Food Safety Research Involving Tomatoes: What We Know and What We Need to Know

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1 Food Safety Research Involving Tomatoes: What We Know and What We Need to Know Robert L. Buchanan, Ph.D. DHHS Food and Drug Administration Center for Food Safety and Applied Nutrition

2 Presentation Tomatoes as a food safety problem What we know some research highlights What we need to know some research needs Concluding remarks

3 Produce Safety During the past 10 years there has been heightened concern about the microbiological safety of fresh produce Focus, particularly in the last several years, has been largely domestic produce

4 Vehicle Categories Category Processed Foods Outbreaks Illnesses 43 3,026 Produce 63 8,040 Sprouts 25 1,565 Seafood 120 2,567 Eggs 234 6,572

5 Produce Outbreaks by Commodity Tomatoes 12 Green Onions 3 Lettuce 12 Mango 2 Romaine Lettuce 4 Almonds 2 Mixed Lettuce 1 Parsley 2 Cabbage 1 Basil 4 Spinach 2 Green Grapes 1 Cantaloupe 7 Snow Peas 1 Melons 2 Basil or Mesclun 2 Honeydew Melon 2 Squash 1 Raspberries 5 Unknown 2

6 History of Tomato Outbreaks 1998 S. Baildon 2000 S. Thompson 2002 S. Newport S. Newport S. Javiana 2004 S. Javiana S. Braenderup 2005 S. Newport S. Braenderup S. Enteritidis 2006 S. Typhimurium S. Newport 86 cases 29 cases 512 cases 12 cases 90 cases 471 cases 123 cases 71 cases 73 cases 73 cases 191 cases 98 cases

7 What We Know

8 Research with Tomatoes The research pertinent to food safety concerns spans over 60 years of work Early work on market diseases still pertinent One of the primary commodities studied under produce safety The amount of research funding has be miniscule compared to animal products Need for better interaction between plant pathologists, horticulturists, and food microbiologists Very little work on the farm

9 Tomatoes: Challenging Common Knowledge Tomatoes are an acidic food that do not support the growth of foodborne pathogens Asplund and Nurmi,, 1991 Small cubes of tomatoes supported growth of Salmonella enterica at 22 and 30 C C but not at 7 C7 Beuchat and Brackett, 1991 Listeria monocytogenes grew on whole cherry tomatoes at 21 C C but not at 10 C L. monocytogenes declined at 10 and 21 C C in chopped tomatoes Wei et al., 1995 Salmonella Montevideo survived on tomato skins and stem scars and grew in puncture wounds and on tomatoes slices at 20 and 25 C

10 Tomatoes: Challenging Common Knowledge Standard wisdom: Tomatoes are an acidic food that do not support the growth of foodborne pathogens Zhuang et al., 1995 Salmonella Montevideo grew on surface of tomatoes at 20 and 30 C C but not at 10 C Weissinger et al., 2000 Growth of Salmonella Baildon in diced tomatoes at 21 and 30 C, and slow decline at 4 C4 Wade and Beuchat,, 2003a Chill injury and co-growth of proteolytic yeast enhanced the growth of Salmonella enterica Wade and Beuchat,, 2003b Salmonella grew in puncture wounds at 15 and 25 C Warriner,, 2006 Variety of Salmonella serovars grew at 25ºC C in tomatoes that had inoculated by vacuum infiltration

11 Tomatoes: Challenging Common Knowledge Standard Wisdom: Interior of tomatoes is sterile Samish et al., % of intact tomatoes have a detectable internal microflora consisting predominately of Xanthomonas,, Pseudomonas, Enterobacter, Escherichia, Flavobacterium, and Corynebacterium Samish and Etinger-Tulezynska Tulezynska,, 1963 Spotting of Serratia marcesens onto the sepals (calyx) led to presence of the bacterium in the tomato Guo et al., 2001 Salmonella enterica injected into stems or brushed on flowers resulted in 1/3 of mature being positive Warriner,, 2006 Inoculation of flowers with a variety of Salmonella serovars led to the microorganism on surface and interior of tomatoes Higher rate with serovars associated with tomato outbreaks

12 Antimicrobial Treatments A number of potential treatments have been evaluated Calcinated calcium Tap water Chlorinated water Wei et al., 1995 Zhuang et al., 1995 Weissinger et al., 2000 Bari et al., 2004 Yuk et al., 2005 Simmons et al., 2006 Hydrogen peroxide Sapers and Jones, 2006 Bari et al., 2002 Peroxyacetic acid Yuk et al, 2005 Chlorine dioxide Yuk et al., 2005 Trisodium phosphate Zhuang and Beuchat, 1996

13 Antimicrobial Treatments A number of potential treatments have been evaluated Electrolyzed alkaline water (GC-100X) Organic acids Kwon et al., 2003 Electrolyzed acidic water Bari et al., 2003 Electrolyzed neutral water Deza et al., 2003 Acidified sodium chlorite Yuk et al., 2005 Ibarra-Sanchez et al., 2004 Yoon et al., 2004 Hydroxypropyl methylcellulose (HPMC) coating Zhuang et al., 1996 Electron beam irradiation Schmidt et al., 2006

14 Antimicrobial Treatments Treatment efficacy rule of thumb 1 to 4 log reduction on unblemished, undamaged, unwaxed skin 1 to 2 log reduction on stem scar 0 to 1 log reduction for puncture wounds 0 to 2 log reduction on internalized cells Spraying or dipping did not make that much difference The primary effect of including antimicrobials in dump tanks and flumes is to reduce cross contamination

15 Antimicrobial Treatments Substantial diversity among results and claims Results influenced by Method of inoculation Site of inoculation Method of application Temperature of application Method of recovery Organic load Internalization (i.e., infiltration) of bacteria into tomato reduces efficacy of antimicrobial treatments Need for standardized testing protocol

16 Infiltration Research with both pathogens and market disease agents have demonstrated potential for uptake of microorganisms into tomatoes Hall et al, 1970 Bartz and Showalter, 1981 Bartz,, 1982 Zhuang et al., 1995 Bartz,, 1999 Ibara-Sanchez et al., 2004 Warriner,, 2006

17 Infiltration Uptake of bacteria into tomatoes fostered by Temperature differential Pressure differential due to hydrostatic head Pulling a vacuum Increased by inclusion of surfactants overcome hydrophobic nature of stem scar Entrance through stem scar, skin breaks and puncture wounds Can we take advantage of this phenomenon to get antimicrobial treatments into the tomato?

18 Primary Production Guan et al., 2005 Foodborne pathogens can survive in many pesticide solutions for at least 48 h Salmonella Enteritidis and E. coli O157:H7 survived on leaves for up to 56 days, but only for 45 hr on tomato skins Rathinasabapathi,, log reduction of Salmonella Montevideo on tomato leaves and green tomatoes after 48 h at 60% RH but no reduction 100% RH Salmonella Montevideo was unaffected by exposure of green tomatoes to ethylene

19 What We Need to Know

20 On the Farm Most critical area in terms of needed knowledge Sources/reservoir of Salmonella? Vectors and vehicles? Internalization? Impact of farm practices?

21 On the Farm Sources/reservoir of Salmonella? Are there environmental reservoirs for Salmonella? Are there domestic or wild animal reservoirs for Salmonella? Are there human reservoirs for Salmonella? Are there specific seasons associated with contamination of tomatoes in the field? What is the prevalence of Salmonella in tomato seeds? How long can Salmonella persist in tomato fields? In plant waste?

22 On the Farm Sources/reservoir of Salmonella? Why are specific serotypes associated with tomatoes? Is it because this reflects their presence in the environment or that they are host- adapted to infect or grow on/in tomatoes?

23 On the Farm What vectors or vehicles are important in transmitting Salmonella from source to tomato plant or fruit? Wild animals Insects Nematodes Water Airborne Humans Irrigation water Pesticide applications Soil Amendments

24 On the Farm What is the potential role of internalization of Salmonella in the tomato fruit? Can Salmonella in seeds be taken up by seedling? Are certain varieties more resistant to internalization? Are there specific times when developing tomato plant is most likely to take up Salmonella through the root system? Can biting insects inoculate the tomato plant or fruit with Salmonella?

25 Potential for internalization of Salmonella? On the Farm What is the practical significance of Salmonella inoculation via the flower? What insect vectors are involved? What is the increased risk due to cracking and splits? At what stage is tomato plant most susceptible to internalization?

26 Farm Practices On the Farm Does the method of cultivation (e.g., stake, bush, black plastic) influence the potential for contamination? Does the method of irrigation influence the potential for contamination? Does the method of harvest influence the level of contamination?

27 Farm Practices Does the method of pesticide application influence the potential for contamination? How amenable are current equipment (e.g,, harvest equipment, totes, pesticide applicators) to disinfection? On the Farm

28 Farm Practices On the Farm What adjacent land uses contribute to the potential for contamination? Are the Salmonella strains associated with tomatoes match the Salmonella strains associated with farm workers? What food handling practices during harvesting contribute to risk of contamination? Can competitive exclusion concepts be applied to tomatoes?

29 Farm Practices On the Farm Does the rate of crop rotations influence the potential for contamination. Are current requirements for composting and/or pasteurization of animal manures sufficient to eliminate Salmonella? Does the plowing under of plant waste increase the survival of Salmonella in the environment?

30 Post-Harvest What is the prevalence of Salmonella in tomatoes not subjected to factors that increase infiltration? What would be the prevalence with a dry processing system?

31 Post-Harvest Are there better approaches for inactivating internalized Salmonella? Are there specific pre- and post-market diseases that foster Salmonella post-harvest contamination or growth? What is the practical increase in risk of Salmonella contamination in chill injured tomatoes? What are the cooling and cold chain requirements that are needed to prevent the growth of Salmonella on tomatoes (How warm can you go and not get growth)? Is growth of internalized Salmonella inhibited until a specific stage of maturity? Is the temperature in the ripening room high enough to support the growth of Salmonella?

32 Post-Harvest Are there marketing practices that contribute to the growth of Salmonella on tomatoes? Are there practical secondary barriers to prevent the growth Salmonella after slicing or dicing tomatoes?

33 Concluding Remarks

34 Concluding Remarks The research needs identified are not all inclusive but reflect the thoughts of a number of people at FDA, CDC and USDA discussing possibilities Have not tried to prioritize research needs We need your help Our most critical needs at this time are risk mitigation options on the farm?

35 Concluding Remarks No magic bullet is on the horizon; need a toolbox full of pre-harvest harvest and post-harvest control measures?

36 Concluding Remarks Thanks in advance for your help!!!!!