Factors That Affect Proliferation of Salmonella in Tomatoes Post-Harvest: The Roles of Seasonal Effects, Irrigation Regime, Crop and Pathogen Genotype
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{"title"=>"Factors that affect proliferation of Salmonella in tomatoes post-harvest: The roles of seasonal effects, irrigation regime, crop and pathogen genotype", "type"=>"journal", "authors"=>[{"first_name"=>"Massimiliano", "last_name"=>"Marvasi", "scopus_author_id"=>"23018966600"}, {"first_name"=>"George J.", "last_name"=>"Hochmuth", "scopus_author_id"=>"6604076637"}, {"first_name"=>"Mihai C.", "last_name"=>"Giurcanu", "scopus_author_id"=>"55251527400"}, {"first_name"=>"Andrée S.", "last_name"=>"George", "scopus_author_id"=>"55994293100"}, {"first_name"=>"Jason T.", "last_name"=>"Noel", "scopus_author_id"=>"36554631800"}, {"first_name"=>"Jerry", "last_name"=>"Bartz", "scopus_author_id"=>"7006093392"}, {"first_name"=>"Max", "last_name"=>"Teplitski", "scopus_author_id"=>"6602786180"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203", "pui"=>"372086483", "sgr"=>"84891894869", "doi"=>"10.1371/journal.pone.0080871", "scopus"=>"2-s2.0-84891894869", "pmid"=>"24324640"}, "id"=>"18720ee0-a56b-39bf-a6d7-456ab6f172c3", "abstract"=>"MAIN OBJECTIVES: Fresh fruits and vegetables become increasingly recognized as vehicles of human salmonellosis. Physiological, ecological, and environmental factors are all thought to contribute to the ability of Salmonella to colonize fruits and vegetables pre- and post-harvest. The goal of this study was to test how irrigation levels, fruit water congestion, crop and pathogen genotypes affect the ability of Salmonella to multiply in tomatoes post-harvest.\\n\\nEXPERIMENTAL DESIGN: Fruits from three tomato varieties, grown over three production seasons in two Florida locations, were infected with seven strains of Salmonella and their ability to multiply post-harvest in field-grown tomatoes was tested. The field experiments were set up as a two-factor factorial split plot experiment, with the whole-plot treatments arranged in a randomized complete-block design. The irrigation treatment (at three levels) was the whole-plot factor, and the split-plot factor was tomato variety, with three levels. The significance of the main, two-way, and three-way interaction effects was tested using the (type III) F-tests for fixed effects. Mean separation for each significant fixed effect in the model was performed using Tukey's multiple comparison testing procedure.\\n\\nMOST IMPORTANT DISCOVERIES AND SIGNIFICANCE: The irrigation regime per se did not affect susceptibility of the crop to post-harvest proliferation of Salmonella. However, Salmonella grew significantly better in water-congested tissues of green tomatoes. Tomato maturity and genotype, Salmonella genotype, and inter-seasonal differences were the strongest factors affecting proliferation. Red ripe tomatoes were significantly and consistently more conducive to proliferation of Salmonella. Tomatoes harvested in the driest, sunniest season were the most conducive to post-harvest proliferation of the pathogen. Statistically significant interactions between production conditions affected post-harvest susceptibility of the crop to the pathogen. UV irradiation of tomatoes post-harvest promoted Salmonella growth.", "link"=>"http://www.mendeley.com/research/factors-affect-proliferation-salmonella-tomatoes-postharvest-roles-seasonal-effects-irrigation-regim", "reader_count"=>28, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>3, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>3, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Nursing and Health Professions"=>1, "Mathematics"=>2, "Agricultural and Biological Sciences"=>14, "Medicine and Dentistry"=>4, "Chemistry"=>1, "Computer Science"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>3}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Mexico"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1302754"], "description"=>"<p>Predicted means and Tukey mean separation (with letter groupings) for the two-way interaction effects of factors Cultivar and Sampling time with respect to susceptibility of tomatoes to proliferation of <i>Salmonella</i>.</p>", "links"=>[], "tags"=>["means", "tukey", "two-way", "cultivar", "sampling", "susceptibility", "tomatoes", "proliferation"], "article_id"=>867968, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.t003", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_means_and_Tukey_mean_separation_with_letter_groupings_for_the_two_way_interaction_effects_of_factors_Cultivar_and_Sampling_time_with_respect_to_susceptibility_of_tomatoes_to_proliferation_of_Salmonella_/867968", "title"=>"Predicted means and Tukey mean separation (with letter groupings) for the two-way interaction effects of factors Cultivar and Sampling time with respect to susceptibility of tomatoes to proliferation of <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302752"], "description"=>"1<p>Only marketable tomatoes were included in these analyses.</p>*<p>Statistically significant interaction.</p>", "links"=>[], "tags"=>["variables", "irrigation"], "article_id"=>867966, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.t001", "stats"=>{"downloads"=>6, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_independent_variables_tomato_cultivar_irrigation_regime_and_season_on_yield_1_/867966", "title"=>"Effects of independent variables (tomato cultivar, irrigation regime and season) on yield<sup>1</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302748"], "description"=>"<p>Relevant weather data (as suggested by <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080871#pone.0080871-Harris1\" target=\"_blank\">[41]</a> was obtained from Florida Automated Weather Network (fawn.ifas.ufl.edu). Precipitation (cm) is shown as grey bars (right y-axis), relative humidity (dotted line), total radiant flux (dashed line), temperature (solid black line) are shown on the left y-axis. Days are plotted on the x-axis. Dates of harvest are shown with an asterisk.</p>", "links"=>[], "tags"=>[], "article_id"=>867962, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Weather_conditions_during_the_production_seasons_/867962", "title"=>"Weather conditions during the production seasons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302743"], "description"=>"<p>Post-harvest proliferation of the type strain of <i>S.</i> Typhimurium ATCC 14028 and a cocktail of six strains of <i>Salmonella</i> (<i>S.</i> Javiana ATCC BAA-1593, <i>S.</i> Montevideo LJH519, <i>S.</i> Newport C6.3, <i>S.</i> Braenderup 04E01347, 04E00783, 04E01556) recovered from tomato-linked outbreaks of salmonellosis was tested in mature and immature tomatoes of three varieties and in peppers. Pairwise comparisons were conducted using the Student’s <i>t</i> test. Lower case letters indicate groupings (p<0.05).</p>", "links"=>[], "tags"=>["differences", "proliferation"], "article_id"=>867957, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g003", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Serotype_level_differences_in_Salmonella_proliferation_in_tomatoes_/867957", "title"=>"Serotype-level differences in <i>Salmonella</i> proliferation in tomatoes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302742"], "description"=>"<p>Tomatoes (cultivars Bonny Best, Solar Fire and Florida-47) were harvested in the field as for the commercial harvest, infected with 10<sup>2</sup> CFU of <i>Salmonella</i> and incubated for a week. Maturity stages of the fruits at the time of infection with <i>Salmonella</i> were assessed using the USDA guide for tomato maturity. Tomato ripeness was assessed using USDA maturity chart. Tomatoes that were at stages 5 or 6 at field harvest were considered “ripe”, those that were harvested at stage 4 or below and then ripened during the experiment, were considered “partially ripe”, and those that were harvested at stage 3 or below and did not ripen beyond stage 5 during the experiment were considered “unripe”. An increase in <i>Salmonella</i> proliferation per fruit, relative to the initial inoculum is plotted. Medians are plotted, whiskers are standard errors. <b>A.</b> Effect of fruit ripeness as the main effect on <i>Salmonella</i> proliferation. <b>B.</b> Effect of the tomato genotype as the main effect on <i>Salmonella</i> proliferation. <b>C.</b> The effect of interactions between tomato genotype and maturity on <i>Salmonella</i> proliferation. Data from all samplings are included in each chart. Lower-case letters within the chart indicate groupings (p<0.05).</p>", "links"=>[], "tags"=>["genotype", "ripeness", "proliferation"], "article_id"=>867956, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_tomato_genotype_and_fruit_ripeness_on_proliferation_of_Salmonella_/867956", "title"=>"Effects of tomato genotype and fruit ripeness on proliferation of <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302751"], "description"=>"<p>The effect of independent variables (tomato cultivar, ripening stage, irrigation regime) on the susceptibility of the crop to proliferation of <i>Salmonella</i>.</p>", "links"=>[], "tags"=>["variables", "ripening", "irrigation", "susceptibility", "proliferation"], "article_id"=>867965, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.t004", "stats"=>{"downloads"=>2, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_independent_variables_tomato_cultivar_ripening_stage_irrigation_regime_on_the_susceptibility_of_the_crop_to_proliferation_of_Salmonella_/867965", "title"=>"The effect of independent variables (tomato cultivar, ripening stage, irrigation regime) on the susceptibility of the crop to proliferation of <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302750"], "description"=>"<p>Tomatoes (cv. Amelia) were grown in Citra, FL in the Spring 2013 production season. Rinsated were collected from field-growth tomatoes in sterile tap water, and these were used to re-inoculate some of the tomatoes. UV disinfection was carried out for 10 min on the blossom end of the tomato, and 10 min on the stem-scar end in a Nuaire Class II Type A2 Biosafety hood under a Sylvania Germicidal Lamp (254 nm). Control tomatoes were not re-inoculated following the surface disinfection. All tomatoes were then infected with <i>Salmonella</i> Typhimurium ATCC 14028.</p>", "links"=>[], "tags"=>["disinfected"], "article_id"=>867964, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proliferation_of_Salmonella_in_surface_disinfected_tomatoes_/867964", "title"=>"Proliferation of <i>Salmonella</i> in surface disinfected tomatoes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302745"], "description"=>"<p>Bacterial spot disease severity and viral symptoms in tomato cv. Bonny Best were ranked based on a 1 10 scale, where 1 is a blemish-free fruit, and 10 is severely damaged fruit (Panels A, B). <i>Xanthomonas, Pseudomonas</i> and <i>Sphingomonas</i> were recovered from the bacterial spot lesions, viral symptoms were consistent with infections by Tomato Yellow Leaf Curl group virus. Fruit cracking and defoliation (as percentage of remaining green foliage) of the tomato cv. Solar Fire was assessed as an indirect measure of plant health (Panels C, D). The survey was conducted in the third production season in Fall 2012, Citra, FL. Double-blind disease severity rankings were conducted by two scientists independently on different days during the growing season; <i>Salmonella</i> proliferation and correlation analyses were conducted by a third scientist. Proliferation of <i>Salmonella</i> in blemish-free tomatoes harvested from these plants was tested. Box plots indicate relative proliferation of the type strain and the outbreak strains in blemish-free tomatoes from the corresponding treatments. The fitted regression lines are displayed in red and the P values (α = 0.05) of the F tests for the slope parameters are: Panel A = 0.0024, Panel B = 0.2508, Panel C = 0.0078 (not significant), and Panel D = 0.0462.</p>", "links"=>[], "tags"=>["symptoms", "susceptibility"], "article_id"=>867959, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g004", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_of_plant_disease_symptoms_with_susceptibility_to_Salmonella_/867959", "title"=>"Correlation of plant disease symptoms with susceptibility to <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302741"], "description"=>"<p>Tomatoes (cultivars Bonny Best, Florida-47, and Solar Fire, indicated on the right y-axis) were grown under differential irrigation regimes: D (“dry”) = 6%, M (“medium”) = 10% (recommended for tomato production), W (“wet”) = 12% volumetric soil moisture contents were imposed within two weeks of the first harvest. Four independent samplings (A, B, C, D, top x-axis) were conducted: once in Spring 2011 and Spring 2012, and twice in Fall 2012. At each sampling, at least 55 tomatoes from each treatment were harvested and infected with ∼10<sup>2</sup> CFU of <i>S.</i> Typhimurium 14028 or the cocktail of the six strains of <i>Salmonella</i> recovered from tomato-related human outbreaks. Upon completion of a 1-week incubation, <i>Salmonella</i> cells were recovered on Xylose Lysine Deoxycholate (XLD) agar and an increase in proliferation was calculated as Log (CFU/fruit<sub>HARVEST</sub>/CFU/fruit<sub>INOCULUM</sub>) and plotted on the y-axis for each tomato cultivar. Data for infections with both types of inocula are shown. “Unripe” tomatoes were mature green (stage 1 of the USDA Color Classification Requirements, <a href=\"http://ucanr.edu/repository/a/a=83755\" target=\"_blank\">http://ucanr.edu/repository/a/a=83755</a>) at field harvest and <i>Salmonella</i> infection and were either breakers, turning, pink or light red (stages 2, 3, 4 or 5) upon completion of the 1 week-long incubation. “Partially ripe” refers for tomatoes that were mature green, breakers, turning or pink (stages 1, 2, 3 or 4) at field harvest and infection with <i>Salmonella</i>, but turned light red or red (stages 5 or 6) upon completion of the incubation. “Ripe” refers to tomatoes that were light red or red (stages 5 or 6) at field harvest and turned or stayed red during the incubation under the laboratory conditions. In box plots boxes include the lower and upper quartiles, thick lines within the box are the medians and whiskers indicate the degree of dispersion of the data. Outlier data are shown as dots.</p>", "links"=>[], "tags"=>["proliferation", "ripe", "un-ripe", "tomatoes", "grown", "irrigation"], "article_id"=>867955, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.g001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Post_harvest_proliferation_of_Salmonella_in_ripe_and_un_ripe_tomatoes_grown_under_different_irrigation_regimes_/867955", "title"=>"Post-harvest proliferation of <i>Salmonella</i> in ripe and un-ripe tomatoes grown under different irrigation regimes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-04 03:05:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1302753"], "description"=>"<p>An asterisk (*) indicates statistically significant interactions between variables.</p>1<p>“Time of harvest” refers to the field sampling date (Spring 2011, Spring 2012 and twice in Fall 2012).</p>", "links"=>[], "tags"=>["iii", "two-way", "three-way", "irrigation", "sampling", "susceptibility", "proliferation"], "article_id"=>867967, "categories"=>["Biological Sciences", "Earth and Environmental Sciences"], "users"=>["Massimiliano Marvasi", "George J. Hochmuth", "Mihai C. Giurcanu", "Andrée S. George", "Jason T. Noel", "Jerry Bartz", "Max Teplitski"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080871.t002", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Type_III_F_tests_for_the_main_two_way_and_three_way_interaction_effects_of_irrigation_levels_tomato_cultivar_Salmonella_strain_tomato_maturity_and_sampling_on_the_susceptibility_of_the_tomato_to_proliferation_of_Salmonella_/867967", "title"=>"Type III F tests for the main, two-way and three-way interaction effects of irrigation levels, tomato cultivar, <i>Salmonella</i> strain, tomato maturity, and sampling on the susceptibility of the tomato to proliferation of <i>Salmonella</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-04 03:05:29"}

PMC Usage Stats | Further Information

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Relative Metric

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