Postharvest intake potential of pathogenic microorganisms in fruit structures
DOI:
https://doi.org/10.15517/am.2024.54094Keywords:
infiltration, bacteria, fruits, postharvest technologyAbstract
Introduction. In recent years, there has been an increase in the consumption of fresh agricultural products, raising concerns about foodborne outbreaks related to these products due to the incorporation of pathogenic microorganisms into the fruits. The aspects related to this incorporation have been studied in some fruits; however, not everything associated with this issue has been clarified. Objective. To investigate and summarize the incorporation of pathogenic microorganisms into fruit structures. Development. This work was conducted in Costa Rica between July 2021 and September 2022. It contrasts the definition of internalization and infiltration and describes the conditions that favor the incorporation of pathogenic microorganisms into fruit, as well as the routes and distribution patterns of the incorporated microorganisms. Control strategies to prevent the incorporation of pathogens into these structures are also discussed. Conclusion. Most research on the incorporation of pathogenic microorganisms into fruits focuses on a few products and yields diverse and sometimes contradictory results. It is pertinent to direct future research towards evaluating the phenomenon under conditions closer to those of commercial operations of interest and to reinforce strategies that ensure the proper implementation of good agricultural practices and good manufacturing practices.
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References
Azofeifa Zumbado, M. F. (2020). Evaluación del potencial de infiltración de tinta en banano variedad cavendish durante la operación de eliminación de látex (desleche) [Tesis de licenciatura, Universidad de Costa Rica]. Repositorio KERWA. https://www.kerwa.ucr.ac.cr/handle/10669/86175
Bartz, J. A. (1982). Infiltration of tomatoes immersed at different temperatures to different depths in suspensions of Erwinia carotovora sbsp. carotovora. Plant Disease, 66(4), 302–306. https://doi.org/10.1094/PD-66-302
Bartz, J. A. (1991). Relation between resistance of tomato fruit to infiltration by Erwinia carotovora subsp. carotovora and bacterial soft rot. Plant Disease, 75(2), 152–155. https://www.apsnet.org/publications/plantdisease/backissues/Documents/1991Articles/PlantDisease75n02_152.PDF
Bartz, J. A. (2006). Internalization and infiltration. In G. M. Sapers, J. R. Gorny, & A. E. Yousef (Eds.), Microbiology of fruits and vegetables (1st ed., pp. 75–94). Taylor and Francis. https://doi.org/10.1201/9781420038934
Bartz, J. A., & Showalter, R. K. (1981). Infiltration of tomatoes by aqueous bacterial suspensions. Phytopathology, 71(5), 515–558. https://doi.org/10.1094/Phyto-71-515
Bartz, J. A., & Tamplin, M. L. (2003). Sales of vegetables for the fresh market: the requirement for hazard analysis and critical control points (HACCP) and sanitation. In J. A. Bartz, & J. K. Brecht (Eds.), Postharvest Physiology and Pathology of Vegetables (Chapter 23, pp. 563–578). Marcel Dekker. https://irrec.ifas.ufl.edu/postharvest/HOS_5085C/Reading%20Assignments/BartzBrecht-23-HACCP%20and%20Sanitation.pdf
Bartz, J. A., Vallad, G. E., & Sargent, S. A. (2021, January 28). Guide to identifying and controlling postharvest tomato diseases in Florida (Publication No. HS866). University of Florida. http://edis.ifas.ufl.edu/hs131
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, 55, 141–150. https://doi.org/10.1016/j.foodcont.2015.02.046
Branquinho Bordini, M. E., Asturiano Ristori, C., Jakabi, M., & Scala Gelli, D. (2007). Incidence, internalization and behavior of Salmonella in mangoes, var. Tommy Atkins. Food Control, 18(8), 1002–1007. https://doi.org/10.1016/j.foodcont.2006.06.003
Brenes Fernández, N. (2022). Evaluación de la sobrevivencia de E. coli ATCC 25922 durante el transporte de banano de exportación y determinación de condiciones de desinfección del fruto durante la operación de desleche [Tesis de licenciatura, Universidad de Costa Rica]. Repositorio SIBDI de la Universidad de Costa Rica. http://repositorio.sibdi.ucr.ac.cr:8080/jspui/handle/123456789/17566
Buchanan, R. L., Edelson, S. G., Miller, R. L., & Sapers, G. M. (1999). Contamination of intact apples after immersion in an aqueous environment containing Escherichia coli O157:H7. Journal of Food Protection, 62(5), 444-450. https://doi.org/10.4315/0362-028X-62.5.444
Burnett, S. L., Chen, J., & Beuchat, L. R. (2000). Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Applied and Environmental Microbiology, 66(11), 4679–4687. https://doi.org/10.1128/AEM.66.11.4679-4687.2000
Burnett, S. L., & Beuchat, L. R. (2002). Differentiation of viable and dead Escherichia coli O157:H7 cells on and in apple structures and tissues following chlorine treatment. Journal of Food Protection, 65(2), 251–259. https://doi.org/10.4315/0362-028x-65.2.251
Carstens, C. K., Salazar, J. K., & Darkoh, C. (2019). Multistate outbreaks of foodborne illness in the United States associated with fresh produce from 2010 to 2017. Frontiers in Microbiology, 10, Article 2667. https://doi.org/10.3389/fmicb.2019.02667
Centers for Disease Control and Prevention. (2022a, February 3). National Outbreak Reporting System (NORS). https://wwwn.cdc.gov/norsdashboard/
Centers for Disease Control and Prevention. (2022b). Multistate Foodborne Outbreak Notices. https://www.cdc.gov/foodborne-outbreaks/active-investigations/all-foodborne-outbreak-notices.html
Chen, Y., Evans, P., Hammack, T. S., Brown, E. W., & Macarisin, D. (2016). Internalization of Listeria monocytogenes in whole avocado. Journal of Food Protection, 79(8), 1440–1445. https://doi.org/10.4315/0362-028X.JFP-16-075
Corey, K. A., & Tan, Z.-Y. (1990). Induction of changes in internal gas pressure of bulky plant organs by temperature gradients. Journal of American Society for Horticultural Science, 115(2), 308–312. https://doi.org/10.21273/JASHS.115.2.308
Deering, A. J., Mauer, L. J., & Pruitt, R. E. (2012). Internalization of E. coli O157:H7 and Salmonella spp. in plants: A review. Food Research International, 45(2), 567–575. https://doi.org/10.1016/j.foodres.2011.06.058
Eblen, B. S., Walderhaug, M. O., Edelson-Mammel, S., Chirtel, S. J., De Jesus, A., Merker, R. I., Buchanan, R. L., & Miller, A. J. (2004). Potential for internalization, growth, and survival of Salmonella and Escherichia coli O157:H7 in oranges. Journal of Food Protection, 67(8), 1578–1584. https://doi.org/10.4315/0362-028X-67.8.1578
Erickson, M. C. (2012). Internalization of fresh produce by foodborne pathogens. Annual Review of Food Science and Technology, 3(1), 283–310. https://doi.org/10.1146/annurev-food-022811-101211
Felkey, K. D., Archer, D. L., Baraz, J. A., Goodrich R. M., & Schneider K. R. (2006). Chlorine disinfection of tomato surface wounds contaminated with Salmonella spp. Hort Technology, 16(2), 253–256. https://doi.org/10.21273/HORTTECH.16.2.0253
Ferreira, M. D., Bartz, J. A., Sargent, S. A., & Brecht, J. K. (1996). As assessment of the decay hazard associated with hydrocooling strawberries. Plant Disease, 80(10), 1117–1122. https://doi.org/10.1094/PD-80-1117
Florida Department of Agriculture and Consumer Services. (2015). Tomato best practices manual. https://www.flrules.org/gateway/ruleno.asp?id=5G-6.009
Food and Agriculture Organization of the United Nations. (2012). Towards the future we want - End hunger and make the transition to sustainable agricultural and food systems. https://www.fao.org/publications/card/en/c/ecc34e77-9678-5e45-9656-57f7c9d434b7/
Food and Agriculture Organization of the United Nations, & World Health Organization. (2017). Code of hygienic practice for fresh fruits and vegetables CXC 53-2003. https://www.fao.org/fao-who-codexalimentarius/codex-texts/codes-of-practice/en/
Food and Drug Administration. (1998, October 26). Guidance to industry: Guide to minimize microbial food safety hazards for fresh fruits and vegetables. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-guide-minimize-microbial-food-safety-hazards-fresh-fruits-and-vegetables
Giannakourou, M. C., & Tsironi, T. N. (2021). Application of processing and packaging hurdles for fresh-cut fruits and vegetables preservation. Foods, 10, Article 830. https://doi.org/10.3390/foods10040830
Girón Revolorio, B., Cano Granados, F., & Monney Castillo, L. (2019). Determinación de la presencia de Escherichia coli en la cáscara y parte comestible del banano y evaluación de su crecimiento durante el proceso de postcosecha y almacenamiento a temperatura controlada. Revista Científica de La Facultad de Ciencias Químicas y Farmacia, 28(2), 26–35. https://doi.org/10.54495/Rev.Cientifica.v28i2.52
Ibarra-Sánchez, L. S., Alvarado-Casillas, S., Rodríguez-García, M. O., Martínez-Gonzáles, N. E., & Castillo, A. (2004). Internalization of bacterial pathogens in tomatoes and their control by selected chemicals. Journal of Food Protection, 67(7), 1353–1358. https://doi.org/10.4315/0362-028X-67.7.1353
Janes, M. E., Kim, K. S., & Johnson, M. G. (2005). Transmission electron microscopy study of enterohemorrhagic Escherichia coli O157:H7 in apple tissue. Journal of Food Protection, 68(2), 216–224. https://doi.org/10.4315/0362-028x-68.2.216
Kenney, S. J., Burnett, S. L., & Beuchat, L. R. (2001). Location of Escherichia coli O157:H7 on and in apples as affected by bruising, washing, and rubbing. Journal of Food Protection, 64(9), 1328–1333. https://doi.org/10.4315/0362-028x-64.9.1328
Lampel, K. A., Al-Khaldi, S., & Cahill, S. M. (Eds.) (2012). Bad bug book (2nd ed.). Food And Drug Administrarion. https://www.fda.gov/food/foodborne-pathogens/bad-bug-book-second-edition
Lefebvre, M., Espinosa, M., Paloma, S.G., Paracchini, M.L., Piorr, A., & Zasada, I. (2015). Agricultural landscapes as multi-scale public good and the role of the Common Agricultural Policy. Journal of Environmental Planning and Management, 58(12), 2088–2112. https://doi.org/10.1080/09640568.2014.891975
Macarisin, D., Wooten, A., de Jesus, A., Hur, M., Bae, S., Patel, J., Evans, P., Brown, E., Hammack, T., & Chen, Y. (2017). Internalization of Listeria monocytogenes in cantaloupes during dump tank washing and hydrocooling. International Journal of Food Microbiology, 257, 165–175. https://doi.org/10.1016/j.ijfoodmicro.2017.06.018
Merker, R., Edelson-Mamel S., Davis, V., & Buchanan, R. (1999). Preliminary experiments on the effect of temperature differences on dye uptake by oranges and grapefruit. United States Food and Drug Administration.
Penteado, A. L., Eblen, B. S., & Miller, A. J. (2004). Evidence of Salmonella internalization into fresh mangos during simulated postharvest insect disinfestation procedures. Journal of Food Protection, 67(1), 181–184. https://doi.org/10.4315/0362-028X-67.1.181
Presidencia de la República, Ministerio de Comercio Exterior, Ministerio de Economía, Industria y Comercio, & Ministerio de Agricultura y Ganadería. (2012, junio 2). Reglamento Técnico Centroamericano Buenas Prácticas de Higiene Para Alimentos No Procesados y Semiprocesados y su Guía de Verificación N° 37057. Sistema Costarricense de Información Jurídica. http://www.pgrweb.go.cr/scij/Busqueda/Normativa/Normas/nrm_texto_completo.aspx?param1=NRTC&nValor1=1&nValor2=72615&nValor3=88718&strTipM=TC#up
Richards, G. M., & Beuchat, L. R. (2004). Attachment of Salmonella Poona to cantaloupe rind and stem scar tissues as affected by temperature of fruit and inoculum. Journal of Food Protection, 67(7), 1359–1364. https://doi.org/10.4315/0362-028x-67.7.1359
Sapers, G. M. (2001). Efficacy of washing and sanitizing methods for disinfection of fresh fruit and vegetable products. Food Technology and Biotechnology, 39(4), 305–311. https://bit.ly/3YCRI30
Segall, R. H., Henry, F. E., & Dow, A. T. (1977). Effect of dump tank water temperature on the incidence of bacterial soft rot of tomatoes. Proceedings of the Florida State Horticultural Society, 90, 204–205.
Soto, M., Chavez, G., Baez, M., Martinez, C., & Chaidez, C. (2007). Internalization of Salmonella typhimurium into mango pulp and prevention of fruit pulp contamination by chlorine and copper ions. International Journal of Environmental Health Research, 17(6), 453–459. https://doi.org/10.1080/09603120701695593
Turner, A. N., Friedrich, L. M., & Danyluk, M. D. (2016). Influence of temperature differential between tomatoes and postharvest water on Salmonella internalization. Journal of Food Protection, 79(6), 922–928. https://doi.org/10.4315/0362-028X.JFP-15-525
United States Environmental Protection Agency. (1997, June 3-4). A set of scientific issues being considered by the agency in connection with the efficacy testing issues concerning public health antimicrobial pesticides (Final Report). Scientific Advisory Panel Meeting, VA, Unites State. https://archive.epa.gov/scipoly/sap/meetings/web/html/060397_mtg.html
Ukuku, D. O., & Fett, W. F. (2004). Method of applying sanitizers and sample preparation affects recovery of native microflora and Salmonella on whole cantaloupe surfaces. Journal of Food Protection, 67(5), 999–1004. https://doi.org/10.4315/0362-028X-67.5.999
Valverde Jiménez, K. (2020). Evaluación del potencial de infiltración de Escherichia coli ATCC 25922 durante el proceso de lavado por inmersión del banano [Tesis de licenciatura, Universidad de Costa Rica]. Repositorio KERWA. https://hdl.handle.net/10669/86192
Wei, C. I., Huang, T. S., Kim, J. M., Lin, W. F., Tamplln, M. L., Aod, J., & Bartz, J. A. (1995). Growth and survival of Salmonella Montevideo on tomatoes and disinfection with chlorinated water. Journal of Food Protection, 58(8), 829–836. https://doi.org/10.4315/0362-028X-58.8.829
Xia, X., Luo, Y., Yang, Y., Vinyard, B., Schneider, K., & Meng, J. (2012). Effects of tomato variety, temperature differential, and post-stem removal time on internalization of Salmonella enterica serovar Thompson in tomatoes. Journal of Food Protection, 75(2), 297–303. https://doi.org/10.4315/0362-028X.JFP-11-078
Yuk, H.-G., Bartz, J. A., & Schneider, K. R. (2005). Effectiveness of individual or combined sanitizer treatments for inactivating Salmonella spp. on smooth surface, stem scar, and wounds of tomatoes. Journal of Food Science, 70(9), 409–414. https://doi.org/10.1111/j.1365-2621.2005.tb08326.x
Zhang, S., & Farber, J. M. (1996). The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiology, 13(4), 311–321. https://doi.org/https://doi.org/10.1006/fmic.1996.0037
Zheng, J., Allard, S., Reynolds, S., Millner, P., Arce, G., Blodgett, R. J., & Brown, E. W. (2013). Colonization and internalization of Salmonella enterica in tomato plants. Applied and Environmental Microbiology, 79(8), 2494–2502. https://doi.org/10.1128/AEM.03704-12
Zhou, B., Luo, Y., Nou, X., Yang, Y., Wu, Y., & Wang, Q. (2014). Effects of postharvest handling conditions on internalization and growth of Salmonella enterica in tomatoes. Journal of Food Protection, 77(3), 365–370. https://doi.org/10.4315/0362-028X.JFP-13-307
Zhuang, R. Y., & Beuchat, L. R. (1996). Effectiveness of trisodium phosphate for killing Salmonella Montevideo on tomatoes. Letters in Applied Microbiology, 22(2), 97–100. https://doi.org/10.1111/j.1472-765X.1996.tb01117.x
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, 61(6), 2127–2131. https://doi.org/10.1128/aem.61.6.2127-2131.1995
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