Inactivation of Salmonella enterica on tomato stem scars by antimicrobial solutions and vacuum perfusion

International Journal of Food Microbiology

Volumn 159, Issue 2, 2012, Pages 84-92

  Gurtler, Joshua B ^a   Smelser, Amanda M ^b   Niemira, Brendan A ^a   Jin, Tony Z ^a   Yan, Xianghe ^a   Geveke, David J ^a  

^a EASTERN REGIONAL RESEARCH CENTER   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Antimicrobial; Salmonella; Sanitizer; Stem scar; Tomato

Indexed keywords

ACETIC ACID; ALCOHOL; CARBOXYLIC ACID; CHLORINE; LACTIC ACID; LEVULINIC ACID; PERACETIC ACID; PHOSPHORIC ACID; SODIUM HYDROXIDE; SULFURIC ACID;

ARTICLE; COLONY FORMING UNIT; CONTROLLED STUDY; HOMOGENATE; INOCULATION; NONHUMAN; PERFUSION; PLANT STEM; SALMONELLA ENTERICA; SCAR; STUDY DESIGN; TEMPERATURE; TOMATO; VACUUM;

ANTI-INFECTIVE AGENTS; CHLORINE; COLONY COUNT, MICROBIAL; DISINFECTANTS; FOOD CONTAMINATION; LYCOPERSICON ESCULENTUM; PLANT STEMS; SALMONELLA; SALMONELLA ENTERICA; VACUUM;

EID: 84867605258     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.08.014     Document Type: Article

References (56)

1. Ahamad H., Marth E.H. Behavior of Listeria monocytogenes at 7, 13, 21 and 35°C in tryptose broth and acidified with acetic, citric, or lactic acid. Journal of Food Protection 1989, 52:688-695.
2. Asplund K., Nurmi E. The growth of Salmonellae in tomatoes. International Journal of Food Microbiology 1991, 12:177-182.
3. Bari M.L., Inatsu Y., Kawasaki S., Nazuka E., Isshiki K. Calcinated calcium killing of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes on the surface of tomatoes. Journal of Food Protection 2002, 65:1706-1711.
4. Bari M.L., Sabina Y., Isobe S., Uemura T., Isshiki K. Effectiveness of electrolyzed acidic water in killing Escherichia coli O157:H7, Salmonella Enteritidis, and Listeria monocytogenes on the surfaces of tomatoes. Journal of Food Protection 2003, 66:542-548.
5. Bari M.L., Nei K.D., Enomoto K., Todoriki S., Kawamoto S. Combination treatments for killing Escherichia coli O157:H7 on alfalfa, radish, broccoli, and mung bean seeds. Journal of Food Protection 2009, 72:631-636.
6. Beuchat L.R., Brackett R.E. Behavior of Listeria monocytogenes inoculated into raw tomatoes and processed tomato products. Applied and Environmental Microbiology 1991, 57:1367-1371.
7. Beuchat L.R., Mann D.A. Survival and growth of acid-adapted and unadapted Salmonella on raw tomatoes as affected by variety, stage of ripeness, and storage temperature. Journal of Food Protection 2008, 71:1572-1579.
8. Beuchat L.R., Nail B.V., Adler B.B., Clavero M.R.S. Efficacy of spray application of chlorinated water in killing pathogenic bacteria on raw apples, tomatoes, and lettuce. Journal of Food Protection 1998, 61:1305-1311.
9. Bhagat A., Mahmoud B.S.M., Linton R.H. Inactivation of Salmoenlla enterica and Listeria monocytogenes inoculated on hydroponic tomatoes using chlorine dioxide gas. Foodborne Pathogens and Disease 2010, 7:677-685.
10. Bidol S.A., Daly E.R., Rickert R.E., Hill T.A., Al Khaldi S., Taylor T.H., Lynch M.F., Painter J.A., Braden C.R., Yu P.A., Demma L., Baron Behravesh C., Olson C.K., Greene S.K., Schmitz A.M., Blaney D.D., Gershman M. Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in restaurants - United States, 2005-2006. Morbidity and Mortality Weekly Report 2007, 56:909-911.
11. Brown D.G., Allen C. Ralstonia solanacearum genes induced during growth in tomato: an inside view of bacterial wilt. Molecular Microbiology 2004, 53:1641-1660.
12. Chaidez C., Lopez J., Vidales J., Campo N.C. Efficacy of chlorinated and ozonated water in reducing Salmonella typhimurium attached to tomato surfaces. International Journal of Environmental Health Research 2007, 17:311-318.
13. Chang A.S., Schneider K.R. Evaluation of overhead spray-applied sanitizers for the reduction of Salmonella on tomato surfaces. Journal of Food Science 2012, 71:M65-M69.
14. Daş E., Gürakan G.C., Bayindirli A. Effect of controlled atmosphere storage, modified atmosphere packaging and gaseous ozone treatment on the survival of Salmonella Enteritidis on cherry tomatoes. Food Microbiology 2006, 23:430-438.
15. Doores S. Organic acids. Antimicrobials in Foods 2005, 91-142. CRC Press, Boca Raton, FL. P.M. Davidson (Ed.).
16. Foster J.W., Hall H.K. Adaptive acidification tolerance response of Salmonella Typhimurium. Journal of Bacteriology 1990, 172:771-778.
17. Gravani R.B. The role of good agricultural practices in produce safety. Microbial Safety of Fresh Produce 2009, 101-117. Wiley-Blackwell Publishing, Ames, IA. X. Fan, B.A. Niemira, C.J. Doona, F.E. Feeherry, R.B. Gravani (Eds.).
18. Grinstead, A.D., and Angevaare, P.A., inventors; Diversey Lever, Inc., assignee. 2003. Food washing composition. US patent 20030099745.
19. Gündüz G.T., Gönül S.A., Karapinar M. Efficacy of sumac and oregano in the inactivation of Salmonella Typhimurium on tomatoes. International Journal of Food Microbiology 2010, 141:39-44.
20. Guo X., Chen J., Brackett R.E., Beuchat L.R. Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Applied and Environmental Microbiology 2001, 67:4760-4764.
21. Guo X., Chen J., Brackett R.E., Beuchat L.R. Survival of Salmonella on tomatoes stored at high relative humidity, in soil, and on tomatoes in contact with soil. Journal of Food Protection 2002, 65:274-279.
22. Gupta L.K., Garg V., Tiwari R.P. Evaluation of ammonium hydroxide as preservative for ground meat. Applied Microbiology and Biotechnology 1988, 4:431-437.
23. Gurtler J.B., Beuchat L.R. Performance of media for recovering stressed cells of Enterobacter sakazakii as determined using spiral plating and ecometric techniques. Applied and Environmental Microbiology 2005, 71:7661-7669.
24. Gurtler J.B., Kornacki J.L. Comparison of media supplements to enhance the recovery of Salmonella spp. from thermally-treated egg albumen. Letters in Applied Microbiology 2009, 49:503-509.
25. Hanning I.B., Nutt J.D., Ricke S.C. Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathogens and Disease 2009, 6:635-648.
26. Ibarra-Sánchez L.S., Alvarado-Casillas S., Rodríguez-García M.O., Martínez-Gonzáles N.E., Castillo A. Internalization of bacterial pathogens in tomatoes and their control by selected chemicals. Journal of Food Protection 2004, 67:1353-1358.
27. Inatsu Y., Kitagawa T., Bari L., Nei D., Juneja V., Kawamoto S. Effectiveness of acidified sodium chlorite and other sanitizers to control Escherichia coli O157:H7 on tomato surfaces. Foodborne Pathogens and Disease 2009, 7:629-635.
28. Inatsu Y., Bari M.L., Nei S., Kawasaki S., Kawamoto S. Effectiveness of different sanitizers to control Escherichia coli O157:H7 on tomato surfaces. Acta Horticulturae 2010, 875:269-274.
29. Iturriaga M.H., Escartín E.F. Changes in the effectiveness of chlorine treatments during colonization of Salmonella Montevideo on tomatoes. Journal of Food Safety 2010, 30:300-306.
30. Iturriaga M.H., Tamplin M., Escartín E. Colonization of tomatoes by Salmonella Montevideo is affected by relative humidity and storage temperature. Journal of Food Protection 2007, 70:30-34.
31. Jensen J.L., Saxena A.D., Keener K.M. Evaluation of treatment methods for reducing bacteria in textured beef. American Society of Agricultural and Biological Engineers Annual Meeting, Reno, NV, June 21-24, Volume 10 2009, 6439-6450. Also accessed online on March 27, 2012 at: http://elibrary.asabe.org/azdez.asp?search=1&JID=5&AID=27245&CID=reno2009&v=&i=&T=2&urlRedirect.
32. Kwon N.H., Kim S.H., Kim J.Y., Lim J.Y., Kim J.M., Jung W.K., Park K.T., Bae W.K., Noh K.M., Choi J.W., Hur J., Park Y.H. Antimicrobial performance of alkaline ionic fluid (GC-100X) and its ability to remove Escherichia coli O157:H7 from the surface of tomatoes. Journal of Food Protection 2003, 66:1604-1610.
33. Lemons KE, inventor; Taylor Fresh Food, Inc., assignee. 2009. Antimicrobial compositions and methods of use thereof. US patent 20090192231.
34. Mahovic M. Disease management: disorders of tomato. Growers Integrated Pest Management Guide for Florida Tomato and Pepper Production 2006, 142-144. University of Florida, Gainesville, FL, Chapter 5. Accessed on 2 September, 2011 at http://ipm.ifas.ufl.edu/resources/success_stories/T%26PGuide. J.L. Gillett, H.N. HansPetersen, N.C. Leppla, D.D. Thomas (Eds.).
35. Neetoo H., Ye M., Chen H. Factors affecting the efficacy of pressure inactivation of Escherichia coli O157:H7 on alfalfa seeds and seed viability. International Journal of Food Microbiology 2009, 131:218-223.
36. Noel J.T., Arrach N., Alagely A., Mcclelland M., Teplitski M. Specific responses of Salmonella enterica on tomato varieties and fruit ripeness identified by in vivo expression technology. PloS One 2010, 5(8).
37. Nou X., Luo Y., Hollar L., Yang Y., Feng H., Millner P., Shelton D. Chlorine stabilizer T-128 enhances efficacy of chlorine against cross-contamination by E. coli O157:H7 and Salmonella in fresh-cut lettuce processing. Food Science 2011, 76:M218-M224.
38. Obaidat M.M., Frank J.F. Inactivation of Salmonella and Escherichia coli O157:H7 on sliced and whole tomatoes by allyl isothiocyanate, carvacrol, and cinnamaldehyde in vapor phase. Journal of Food Protection 2009, 72:315-324.
39. Pao S., Kelsey D.F., Long W. Spray washing of tomatoes with chlorine dioxide to minimize Salmonella on inoculated fruit surfaces and cross-contamination from revolving brushes. Journal of Food Protection 2009, 72:2448-2452.
40. Park E.J., Alexander E., Taylor G.A., Costa R., Kang D.H. Fate of foodborne pathogens on green onions and tomatoes by electrolysed water. Letters in Applied Microbiology 2008, 46:519-525.
41. Raiden R.M., Sumner S.S., Eifert J.D., Pierson M.D. Efficacy of detergents in removing Salmonella and Shigella spp. from the surface of fresh produce. Journal of Food Protection 2003, 66:2210-2215.
42. Rathinasabapathi B. Survival of Salmonella Montevideo on tomato leaves and mature green tomatoes. Journal of Food Protection 2004, 67:2277-2279.
43. Sapers G.M., Jones D.M. Improved sanitizing treatments for fresh tomatoes. Journal of Food Safety 2006, 71:M252-M256.
44. Shi X., Namvar A., Kostrzynska M., Hora R., Warriner K. Persistence and growth of different Salmonella serovars on pre- and postharvest tomatoes. Journal of Food Protection 2007, 70:2725-2731.
45. Sommers C.H., Sites J.E., Musgrove M. Ultraviolet light (254nm) inactivation of pathogens on foods and stainless steel surfaces. Journal of Food Safety 2010, 30:470-490.
46. Stopforth J.D., Yoon Y., Belk K.E., Scanga J.A., Kendall P.A., Smith G.C., Sofos J.N. Effect of simulated spray chilling with chemical solutions on acid-habituated and non-acid-habituated Escherichia coli O157:H7 cells attached to beef carcass tissue. Journal of Food Protection 2004, 67:2099-2106.
47. Tamir-Ariel D., Navon N., Burdman S. Identification of genes in Xanthomonas campestris pv. vesicatoria induced during its interaction with tomato. Journal of Bacteriology 2007, 189:6359-6371.
48. Valazquez L.d.C., Barbini N.B., Escudero M.E., Estrada C.L., de Guzman A.M.S. Evaluation of chlorine, benzalkonium chloride, and lactic acid as sanitizers for reducing Escherichia coli O157:H7 and Yersinia enterocolitica on fresh vegetables. Food Control 2009, 20:262-268.
49. Venkitanarayanan K.S., Lin C.M., Bailey H., Doyle M.P. Inactivation of Escherichia coli O157:H7, Salmonella Enteritidis, and Listeria monocytogenes on apples, oranges, and tomatoes by lactic acid with hydrogen peroxide. Journal of Food Protection 2002, 65:100-105.
50. Wei C.I., Huang T.S., Kim J.M., Lin W.F., Tamplin M.L., Bartz J.A. Growth and survival of Salmonella Montevideo on tomatoes and disinfection with chlorinated water. Journal of Food Protection 1995, 58:829-836.
51. Weissinger W.R., Chantarapanont W., Beuchat L.R. Survival and growth of Salmonella baildon in shredded lettuce and diced tomatoes, and effectiveness of chlorinated water as a sanitizer. International Journal of Food Microbiology 2000, 62:123-131.
52. Wesche A.M., Gurtler J.B., Marks B.P., Ryser E.T. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. Journal of Food Protection 2009, 72:1121-1138.
53. Yoon Y., Stopforth J.D., Kendall P.A., Sofos J.N. Inactivation of Salmonella during drying and storage of Roma tomatoes exposed to predrying treatments including peeling, blanching, and dipping in organic acid solutions. Journal of Food Protection 2004, 67:1344-1352.
54. Yuk H.G., Bartz J.A., Schneider K.R. Effectiveness of individual or combined sanitizer treatments for inactivating Salmonella spp. on smooth surface, stem scar, and wounds of tomatoes. Journal of Food Science 2005, 70:M409-M414.
55. Zhuang R.Y., Beuchat L.R. Effectiveness of trisodium phosphate for killing Salmonella Montevideo on tomatoes. Letters in Applied Microbiology 1996, 22:97-100.
56. Zhuang R.Y., Beuchat L.R., Angulo F.J. Fate of Salmonella Montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Applied and Environmental Microbiology 1995, 61:2127-2131.