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Contamination of Foods by Pathogens in the Environment Michael P. Doyle.

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1 Contamination of Foods by Pathogens in the Environment Michael P. Doyle

2 Reservoirs of Enteric Foodborne Pathogens Carried in intestinal tract of wild and domestic animals (including cattle, poultry, and swine) and/or symptomatic and occasionally asymptomatic people Includes Salmonella, Campylobacter, enterohemorrhagic E. coli O157:H7 (principally cattle)

3 Primary Sources of Enteric Foodborne Pathogens that Contaminate Foods Animal manure Human feces

4 Transmission of Enteric Foodborne Pathogens to Foods Direct or indirect contact with animal or human feces Fecal matter can contaminate foods through: Use as a soil fertilizer in fields Polluted irrigation or processing water Defecation by animals in vicinity of produce fields or processing areas Presence on contact surfaces of food handling equipment Transmission by insects such as flies Human carriers with poor personal hygiene harvesting or handling foods

5 The Manure Glut: A Growing Environmental Threat Five tons of animal manure is produced annually nationwide for every person living in the United States -The amount of animal manure is 130 times greater than the amount of human waste produced -Cattle, hogs, chickens and turkey produced an estimated 1.36 billion tons of manure in 1997 Democratic Staff of U.S. Senate Agriculture Committee (1998) “Animal Waste Pollution in America: An Emerging National Problem”

6 The U.S. Manure Glut (1997 estimates) Animal Solid Waste (Tons/yr) Cattle 1,229,190,000 Hogs 112,652,300 Chickens 14,394,000 Turkeys 5,425,000 TOTAL 1.36 billion

7 Reported Levels of Pathogens in Animal Manures PathogenAnimal Cattle PoultrySheep (CFU or Oocysts/g) Campylobacter 10 4 - 10 8 10 4 - 10 7 up to 10 5 Salmonella up to 10 8 - 10 10 10 4 - 10 7 no information E. coli O157:H7 10 2 - 10 5 — up to 10 8

8 Fate of Salmonella Typhimurium and E. coli O157:H7 on Vegetables in Fields Treated with Contaminated Manure Composts or Irrigation Water Mahbub Islam, Jennie Morgan, Michael Doyle, Sharad Phatak, Patricia Millner and Xiuping Jiang

9 Objective To determine the fate of an avirulent strain of Salmonella Typhimurium or E. coli O157:H7 on harvestable vegetables and in surrounding soil when manure composts of different types or irrigation water contaminated with salmonellae or E. coli O157:H7 are applied to soil in fields typical of those used for vegetable production

10 Research Approach Studies were done in fields on the Horticulture Farm of the University of Georgia Experiment Station in Tifton Avirulent Salmonella enterica serovar Typhimurium (x3985σcrp11, cya12) or Avirulent Escherichia coli O157:H7 (strain B6914) without stx1 and stx2 used for inoculation -Inoculate composts at 10 7 cfu/g -Inoculate irrigation water at 10 5 cfu/ml

11 Research Approach Three types of manure compost were applied separately to soil as strips at 2 tons/acre (41.6 g/sq ft) -Poultry manure compost -Dairy cattle manure compost -Alkaline-stabilized dairy manure compost (NVIRO-4) -Composts prepared by Patricia Millner (USDA) No chemical treatments were applied

12 Research Approach Vegetable crops -Carrots -Radishes Leaf lettuce -Parsley -Onions

13 Lettuce ○ = irrigation water solid = composts □ = control

14 Parsley ○ = irrigation water solid = composts □ = control

15 Carrots ○ = irrigation water solid = composts □ = control

16 Radishes ○ = irrigation water solid = composts □ = control

17 Onions ○ = irrigation water solid = composts □ = control

18 Carrots ○ = irrigation water solid = composts □ = control

19 Parsley ○ = irrigation water solid = composts □ = control

20 Lettuce ○ = irrigation water solid = composts □ = control

21 Conclusions Salmonella survival or occurrence was greatest: -On carrots (203 days) -In soil on which carrots and radishes were grown (231 days); parsley was 203-231 days Salmonella survival or occurrence was least: -On lettuce (63 days) and radishes (84 days) -In soil on which lettuce was grown (161 days) Salmonella occurrence was intermediate: -On parsley (161 days)

22 Conclusions E. coli O157 survival or occurrence was greatest: -On parsley (177 days) and carrots (175 days) -In soil on which parsley (217 days) and carrots (196 days) were grown E. coli O157 survival or occurrence was least: -On lettuce (77 days) and onions (84 days) -In soil on which lettuce (154 days) and onions (168 days) were grown

23 Conclusions Once E. coli O157:H7 or Salmonella are introduced into soil or onto seedlings, either via contaminated irrigation water or compost, these bacteria can contaminate for months vegetables and the soil in which vegetables are grown

24 Prevalence of Salmonella on U.S.- Grown Produce Produce TypeNo. SampledNo. Positive Cantaloupe 1644 Celery 1200 Cilantro 851 Green Onions 930 Lettuce 1421 Parsley 900 Strawberries 1360 Tomatoes 1980 Total1028 6 (0.6%) U.S. Food and Drug Administration 2002

25 Prevalence of Salmonella on Imported Produce 35 (3.5%) 1003 Total 0 20Tomatoes 1 143Strawberries 1 180Scallions 1 84Parsley 1 116 Lettuce (loose-leaf) 6 12Culantro 16 177Cilantro 1 84Celery 8 151Cantaloupe 0 36Broccoli No. PositiveNo. SampledProduce Type

26 Examples of Outbreaks of Salmonellosis Associated with Fresh-cut Lettuce 392 cases of S. Typhimurium PT204b infection in Iceland, England, Wales, The Netherlands, Scotland, and Germany in Summer of 2000 -Vehicle - shredded lettuce (Crook et al., Salmonella & Salmonellosis 2002:387-391) 19 cases of S. Newport PT33 infection in England and Wales between Jan - Jun 2001 -Vehicle - retail, pre-packaged, ready-to-eat Four Leaf salad -Same indistinguishable strain (PFGE, phage type) isolated from intact product obtained at retail and from patient isolates (Ward et al., Salmonella & Salmonellosis 2002:433-434)

27 Microbiological Study of RTE Salad Vegetables for Foodborne Pathogens in the UK Sources of Salmonella included: -The one isolate of S. Newport PT33 was indistinguishable by subtyping from 19 S. Newport PT33 isolates from cases of salmonellosis identified throughout England and Wales 1. S. Newport PT33Four-leaf saladSpainConventional grower 2. S. UmbiloWild rocket saladItalyOrganic grower 3. S. DurbanOrganic saladItalyOrganic grower 4. S. UmbiloFour-leaf saladItalyOrganic grower 5. S. UmbiloWild rocket saladItalyOrganic grower

28 Salmonellosis Outbreak Associated with Cantaloupes More than 400 cases of Salmonella Poona infection in 23 states and Canada during June-July 1991 Vehicle - cantaloupe -Likely source of cantaloupe was Rio Grande region of Texas -Implicated cantaloupe associated with fruit salads from salad bars FDA survey of imported cantaloupes and watermelons at US border in 1990 and 1991 isolated Salmonella spp. From about 1% of rinds

29 Examples of Salmonellosis Outbreaks Associated with Melons 58 Multistate, Canada S. PoonaCantaloupe2002 50MultistateS. Poona Cantaloupe 2001 47MultistateS. PoonaCantaloupe2000 22Canada S. Oranienburg Cantaloupe1998 24CaliforniaS. SaphraCantaloupe1997 > 400MultistateS. PoonaCantaloupe1991 39MichiganS. JavianaWatermelon1991 7245MultistateS. ChesterCantaloupe1989-90 18Illinois S. Oranienburg Watermelon1979 17MassachusettsS. MiamiWatermelon1954 No. of CasesLocationPathogenType of MelonYear

30 Examples of Outbreaks of Salmonellosis Associated with Tomatoes Two multistate (midwest) outbreaks of salmonellosis identified by laboratory-based surveillance In 1990, 176 cases of S. Javiana In 1993, 100 cases of S. Montevideo Source: Tomatoes from a single South Carolina tomato packer -Contamination likely occurred at packing shed -Field-grown tomatoes dumped into common water bath -Tomatoes placed in water cooler then tomato pulp absorb water and salmonellae into core tissues through stem scar

31 Examples of Outbreaks of Salmonellosis Associated with Tomatoes Packing Shed512 24 States S. Newport2002 Field Contamination 85 Multistate S. Bailden 1998-99 Packing Shed100 Multistate S. Montevideo 1993 Packing Shed176 Multistate S. Javiana1990 Likely Source of Contamination No. of Cases LocationPathogenDate

32 Conclusions -Feces are the primary source of enteric pathogen contamination of foods -Cattle manure is the dominant type of manure applied to soil -A wide variety of pathogens contaminate cattle manure, often in 10 to 25% of samples -Pathogens can survive in manure/compost- amended soil and on produce grown in such soil for extended periods of time (many months)

33 Conclusions Practical and effective treatments are needed at the farm to reduce intestinal carriage of pathogens by animals (especially cattle) and to reduce/eliminate pathogens in manure

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