Influence of suspension liquid total solids on E. coli O157:H7 survival and transfer efficacy between green tomatoes and cardboard
Keywords:tomatoes, cardboard, E. coli O157:H7, survival, transfer, cross-contamination, ATP luciferase test
The objectives of this study were: a) to determine E. coli O157:H7 survival on tomatoes and cardboard squares post-drying, stored at 25 ºC in humidified environment for four days, in buffered peptone water (BPW), and 0.1% diluted peptone (DP); b) to determine pathogen transfer rates (0, 1.5, or 24-hours drying post-inoculation), from inoculated tomato surfaces to uninoculated cardboard squares and conversely; and c) to evaluate SystemSure Plus ATP luminometer for recognizing contamination on visibly soiled (BPW) or visible clean (DP) cardboard. In tomato inoculation studies, E. coli O157:H7 survived better on the fruit when the inoculum was prepared using DP as compared to BPW. The 1.5-hours post drying counts of 5.34 and 5.76 log10 CFU.mL-1 in the rinsate substantially declined to 1.45 and 1.17 log10 CFU.mL-1 on day four, for DP and BPW, respectively. In cardboard inoculation studies, E. coli O157:H7 persisted for four days, with 1.5-hours post-drying counts and day four counts of 4.53 (DP) and 2.55 log10 CFU.mL-1 (BPW), contrary to 3.81 (DP) and 1.92 log10 CFU.mL-1 (BPW). Under the first impression, the slower die-off of E. coli O157:H7 on cardboard questions the possibility of reusing cardboard boxes due to the potential for cross-contamination. In wet transfer (0 hour drying) trials, both tomato-to-cardboard and cardboard-to-tomato yielded 100% positive transfers irrespective of diluent type. Dry transfer (1.5-hours drying interval post inoculation) from tomato-to-cardboard were 100% positive, but no positives were noted when inoculated, dried cardboard was contacted to tomatoes, irrespective of diluent. Results of transfers with BPW as the diluent showed 100% positive transfer from 24-hours dry tomatoes-to-cardboard, as inoculation spots on the tomatoes remained moist due to hygroscopic nature of solutes in BPW. Conversely, only a 40% positive transfer rate was observed under the same conditions with DP as diluent. No positive transfers were recorded from 24-hours dry cardboard-to-tomatoes, irrespective of diluent type. Though E. coli O157:H7 survived better on the surface of cardboard compared to the surface of tomatoes on day four, the dry transfers were more efficient from tomatoes-to-cardboard than conversely, possibly due to smooth and hydrophobic properties of the tomato, and rough and porous surface of the cardboard. ATP luciferase UltrasnapTM swab test showed 9/9 “pass” results for sterile liquid DP and BPW, while 9/9 “fail” results were observed with liquid peptone and BPW contaminated at ca. 9.0 log10 CFU.mL-1E. coli O157:H7. Cardboard squares treated and dried, with sterile DP, showed 8/9 “pass” ATP luciferase results, and 1/9 “warning”, while cardboard squares with contaminated DP showed 9/9 “fail” result. Cardboard squares treated and dried, with sterile BPW, showed 7/9 “pass” ATP luciferase results, and 2/9 “warning”, while cardboard squares with contaminated BPW showed 9/9 “fail” result. Luminometer can simplify detection of microbial load, as well as organic residues, helping to check cardboard boxes for cleanness.
Allen, R. L., Warren, B. R., Archer, D. L., Schneider, K. R., Sargent, S. A. 2005. Survival of Salmonella spp. on the surfaces of fresh tomatoes and selected packing line materials. HortTechnology, vol. 15, no. 4, p. 831-836. https://doi.org/10.21273/HORTTECH.15.4.0831
Bartz, J. A., Yuk, H. G., Mahovic, M. J., Warren B. R., Sreedharan, A., Schneider, K. R. 2015. Internalization of Salmonella enterica by tomato fruit. Food Control, vol. 55, p. 141-150. https://doi.org/10.1016/j.foodcont.2015.02.046
Beuchat, R. Y., Ryu, J. H., 1997. Produce handling and processing practices. Emerging Infectious Disease, vol. 3, p. 439-465. https://doi.org/10.3201/eid0304.970407
Beuchat, L. R., Mann, D. A. 2008. Survival and growth of acid-adapted and unadapted salmonella in and on raw tomatoes as affected by variety, stage of ripeness, and storage temperature. Journal of Food Protection, vol. 71, no. 8, p. 1572-1579. https://doi.org/10.4315/0362-028x-71.8.1572
Buchholz, A. L., Davidson, G. R., Marks, B. P., Todd, E. C., Ryser, E. T. 2012. Transfer of Escherichia coli O157:H7 from equipment surfaces to fresh-cut leafy greens during processing in a model pilot-plant production line with sanitizer-free water. Journal of Food Protection, vol. 75, no. 11, p. 1920-1929. https://doi.org/10.4315/0362-028X.JFP-11-558.
Ceresa, L., Ball, P. 2005. Chapter 9. Using ATP bioluminescence for microbiological measurements in pharmaceutical manufacturing. In Miller M. J. Encyclopedia of rapid microbiological methods. Bethesda, MD : PDA/DHI Publishers. ISBN 978-193-01148-5-2.
Chen, F. C., Godwin, S. L. 2006. Comparison of a rapid ATP bioluminescence assay and standard plate count methods for assessing microbial contamination of consumers' refrigerators. Journal of Food Protection, vol. 69, no. 10, p. 2534-2538. https://doi.org/10.4315/0362-028X-69.10.2534
Croby, R., Lanni, V., Kistler, V., Dato, V., Weltman, A., Yozviak, C., Waller, K., Nalluswami, K., Moll, M., Lockett, J., Montgomery, S., Lyuch, M., Braden, C., Gupta, S. K., Dubois, A. 2005. Outbreaks of Salmonella infections associated with eating Roma tomatoes-United States and Canada, 2004. Morbidity and Mortality Weekly Report, vol. 54, p. 325-328.
Cummings, K., Barrett, E., Mohle-Boetani, J. C., Brooks J. T., Farrar, J, Hunt, T., Fiore, A., Komatsu, K., Werner, S. B., Slutsker, L. 2001. A multistate outbreak of Salmonella enterica serotype Baildon associated with domestic raw tomatoes. Emerging Infectious Disease, vol. 7, p. 1046-1048. https://doi.org/10.3201/eid0706.010625
Daş, E., Gürakan, G. C., Bayindirli, A. 2006. Effect of controlled atmosphere storage, modified atmosphere packaging and gaseous ozone treatment on the survival of Salmonella Enteritidis on cherry tomatoes. Food Microbiology, vol. 23, no. 5, p. 430-438. https://doi.org/10.1016/j.fm.2005.08.002
FDACS. 2018. Florida Department of Agriculture and Consumer Services. Florida Crops and Product, Overview of Florida Agriculture. Available at: http://www.Florida-Agriculture.com/consumers/crops/agoverview/
FAOSTAT. 2017. Food and Agriculture Organization of the United Nations. Commodities by country. Countries by commodity. Available at: http://www.fao.org
Gurtler, J. B., Harlee, N. A., Smelser, A. M., Schneider, K. R 2018. Salmonella enterica contamination of market fresh tomatoes: A review. Journal of Food Protection, vol. 81, no. 7, p. 1193-1213. https://doi.org/10.4315/0362-028X.JFP-17-395
Guo, X., Chen, J., Brackett, R. E., Beuchat, L. R. 2002. Survival of Salmonella on tomatoes stored at high relative humidity, in soil, and on tomatoes in contact with soil. Journal of Food Protection, vol. 65, no. 2, p. 274-279. https://doi.org/10.4315/0362-028x-65.2.274
Hirai, Y. 1991. Survival of bacteria under dry conditions; from a viewpoint of nosocomial infection. Journal of Hospital Infection, vol. 19, no. 3, p. 191-200. https://doi.org/10.1016/0195-6701(91)90223-U
Jensen, D. A., Friedrich, L. M., Harris, L. J., Danyluk, M. D., Schaffner, D. W. 2013. Quantifying transfer rates of Salmonella and Escherichia coli O157:H7 between fresh-cut produce and common kitchen surfaces. Journal of Food Protection, vol. 6, no. 9, p. 1530-1538. https://doi.org/10.4315/0362-028x.jfp-13-098.
Jensen, D. A., Danyluk, M. D., Harris, L. J., Schaffner, D. W. 2017. Quantifying bacterial cross-contamination rates between fresh-cut produce and hands. Journal of Food Protection, vol. 80, no. 2, p. 213-219. https://doi.org/10.4315/0362-028X.JFP-16-240
Jung, J., Friedrich, L. M., Danyluk, M. D., Schaffner, D. W. 2017. Quantification of transfer of Salmonella from citrus fruits to peel, edible portion, and gloved hands during hand peeling. Journal of Food Protection, vol. 80, no. 6, p. 933-939. https://doi.org/10.4315/0362-028X.JFP-16-423
Kusumaningrum, H. D., Riboldi, G., Hazeleger, W. C., Beumer, R. R. 2003. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. International Journal of Food Microbiology, vol. 85, no. 3, p. 227-236. https://doi.org/10.1016/S0168-1605(02)00540-8
Lang, M. M., Harris, L. J., Beuchat, L. R. 2004. Evaluation of inoculation method and inoculum drying time for their effects on survival and efficiency of recovery of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes inoculated on the surface of tomatoes. Journal of Food Protection, vol. 67, no. 4, p. 732-741. https://doi.org/10.4315/0362-028X-67.4.732
Larson, E. L., Aiello, A. E., Gomez-Duarte, C., Lin, S. X., Lee, L., Della-Latta, P., Lindhardt, C. 2003. Bioluminescence ATP monitoring as a surrogate marker for microbial load on hands and surfaces in the home. Food Microbiology, vol. 20, no. 6, p. 735-739. https://doi.org/10.1016/s0740-0020(03)00041-8
Møretrø, T., Heir, E., Mo, K. R., Habimana, O., Abdelgani, A., Langsrud, S. 2010. Factors affecting survival of Shigatoxin-producing Escherichia coli on abiotic surfaces. International Journal of Food Microbiology, vol. 138, no. 1-2, p. 71-77. https://doi.org/10.1016/j.ijfoodmicro.2010.01.002
Schilling, M. W., Yoon, Y., Tokarskyy, O., Pham, A. J., Williams, R. C., Marshall, D. L. 2009. Effects of ionizing irradiation and hydrostatic pressure on Escherichia coli O157:H7 inactivation, chemical composition, and sensory acceptability of ground beef patties. Meat Science, vol. 81, no. 4, p. 705-710. https://doi.org/10.1016/j.meatsci.2008.10.023
Shama, G., Malik D. J. 2013. The uses and abuses of rapid bioluminescence-based ATP assays. International Journal of Hygiene and Environmental Health, vol. 216, no. 2, p. 115-125. https://doi.org/10.1016/j.ijheh.2012.03.009
Shi, X., Namvar, A., Kostrzynska, M., Hora, R., Warriner, K. 2007. Persistence and growth of different Salmonella serovars on pre- and postharvest tomatoes. Journal of Food Protection, vol. 70, no. 12, p. 2725-2731. https://doi.org/10.4315/0362-028X-70.12.2725
Siroli, L., Patrignani, F., Serrazanetti, D. I., Chiavari, C., Benevelli, M., Grazia, L., Lanciotti, R. 2017. Survival of spoilage and pathogenic microorganisms on cardboard and plastic packaging materials. Frontiers in Microbiology, vol. 8, p. 10. https://doi.org/10.3389/fmicb.2017.02606
Tokarskyy, O., Marshall, D. L., Schilling, M. W., Willeford, K. O. 2009. Comparison of methods to verify end point cooking temperature of channel catfish (ictalurus punctatus) fillets. Journal of Muscle Foods, vol. 20, no. 3., p. 325-340. https://doi.org/10.1111/j.1745-4573.2009.00151.x
Tokarskyy, O., De, J., Fatica, M. K., Brecht, J., Schneider, K. R. 2018. Survival of Escherichia coli O157:H7 and Salmonella on bruised and unbruised tomatoes from three ripeness stages at two temperatures. Journal of Food Protection, vol. 81, no. 12, p. 2028-2034. https://doi.org/10.4315/0362-028X.JFP-18-220
Tokarskyy, O., Korda, M. 2019. Microbiological comparison of visibly dirty and visibly clean mature green tomatoes before and after treatments with deionized water or chlorine in model overhead spray brush roller system. Potravinarstvo Slovak Journal of Food Sciences, vol. 13, no. 1, p. 779-783. https://doi.org/10.5219/1178
Tokarskyy, O., Schneider, K. R. 2019. Influence of temperature, humidity, and diluent type on survival of Salmonella spp. on the surface of raw tomatoes. Potravinarstvo Slovak Journal of Food Sciences, vol. 13, no. 1, p. 325-330. https://doi.org/10.5219/1121
Underthun, K., De, J., Gutierrez, A., Silverberg, R., Schneider, K. R. 2018. Survival of Salmonella and Escherichia coli in two different soil types at various moisture levels and temperatures. Journal of Food Protection, vol. 81, no. 1, p. 150-157. https://doi.org/10.4315/0362-028X.JFP-17-226
Wei, C. I., Huang, T. S., Kim, J. M., Lin, W. F., Tamplin, M. L., Bartz, J. A. 1995. Growth and survival of Salmonella montevideo on tomatoes and disinfection with chlorinated water. Journal of Food Protection, vol. 58, no. 8, p. 829-838. https://doi.org/10.4315/0362-028X-58.8.829
Zhuang, R. Y., Beuchat, L. R., Angulo, F. J. 1995. Fate of Salmonella Montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Applied and Environmental Microbiology, vol. 61, no. 6, p. 2127-2131.
How to Cite
LicenseAuthors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).