Growth of Salmonella enterica in foliar pesticide solutions and its survival during field production and postharvest handling of fresh market tomato

Journal of Applied Microbiology

Volumn 114, Issue 5, 2013, Pages 1547-1558

  Lopez Velasco, G ^a   Tomas Callejas, A ^a   Diribsa, D ^a   Wei, P ^a   Suslow, T V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Foliar pesticide solutions; Food safety; Preharvest water; Salmonella serovars; Survival; Tomato

Indexed keywords

COMMERCE; FOOD SAFETY; FRUITS; GROWTH KINETICS; WATER POLLUTION;

FOLIAR PESTICIDE SOLUTION; FOOD-SAFETY; IN-VITRO; PESTICIDE SOLUTIONS; POSTHARVEST; PREHARVE WATER; SALMONELLA ENTERICA; SALMONELLA SEROVARS; SURVIVAL; TOMATO;

SALMONELLA;

HYPOCHLORITE SODIUM; PESTICIDE; TAP WATER;

CROP PRODUCTION; GROWTH RATE; HARVESTING; MICROBIAL COMMUNITY; MICROBIOLOGY; PESTICIDE; SURVIVAL; VEGETABLE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; CROP PRODUCTION; IN VITRO STUDY; LEAF LITTER; MARKET; NONHUMAN; POSTHARVEST PERIOD; SALMONELLA ENTERICA; STORAGE TEMPERATURE; TEMPERATURE; TOMATO; WATER CONTAMINATION; WATER QUALITY; WATER SUPPLY;

LYCOPERSICON ESCULENTUM; SALMONELLA; SALMONELLA ENTERICA;

EID: 84876413212     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12150     Document Type: Article

References (40)

1. Aislabie, J. and Lloyd-Jones, G. (1995) A review of bacterial degradation of pesticides. Australian J Soil Res 33, 925-942.
2. Barak, J.D., Kramer, L.C. and Hao, L.Y. (2011) Colonization of tomato plants by Salmonella enterica is cultivar dependent, and type 1 trichomes are preferred colonization sites. Appl Environ Microbiol 77, 498-504.
3. Centers for Disease Control and Prevention (2011) CDC estimates of foodborne illness in the United States. Available at: http://wwwcdcgov/foodborneburden/2011-foodborne-estimateshtml. Accession date: November 2012.
4. Cummings, K., Barrett, E., Mohle-Boetani, J.C., Brooks, J.T., Farrar, J., Hunt, T., Fiore, A., Komatsu, K. et al. (2001) A multistate outbreak of Salmonella enterica serotype Baildon associated with domestic raw tomatoes. Emerg Infect Dis 7, 1046-1048.
5. Curtiss, R. III and Kelly, S.M. (1987) Salmonella Typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun 55, 3035-3043.
6. Dinu, L.D., Delaquis, P. and Bach, S. (2009) Nonculturable response of animal enteropathogens in the agricultural environment and implications for food safety. J Food Prot 72, 1342-1354.
7. Duffy, E.A., Lucia, L.M., Kells, J.M., Castillo, A., Pillai, S.D. and Acuff, G.R. (2005) Concentrations of Escherichia coli and genetic diversity and antibiotic resistance profiling of Salmonella isolated from irrigation water, packing shed equipment, and fresh produce in Texas. J Food Prot 68, 70-79.
8. Espinoza-Medina, I.E., Rodriguez-Leyva, F.J., Vargas-Arispuro, I., Islas-Osuna, M.A., Acedo-Felix, E. and Martinez-Tellez, M.A. (2006) PCR identification of Salmonella: potential contamination sources from production and postharvest handling of cantaloupes. J Food Prot 69, 1422-1425.
9. Food and Drug Administration (2011) Food safety modernization act. Available at: http://www.gpo.gov/fdsys/pkg/PLAW-111publ353/pdf/PLAW-111publ353.pdf. Access date: October 1, 2012.
10. Franz, E. and van Bruggen, A.H. (2008) Ecology of E. coli O157:H7 and Salmonella enterica in the primary vegetable production chain. Crit Rev Microbiol 34, 143-161.
11. Greene, S.K., Daly, E.R., Talbot, E.A., Demma, L.J., Holzbauer, S., Patel, N.J., Hill, T.A., Walderhaug, M.O. et al. (2008) Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiol Infect 136, 157-165.
12. Guan, T.Y., Blank, G., Ismond, A. and Van Acker, R. (2001) Fate of foodborne bacterial pathogens in pesticide products. J Sci Food Agric 81, 503-512.
13. Guan, T.T., Blank, G. and Holley, R.A. (2005) Survival of pathogenic bacteria in pesticide solutions and on treated tomato plants. J Food Prot 68, 296-304.
14. Gupta, A. and Crowe, C. (2001) Multi-State Outbreak of Salmonella Thompson, November-December, 2000. Atlanta, GA: Center for Disease Control and Prevention.
15. Gupta, S.K., Nalluswami, K., Snider, C., Perch, M., Balasegaram, M., Burmeister, D., Lockett, J., Sandt, C. et al. (2007) Outbreak of Salmonella Braenderup infections associated with Roma tomatoes, northeastern United States, 2004: a useful method for subtyping exposures in field investigations. Epidemiol Infect 135, 1165-1173.
16. Hanning, I.B., Nutt, J.D. and Ricke, S.C. (2009) Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathog Dis 6, 635-648.
17. Hassan, J.O. and Curtiss, R. III (1990) Control of colonization by virulent Salmonella Typhimurium by oral immunization of chickens with avirulent ΔcyaΔcrp S. Typhimurium. Res Microbiol 141, 839-850.
18. Herwaldt, B.L. and Beach, M.J. (1999) The return of Cyclospora in 1997: another outbreak of cyclosporiasis in North America associated with imported raspberries. Cyclospora Working Group. Ann Intern Med 130, 210-220.
19. Hochbert, E.G. (1996) The market for agricultural pesticides inert ingredients. In Pesticide Formulation and Adjuvant Technology ed. Foy, C.L. and Pritchard, D.W. pp. 203-208. Boca Raton, FL: CRC Press.
20. Horby, P.W., O'Brien, S.J., Adak, G.K., Graham, C., Hawker, J.I., Hunter, P., Lane, C., Lawson, A.J. et al. (2003) A national outbreak of multi-resistant Salmonella enterica serovar Typhimurium definitive phage type (DT) 104 associated with consumption of lettuce. Epidemiol Infect 130, 169-178.
21. Lopez-Velasco, G., Sbodio, A., Tomas-Callejas, A., Wei, P., Tan, K.H. and Suslow, T.V. (2012a) Assessment of root uptake and systemic vine-transport of Salmonella enterica sv. Typhimurium by melon (Cucumis melo) during field production. Int J Food Microbiol 158, 65-72.
22. Lopez-Velasco, G., Tomas-Callejas, A., Sbodio, A., Artes-Hernandez, F. and Suslow, T.V. (2012b) Chlorine dioxide dose, water quality and temperature affect the oxidative status of tomato processing water and its ability to inactivate Salmonella. Food Control 26, 28-35.
23. Mody, R.K., Greene, S.A., Gaul, L., Sever, A., Pichette, S., Zambrana, I., Dang, T., Gass, A. et al. (2011) National outbreak of Salmonella serotype saintpaul infections: importance of Texas restaurant investigations in implicating jalapeno peppers. PLoS ONE 6, e16579.
24. Ng, P.J., Fleet, G.H. and Heard, G.M. (2005) Pesticides as a source of microbial contamination of salad vegetables. Int J Food Microbiol 101, 237-250.
25. Olaimat, A.N. and Holley, R.A. (2012) Factors influencing the microbial safety of fresh produce: a review. Food Microbiol 32, 1-19.
26. Pachepsky, Y.A., Shelton, D.R., Mclain, J.E., Patel, J.R. and Mandrell, R.E. (2011) Irrigation waters as a source of pathogenic microorganisms in produce: a review. Adv Agron. 113, 73-138.
27. Park, E.J., Alexander, E., Taylor, G.A., Costa, R. and Kang, D.H. (2009) The decontaminative effects of acidic electrolyzed water for Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocytogenes on green onions and tomatoes with differing organic demands. Food Microbiol 26, 386-390.
28. Pham, C.H., Min, J. and Gu, M.B. (2004) Pesticide induced toxicity and stress response in bacterial cells. Bull Environ Contam Toxicol 72, 380-386.
29. Rajabi, M., Jones, M., Hubbard, M., Rodrick, G. and Wright, A.C. (2011) Distribution and Genetic Diversity of Salmonella enterica in the Upper Suwannee River. Int J Food Microbiol 2011, 461321.
30. Ribot, E.M., Fair, M.A., Gautom, R., Cameron, D.N., Hunter, S.B., Swaminathan, B. and Barrett, T.J. (2006) Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3, 59-67.
31. Santo Domingo, J.W., Harmon, S. and Bennett, J. (2000) Survival of Salmonella species in river water. Curr Microbiol 40, 409-417.
32. Stine, S.W., Song, I., Choi, C.Y. and Gerba, C.P. (2011) Application of pesticide sprays to fresh produce: a risk assessment for Hepatitis A and Salmonella. Food Environ Virol 3, 86-91.
33. Suslow, T.V. (2010) Standards for irrigation and foliar contact water. Produce safety project issue brief. Available at: http://www.producesafetyproject.org/admin/assets Accessed date: December 19, 2011.
34. Suslow, T.V., Oria, M.P., Beuchat, L.R., Garrett, E.H., Parish, M.E., Harris, L.J. and Busta, F.F. (2003) Production practices as risk factors in microbial food safety of fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2, 38-77.
35. Tomas-Callejas, A., Lopez-Velasco, G., Camacho, A.B., Artes, F., Artes-Hernandez, F. and Suslow, T.V. (2011) Survival and distribution of Escherichia coli on diverse fresh-cut baby leafy greens under preharvest through postharvest conditions. Int J Food Microbiol 151, 216-222.
36. Tomas-Callejas, A., Lopez-Velasco, G., Valadez, A.M., Sbodio, A., Artes-Hernandez, F., Danyluk, M.D. and Suslow, T.V. (2012) Evaluation of current operating standards for chlorine dioxide in disinfection of dump tank and flume for fresh tomatoes. J Food Prot 75, 304-313.
37. Tournas, V.H. (2005) Spoilage of vegetable crops by bacteria and fungi and related health hazards. Crit Rev Microbiol 31, 33-44.
38. United Fresh (2008) Commodity specific food safety guidelines for the fresh tomato supply chain. Availabe at: http://www.unitedfresh.org/assets/files/TomatoGuidelinesJuly08FINAL.pdf. Accessed: September 2012.
39. Wang, G., Zhao, T. and Doyle, M.P. (1996) Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces. Appl Environ Microbiol 62, 2567-2570.
40. Winfield, M.D. and Groisman, E.A. (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69, 3687-3694.