Food Control 110 (2020) 107005

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Food Control
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Inactivation of Salmonella in cherry tomato stem scars and quality T

preservation by pulsed light treatment and antimicrobial wash☆
Juncai Lenga,b, Sudarsan Mukhopadhyayb,∗, Kimberly Sokoraib, Dike O. Ukukuc, Xuetong Fanb,
Modesto Olanyac, Vijay Junejab
a
Key Laboratory of Food Nutrition and Safety, Ministry of Education of China, College of Food Engineering and Biotechnology, Tianjin University of Science and
Technology, Tianjin, 300457, PR China
b
Residue Chemistry & Predictive Microbiology Research Unit,U.S. Department of Agriculture, Agricultural Research Service, Eastern Regional Research Center, Wyndmoor,
PA, 19038, USA
c
Food Safety Intervention Technology Research Unit,U.S. Department of Agriculture, Agricultural Research Service, Eastern Regional Research Center, Wyndmoor, PA,
19038, USA

A R T I C LE I N FO A B S T R A C T

Keywords: The objective of this study was to evaluate the effectiveness of pulsed light (PL) treatment, a novel antimicrobial
Salmonella (LAPEN) wash and combinations thereof in inactivating Salmonella on stem scars of cherry tomato. The treat-
Antimicrobial ment effects on background microbiota and sensory quality was also investigated while in storage for 21 days at
Pulsed light 10 °C. Three serotypes of Salmonella enterica were chosen to prepare inoculum for the current investigation for
Tomato
their link with tomato and produce outbreaks. Stem scars of tomato were spot inoculated before being treated
Native microbiota
Quality
with PL (1–63 J/cm2), LAPEN sanitizer (2 min) or combinations of PL with LAPEN Sanitizer. Significant in-
activation was observed at low doses of PL. A 30 s treatment equivalent to a dose of 31.5 J/cm2, was found
optimal. The optimal dose provided 2.3 log reduction of Salmonella while a 2 min wash in LAPEN sanitizer
provided 2.1 log CFU/g reduction on stem scars. Two possible sequences of PL and LAPEN combinations were
explored. For PL-LAPEN combination, inoculated tomatoes were initially exposed to optimum PL dose (31.5 J/
cm2) and then washed 2 min in LAPEN sanitizer whereas for LAPEN-PL combination, tomatoes were initially
immersed 2 min in LAPEN prior to PL treatment. Treatment of PL-LAPEN demonstrated a strong synergistic
inactivation as no Salmonella survivor were detectable after treatment indicating greater than 5 log reduction,
whereas LAPEN-PL combination revealed a compound inactivation providing 4.5 logs reduction of the pathogen.
The PL-LAPEN treatment not only reduced native microbiota of tomato but also hindered their growth while in
storage for three weeks. The firmness and visual appearance quality of tomato were not significantly influenced
due to PL-LAPEN combination treatment until day 21, when the texture of treated tomato was significantly
influenced. Overall, the results reveal that PL-LAPEN combination treatment can be implemented as a novel
approach to enhance microbial safety and quality of cherry tomato.

1. Introduction increased consumption the number of tomato and produce related

Consumer preference for fresh fruits and vegetables are growing for
their nutrition and various other health benefits (Abete et al., 2013).
Tomatoes including cherry tomatoes are popular both as a fruit for
snaking purpose and as vegetable in salad dish. Due to the presence of a
variety of antioxidant and heart healthy compounds consumption of
tomato has increased (Raffo et al., 2002). Regrettably, due to the
outbreaks also escalated (Olaimat and Holley, 2012). Tomatoes, in-
cluding cherry tomatoes, been reported to be associated with salmo-
nellosis outbreaks in recent years (CDC, 2019). During 1996 to 2008,
tomatoes were linked with several incidences of food related illness
comprising for approximately 17% of entire produce associated out-
breaks of foodborne illness in the US (Gravani, 2009). Bacterial pa-
thogen linked with these verified salmonellosis cases was Salmonella

☆
Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation
or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.
∗
Corresponding author.
E-mail addresses: Juncai.leng@ars.usda.gov (J. Leng), Sudarsan.mukhopadhyay@ars.usda.gov (S. Mukhopadhyay), Kimberly.sokorai@ars.usda.gov (K. Sokorai),
Dike.ukuku@ars.usda.gov (D.O. Ukuku), Xuetong.fan@ars.usda.gov (X. Fan), modesto.olanya@ars.usda.gov (M. Olanya), Vijay.juneja@ars.usda.gov (V. Juneja).

https://doi.org/10.1016/j.foodcont.2019.107005
Received 3 September 2019; Received in revised form 22 October 2019; Accepted 13 November 2019
Available online 16 November 2019
0956-7135/ Published by Elsevier Ltd.
J. Leng, et al.
(Bidol et al., 2007), predominantly, serovars of Baildon, Typhimurium,
Newport, and Montevideo (Hanning, Nutt, & Ricke, 2009).
Contamination of tomato with Salmonella spp. may occur at any
point during the growing, harvesting or processing via multiple man-
ners as irrigation or wash water, bird or animal feces, composts or
manures, or workers contaminated with pathogens (Hanning et al.,
2009). Once contaminated, Salmonella may enter inside the fruit from
surface through surface cuts or wounds or through the stem or blossom
scars and can survive and multiply in the low pH of tomato (Asplund
and Nurmi, 1995; Beuchat and Mann, 2008). The precise moment of
contamination is usually unknown and at the time tomato arrive for
packing, it may contain a population of as high as 6 logs (Parnell,
Harris, & Suslow, 2005). Hence, postharvest intervention is very crucial
to avoid Salmonella contamination and to prevent outbreaks of food-
borne illness since Salmonella is reported to be resistant to decontami-
nation by simply water washing process (Aguiló-Aguayo, Charles,
Renard, Page, & Carlin, 2013). In order to avoid tomato-related out-
breaks, a broad spectrum of chemical sanitizers has been researched
with different extent of success (Beuchat, 1998). Current practice in
produce industry is use of chlorine containing sanitizers to minimize
bacterial load and reduce the chances of cross contamination. In prac-
tice, tomatoes are treated with 200 ppm free chlorine for 2 min in the
flume tanks before packing (Bartz et al., 2001). The fact that the
chlorine treatment efficacy is low to about 2 log reduction for patho-
gens like Salmonella (Yuk, Bartz, & Schneider, 2005) and that even a
higher concentration, as high as 320 ppm for 2 min, of chlorine is un-
able to inactivate Salmonella entirely (Zhuang, Beuchat, & Angulo,
1995), indicates the weakness of chlorine wash and stress the need for
efficacious alternate decontamination method for tomato. Also,
chlorine reacts with the organic matter (Solomon, Potenski, &
Matthews, 2002) present in wash water forming organochlorine com-
pounds and loses its decontamination ability in the process. The by-
product organochlorine is believed to be a carcinogen (Richardson
et al., 1998) and hence can raise regulatory concerns (Artes, Gomez,
Aguayo, Escalona, & Artes-Hernundez, 2009). Considering these issues
involving consumer safety, health and the underlying environmental
concerns, there is a strong demand for development of a chlorine free
decontamination technology for produce like tomato (Ibarra-Sanchez,
Alvarado-Casillas, Rodriguez-Garcia, Martinez-Gonzales, & Castillo,
2004).
A number of unique nonthermal food safety intervention technol-
ogies have been proposed and investigated during the past decade,
Among these diverse innovations are organic acids (Mukhopadhyay,
Ukuku, & Juneja, 2015), ozone (Tokala, Singh, & Payne, 2018),
bioactive sanitizer coating (Mukhopadhyay et al., 2018a), electrolyzed
water (Graca, 2017), ultraviolet (UV–C) light (Sommers, Sites, &
Musgrove, 2010), high hydrostatic pressure (Mukhopadhyay et al.,
2017) and cold plasma (Niemira & Cooke, 2010). These chemical and
physical interventions are capable to inactivate pathogens to different
extent based on the type of produce and the nature of bacterial pa-
thogens. However, none of these technologies have been adopted by the
industry due to either economic concern, lack of efficiency, or the ad-
verse effect on quality.
Pulsed light (PL) technology has evolved as an efficient non-thermal
intervention for inactivation of pathogens in produce, meat and other
commodities. PL technology uses transient powerful arrays of broad
spectrum light pulses, ranging from UV to infrared (200–1100 nm), for
decontamination of food and has been approved for food surface de-
contamination (FDA, 1996). PL acts by interrupting cell replication by
damaging the DNA strands of microorganism via photochemical action
of UV constituent of the light (Mukhopadhyay, Ukuku, Juneja, Nayak,
& Olanya, 2018b). Besides the photochemical means of injuring DNA,
PL also inactivate microorganisms by means of photothermal and
photophysical actions (Krishnamurthy, 2007). Several reports ex-
pressed positive view of this technology for inactivation of bacterial
pathogens, reduction of microbiota and preservation of quality (Ramos-
2
Food Control 110 (2020) 107005
Villarroel, Aron-Maftei, Martín-Belloso, & Soliva-Fortuny, 2012). PL
treatment generates heat via photothermal action and hence extended
PL exposure to achieve 5-log reduction for a comparable pasteurizing
level intensity can be harmful to quality of produce which known to be
heat sensitive (Bialka and Demirci, 2008). Therefore, instead of prolong
PL treatment, a combination of short PL exposure with active sanitizer
treatment may provide the stipulated inactivation with fewer adverse
quality effects. While developing decontamination method for tomato it
is important to consider stem scars location since steam scars of tomato
are known to harbor pathogens preferentially than surface. Also, mass
transport diffusion of sanitizer molecules to steam scars faces an extra
challenge due to the porous morphology of stem scars with respect to
smooth surface, hindering the inactivation effort (Mukhopadhyay,
Ukuku, Juneja, & Fan, 2014a).
According to the available information, no investigation has been
reported evaluating inactivation of Salmonella enterica on stem scars of
cherry tomatoes employing either PL treatment or integrated treatment
of PL and antimicrobial wash. Therefore, the objective of this study was
to evaluate and optimize PL treatment efficacy on decontamination of
cherry tomato stem scars contaminated with Salmonella. The other
objective was to examine the effectiveness of a new formulation anti-
microbial, LAPEN wash and the integrated treatments of PL and LAPEN
against Salmonella. The third and the final objective was to assess the
influence of most effective combined treatment on the background
microbiota and the apparent quality of cherry tomato.
2. Materials and methods
2.1. Strains, growth conditions, and inoculum
Three serotypes of S. enterica (S. Montevideo G4639, S. Newport
H1275, and S. Stanley H0558) was used to prepare a cocktail for the
current investigation. These strains were selected for their involvement
with produce related outbreaks. S. Newport H1275 and S. Stanley
H0558, were received from Dr. Patricia Griffin, Center for Disease
Control and Prevention, Atlanta, GA. These two strains were involved in
alfalfa sprout-related outbreaks. The third strain S. Montevideo G4639,
was isolated from tomato related outbreak and was obtained from Dr.
Larry Beuchat of University of Georgia. The individual Salmonella
strains were grown in Tryptic soy broth (TSB, Difco, BD) and cells were
harvested, washed and suspended in 0.1% (w/v) peptone water (PW,
BBL, BD Difco) and finally combined in a manner described by
Mukhopadhyay et al. (2018a) to obtain a cocktail of three strains of
Salmonella with target population of 8–9 log CFU/ml. prior to in-
oculation.
2.2. Sample preparation
Whole cherry tomatoes (Solanum lycopersicum), of uniform size/
weight (~20 g) with fully intact stems and devoid of cuts, bruises or
scars were purchased from a local super market (Philadelphia, PA) day
before experiment and stored overnight in a refrigerator. On the day of
experiment, tomatoes were taken out of the refrigerator and placed
inside a biological hood for 2 h to adjust to room temperature.
Tomatoes were then washed for 2 min with 200 ppm of chlorine as
described previously (Mukhopadhyay et al., 2018a) prior to inocula-
tion. However, chlorine wash was not performed for a set of tomatoes
selected for the determination of background microbial populations.
2.3. Inoculation of cherry tomatoes
Tomatoes were spot inoculated at stem scars since spot inoculation
method allows the application of a known amount/number of cells onto
the surfaces, regardless of weight/size of produce. Fifty microliters
(approx. 5 drops) of the mixed culture suspension of Salmonella con-
taining population of 8–9 log CFU/ml was carefully spotted, using an
J. Leng, et al.
appropriate accurate pipette, on the stem scar sites of cherry tomatoes
at ambient air temperature. For preparation of inoculum, the individual
Salmonella strains were grown in 5 ml Tryptic soy broth (TSB, Difco,
BD) incubated in static at 37 °C for 24 h. After 24 h of incubation, a loop
transfer of these strains was made into new 5 ml Tryptic soy broth and
were similarly incubated at 37 °C for 24 h. A final transfer of 0.2 ml was
made into 50 ml TSB with incubation at 37 °C for 18 h. The bacterial
cells were harvested by centrifugation (5000×g, 15 min) at 4 °C. Cell
pellets were washed twice in 0.1% (w/v) peptone water (PW, BBL, BD
Difco) and was finally suspended in PW to achieve a target level of
about 8–9 log CFU/ml. To enumerate population densities in each cell
suspension, appropriate dilutions (in 0.1% PW) were spiral plated, in
duplicate, on tryptic soy agar (TSA; BD Difco) plates. Equal volumes of
cultures were combined in a separate sterile test tube to obtain a
cocktail of three strains of Salmonella prior to inoculation of tomatoes.
Inoculated tomatoes were placed on sterile petri dishes and air-dried at
room temperature (22 ± 2 °C) in a biosafety cabinet (NuareTM,
Plymouth, MN, USA) for 3 h to allow the bacterial attachment. Four
tomatoes were used for each treatment per replicate. Three replicates of
experiments were conducted. Experiments were independently re-
plicated at different times (weeks). Freshly grown inoculum and fresh
new batches of tomatoes were used for each replicate. Following in-
oculation and cell attachment, tomatoes were subjected to PL and/or
sanitizer treatment as described below.
2.4. Pulsed light treatment of tomatoes
A small, laboratory size, pulse light unit (Steri Pulse, Xenon, MA)
was used for PL treatment of cherry tomato. The unit contained a quartz
lamp (LH 840) light source which delivered 3 light pulses per second of
width ~ 500 μs and wavelength in range of 180–1000 nm of which
~40% falls in the UV region. Energy delivered by Steri Pulse unit was
measured by a Vega laser power meter (OPHIR Photonics, North Logan,
UT, USA). Four inoculated tomatoes were arranged in a sterile petri
dish with inoculated stem scars facing upwards to the light source at a
distance of about 14 cm from the light source. The fluence energy de-
livered to the tomato, at this distance, by a single pulse was 0.35 J/cm2.
Tomatoes were exposed to PL for 1s (1.05 J/cm2) to maximum 1 min
(63 J/cm2). Exposure beyond 1 min were not explored due to sub-
stantial temperature increase (> 50 °C) from the heat generated by the
PL exposure. Experiments were conducted independently in triplicate.
2.5. Sanitizer wash of tomato stem scars
Tomatoes were washed with a novel sanitizer formulation for 2 min
before and after PL treatment to assess the effects of combination
treatments. This novel antimicrobial solution was formulated from
GRAS (generally regarded as safe) compounds, consisting short chain
organic acids, EDTA and Nisin. First, EDTA (7.44 g; Sigma, St Louis,
MO) was mixed in 100 ml 0.02 N hydrochloric acid (HCl, pH 2), fol-
lowed by addition of Nisin (l06 I. U.; Sigma, St. Louis, MO) at 33 mg and
then 500 mL distilled deionized water was added. The solution was
placed on a hot plate/stirrer (Corning, USA) set at medium speed/heat
(setting 5). Ascorbic acid (5 g, Sigma Aldrich, St. Louis, MO) was added
to the solution while mixing followed by addition of calcium propionate
(5 g, Fisher Scientific Co., Pittsburgh, PA) and lactic acid (1%, Sigma
Aldrich, St. Louis, MO) in that order. Finally, the solution was brought
to volume (1000 ml) with distilled deionized water and the final pH of
the solution, measured by a pH meter (TS 625, Thomas Scientific,
Swedesboro, NJ), was 3.0 ± 0.2. The formulated antimicrobial was
referred as LAPEN. Combination treatment of PL and LAPEN sanitizer
wash were achieved as per two possible scenarios, namely initial ex-
posure of stems cars to optimum PL dose followed by 2 min wash in
LAPEN sanitizer (PL-LAPEN) and the reverse, that is, 2 min wash in
LAPEN sanitizer followed by optimum PL dose treatment (LAPEN-PL).
In short, PL treated or untreated tomatoes were washed for 2 min at
3
Food Control 110 (2020) 107005
room temperature (22 ± 2 °C), while agitated mildly in 500 mL freshly
prepared LAPEN solution in a 1 L sterile beaker. Agitation speed
(150–250 rpm) was controlled to assure complete coverage of tomatoes
in the solution. All combination experiments were conducted in in-
dependent triplicates.
2.6. Microbial enumeration
To calculate the survivor's population, steam scars (ca. 5 g) were
excised from treated and untreated tomato, added to about 40 ml
peptone water (PW), pummeled 2 min at 250 rpm using a Stomacher
(Seward, Worthington, UK). Resulting homogenate was diluted with
0.1% PW and Salmonella population was enumerated on Xylose-lysine-
tergitol 4 (XLT-4, BBL, BD Difco), incubated at 37 °C for 24 h according
to Mukhopadhyay et al. (2018a).
Total aerobic bacteria (TAB) population were enumerated by plate
count agar (PCA, BD Difco) method and mold and yeast (M&Y) popu-
lation were determined on dichloran rose bengal chlortetracycline agar
(DRBC, BD Difco). The DRBC plates were incubated at 25 °C for 5 d and
PCA plates were incubated at 37 °C for 24 h.
2.7. Post treatment storage
To determine the treatment effects on microbial & sensory quality
during storage, the untreated tomato (control) and tomato treated with
PL and combinations of PL and antimicrobial LAPEN were analyzed
immediately after experiments (day 0) and then packaged separately in
a plastic container (Clear PAC®, Dart Container Corp., Mason, MI, USA)
with a lid perforated with 4 holes (0.6 mm dia.) and stored at 10 °C for
21 days. Stored tomatoes were analyzed on day 1, day 7, day 14 and
day 21.
2.8. Color and texture analyses
The color of control and treated tomatoes was measured at 0, 7, 14
and 21 days of storage at 10 °C. Color (CIE L*, a*, b*) was measured
using Hunter Lab Ultra Scan VIS with Easy Match QC Software, Version
4.03.00 (Hunter Associates Laboratory, Inc., Reston, VA, USA), where
the L* values indicate the lightness of the tomato surface while a* and
b* values represent redness and yellowness of tomatoes, respectively.
Hunter Lab values (L*, a* and b*) were measured using RSEX
(Reflectance Specular Excluded), 0.375 in. measuring aperture, with
D65/10° illuminant-viewing geometry, and standardized with black
and white tiles. Readings were taken on two sides of each tomato as
described by Mukhopadhyay et al. (2014a), a total of 8 readings per
container. Experiments were conducted in triplicate. Hue and chroma
values were calculated from the following equations: Hue = tan−1 (b*/
a*) and chroma = (a*2 + b*2)1/2.
Texture of fruit was measured using a TA.XT.Plus Texture Analyzer
with Texture Expert Software, Version 1.22 (Texture Technology Corp.,
Scarsdale, NY, USA). A return-to-start (RTS) method was used to
measure the maximum force as texture according to Mukhopadhyay
et al. (2014a).
2.9. Data analyses
Experiments were repeated three times on different days using dif-
ferent batches of tomatoes. Data from each treatment were subjected to
analysis of variance (ANOVA) using SAS statistical package (version
9.4, SAS Institute Inc., Cary, NC, USA). Significant (p < 0.05) mean
values determined were calculated using Bonferroni LSD method
(Miller, 1981).
J. Leng, et al.
3. Results and discussion
3.1. Optimization of pulsed light treatment for inactivation of Salmonella
enterica in stem scars of cherry tomato
The impact of various PL doses on behavior of Salmonella in cherry
tomatoes stem scars is presented in Fig. 1. The mean initial recovered
population from stem scars was 7.1 ± 0.6 log CFU/g. The population
of Salmonella decreased with increasing PL doses. Significant germicidal
effect of PL was observed at the initial lower doses. Thus, just 3 pulses
or 1 s exposure of stem scars to PL, equivalent to a fluence dose of
1.05 J/cm2, was sufficient to yield 1.5 ± 0.4 log CFU/g reduction of
the pathogen. It is evident from Fig. 1 that the survivor population
decreased rapidly with the increase of PL dose. Accordingly, as the dose
raised from 0 to 31.5 J/cm2 (30 s), the Salmonella populations in the
stem scars decreased to 4.8 log CFU/g from initial population of 7.1 log
CFU/g, providing 2.3 log CFU/g reduction of the pathogen. This in-
dicates about 1½-fold (~50%) improvement in reduction as treatment
duration increased to 30 s from 1 s. Even though survivor population
reduced with time (Fig. 1), exposure beyond 30 s failed to deliver ex-
pected additional boost in reduction, indicating a slower rate of in-
activation with extended exposure past 30 s. In fact, as PL dose in-
creased by 2-folds from 31.5 J/cm2 (30 s) to 63 J/cm2 (60 s), the
Salmonella populations declined from 4.8 to 4.6 log CFU/g, i.e., a re-
duction of only 0.2 log. The inactivation efficacy, however, was highly
affected (p < 0.05) at low range of PL doses from 1.05 to 5.25 J/cm2.
Thus, as shown in Fig. 1, greater than 1 log CFU/g reduction of Sal-
monella can be gained in stem scars employing a dose lower than 1 J/
cm2. Fig. 1 clearly indicates that higher exposure time/dose contribute
to better inactivation of the pathogen. However, although inactivation
continues to increase with time, no significant difference was observed
beyond 31.5 J/cm2 (30 s). This behavior can be attributed to the in-
activation nature of the UV segment of PL which is the main cause of
bactericidal activity that destroy bacteria by blocking DNA replication.
Bacterial cellular injury usually begins at a low initial dose and as the
dose outpaces the cellular damage threshold, a fast-fatal cellular injury
takes place (Sastry, Datta, & Worobo, 2000) and despite the progression
of injury with increased exposure, the cell death tends to stabilize.
Reports on PL treatment for inactivation Salmonella on tomato stem
scars is not available. Williams et al. (2012) investigated the efficacy of
pulsed ultraviolet light alone and in combination with sanitizer treat-
ment for Salmonella inactivation on whole tomato surface for 8 days.
4
Food Control 110 (2020) 107005
Fig. 1. Effect of pulsed light (PL) on of
Salmonella enterica inoculated on stems scars
of cherry tomato. Recovered population of
Salmonella in stem scar was 7.1 ± 0.72
log10 CFU/g. Data are expressed as
means ± 1sd (sd = standard deviation;
n = 3). Vertical error bars represent stan-
dard deviation of mean. Mean values, in the
same column, with same letters are not sig-
nificantly different (p > 0.05).
The authors achieved 1.35 log reductions of Salmonella with 60 s pulsed
ultraviolet light treatments alone. Using 200 pulses (~66 s exposure),
Rowan et al. (1999) achieved 1.6 log reduction of Salmonella enteritidis
on tryptone soya-yeast agar surface (TSYEA). Luksiene, Buchovec,
Kairyte, Paskeviciute, and Viskelis (2012) reported reduction in the
range of 1.3–1.8 logs for Salmonella on tomato surface by high-power
PL treatment. Recently, Huang and Chen (2019a) investigated the ef-
ficacy of PL and water wash combination on inactivation of Salmonella.
The authors obtained 4.4 logs reduction of spot inoculated Salmonella
on grape tomatoes surface with 1 min PL (0.3 J/cm2/pulse; 3 pulses/s)
in combination with water washing treatments; whereas for dip-in-
oculated tomatoes, the same PL and water wash combination treatment
reduced Salmonella population by 2.3 logs. In this study, a 1 min intense
pulsed light treatment inactivated 2.5 logs of a Salmonella composite on
stem scars of cherry tomato.
During experiments, temperature inside the PL chamber containing
tomato was substantially elevated. Pulsed light treatment is known to
generate ample heat by photothermal action of the light (Bialka and
Demirci, 2008). Produce like tomatoes are sensitive to heat as it cause
many physical and chemical changes in the produce including nutri-
tional and sensorial quality damage (Hidalgo, Pompei, & Zambuto,
1998). The intensity of PL treatment depends on the distance of the
produce from pulsed light source and treatment time. With distance
from the light source to the produce surface (~14 cm) being fixed by
the manufacturer, the only variable that can be optimized is the ex-
posure time, to control the intensity of treatment and thus to limit the
mean produce surface temperature. As shown in Fig. 1, min PL exposure
leads to 2.5 logs reduction of Salmonella whereas, merely 30 s treatment
reduced the population by 2.3 logs, meaning that greater than 90% of
maximum reduction efficacy can be achieved very fast, with in 30 s,
while the residual (~10%) reduction was gained over remaining 30 s.
Hence, considering the Salmonella inactivation characteristics of PL in
tomato stem scars, the optimum PL treatment time was selected to be
30 s as this choice provides maximum efficacy with minimum energy
expenditure and quality effects.
3.2. Influence of new formula antimicrobial and integrated treatment of
pulsed light with antimicrobial rinse on Salmonella in tomato stem scars
Fig. 2 shows the effects of antimicrobial wash and its combination
with optimum PL dose (31.5 J/cm2) for inactivation of Salmonella in
stem scars. The initial survivor count from untreated (control) tomato
J. Leng, et al.
was 5.9 ± 0.6 log CFU/g. 2 min wash in LAPEN antimicrobial for-
mulation reduced Salmonella by 2.1 log whereas 30 s (31.5 J/cm2) PL
treatment yielded about 10% higher (2.3 log) reduction of the target
pathogen. Sanitizer wash or the PL treatment alone by itself was unable
to provide pasteurization intensity inactivation (> 5 log) as endorsed
by FDA (FDA, 2001) as the basis of safe microbiological characteristics
for food processing. But the combinations of 2 min LAPEN wash and
30 s PL exposure evidenced a potent inactivation ability towards Sal-
monella (Fig. 2). In the combination treatment protocol, LAPEN anti-
microbial wash was chosen with pulsed light as LAPEN and PL arrest
bacterial growth via unique separate mechanisms. Two different com-
bination options were examined. In one, tomatoes were washed in
LAPEN sanitizer for 2 min and then treated with PL for 30 s (LAPEN-PL)
but in the second option treatment sequence was reversed, i.e., toma-
toes were PL treated (30 s; 31.5 J/cm2) first and then washed (2 min) in
LAPEN sanitizer (PL-LAPEN). Both of these combination treatment
schemes showed potent inactivation capability against Salmonella
(Fig. 2). The treatment combination, LAPEN-PL, decreased Salmonella
by 4.5 log CFU/g, hinting a compound inhibition effect of two in-
dividual treatments. But the reverse combination treatment strategy
(PL-LAPEN) significantly enhanced inactivation since no survivors were
detectable after treatment. This treatment combination of PL-LAPEN,
reduced Salmonella population in steams scars by greater than 5 logs,
indicating a strong synergistic inhibition (Fig. 2). Exposure to PL prior
to aqueous sanitizer wash provides the best scenario probably be due to
the fact that PL mainly a surface decontamination technique and has
only a narrow penetration capacity in nontransparent opaque media.
Thus, a lower efficacy in case of LAPEN-PL treatment, may be due to the
formation of aqueous thin film of sanitizer solution in the stem scars
from LAPEN wash and the resulting film shielding effect hindering PL
penetration to reach the bacterial cells.
Limited reports available on inactivation of bacterial pathogens in
stem scars of tomato and related quality effects. Yuk et al. (2005) re-
ported pathogens, including Salmonella in stem scars area need more
harsher treatment to decontaminate. Nevertheless, if the processing
intensity is high, as is the case with single interventions, it could result
adverse quality effect. Combination treatment is the best option for this
situation (Mukhopadhyay and Gorris, 2014b). Studies on Salmonella
inactivation in tomato stem scars employing PL and sanitizer combi-
nation is not available. Some researchers studied the inactivation effi-
cacy of combination treatment using surface inoculation, but none
5
Food Control 110 (2020) 107005
Fig. 2. Survival of Salmonella enterica in
cherry tomato stem scars as influenced by
PL, LAPEN antimicrobial containing short
chain organic acid, ethylenediaminete-
traacetic acid and Nisin, and two combina-
tions of PL treatment with LAPEN wash (PL-
LAPEN & LAPEN-PL). Initial Salmonella
population from untreated scars (control)
was 5.9 ± 0.55 log CFU/g. The dotted
horizontal line indicates the detection limit
(0.7 log CFU/g).
looked at the inactivation characteristics of pathogens specifically on
the stem scars. Williams et al. (2012) reported inactivation of Salmo-
nella on surface of tomato using combination of pulsed UV (PUV) and
chemical sanitizer wash. The efficacy PUV in combination with per-
acetic acid, hydrogen peroxide and a commercial GRAS disinfectant
were investigated. Authors reported less than 2 log reductions by 60 s
PUV treatment. But integration of PUV and hydrogen peroxide (1%)
reduced Salmonella by more than 4 logs while in storage for 8 days.
Huang and Chen (2019b) reported the effects of combination of
1 min PL treatment with 2 min wash at 30 °C with either water, chlorine
(10 ppm) or hydrogen peroxide (1%) on inactivation of spot and dip
inoculated pathogen on grape tomatoes. Authors obtained > 5 log re-
duction of Salmonella using PL treatment with H2O2 and with chlorine
for spot inoculated Salmonella. For dip inoculated samples, reduction
was about 3 logs. It is important to note the authors used 1 min PL
treatment with 2 min hot sanitizer wash for spot or dip inoculated grape
tomatoes. These previous reports addressed Salmonella inactivation on
the surface, while pathogens in stem scars require more stringent
treatment. The combination treatment presented in the current work
evaluated inactivation of Salmonella in stem scars, employing a low
(30 s) PL exposure with 2 min sanitizer wash at room temperature to
avoid deleterious thermal effect on tomato quality and yielded a pas-
teurization intensity reduction (> 5 log) for Salmonella on stem scars of
tomato.
Efficacy of 200 ppm chlorine wash, which is currently practiced
industry wide, is about 2-log for Salmonella (Beuchat, Nail, Adler, &
Clavero, 1998). In this study, both PL treatment (30 s) and two com-
bination treatments of PL with LAPEN (PL-LAPEN and LAPEN-PL),
provided significantly better inactivation of Salmonella on stem scars
compared to current industrial method of 200 ppm chlorine wash,
suggesting that simply PL treatment or combination of PL treatment
with LAPEN sanitizer have the future in tomato industry for use as a
safe and effective non-chlorine based method.
3.3. Survival of Salmonella in stem scars after treatment with PL and
LAPEN while in storage at 10 °C
Fate of Salmonella in cherry tomato was evaluated for three weeks
during storage at 10 °C. Fig. 3 shows the fate of survivors in stem scars
of untreated and tomato treated with four different methods, namely,
PL, LAPEN, PL-LAPEN and LAPEN-PL, over 3 weeks of storage.
J. Leng, et al.
Fig. 3. Survivor population in cherry tomato stem scars while in storage for 3 weeks at 10 °C as influenced by 30 s PL exposure, 2 min wash in new formula
antimicrobial (LAPEN), and two integrated treatments of PL with LAPEN. * - Population under limit of detection (LOD < 0.7 log CFU/g).
Salmonella population in control sample was about 5.9 log on day 1
which remain unchanged for 21days. PL exposure lowered population
to about 3.6 log CFU/g on day 1 and then down to 2.1 log on day 21,
equivalent to 3.8 log reduction over 3 weeks (Fig. 3). In the case of
LAPEN treatment, the Salmonella population in treated samples was
decreased to 1.7 log CFU/g on day 21. Salmonella populations in
combined treated samples were predominantly below the detection
level during storage. The combination of LAPEN and PL treatment
(LAPEN-PL), inactivated populations from 5.9 to 1.3 on day 1 but
during storage, from day 7, Salmonella was not detectable as population
reduced to under the detection level. The combination treatment of
30 s PL followed by 2 min LAPEN wash (PL-LAPEN) delivered a lethal
inactivation (> 5-logs) reducing populations to undetectable range
after treatment on day 1 and the populations resided at this un-
detectable level during the entire storage period. Therefore, the com-
bined treatment of PL-LAPEN was able to inactivate and maintain
Salmonella in stem scars below detection level and no regrowth was
observed during storage. Hence, PL-LAPEN provides the best treatment
option among the four different methods tested to control survival and
growth of Salmonella in cherry tomato (see Fig. 3).
Combination of organic acid (0.5%) wash with coating (chitosan)
was reported to eliminate Salmonella spp. in grape tomato after treat-
ment and during storage at 10 °C for 3 weeks (Mukhopadhyay, 2018a).
Combinations treatment of cold plasma (400–900 W) for 2–10 min with
cold storage was reported to eradicate Salmonella population in cherry
tomato (Kim and Min, 2017). The findings of this work are in general
consensus the with published report. Treatments may initially lower the
bacterial population, but the population can increase and surpass the
initial value during storage (Gonzalez, Luo, Ruiz-Cruz, & Cevoy, 2004).
In the work, PL-LAPEN combination reduced survivors in stem scars
under detection level and the treatment also prevented any regrowth
during cold storage, while the Salmonella population in untreated to-
mato were unchanged during entire storage (Fig. 3). This signifies the
potential of PL-LAPEN combination treatment as an effective post-
harvest intervention technology for tomato.
3.4. Influence of combined processing of PL and LAPEN (PL-LAPEN) on
native microflora
One of the major concern for produce industry is the limited shelf
life and quality deterioration. Fruits and vegetables usually have short
shelf life of up to 14 days (Cantwell & Suslow, 2002) and for tomatoes
shelf life is about 21 days if kept in controlled environment (Kader,
2002). Bacteria and fungi are the two major culprit responsible for
spoilage of tomato (Bartz, Sargent, & Mahovic, 2013). The typical
6
Food Control 110 (2020) 107005
storage temperature for tomato is 10 °C. Factors that influence the
survival of native microbiota in fresh produce includes produce type,
load and nature of microbiota, and the effectiveness of post-harvest
treatment. Hence, effective treatment to reduce spoilage microorgan-
isms in produce is important for quality maintenance and extension of
shelf life.
No report is available concerning the effects of PL and sanitizer
wash combination treatment on microbial loads in cherry tomato. The
combined treatment (PL-LAPEN) influence for reducing total aerobic
bacteria (TAB) and mold and yeast (M&Y) was examined for 3 weeks at
10 °C. Fig. 4 shows the treatment influence on background microbiota.
The TAB population in control sample increased from 3.6 ± 0.7 log
CFU/g on day 1–5.7 ± 0.5 log CFU/g on day 21 while in storage. This
represents > 2 logs increase for TAB in 21 days. The PL-LAPEN treat-
ment, reduced TAB populations to 2.2 ± 0.4 log CFU/g on day 1 in-
dicating 1.4 log CFU/g of initial reduction of TAB population. There
was no increase in TAB count for treated tomato until day 7 after which
the TAB counts increased gradually reaching to a level of 2.9 ± 0.3 log
CFU/g at day 21 which is significantly (p < 0.05) lower compared to
that of untreated tomato. This is probably due to the sublethal damage
of organisms by PL disabling the population to adapt in low tempera-
ture storage. Combined PL-LAPEN treatment was able to inactivate M&
Y population entirely after treatment (day 1) with no growth resurgence
while in storage for entire 21 days. However, during storage the M&Y
population of control sample increased to 3.6 log CFU/g on day 21 from
an initial value of 1.8 log CFU/g (Fig. 4). Unlike the control, no decay
(fungal or soft rots) was observed on treated samples during storage.
PL treatment reported to reduce the TAB populations by up to 2.04
logs for eight minimally processed produce (Gomez-Lopez, Devlieghere,
Bonduelle, & Debevere, 2005). Organic acid wash and chitosan-allyl
isothiocyanate coating treatment combination for grape tomato re-
ported to provide 1.3 log reduction in TAB population while elim-
inating the M&Y population (Mukhopadhyay et al., 2018a). Combina-
tion of static UV treatment (6 kJ/m2) and 2 min wash in HEN sanitizer
reduced TAB count by 1.7 logs in plum tomato (Mukhopadhyay et al.,
2015) while pulsed UV and LAPEN sanitizer combination presented in
this study reduced 1.4 logs of TAB population. The results presented in
this work indicate an efficacious treatment strategy that may be used to
ensure the microbial safety of tomato and control of spoilage organisms
to promote microbial stability and extension of shelf life.
3.5. Combination treatment influence on cherry tomato quality
3.5.1. Texture
Texture or firmness is an important factor for consumer purchase
J. Leng, et al. Food Control 110 (2020) 107005

Fig. 4. Influence of PL-LAPEN combination treatment on total aerobic bacteria (TAB) and mold and yeast (M &Y) population in control and treated cherry tomato
while in storage for 3 weeks. ⁎ - Population under detection limit (LOD < 1 log CFU/g).

Table 1
Color and firmness quality of cherry tomato as influenced by PL-LAPEN combined treatment and storage.
Treatment Storage at 10 °C (day) Color parameters Texture Maximum Force, (g)

L* a* b* (a*/b*) Hue Chroma

Control 1 37.5 ± 1.4a 22.5 ± 1.9a 22.1 ± 2.4a 1.02 44.5 ± 1.1a 31.5 ± 0.9a 1053 ± 102a
7 35.9 ± 2.2a 20.8 ± 2.1a 20.1 ± 1.8a 1.03 44.1 ± 0.8a 28.9 ± 1.2a 987 ± 83a
14 35.4 ± 0.8a 22.2 ± 0.9a 21.4 ± 1.9a 1.04 43.9 ± 1.3a 30.8 ± 1.6a 1021 ± 120a
21 35.5 ± 1.1a 23.2 ± 1.1a 21.2 ± 2.1a 1.09 42.4 ± 0.9a 31.4 ± 1.1a 951 ± 42a

Treated (PL-LAPEN) 1 36.9 ± 1.5a 22.8 ± 1.3a 22.3 ± 1.6a 1.02 44.4 ± 0.4a 31.9 ± 1.6a 997 ± 72a
7 36.6 ± 1.1a 21.7 ± 1.5a 21.2 ± 1.9a 1.02 42.9 ± 1.2a 31.1 ± 0.9a 973 ± 93a
14 36.8 ± 0.9a 22.5 ± 0.9a 19.4 ± 2.4b 1.16 40.8 ± 1.1a 29.7 ± 2.1a 981 ± 82a
21 37.2 ± 1.2a 22.7 ± 1.1a 18.9 ± 1.1b 1.19 39.8 ± 1.5a 29.5 ± 1.8a 877 ± 47b

Data are expressed as means ± 1sd (sd = standard deviation; n = 3).

Data followed by the different letters, in the same column, are significantly different (p < 0.05).
Hue = tan−1 (b*/a*) and Chroma = (a*2+b*2)1/2.

decision. Effect of PL-LAPEN combination treatment on the firmness of
cherry tomatoes measured in terms of textural strength is presented in
Table 1. Both control and treated tomatoes lost firmness while in sto-
rage. Typically, the PL-LAPEN treated samples lost more firmness, re-
quiring lesser force to puncher compared to control (Table 1). For
control tomato, loss in firmness was not significant during entire sto-
rage. However, for treated sample, loss in firmness was not significant
only until day 14, but upon subsequent storage, on day 21, the loss
appeared to be significant (p < 0.05).
Oxidants, like ozone, has been reported to damage feruloylated or
phenolic cross-linkage of cell wall pectin or other polymers including
structural protein resulting in a deterioration of firmness quality of
produce (Hong and Gross, 1998). PL treatment is known to generate
heat and a small amount of ozone (Bialka and Demirci, 2008). The
injury of tomato tissues by heat or by oxidation from liberated ozone or
the depletion of cell turgidity due to loss of water (Akbas & Olmez,
2007) could be the probable reason for greater loss of firmness for
treated samples.
3.5.2. Color parameters
Postharvest processing and storage can induce some changes in
produce color due to minor physiochemical and biochemical variations.
Table 1 shows the changes in color of cherry tomatoes due to combined
PL-LAPEN processing. Color of tomato surface has been evaluated in
terms of three principal instrumental color parameters namely L*, a*
and b* representing the lightness, redness and yellowness respectively
(Artes, Conesa, Harnendez, & Gil, 1999). Processing did not influence
the color of tomato significantly as the color parameter values remain
mostly unchanged after PL-LAPEN combined treatment (Table 1). Both
L* and a* (lightness and redness) values for control untreated and
treated tomatoes were unchanged for 3 weeks during storage. Treat-
ment also did not affect the b* value or yellowness of tomatoes on day 1
and during storage until day 7. However as indicated in Table 1, upon
subsequent storage (on day 14 and day 21) PL-LAPEN processed to-
matoes exhibited lower (p < 0.05) b* values. This decline in yellow-
ness of treated tomatoes was not clearly noticeable due to perhaps the
intense redness of tomato. Estimated ‘hue’ value and the color purity
factor ‘chroma’ were mostly unaffected by the PL-LAPEN treatment and
during 21 days storage. Visual appearance of treated tomatoes was si-
milar to control. The redness factor (a*/b*) were mostly unaffected by
the PL-LAPEN treatment during storage. The redness factor (a*/b*) is
an indicator of characteristic red color of tomato. USDA criteria for
acceptable (a*/b*) values for red stage tomatoes ranges from 0.95 to
1.21 (Batu, 2004). In the present work (Table 1), treated tomatoes had
(a*/b*) values of > 1 on all sampling days indicating their market ac-
ceptably.

7
J. Leng, et al.
Reports indicated static UV light treatment (0.60–6.0 kJ/m2) in-
fluenced no change in color and firmness quality of grape tomato
during storage (Mukhopadhyay et al., 2014a). Jiang et al. (2017)
evaluated in-package antimicrobial influence on quality of produce and
reported no change for 21 days storage. Organic acid wash and chit-
osan-allyl isothiocyanate coating combination also reported no sig-
nificant change in firmness and color for grape tomato while in storage
at 10 °C (Mukhopadhyay et al., 2018a). In this study, tomato color and
firmness remained unaffected due to combined processing (PL-LAPEN)
and during storage. Consumer initial impression and purchase tendency
depends largely on the visual appearance and firmness factors of pro-
duce. Results of this study signifies the acceptability of cherry tomatoes
treated with PL and LAPEN sanitizer combination.
4. Conclusions
In summary, our results demonstrated that a short 30s pulsed light
treatment combined with 2 min wash in a newly formulated sanitizer,
LAPEN, can inactivate Salmonella on stem scars of cherry tomatoes by
greater than 5 logs with no regrowth possibility of the pathogen during
cold storage at 10 °C for 3 weeks. This treatment combination is effi-
cient for regulating microbiota since aerobics load (TAB) was sig-
nificantly declined and no major regrowth during storage while popu-
lation of yeast and mold (Y&M) count fell below the detection level
after treatment and remained unchanged during storage. Furthermore,
none of the quality attributes such as color and firmness were affected
by the treatment, except that the treated fruits were slightly softer
during the latter part of storage.
PL treatment is FDA approved safe and effective technology while
the ingredients of LAPEN are all GRAS compounds. Results of the
present study indicate that PL-LAPEN combination treatment is suitable
for use to inactivate Salmonella in cherry tomato to enhance microbial
safety, retain quality and prolong shelf life. Additional research is
needed for optimization of key process variables and the work asso-
ciated with pilot scale-up study for validation, cost estimation and
marketability.
Declaration of competing interest
We, the authors declares no conflict of interest for this research
work.
Acknowledgment
Authors acknowledge contribution of outstanding technical assis-
tance from Louis Colaruotolo of University of Massachusetts, Amherst
and Anita Parameswaran of USDA, Wyndmoor. Mention of commercial
names or products in the report intended to provide specific informa-
tion only and do not carry USDA endorsement. This is work was sup-
ported by the CRIS project 8072-41000-101-00D through USDA, ARS
National Program 108. USDA is an equal opportunity provider and
employer.
References
Abete, I., Perez-Cornago, A., Navas-Carretero, S., Bondia-Pons, I., Zulet, M. A., &
Martinez, J. A. (2013). A regular lycopene enriched tomato sauce consumption in-
fluences antioxidant status of healthy young-subjects: A crossover study. Journal of
Functional Foods, 5, 28–35.
Aguiló-Aguayo, I., Charles, F., Renard, C. M. G. C., Page, D., & Carlin, F. (2013). Pulsed
light effects on surface decontamination, physical qualities and nutritional compo-
sition of tomato fruit. Postharvest Biology and Technology, 86, 29–36.
Akbas, M. Y., & Olmez, H. (2007). Effectiveness of organic acid, ozonated water and
chlorine dippings on microbial reduction and storage quality of fresh‐cut iceberg
lettuce. Journal of the Science of Food and Agriculture, 87, 2609–2616.
Artes, F., Conesa, M. A., Harnendez, S., & Gil, M. I. (1999). Keeping quality of fresh-cut
tomato. Postharvest Biology and Technology, 17, 153–162.
Artes, F., Gomez, P., Aguayo, E., Escalona, V., & Artes-Hernundez, F. (2009). Sustainable
sanitation techniques for keeping quality and safety of fresh-cut plant commodities.
8
Food Control 110 (2020) 107005
Postharvest Biology and Technology, 51, 287–296.
Asplund, K., & Nurmi, E. (1995). The growth of Salmonella in tomatoes. International
Journal of Food Microbiology, 13, 177–182.
Bartz, J. A., Eayre, C. G., Mahovic, M. J., Concelmo, D. E., Brecht, J. K., & Sargent, S. A.
(2001). Chlorine concentration and the inoculation of tomato fruit in packinghouse
dump tanks. Plant Disease, 85, 885–889.
Bartz, J. A., Sargent, S. A., & Mahovic, M. (2013). Guide to identifying and controlling
postharvest tomato diseases in FloridaUF/IFAS Extension Publication. Document
HS866, accessed 5/20/2019 from EDIS website at http://edis.ifas.ufl.edu/hs131.
Batu, A. (2004). Determination of acceptable firmness and color values of tomatoes.
Journal of Food Engineering, 61, 471–475.
Beuchat, L. R., & Mann, D. A. (2008). Survival and growth of acid-adapted and un-
adapted Salmonella on raw tomatoes as affected by variety, stage of ripeness, and
storage temperature. Journal of Food Protection, 71, 1572–1579.
Beuchat, L. R., Nail, B. V., Adler, B. B., & Clavero, M. R. S. (1998). Efficacy of spray
application of chlorinated water in killing pathogenic bacteria on raw apples, to-
matoes, and lettuce. Journal of Food Protection, 61, 1305–1311.
Bialka, K. L., & Demirci, A. (2008). Efficacy of pulsed UV-light for the decontamination of
Escherichia coli O157:H7 and Salmonella spp. on raspberries and strawberries.
Journal of Food Science, 73, 201–207.
Bidol, S. A., Daly, E. R., Rickert, R. E., Hill, T. A., Al Khaldi, S., Taylor, T. H., et al. (2007).
Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in
restaurants – United States, 2005–2006. Morbidity and Mortality Weekly Report,
56(35), 909–911.
Cantwell, M. I., & Suslow, T. V. (2002). Postharvest handling systems: Fresh-cut fruits and
vegetables. In A. A. Kader (Ed.). Postharvest technology of horticultural crops (pp. 445–
463). Davis CA: University of California.
CDC (Centers for Disease Control and Prevention). Multistate outbreaks of Salmonella infec-
tions associated with raw tomatoes eaten in restaurant. (2019). https://search.cdc.gov/
search/?query=tomato&sitelimit=&utf8=%E2%9C%93&affiliate=cdc-main
Accessed, April 5, 2019.
FDA (Food and Drug Administration) (1996). Code of federal regulations. Pulsed Light for
the Treatment of Food 21CFR179.41.
FDA (Food and Drug Administration) (2001). 21 CFR Part 120 hazard analysis and critical
control point (HAACP); procedures for the safe and sanitary processing and importing
of juice. Final Rule. Available from: http://www.fda.gov/OHRMS/DOCKETS/98fr/
011901d.pdf.
Gomez-Lopez, V. M., Devlieghere, F., Bonduelle, V., & Debevere, J. (2005). Intense light
pulses decontamination of minimally processed vegetables and their shelf-life.
International Journal of Food Microbiology, 103(1), 79–89.
Gonzalez, R. J., Luo, Y., Ruiz-Cruz, S., & Cevoy, A. L. M. (2004). Efficacy of sanitizers to
inactivate Escherichia coli O157:H7 on fresh-cut carrot shreds under simulated process
water conditions. Journal of Food Protection, 67, 2375–2380.
Gravani, R. B. (2009). The role of good agricultural practices in produce safety. In X. Fan,
B. A. Niemira, C. H. Doona, F. E. Feeherry, & R. B. Gravani (Eds.). Microbial safety of
fresh produce (pp. 101–117). Ames, IA: IFT Press/Wiley-Blackwell.
Graça, A., Santo, D., Quintas, C., & Nunes, C. (2017). Growth of Escherichia coli,
Salmonella enterica and Listeria spp., and their inactivation using electrolyzed water,
on ‘Rocha’ fresh-cut pears. Food Control, 77, 41–49.
Hanning, I. R., Nutt, J. D., & Ricke, S. C. (2009). Salmonellosis outbreaks in the United
States due to fresh produce: Sources and potential intervention measures. Foodborne
Pathogen and Disease, 6, 635–648.
Hidalgo, A., Pompei, C., & Zambuto, R. (1998). Heat damage evaluation during tomato
products processing. Journal of Agricultural and Food Chemistry, 46(10), 4387–4390.
Hong, J. H., & Gross, K. C. (1998). Surface sterilization of whole tomato fruit with sodium
hypochlorite influences subsequent postharvest behavior of fresh-cut slices.
Postharvest Biology and Technology, 13, 51–58.
Huang, R., & Chen, H. (2019a). Comparison of water-assisted decontamination systems of
pulsed light and ultraviolet for Salmonella inactivation on blueberry, tomato, and
lettuce. Journal of Food Science, 84(5), 1145–1150.
Huang, R., & Chen, H. (2019b). Sanitation of tomatoes based on a combined approach of
washing process and pulsed light in conjunction with selected disinfectants. Food
Research International, 116, 778–785.
Ibarra-Sanchez, L. S., Alvarado-Casillas, S., Rodriguez-Garcia, M. O., Martinez-Gonzales,
N. E., & Castillo, A. (2004). Internalization of bacterial pathogens in tomatoes and
their control by selected chemicals. Journal of Food Protection, 67, 1353–1358.
Jiang, Y., Sokorai, K. J., Pyrgiotakis, G., Demokritou, P., Li, X., Mukhopadhyay, S., et al.
(2017). Cold Plasma-activated hydrogen peroxide aerosol inactivates Escherichia coli
0157:H7, Salmonella Typhimurium, and Listeria innocua and maintains quality of grape
tomato, spinach and cantaloupe. International Journal of Food Microbiology, 249,
53–60.
Kader, A. A. (2002). Postharvest technology of horticultural crops (3rd ed.). University of
California Division of Agriculture and Natural Resources (Publication 3311.
Kim, J. H., & Min, S. C. (2017). Microwave-powered cold plasma treatment for improving
microbiological safety of cherry tomato against Salmonella. Postharvest Biology and
Technology, 127, 21–26.
Krishnamurthy, K., Demirci, A., & Irudayaraj, J. M. (2007). Inactivation of Staphylococcus
aureus in milk using flow-through pulsed UV-light treatment system. Journal of Food
Science, 72(7), M233–M239.
Luksiene, Z., Buchovec, I., Kairyte, K., Paskeviciute, E., & Viskelis, P. (2012). High-power
pulsed light for microbial decontamination of some fruits and vegetables with dif-
ferent surfaces. Journal of Food Agriculture and Environment, 1010, 162–167.
Miller, R. G., Jr. (1981). Simultaneous statistical inference (2nd ed.). New York, NY:
Springer-Verlag.
Mukhopadhyay, S., & Gorris, L. G. M. (2014b). Hurdle technology. In C. A. Batt, & M. L.
Tortorello (Vol. Eds.), Encyclopedia of food microbiology: Vol. 2, (pp. 221–227). UK:
J. Leng, et al.
Elsevier Ltd, Academic Press.
Mukhopadhyay, S., Sokorai, K. J., Ukuku, D. O., Fan, X., & Juneja, V. K. (2017). Effect of
high hydrostatic pressure processing on the background microbial loads and quality
of cantaloupe puree. Food Research International, 91, 55–62.
Mukhopadhyay, S., Sokorai, K. J., Ukuku, D. O., Jin, T., Fan, X., Olanya, M., et al.
(2018a). Inactivation of Salmonella in grape tomato stem scars by organic acid wash
and chitosan-allyl isothiocyanate coating. International Journal of Food Microbiology,
266, 234–240.
Mukhopadhyay, S., Ukuku, D. O., & Juneja, V. K. (2015). Effects of integrated treatment
of nonthermal UV-C light and different antimicrobial wash on Salmonella enterica on
plum tomatoes. Food Control, 56, 147–154.
Mukhopadhyay, S., Ukuku, D. O., Juneja, V., & Fan, X. (2014a). Effects of UV-C treatment
on inactivation of Salmonella enterica and Escherichia coli O157:H7 on grape tomato
surface and stem scars, microbial loads, and quality. Food Control, 44, 110–117.
Mukhopadhyay, S., Ukuku, D. O., Juneja, V. K., Nayak, B., & Olanya, M. (2018b).
Principles of food preservation. In V. Juneja, H. P. Dwivedi, & J. Sofos (Eds.).
Microbial control and food preservation: Theory and practice (pp. 17–39). New York, NY:
Springer International Publishing AG.
Niemira, B. A., & Cooke, P. H. (2010). Escherichia coli O157:H7 biofilm formation on
romaine lettuce and spinach leaf surfaces reduce efficacy of irradiation and sodium
hypochlorite washes. Journal of Food Science, 75(5), M270–M277.
Olaimat, A. N., & Holley, R. A. (2012). Factors influencing the microbial safety of fresh
produce: A review. Food Microbiology, 32, 1–19.
Parnell, T., Harris, L., & Suslow, T. (2005). Reducing Salmonella on cantaloupes and
honeydew melons using wash practices applicable to postharvest handling, food
service, and consumer preparation. International Journal of Food Microbiology, 99(1),
59–70.
Raffo, A., Leonardi, C., Fogliano, V., Ambrosino, P., Salucci, M., Gennaro, L., et al. (2002).
Nutritional value of cherry tomatoes (Lycopersicon esculentum cv. Naomi F1) har-
vested at different ripening stages. Journal of Agricultural and Food Chemistry, 50,
6550–6556.
Food Control 110 (2020) 107005
Ramos-Villarroel, A. Y., Aron-Maftei, N., Martín-Belloso, O., & Soliva-Fortuny, R. (2012).
Influence of spectral distribution on bacterial inactivation and quality changes of
fresh-cut watermelon treated with intense light pulses. Postharvest Biology and
Technology, 69, 32–39.
Richardson, S. D., Thruston, A. D., Caughran, T. V., Collete, T. W., Patterson, K. S., &
Lynkins, B. W. (1998). Chemical by-products of chlorine and alternative disin-
fectants. Food Technology, 52, 58–61.
Rowan, N. J., McGregor, S., Anderson, J., Fouracre, R., McIlvaney, L., & Farish, O. (1999).
Pulsed-light inactivation of food-related microorganisms. Applied and Environmental
Microbiology, 65, 1312–1315.
Sastry, S. K., Datta, A. K., & Worobo, R. W. (2000). Ultraviolet light. Kinetics of microbial
inactivation for alternative food processing technologies. Journal of Food Science,
Special Supplement, 90–93.
Solomon, E. B., Potenski, C. J., & Matthews, K. R. (2002). Effect of irrigation method on
transmission to and persistence of Escherichia coli O157:H7 on lettuce. Journal of Food
Protection, 65, 673–676.
Sommers, C. H., Sites, J. E., & Musgrove, M. T. (2010). Ultraviolet light (254 NM) in-
activation of pathogens on foods and stainless-steel surfaces. Journal of Food Safety,
30, 470–479.
Tokala, V. Y., Singh, Z., & Payne, A. D. (2018). Postharvest uses of ozone application in
fresh horticultural produce. Postharvest Biology Nanotechnology, 129–170.
Williams, L., Yang, W., English, T., English, N., Johnson, J., Rababah, T., et al. (2012).
Disinfection of Salmonella spp. on tomato surface by pulsed ultraviolet light and se-
lected sanitizers. International Journal of Food Engineering, 8(1), 1–12.
Yuk, H., Bartz, J. A., & Schneider, K. R. (2005). Effectiveness of individual or combined
sanitizer treatments for inactivating Salmonella spp. on smooth surface, stem scar,
and wounds of tomatoes. Journal of Food Science, 70, 409–414.
Zhuang, R. Y., Beuchat, L. R., & Angulo, F. J. (1995). Fate of Salmonella Montevideo on
and in raw tomatoes as affected by temperature and treatment with chlorine. Applied
and Environmental Microbiology, 61, 2127–2131.