Ecological prevalence, genetic diversity, and epidemiological aspects of Salmonella isolated from tomato agricultural regions of the Virginia Eastern Shore

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Bell, Rebecca L ^a   Zheng, Jie ^a   Burrows, Erik ^a   Allard, Sarah ^a   Wang, Charles Y ^a   Keys, Christine E ^a   Melka, David C ^a   Strain, Errol ^a   Luo, Yan ^a   Allard, Marc W ^a,c   Rideout, Steven ^b   Brown, Eric W ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Environmental reservoirs; Epidemiological impact; Prevalence and diversity; Salmonella Newport; Tomatoes

Indexed keywords

GENOMIC DNA;

AGRICULTURE; ARTICLE; BACTERIUM CULTURE; BACTERIUM ISOLATE; CONTROLLED STUDY; ECOLOGY; GENE SEQUENCE; GENETIC VARIABILITY; NONHUMAN; POLYMERASE CHAIN REACTION; PREVALENCE; PULSED FIELD GEL ELECTROPHORESIS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA JAVIANA; SALMONELLA NEWPORT; SINGLE NUCLEOTIDE POLYMORPHISM; TOMATO; UNITED STATES;

LYCOPERSICON ESCULENTUM; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR NEWPORT; SALMONELLA JAVIANA;

EID: 84931270281     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00415     Document Type: Article

References (54)

1. Allard, M. W., Luo, Y., Strain, E., Li, C., Keys, C. E., Son, I., et al. (2012). High resolution clustering of Salmonella enterica serovar Montevideo strains using a next-generation sequencing approach. BMC Genomics 13:32. doi: 10.1186/1471-2164-13-32.
2. Allard, M. W., Luo, Y., Strain, E., Pettengill, J., Timme, R., Wang, C., et al. (2013). On the evolutionary history, population genetics and diversity among isolates of Salmonella Enteritidis PFGE pattern JEGX01.0004. PLoS ONE 8:e55254. doi: 10.1371/journal.pone.0055254.
3. Andrews, W. H., Jacobson, A., and Hammack, T. S. (2011). "Salmonella," in Bacteriological Analytical Manual (U.S. Food and Drug Administration). Available online at: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm.
4. Angelo, K. M., Chu, A., Anand, M., Nguyen, T. A., Bottichio, L., Wise, M., et al. (2015). Outbreak of salmonella newport infections linked to cucumbers-United States, 2014. MMWR Morb. Mortal. Wkly. Rep. 64, 144-147.
5. Barak, J. D., Liang, A., and Narm, K. E. (2008). Differential attachment to and subsequent contamination of agricultural crops by Salmonella enterica. Appl. Environ. Microbiol. 74, 5568-5570. doi: 10.1128/AEM.01077-08.
6. Barak, J. D., and Liang, A. S. (2008). Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS ONE 3:e1657. doi: 10.1371/journal.pone.0001657.
7. Bennett, S. D., Littrell, K. W., Hill, T. A., Mahovic, M., and Behravesh, C. B. (2014). Multistate foodborne disease outbreaks associated with raw tomatoes, United States, 1990-2010: a recurring public health problem. Epidemiol. Infect. 143, 1352-1359. doi: 10.1017/S0950268814002167.
8. Cao, G., Meng, J., Strain, E., Stones, R., Pettengill, J., Zhao, S., et al. (2013). Phylogenetics and differentiation of Salmonella Newport lineages by whole genome sequencing. PLoS ONE 8:e55687. doi: 10.1371/journal.pone.0055687.
9. CDC. (2005). Outbreaks of Salmonella infectons associated with eating Roma tomatoes-United States and Canada, 2004. MMWR Morb. Mortal. Wkly. Rep. 54, 325-328.
10. CDC. (2007). Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in restaurants-United States, 2005-2006. MMWR Morb. Mortal. Wkly. Rep. 56, 909-911.
11. CDC. (2009). Standard Protocol Molecular Determination of Sertoype in Salmonella. Atlanta, GA: Center for Disease Control and Prevention.
12. CDC. (2011). Vital signs: incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveillance network, 10 U.S. sites, 1996-2010. MMWR Morb. Mortal. Wkly. Rep. 60, 749-755.
13. Christensen, L. S., Josefsen, M. H., Pedersen, K., Christensen, J., Bonnichsen, L., Sorensen, G., et al. (2011). Real-time monitoring of Salmonella enterica in free-range geese. Appl. Environ. Microbiol. 77, 3160-3162. doi: 10.1128/AEM.02356-10.
14. Deer, D. M., Lampel, K. A., and Gonzalez-Escalona, N. (2010). A versatile internal control for use as DNA in real-time PCR and as RNA in real-time reverse transcription PCR assays. Lett. Appl. Microbiol. 50, 366-372. doi: 10.1111/j.1472-765X.2010.02804.x.
15. Doyle, M. P., and Erickson, M. C. (2008). Summer meeting 2007-the problems with fresh produce: an overview. J. Appl. Microbiol. 105, 317-330. doi: 10.1111/j.1365-2672.2008.03746.x.
16. Fallacara, D. M., Monahan, C. M., Morishita, T. Y., Bremer, C. A., and Wack, R. F. (2004). Survey of parasites and bacterial pathogens from free-living waterfowl in zoological settings. Avian Dis. 48, 759-767. doi: 10.1637/7185-032904R.
17. Feare, C. J., Sanders, M. F., Blasco, R., and Bishop, J. D. (1999). Canada goose (Branta canadensis) droppings as a potential source of pathogenic bacteria. J. R. Soc. Promot. Health 119, 146-155. doi: 10.1177/146642409911900303.
18. Fish, J. T., and Pettibone, G. W. (1995). Influence of freshwater sediment on the survival of Escherichia coli and Salmonella sp. as measured by three methods of enumeration. Lett. Appl. Microbiol. 20, 277-281. doi: 10.1111/j.1472-765X.1995.tb00445.x.
19. Garcia, R., Baelum, J., Fredslund, L., Santorum, P., and Jacobsen, C. S. (2010). Influence of temperature and predation on survival of Salmonella enterica serovar Typhimurium and expression of invA in soil and manure-amended soil. Appl. Environ. Microbiol. 76, 5025-5031. doi: 10.1128/AEM.00628-10.
20. González-Escalona, N., Brown, E. W., and Zhang, G. (2012). Development and evaluation of a multiplex real-time PCR (qPCR) assay targeting ttrRSBCA locus and invA gene for accurate detection of Salmonella spp. in fresh produce and eggs. Food Res. Int. 48, 202-208. doi: 10.1016/j.foodres.2012.03.009.
21. Gonzalez-Escalona, N., Hammack, T. S., Russell, M., Jacobson, A. P., De Jesus, A. J., Brown, E. W., et al. (2009). Detection of live Salmonella sp. cells in produce by a TaqMan-based quantitative reverse transcriptase real-time PCR targeting invA mRNA. Appl. Environ. Microbiol. 75, 3714-3720. doi: 10.1128/AEM.02686-08.
22. Gorski, L., Parker, C. T., Liang, A., Cooley, M. B., Jay-Russell, M. T., Gordus, A. G., et al. (2011). Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl. Environ. Microbiol. 77, 2734-2748. doi: 10.1128/AEM.02321-10.
23. Greene, S. K., Daly, E. R., Talbot, E. A., Demma, L. J., Holzbauer, S., Patel, N. J., et al. (2008). Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiol. Infect. 136, 157-165. doi: 10.1017/S095026880700859X.
24. Gruszynski, K., Pao, S., Kim, C., Toney, D. M., Wright, K., Colon, A., et al. (2014). Evaluating gulls as potential vehicles of Salmonella enterica serotype Newport (JJPX01.0061) contamination of tomatoes grown on the eastern shore of Virginia. Appl. Environ. Microbiol. 80, 235-238. doi: 10.1128/AEM.02809-13.
25. Gruszynski, K., Pao, S., Kim, C., Toney, D., Wright, K., Ross, P. G., et al. (2013). Evaluating wildlife as a potential source of Salmonella serotype newport (JJPX01.0061) contamination for tomatoes on the eastern shore of Virginia. Zoonoses Public Health 61, 157-227. doi: 10.1111/zph.12061.
26. Guo, X., Chen, J. R., Brackett, R. E., and Beuchat, L. R. (2001). Survival of Salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Appl. Environ. Microbiol. 67, 4760-4764. doi: 10.1128/AEM.67.10.4760-4764.2001.
27. Haley, B. J., Cole, D. J., and Lipp, E. K. (2009). Distribution, diversity, and seasonality of waterborne salmonellae in a rural watershed. Appl. Environ. Microbiol. 75, 1248-1255. doi: 10.1128/AEM.01648-08.
28. 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. doi: 10.1089/fpd.2008.0232.
29. Hebrard, M., Viala, J. P., Meresse, S., Barras, F., and Aussel, L. (2009). Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J. Bacteriol. 191, 4605-4614. doi: 10.1128/JB.00144-09.
30. Hedberg, C. W., Angulo, F. J., White, K. E., Langkop, C. W., Schell, W. L., Stobierski, M. G., et al. (1999). Outbreaks of salmonellosis associated with eating uncooked tomatoes: implications for public health. Epidemiol. Infect. 122, 385-393. doi: 10.1017/S0950268899002393.
31. Hintz, L. D., Boyer, R. R., Ponder, M. A., Williams, R. C., and Rideout, S. L. (2010). Recovery of Salmonella enterica newport introduced through irrigation water from tomato (Lycopersicum esculentum) fruit, roots, stems, and leaves. Hortscience 45, 675-678.
32. Islam, M., Morgan, J., Doyle, M. P., Phatak, S. C., Millner, P., and Jiang, X. (2004). Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl. Environ. Microbiol. 70, 2497-2502. doi: 10.1128/AEM.70.4.2497-2502.2004.
33. Klimke, W., Agarwala, R., Badretdin, A., Chetvernin, S., Ciufo, S., Fedorov, B., et al. (2009). The national center for biotechnology information's protein clusters database. Nucleic Acids Res. 37, D216-D223. doi: 10.1093/nar/gkn734.
34. Malorny, B., Paccassoni, E., Fach, P., Bunge, C., Martin, A., and Helmuth, R. (2004). Diagnostic real-time PCR for detection of Salmonella in food. Appl. Environ. Microbiol. 70, 7046-7052. doi: 10.1128/AEM.70.12.7046-7052.2004.
35. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380. doi: 10.1038/nature03959.
36. Micallef, S. A., Rosenberg Goldstein, R. E., George, A., Kleinfelter, L., Boyer, M. S., McLaughlin, C. R., et al. (2012). Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid-Atlantic tomato farms. Environ. Res. 114, 31-39. doi: 10.1016/j.envres.2012.02.005.
37. Nyberg, K. A., Vinneras, B., Ottoson, J. R., Aronsson, P., and Albihn, A. (2010). Inactivation of Escherichia coli O157:H7 and Salmonella Typhimurium in manure-amended soils studied in outdoor lysimeters. Appl. Soil Ecol. 46, 398-404. doi: 10.1016/j.apsoil.2010.10.004.
38. Patchanee, P., Molla, B., White, N., Line, D. E., and Gebreyes, W. A. (2010). Tracking salmonella contamination in various watersheds and phenotypic and genotypic diversity. Foodborne Pathog. Dis. 7, 1113-1120. doi: 10.1089/fpd.2010.0572.
39. Quince, C., Lanzen, A., Curtis, T. P., Davenport, R. J., Hall, N., Head, I. M., et al. (2009). Accurate determination of microbial diversity from 454 pyrosequencing data. Nat. Methods 6, 639-641. doi: 10.1038/nmeth.1361.
40. 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. Microbiol. 2011:461321. doi: 10.1155/2011/461321.
41. Ribot, E. M., Fair, M. A., Gautom, R., Cameron, D. N., Hunter, S. B., Swaminathan, B., et al. (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. doi: 10.1089/fpd.2006.3.59.
42. Strawn, L. K., Fortes, E. D., Bihn, E. A., Nightingale, K. K., Grohn, Y. T., Worobo, R. W., et al. (2013). Landscape and meteorological factors affecting prevalence of three food-borne pathogens in fruit and vegetable farms. Appl. Environ. Microbiol. 79, 588-600. doi: 10.1128/AEM.02491-12.
43. Swaminathan, B., Barrett, T. J., Hunter, S. B., Tauxe, R. V., and Force, C. D. C. P. T. (2001). PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerging Infect. Dis. 7, 382-389. doi: 10.3201/eid0703.017303.
44. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121.
45. Trujilllo, S., Bell, R. L., Brzoska, P., Wong, L., Tebbs, R., Furtado, M., et al. (2011). "Evaluation of a fast real time PCR method for the detection of Salmonella spp.," in 111th General Meeting of the American Society for Microbiology (New Orleans, LA).
46. USDA ERS. (2009). Vegetables and Melons: Tomatoes [Online]. USDA, Economic Research Service. Available online at: http://www.ers.usda.gov/Briefing/Vegetables/tomatoes.htm (Accessed November 11, 2011).
47. Walters, S. P., Thebo, A. L., and Boehm, A. B. (2011). Impact of urbanization and agriculture on the occurrence of bacterial pathogens and stx genes in coastal waterbodies of central California. Water Res. 45, 1752-1762. doi: 10.1016/j.watres.2010.11.032.
48. Wells, J. M., and Butterfield, J. E. (1997). Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Dis. 81, 867-872. doi: 10.1094/PDIS.1997.81.8.867.
49. Wells, J. M., and Butterfield, J. E. (1999). Incidence of Salmonella on fresh fruits and vegetables affected by fungal rots or physical injury. Plant Dis. 83, 722-726. doi: 10.1094/PDIS.1999.83.8.722.
50. 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. doi: 10.1128/AEM.69.7.3687-3694.2003.
51. Wong, L., Zoder, P., Hacker, K., Nunez, A., Brzoska, P., Brevnov, M., et al. (2011). "Development and evaluation of a four-color multiplex real-time PCR assay for Salmonella detection in tomatoes," in International Association for Food Protection Annual Meeting (Milwaukee, WI).
52. Zhang, G., Brown, E. W., and Gonzalez-Escalona, N. (2011). Comparison of real-time PCR, reverse transcriptase real-time PCR, loop-mediated isothermal amplification, and the FDA conventional microbiological method for the detection of Salmonella spp. in produce. Appl. Environ. Microbiol. 77, 6495-6501. doi: 10.1128/AEM.00520-11.
53. Zheng, J., Allard, S., Reynolds, S., Millner, P., Arce, G., Blodgett, R. J., et al. (2013). Colonization and internalization of Salmonella enterica in tomato plants. Appl. Environ. Microbiol. 79, 2494-502. doi: 10.1128/AEM.03704-12.
54. Zwickl, D. J. (2006). Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion. Ph.D. The University of Texas at Austin.