times of 1 and 24 h.

Spray-inoculated tomatoes were 1.03 and 4.34 log CFU/ml at 1 and 24 h, no recovery from chlorine.

 

Evaluate methods for applying inoculum and to examine the effect of inoculum drying time on survival and recovery of foodborne pathogens inoculated onto the surface of raw, ripe tomatoes.

Lang et al., 2004

Firm tomato at the light-red stage of ripeness, free of external defects

Unknown

E. coli NRRL B-766 (ATCC 9637), a nonpathogenic surrogate for Salmonella (USDA-ARS-NCAUR - L.K. Nakamura)

(min)

2

3

5

5% H2O2

60

9.71 log CFU/ml

Reduction of 0.95–1.90 log CFU/g

 

Effect of treatment time and surfactant addition on efficacy of 5% H2O2 in reducing population of E. coli NRRL B-766 on dip-inoculated tomatoes held 24 h at 20°C prior to treatment.

Sapers and Jones, 2006

Firm tomato at the light-red stage of ripeness, free of external defects

Unknown

E. coli NRRL B-766

(ATCC 9637), a nonpathogenic surrogate for Salmonella (USDA-ARS-NCAUR – L.K. Nakamura)

(h)

24

48

1% or 5 % H2O2 (2 min or 15 min)

20

60

5.62 log CFU/g (48 h)

Reduction of 1.12 to 2.04 log CFU/g (48 h)

 

Efficacy of H2O2 in reducing the population of E. coli NRRL B-766 on dip-inoculated tomatoes, as affected by post-inoculation storage at 20°C.

Sapers and Jones, 2006

Firm tomato at the light-red stage of ripeness, free of external defects

Unknown

E. coli NRRL B-766 (ATCC 9637), a nonpathogenic surrogate for Salmonella (USDA-ARS-NCAUR - L.K. Nakamura)

48 h

200 ppm chlorine

4

3.98 log CFU/mL

Reduction of 1.16 CFU/g

 

Efficacy of water rinse and 200 ppm Cl2 treatment in reducing the population of E. coli NRRL B-766 on dip-inoculated tomatoes, as affected by post-inoculation storage at 4°C.

Sapers and Jones, 2006

Red, ripe

No

E. coli O157:H7

CR-3, MN-28, MY-29, DT-66 (Bovine feces) (Japan)

100 µl spot inoculated

30 min

Calcinated calcium 0.5% (wt/vol), 200 ppm chlorine water, or sterile distilled water

22

7.63–7.85 log CFU/tomato for E. coli O157:H7

Reduction:

Treatment with 200 ppm chlorine and calcinated calcium resulted in 3.40 and 7.85 log reductions of E. coli O157:H7, respectively.

Antimicrobials were sprayed on.

 

Bari et al., 2002

Roma

(Lycopersicon esculentum)

Unknown

A 3-strain mixture of L. monocytogenes (Scott A, F5069 and LCDC 81-861)

Spot inoculated

NA

X-ray (# kGy/16 min)

0.1

0.5

0.75

1.0

1.5

22

Three or two strains of each bacterium were mixed with an equal volume to give approximately 107-9CFU/ml

Reduction:

~2.3 log CFU/tomato reduction of L. monocytogenes were achieved by treatment with 0.75 kGy X-ray, respectively.

More than a 5 log CFU/tomato reduction was achieved at 1.0 or 1.5 kGy X-ray for all tested pathogens.

Relative humidity: 55–60%

Inactivation of inoculatedListeria monocytogeneson whole Roma tomato surfaces.

Mahmoud, 2010

Vine-ripened

(Lycopersicon esculentum Mill., cv Rutgers)

No

L. monocytogenes strains G1091 (Coleslaw), F8255 (Peach/plum), F8369 (Corn), HO222 (Potato), and F8027 (Celery)

50ml spot inoculated or dip inoculated in 5 liters for 1 min or 50ml spray inoculated for 2 sec with thin-layer chromatography reagent sprayer at 22°C for 1 or 24 h

Agitated at 150 rpm for 5 min

Sterile deionized water (control) or chlorine (200 mg/ml) solution

NA

L. monocytogenes spot and spray inocula to each tomato were 7.37 log CFU/ml.

Dip could not be determined.

Reduction:

Spot reduced by 1.00 and 1.54 log CFU/ml within 1 and 24 h.

Reductions on spray-inoculated tomatoes were 0.52 and 1.45 log CFU/ml for 1 and 24 h.

 

L. monocytogenes is known to be more resistant than E. coli O157:H7 and Salmonella to stresses. Higher numbers of cells were recovered from dip-inoculated tomatoes compared with spot- or spray- inoculated tomatoes, regardless of drying time or treatment.

Lang et al., 2004

Red, ripe

No

Listeria monocytogenes ATCC 43256, ATCC 49594, JCM 7676, JCM 7672, JCM 7671

100 µl spot inoculated

30 min

Calcinated calcium 0.5% (wt/vol)

200 ppm chlorine water sterile distilled water

22

7.54 -7.59 log CFU/tomato for L. monocytogenes

Reduction:

Treatment with 200 ppm chlorine and calcinated calcium reduced L. monocytogenes numbers by 2.27 and 7.59 log CFU per tomato, respectively.

Antimicrobials were sprayed on

 

Bari et al., 2002

Roma

Untreated (no washing, oiling, or waxing)

No

E. carotovora ATCC 495, ATCC 15359, ATCC 25272

300 µl spot inoculated

(s)

2

4

6

10

ClO2 – (ppm)

(High)

20

10

5

(Low)

0

1

3

5

10

23

7 log CFU/ml E. carotovora

Reduction:

A full minute of contact with ClO2 at 20 and 10 ppm was required to achieve a 5 log reduction of E. carotovora on freshly spot-inoculated tomatoes.

Immersing wet-inoculated tomatoes in water (0 ppm ClO2) for 1 min alone reduced E. carotovora by about 1.9 log CFU/cm2.

On inoculated fruit surfaces, populations decreased>3 log CFU/cm2 during desiccation at 24°C for 24 h.

Populations of air-dried Erwinia were not significantly reduced by ClO2 at ≤20 ppm after 1 min.

For each treatment, nine inoculated tomatoes were immersed in 2 liters of ClO2 or water for 20 to 60 s.

Relative humidity: 40–50%

Researchers investigated the sanitizing effects of a ClO2 solution on E. carotovora in water, on tomato surfaces, and between tomato loads.

Pao et al., 2007

Roma, diced at the light-red to red stages

Unknown

S.Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Canataloupe)

S. Montevideo (Tomato)

Acid- and non-acid adapted environment, 5ml inoculation of inoculums in 450 g diced tomatoes

(d)

0

3

6

9

NA

4

12

21

Acid low 0.88 log CFU/g

Acid high 2.88 log CFU/g

No acid low 0.99 log CFU/g

No acid high 2.99 log CFU/g

Growthat 10 days for:

Acid low at 12°C and 21°C, ~1.32 and ~8.22 log CFU/g.

Acid high at 12°C and 21°C, ~3.62 log CFU/g and ~5.32 log CFU/g.

No acid low at 12°C and 21°C, ~1.61 log CFU/g and ~7.71 log CFU/g.

No acid high at 12°C and 21°C, ~3.81 CFU/g, and ~4.81 log CFU/g

 

Survival and growth of acid-adapted and not acid-adapted cells in diced Roma tomatoes.

Beuchat and Mann, 2008

Diced

Unknown

Separately:

S. Enteritidis NVI 153 (Cow)

S. Infantis NVI 110 (Broiler chicken)

S. Typhimurium NVI 199 (Broiler chicken) (Finland)

Spot inoculated

6

24

48

NA

7 (only 48 h)

22

30

1–2 × 102 CFU/g

Growth:

S. Infantis - No growth at 7°C; At 48 h, 2.4 × 108 CFU/g at 22°C, and 4.5 × 107 CFU/g at 30°C.

S. Enteritidis - No growth at 7°C; At 48 h, 8 × 108 CFU/g at 22°C, and 6 × 107 CFU/g at 30°C.

S. Typhimurium - No growth at 7°C; At 48 h, 1.1 × 108 CFU/g at 22°C, and 5 × 107 CFU/g at 30°C.

   

Asplund and Nurmi, 1991

Diced, Round, red, ripened tomato

Unknown

S. Braenderup (Tomato) (CDC)

Diced tomatoes at room temp. (22°C) were spot inoculated (at stem scar) with 0.1 ml of inoculum.

120 s

High pressure processing (MPa)

350

450

550

20

Diced, 5.93 log CFU/g

Reduction:

550 MPa Diced, 3.65 log CFU/g reduction

 

To determine the effect of pressure to reduce or remove S. enterica from whole red Round tomatoes.

Maitland et al., 2011

Diced grape tomato Lycopersicon esculentum mill.

Unknown

S. Poona (Cantaloupe)

S. Stanley H 1256 (Alfalfa sprouts)

S. Baildon (Tomato)

S. Typhimurium DT 104 (Resistant to multiple antibiotics)

S. Montevideo (Tomato) (University of Georgia – M. Harrison)

Spot inoculated 100 µl

At 4°C and 10°C (d)

0

4

7

10

At 25°C (h)

0

4

7

10

Allyl isothiocyanate (AIT, from mustard and horseradish)

Carvacrol (from oregano)

Cinnamaldehyde (from cinnamon)

5, 10, and 15 µl (equivalent to 41.5, 83.3, and 125 µl/liter of air, respectively) of ≥97% pure carvacrol or ≥98% pure cinnamaldehyde or 1, 2, and 4 µl (equivalent to 8.3, 16.6, and 33.3 µl/liter of air, respectively) of ≥98% pure AIT

4

10

25

Sliced tomatoes, 100 µl 6.7 log CFU/ml placed on 10 separate spots

Reduction:

AIT exhibited the highest antimicrobial activity followed by cinnamaldehyde. The lowest level of AIT (8.3 µl/liter of air) inactivated Salmonella on sliced tomatoes by 1.0 and 3.5 log at 4 and 10°C, respectively, in 10 days and by 2.8 log at 25°C in 10 h.

Overall, greater inactivation occurred at 10 than at 4°C and on the tomato surface than between slices.

 

Elucidate the effect of antimicrobials' activity on pathogen inactivation on tomato skin (using whole tomatoes).

Obaidat and Frank, 2009

Stem scar tissue

light red, Round

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

Acid- and non-acid adapted environment, 20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid-adapted cells: Round, light red, 2.05 and 1.84 CFU/g

Growth at 10 days for Light red, Round:

Acid-adapted stem at 12°C and 21°C, ~2.05 log CFU/g and ~4.05 log CFU/g

Not acid-adapted stem at 21°C and 21°C, ~0.76 log CFU/g and ~2.66 log CFU/g

 

Survival and growth of acid-adapted and not acid-adapted cells in Round tomatoes.

Beuchat and Mann, 2008

Stem scar tissue of light-red Roma

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

Acid- and non-acid adapted environment, 20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid-adapted cells: Roma, light red, 2.00 and 2.01 CFU/g

Growth at 10 days, Roma light red:

Acid-adapted stem at 12°C and 21°C, ~1.5 log CFU/g and ~3.8 log CFU/g

Not acid-adapted stem at 21°C and 21°C, ~2.29 log CFU/g and ~4.19 log CFU/g

 

Survival and growth of acid-adapted and not acid adapted cells in Roma tomatoes.

Beuchat and Mann, 2008

Stem scar tissues of Round and Roma, initially at the turning and/or pink stages of ripeness

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

20ml syringe inoculated

12°C (d)

0

3

6

10

14

27

21°C (d)

0

3

6

10

14

NA

12

21

Pre-inoculation 4 log CFU/ml and post-inoculation 0.08 log CFU/g

Growth:

Salmonella increased significantly in the stem scar of tomatoes stored at both temps.

Higher populations (4.9 to 8.4 log CFU/g) were reached at 21°C than at 12°C (3.3 to 4.9 log CFU/g) in tomatoes stored for 14 and 27 days, respectively

Tomatoes were held up to 27 days at 12 or 21°C with 15 and 36% relative humidity before experiment.

Survival and growth of Salmonella in Round and Roma tomatoes.

Beuchat and Mann, 2008

Stem scar on the skin surface of grape tomato

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

Not adapted to acidic environment

20ml inoculated

14 d

NA

4

12

21

1.76 log CFU/ml (57 CFU/ml)

Growth at 14 days:

Stem at 12°C and 21°C, ~2.65 and ~4.05 log CFU/g

 

Survival and growth of Salmonella in and on grape tomatoes.

Beuchat and Mann, 2008

Stem scar tissue of green tomato

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

Acid- and non-acid adapted environment

20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid-adapted cells: Green, 2.03 and 1.78 log CFU/g

Growthat 10 days for Green:

Acid-adapted stem at 12°C and 21°C, ~0.067 log CFU/g and ~1.77 log CFU/g

Not acid-adapted stem at 21°C, ~3.22 log CFU/g

 

Survival and growth of acid-adapted and not acid-adapted cells in green tomatoes.

Beuchat and Mann, 2008

Round - Pulp of light red

Unknown

S. Agona (Alfalfa sprouts)

S. Baildon (Diced tomato)

S. Gaminara (Orange juice)

S. Michigan (Cantaloupe)

S. Montevideo (Tomato)

Acid- and non-acid adapted environment

20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid-adapted cells: Round, light red, 2.05 and 1.84 CFU/g

Growth at 10 days for Light red Round:

Acid pulp at 12°C and 21°C, ~3.95 log CFU/ml and ~5.45 log CFU/ml

Not acid-adapted pulp at 12°C and 21°C, ~2.46 log CFU/g and ~5.56 log CFU/g.

 

Survival and growth of acid-adapted and not acid adapted cells in Round tomatoes.

Beuchat and Mann, 2008

Round and Roma tomato pulp (radial pericarp) initially at the turning and/or pink stages of ripeness

Unknown

S. Agona

S. Baildon

S. Gaminara

S. Michigan

S. Montevideo

20ml syringe inoculated

12°C (d)

0

3

6

10

14

27

21°C (d)

0

3

6

10

14

NA

12

21

Pre-inoculation 4 log CFU/ml, and post-inoculation 0.08 log CFU/g

Growth:

Salmonella increased significantly in the pulp tissues of tomatoes stored at both temps.

Higher populations (4.9 to 8.4 log CFU/g) were reached at 21°C than at 12°C (3.3 to 4.9 log CFU/g) in tomatoes stored for 14 and 27 days, respectively.

Tomatoes were held up to 27 days at 12 or 21°C with 15 and 36% relative humidity before experiment.

Survival and growth of Salmonella in Round and Roma tomatoes.

Beuchat and Mann, 2008

Pulp of light-red Roma tomato

Unknown

S. Agona

S. Baildon

S. Gaminara

S. Michigan

S. Montevideo

Acid- and non-acid adapted environment

20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid adapted cells: Roma light red 2.00 and 2.01 CFU/g

Growth at 10 days Roma light red:

Acid-adapted pulp at 12°C and 21°C, ~3.5 log CFU/ml and ~6.0 log CFU/ml

Not acid-adapted pulp at 12°C and 21°C, ~3.29 log CFU/g and ~5.19 log CFU/g

 

Survival and growth of acid-adapted and not acid-adapted cells in Roma tomatoes.

Beuchat and Mann, 2008

Pulp tissues on the skin surface of grape tomato

Unknown

S. Agona

S. Baildon

S. Gaminara

S. Michigan

S. Montevideo

Acid- and non-acid adapted environment

20ml syringe inoculated

14 d

NA

4

12

21

1.76 log CFU/ml (57 CFU/ml)

Growth at 14 days:

Pulp at 12°C and 21°C, ~3.35 and ~4.85 log CFU/g

 

Survival and growth ofSalmonellain and on grape tomatoes.

Beuchat and Mann, 2008

Pulp of green tomato

Unknown

S. Agona

S. Baildon

S. Gaminara

S. Michigan

S. Montevideo

Acid- and non-acid adapted environment

20ml syringe inoculated

(d)

0

3

6

10

NA

12

21

Acid-adapted and not acid-adapted cells: Green 2.03 and 1.78 log CFU/g

Growth at 10 days for Green:

Acid-adapted pulp at 12°C and 21°C, ~1.47 log CFU/ml and ~3.77 log CFU/ml

Not acid-adapted pulp at 12°C and 21°C, ~1.52 log CFU/g and ~4.02 log CFU/g.

 

Survival and growth of acid-adapted and not acid-adapted cells in green tomatoes.

Beuchat and Mann, 2008

Salsa with either fresh Roma tomato or canned whole tomato, different salsa recipes

Unknown

S. Typhimurium, DT 104 (Beef isolate) and PTC 1 (Poultry isolate)

two S. Enteritidis, H4639 (Clinical isolate) and MH24981 (Environmental isolate)

one S. Heidelberg, MH27651 (Turkey isolate)

100ml spot inoculated

(d)

0

1

2

3

7

NA

21

5-6 log CFU/tomato

Salsa, depending on its ingredients, could be inhibitory to, or support the survival and possibly growth of, Salmonella during storage.

Salsa can be formulated with ingredient combinations such as lime juice plus fresh garlic to prevent or suppress the growth of Salmonella.

Inoculated whole tomatoes, then chopped them

Fate of Salmonella in salsas.

Ma et al., 2010

Salsa, ripened Roma tomato, intact

Unknown

S. Typhimurium, DT 104 (Beef isolate) and PTC 1 (Poultry isolate)

two S. Enteritidis, H4639 (Clinical isolate) and MH24981 (Environmental isolate)

one S. Heidelberg, MH27651 (Turkey isolate)

20ml spot inoculated, air dried 1 h RT

(d)

0

1

2

5

7

NA

4

12

21

Inoculated at 5.36 log CFU/g and after spot-inoculation was 2.47 log CFU/g

Growth on surface of raw whole tomato:

At 21°C, 4-5 log CFU/g growth

No growth observed at 4 and 12°C

Relative humidity: 55-65%

Inoculated whole tomatoes, then chopped them

Survival and growth of Salmonella on intact tomato, jalapeo, and cilantro.

Ma et al., 2010

Salsa, ripened Roma tomato, diced

Unknown

S. Typhimurium, DT 104 (Beef isolate) and PTC 1 (Poultry isolate)

two S. Enteritidis, H4639 (Clinical isolate) and MH24981 (Environmental isolate)

one S. Heidelberg,

MH27651 (Turkey isolate)

100ml spot inoculated

(d)

0

1

2

5

7

NA

4

12

21

~4 log CFU/g

Growth on chopped tomato:

No growth at 4°C (kept at 3-4 log CFU/g)

Growth at 12°C at 6.02 log CFU/g and a decrease in growth at <1 log CFU/g (day 2) at 21°C

 

Survival and growth of Salmonella in chopped tomatoes, jalapeño peppers, and cilantro.

Ma et al., 2010

Restaurant-made salsa with red tomato

Unknown

S. Enteritidis

S. Typhimurium

S.Thompson ATCC 8391

Spot inoculated on salsa container

For 20°C

(h)

0

2

4

6

24

For 4°C

(d)

0

1

3

5

7

NA

20

4

15-20 CFU/sample

   

Comparison of detection methods between CHROMagar, XLD, and RapidCheck SELECT. RapidCheck SELECT was best to detect Salmonella under both temps. at all time points except 5 s, 7 d at 4°C.

Franco et al., 2010

Restaurant-made salsa with red tomato

Unknown

S.aureusATCC 29247, ATCC 12600-U, and ATCC 35548

Spot inoculated on salsa container

For 20°C

(h)

0

2

4

6

24

For 4°C

(d)

0

1

3

5

7

NA

20

4

Low (3.2 log CFU/g)

High (4.2 log CFU/g)

Reduction:

At 20°C, 1.1 log CFU/g for low and 0.6 log CFU/g for high

At 4°C, 1.7 log CFU/g for low and 2.5 log CFU/g for high

pH at 4°C ranged from 3.96 to 3.65

pH at 20°C ranged from 3.95 to 3.73

Survival study.

Franco et al., 2010

Cultivar Better Boy tomato seeds grown for 7 days or until cotyledons emerged

No

S. Montevideo (Tomato)

S. Michigan (Cantaloupe)

S. Poona (Cantaloupe)

S. Hartford (Orange juice)

S. Enteritidis (Eggs) (CDC)

All ampicillin resistant

Plants with intact or cut roots were then transferred to trays containing 4 liters of Hoagland solution inoculated with the five-serotype mixture.

7 d

NA

25°C

Hoagland solution modified to contain ampicillin (100 g/ml) in order to obtain a preparation containing 4.55 log CFU/ml

Detection:

Within 1 day of exposure of plant roots to nutrient solution containing ca. 4.5 log CFU of the pathogen/ml, populations were 3.0 log CFU/g of hypocotyls and cotyledons, and 3.4 log CFU/g of stems.

Populations > 3.4 log CFU/g of hypocotyl/cotyledon, stem, and leaf tissue of plants grown for 9 days were detected.

Hypocotyls, cotyledons, stem, leaves

Investigate the possibility of association of Salmonellae with hypocotyls, cotyledons, stems, and leaves of young plants grown in a hydroponic nutrient solution inoculated with the pathogen.

Guo et al., 2002 AEM

Tomato seeds

(Lycopersicon esculentum variety Abigail VFET)

Unknown

S. Javiana 5913 (Chicken feces)

S. Javiana 6027 (Bovine feces)

S. Montevideo (Tomato)

S. Newport (Alfalfa sprouts)

S. Enteritidis (Egg)

S. Hadar (Poultry house)

S. Typhimurium (Pork slaughter line)

S. Dublin (Raw milk)

S. Senftenberg (Alfalfa sprouts)

S. Infantis (Clinical isolate) (University of Guelph)

100 µl spot inoculated

6–7 weeks

NA

NA

100-µl aliquots of Salmonella suspension (107 CFU/ml) were introduced onto the flowers of the plants.

Detection:

The lowest recovery was observed for serovar Dublin (14%), and the highest was observed for Javiana 6027 (84%). Salmonella serovars introduced onto the flowers of growing plants were recovered on and within the developing tomato fruit.

Of all the Salmonella serovars tested, Montevideo appeared to be more adapted to survival within tomatoes and was recovered from 90% of the fruit screened.

Batches (five batches per serovar, three fruits per batch) were screened for the presence of Salmonella on the surface and in internal tissue.

Inoculation of tomato plants with Salmonella.

Shi et al., 2007

Tomato plants

‘Bonnie Select’

No

S. Montevideo ATCC 8387

Spot inoculated

48 h

NA

NA

6.6 log CFU/leaflet

Reductions of 3-4 log CFU/leaflet occurred when leaves were dried after inoculation.

When leaves were supported in a hydroponic nutrient medium and incubated at 100% RH, there was no significant reduction for at least six days.

Salmonella on the surface of excised leaves, leaf disks, and fruit pericarp disks under dry (60% RH) and high-humidity (100% RH) conditions

Examine the survival of Salmonella Montevideo on tomato leaves.

Rathinasabapathi, 2004

Tomato plants

‘Bonnie Select’

No

S. Montevideo ATCC 8387

Spot inoculation

6 d

 

20

 

No significant effect on the survival of Salmonella on leaf surfaces

100 ppm Ethylene at 100% RH

With high relative humidity and the addition of ethylene, it was examined for the pathogen’s survival on tomato leaves.

Rathinasabapathi, 2004

Tomato plants

‘Better Boy,’ harvested when red-ripe color was achieved

No

Separately:

S. Montevideo (Tomato)

S. Michigan (Cantaloupe)

S. Poona (Cantaloupe)

S. Hartford (Orange juice)

S. Enteritidis (Egg) (CDC)

Brushed by using a small paintbrush saturated with inoculum, or 25-gauge syringe needle stem injected

27–49 d

NA

NA

Open flower: 9 log CFU/ml

Stem injection before and after flowering: 7.5 log CFU/50ml

Detection:

Eleven of thirty tomatoes (37%) harvested from inoculated plants were positive for all Salmonella serotypes except S. Hartford. Presumptive Salmonella was detected in enriched samples of peptone wash water, stem scar tissue, and pulp of tomatoes from inoculated plants. Salmonella was detected on or in tomatoes from plants receiving stem inoculation before or after flower set and on or in tomatoes that developed from inoculated flowers.

 

Determine the fate of Salmonella inoculated into tomato stems and onto tomato flowers.

Guo et al., 2001

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Footnotes

1.

This document is FSHN12-06, one of a series of the Food Science and Human Nutrition Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Published May 2012, June 2012. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

Angela M. Valadez, graduate research assistant, CREC (Citrus Research and Education Center, Lake Alfred, FL); Keith R. Schneider, associate professor, FSHN (Food Science and Human Nutrition Department, UF Main Campus); Michelle D. Danyluk (contact author), assistant professor, CREC; Institute of Food and Agricultural Sciences; University of Florida; Gainesville, FL 32611.

This review was supported by USDA NIFA Specialty Crops Research Initiative Grant 2009-51181-05783 and the Center for Produce Safety.


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U.S. Department of Agriculture, UF/IFAS Extension Service, University of Florida, IFAS, Florida A & M University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Nick T. Place, dean for UF/IFAS Extension.