Relevance of fresh fruits and vegetables in foodborne outbreaks and the significance of the physiological state of bacteria
DOI:
https://doi.org/10.3989/arbor.2020.795n1005Keywords:
fresh produce, viable but non cultivable, food safety, pathogenic bacteria, primary productionAbstract
Fruits and vegetables have always been in the news, mainly because of their beneficial properties for human health. However, they increasingly occupy headlines due to their involvement in foodborne outbreaks. This is the reason why, since 2008, many international organizations consider fruit and vegetables risky food. One major microbiological concern regarding the safety of leafy greens is that pathogenic microorganisms are able to adhere to and survive on plant tissue during cultivation and processing, coexist with epiphytic bacteria and persist for long periods of time. The prevalence of pathogenic microorganisms in fruits and vegetables is low (<1%) and enumeration of pathogenic or indicator bacteria usually show very low numbers, which do not explain the high number of microbiological alerts associated with this types of products. However, concerns have been raised regarding how representative the enumeration of bacteria using plate count techniques may be. Several studies have shown that when bacteria are subjected to different stresses, they enter into a temporary state of low metabolic activity in which the cells can persist for long periods of time without cell division, called latency or viable but non-culturable (VBNC). The significance that the physiological state of bacteria might have in the development of foodborne diseases caused by fruits and vegetables is getting a lot of attention and much research is now focused on this topic.
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Anderson, M., Bollinger, D., Hagler, A., Hartwell, H., Rivers, B., Ward, K. y Steck, T. R. (2004). Viable but nonculturable bacteria are present in mouse and human urine specimens. Journal of Clinical Microbiology, 42 (2), pp. 753-758. https://doi.org/10.1128/JCM.42.2.753-758.2004 PMid:14766848 PMCid:PMC344478
Anuchin, A. M., Mulyukin, A. L., Suzina, N. E., Duda, V. I., El-Registan, G. I. y Kaprelyants, A. S. (2009). Dormant forms of Mycobacterium smegmatis with distinct morphology. Microbiology, 155 (4), pp. 1071-1079. https://doi.org/10.1099/mic.0.023028-0 PMid:19332809
Anvarian, A. H. P., Smith, M. P. y Overton, T. W. (2016). The effects of orange juice clarification on the physiology of Escherichia coli; growth-based and flow cytometric analysis. International Journal of Food Microbiology, 219, pp. 38-43. https://doi.org/10.1016/j.ijfoodmicro.2015.11.016 PMid:26705746
Asakura, H., Kawamoto, K., Haishima, Y., Igimi, S., Yamamoto, S. y Makino, S. I. (2008). Differential expression of the outer membrane protein W (OmpW) stress response in enterohemorrhagic Escherichia coli O157:H7 corresponds to the viable but non-culturable state. Research in Microbiology, 159 (9-10), pp. 709-717. https://doi.org/10.1016/j.resmic.2008.08.005 PMid:18824229
Aurass, P., Prager, R. y Flieger, A. (2011). EHEC/EAEC O104:H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environmental Microbiology, 13 (12), pp. 3139-3148. https://doi.org/10.1111/j.1462-2920.2011.02604.x PMid:21951606
Ayrapetyan, M., Williams, T. C., Baxter, R. y Oliver, J. D. (2015). Viable but nonculturable and persister cells coexist stochastically and are induced by human serum. Infection and Immunity, 83 (11), pp. 4194-4203. https://doi.org/10.1128/IAI.00404-15 PMid:26283335 PMCid:PMC4598401
Berney, M., Hammes, F., Bosshard, F., Weilenmann, H. U. y Egli, T. (2007). Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Applied Environmental Microbiology, 73 (10), pp. 3283-3290. https://doi.org/10.1128/AEM.02750-06 PMid:17384309 PMCid:PMC1907116
Besnard, V., Federighi, M. y Cappelier, J. M. (2000). Evidence of Viable but Non-culturable state in Listeria monocytogenes by direct viable count and CTC-DAPI double staining. Food Microbiology, 17 (6), pp. 697-704. https://doi.org/10.1006/fmic.2000.0366
Besnard, V., Federighi, M., Declerq, E., Jugiau, F. y Cappelier, J. M. (2002). Environmental and physico-chemical factors induce VBNC state in Listeria monocytogenes. Veterinary Research, 33 (4), pp. 359-370. https://doi.org/10.1051/vetres:2002022 PMid:12199363
Bridier, A., Hammes, F., Canette, A., Bouchez, T. y Briandet, R. (2015). Fluorescence-based tools for single-cell approaches in food microbiology. International Journal of Food Microbiology, 213, pp. 2-16. https://doi.org/10.1016/j.ijfoodmicro.2015.07.003 PMid:26163933
Cappelier, J. M., Besnard, V., Roche, S. M., Velge, P. y Federighi, M. (2007). Avirulent viable but non culturable cells of Listeria monocytogenes need the presence of an embryo to be recovered in egg yolk and regain virulence after recovery. Veterinary Research, 38 (4), pp. 573-583. https://doi.org/10.1051/vetres:2007017 PMid:17540159
Cook, K. L. y Bolster, C. H. (2007). Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. Journal of Applied Microbiology, 103 (3), pp. 573-583. https://doi.org/10.1111/j.1365-2672.2006.03285.x PMid:17714390
Costa, K., Bacher, G., Allmaier, G., Dominguez-Bello, M. G., Engstrand, L., Falk, P., de Pedro, M. A. y García-del Portillo F. (1999). The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. Journal of Bacteriology, 181 (12), pp. 3710-3715. https://doi.org/10.1128/JB.181.12.3710-3715.1999 PMid:10368145
Cunningham, E., O'Byrne, C. y Oliver, J. D. (2009). Effect of weak acids on Listeria monocytogenes survival: evidence for a viable but nonculturable state in response to low pH. Food Control, 20 (12), pp. 1141-1144. https://doi.org/10.1016/j.foodcont.2009.03.005
Day, A. P. y Oliver J. D. (2004). Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but non-culturable state. Journal of Microbiology, 42 (2), pp. 69-73.
Ding, T., Suo, Y., Xiang, Q., Zhao, X., Chen, S., Ye, X. y Liu D. (2017). Significance of viable but nonculturable Escherichia coli: induction, detection, and control. Journal of Microbiology and Biotechnology, 27 (3), pp. 417-428. https://doi.org/10.4014/jmb.1609.09063 PMid:27974738
Dinu, L. D. y Bach, S. (2011). Induction of viable but nonculturable Escherichia coli O157:H7 in the phyllosphere of lettuce: a food safety risk factor. Applied Environmental Microbiology, 77 (23), pp. 8295-8302. https://doi.org/10.1128/AEM.05020-11 PMid:21965401 PMCid:PMC3233046
EFSA Panel on Biological Hazards (BIOHAZ). (2013). Scientific Opinion on the Risk Posed by Pathogens in Food of Non-animal Origin. Part 1 (outbreak data analysis and risk ranking of food/ pathogen combinations). EFSA Journal, 11 (1), 3025. https://doi.org/10.2903/j.efsa.2013.3025
Elizaquível, P., Sánchez, G. y Aznar, R. (2012). Quantitative detection of viable foodborne E. coli O157:H7, Listeria monocytogenes and Salmonella in fresh-cut vegetables combining propidium monoazide and real-time PCR. Food Control, 25 (2), pp. 704-708. https://doi.org/10.1016/j.foodcont.2011.12.003
Fakruddin, M, Bin Mannan, K. S. y Andrews, S. (2013). Viable but Non culturable Bacteria: Food Safety and Public Health Perspective. ISRN Microbiology, 2013, 703813. https://doi.org/10.1155/2013/703813 PMid:24191231 PMCid:PMC3804398
Fang, J., Wu, Y., Qu, D., Ma B., Yu X., Zhang, M. y Han, J. (2018). Propidium monoazide Real-time loop-mediated isothermal amplification for specific visualization of viable Salmonella in food. Letters in Applied Microbiology, 67 (1), pp. 79-88. https://doi.org/10.1111/lam.12992 PMid:29665023
Fischer-Le Saux, M., Hervio-Heath, D., Loaec, S., Colwel, R. R. y Pommepuy, M. (2002). Detection of cytotoxin-hemolysin mRNA in nonculturable populations of environmental and clinical Vibrio vulnificus strains in artificial seawater. Applied Environmental Microbiology, 68 (11), pp. 5641-5646. https://doi.org/10.1128/AEM.68.11.5641-5646.2002 PMid:12406760 PMCid:PMC129913
Fittipaldi, M., Nocker, M. A. y Codony, F. (2012). Progress in understanding preferential detection of live cells using viability dyes in combination with DNA amplification. Journal Microbiology Methods, 91 (2), pp. 276-289. https://doi.org/10.1016/j.mimet.2012.08.007 PMid:22940102
Gensberger, E. T., Polt, M., Konrad-Köszler, M., Kinner, P., Sessitsch, A. y Kostic, T. (2014). Evaluation of quantitative PCR combined with PMA treatment for molecular assessment of microbial water quality. Water Research, 67, pp. 367-376. https://doi.org/10.1016/j.watres.2014.09.022 PMid:25459225
Habimana, O., Nesse, L. L., Møretrø. T., Berg, K., Heir, E., Vestby, L. K. y Langsrud. S. (2014). The persistence of Salmonella following desiccation under feed processing environmental conditions: a subject of relevance. Letters in Applied Microbiology, 59 (5), pp. 464-470. https://doi.org/10.1111/lam.12308 PMid:25046569
Highmore, C. J., Warner, J. C., Rothwell, S. D., Wilks, S. A. y Keevil, C. W. (2018). Viable-but nonculturable Listeria monocytogenes and Salmonella enterica serovar thompson induced by chlorine stress remain infectious. MBio, 9 (2), e00540-18. https://doi.org/10.1128/mBio.00540-18 PMid:29666286 PMCid:PMC5904417
Kana, B. D., Gordhan B. G., Downing K. J., Sung N., Vostroktunova G., Machowski E. E., Tsenova, L., Young, M., Kaprelyants, A., Kaplan, G. y Mizrahi V. (2008). The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Molecular Microbiology, 67 (3), pp. 672- 684. https://doi.org/10.1111/j.1365-2958.2007.06078.x PMid:18186793 PMCid:PMC2229633
Kell, D. B., Kaprelyants, A. S., Weichart, D. H., Harwood, C. R. y Barer, M. R. (1998). Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie van Leeuwenhoek, 73 (2), pp. 169-187. https://doi.org/10.1023/A:1000664013047 PMid:9717575
Lai, C. J., Chen, S. Y., Lin, I. H., Chang, C. H. y Wong, H. C. (2009). Change of protein profiles in the induction of the viable but non culturable state of Vibrio parahaemolyticus. International Journal of Food Microbiology, 135 (2), pp. 118- 124. https://doi.org/10.1016/j.ijfoodmicro.2009.08.023 PMid:19735955
Li, D., Tong, T., Zeng, S., Lin, Y., Wu, S. y He, M. (2014). Quantification of viable bacteria in wastewater treatment plants by using propidium monoazide combined with quantitative PCR (PMA-qPCR). Journal of Environmental Sciences, 26 (2), pp. 299-306. https://doi.org/10.1016/S1001-0742(13)60425-8
Mascher, F., Hase, C., Moenne-Loccoz, Y. y Défago, G. (2000). The viable-but-nonculturable state induced by abiotic stress in the biocontrol agent Pseudomonas fluorescens CHA0 does not promote strain persistence in soil. Applied and Environmental Microbiology, 66 (4), pp. 1662-1667. https://doi.org/10.1128/AEM.66.4.1662-1667.2000 PMid:10742257 PMCid:PMC92038
Makino, S. I., Kii, T., Asakura, H., Shirahata, T., Ikeda, T., Takeshi, K. y Itoh, K. (2000). Does enterohemorrhagic Escherichia coli O157:H7 enter the viable but non culturable state in salted salmon roe? Applied Environmental Microbiology, 66 (12), pp. 5536-5539. https://doi.org/10.1128/AEM.66.12.5536-5539.2000 PMid:11097946 PMCid:PMC92500
Moyle, A. L., Harris, L. J. y Marco, M. L. (2013). Assessments of total and viable Escherichia coli O157:H7 on field and laboratory grown lettuce. PLoS One, 8 (7), e70643. https://doi.org/10.1371/journal.pone.0070643 PMid:23936235 PMCid:PMC3728298
Nicolò, M. S. y Guglielmino, S. P. P. (2012). Viable but nonculturable bacteria in food. En Maddock, J. (ed.). Public Health-Methodology, Environmental and Systems Issues. Rjeka: InTech, pp. 189-216.
Nkuipou-Kenfack, E., Engel, H., Fakih, S. y Nocker, A. (2013). Improving efficiency of viability-PCR for selective detection of live cells. Journal of Microbiological Methods, 93 (1), pp. 20-24. https://doi.org/10.1016/j.mimet.2013.01.018 PMid:23389080
Nocker, A. y Camper, A. K. (2009). Novel approaches toward preferential detection of viable cells using nucleic acid amplification techniques. FEMS. Microbiology Letter, 291 (2), pp. 137-142. https://doi.org/10.1111/j.1574-6968.2008.01429.x PMid:19054073
Nyström, T. (2003). Nonculturable bacteria: programmed survival forms or cells at death's door? Bioessays, 25 (3), pp. 204-211. https://doi.org/10.1002/bies.10233 PMid:12596224
Oliver, J. D. (2005). The viable but nonculturable state in bacteria. Journal of Microbiology, 43 (1), pp. 93-100.
Oliver, J. D. (2010). Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiology Reviews, 34 (4), pp. 415-425. https://doi.org/10.1111/j.1574-6976.2009.00200.x PMid:20059548
Pommepuy, M., Butin, M., Derrien, A., Gourmelon, M., Colwell, R. y Cormier, M. (1996). Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to seawater and sunlight. Applied Environmental Microbiology, 62 (12), pp. 4621-4626. https://doi.org/10.1128/AEM.62.12.4621-4626.1996 PMid:8953732
Rastogi, G., Sbodio, A., Tech, J. J., Suslow, T. V., Coaker, G. L. y Leveau J. H. (2012). Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. The ISME Journal, 6 (10), pp. 1812-1822. https://doi.org/10.1038/ismej.2012.32 PMid:22534606 PMCid:PMC3446804
Sieracki, M. E., Cucci, T. L. y Nicinski, J. (1999). Flow cytometric analysis of 5-cyano-2,3-ditolyl tetrazolium chloride activity of marine bacterioplankton in dilution cultures. Applied Environmental Microbiology, 65 (6), pp. 2409-2417. https://doi.org/10.1128/AEM.65.6.2409-2417.1999 PMid:10347021
Signoretto, C., Lleo, M. D. M. y Canepari. P. (2002). Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Current Microbiology, 44 (2), pp. 125-131. https://doi.org/10.1007/s00284-001-0062-0 PMid:11815857
Tamburini, S., Foladori, P., Ferrentino, G., Spilimbergo, S. y Jousson, O. (2014). Accurate flow cytometric monitoring of Escherichia coli subpopulations on solid food treated with high pressure carbon dioxide. Journal of Applied Microbiology, 117 (2), pp. 440-450. https://doi.org/10.1111/jam.12528 PMid:24766564
Tombini Decol, L., López-Gálvez, F., Truchado, P., Tondo, E. C., Gil, M. I. y Allende, A. (2019). Suitability of chlorine dioxide as a tertiary treatment for municipal wastewater and use of reclaimed water for overhead irrigation of baby lettuce. Food Control, 96, pp. 186- 193. https://doi.org/10.1016/j.foodcont.2018.08.036
Truchado, P., Gil, M. I., Kostic, T. y Allende, A. (2016). Optimization and validation of a PMA-qPCR method for Escherichia coli quantification in primary production. Food Control, 62, pp. 150- 156. https://doi.org/10.1016/j.foodcont.2015.10.014
Van der Linden, I., Cottyn, B., Uyttendaele, M., Vlaemynck, G., Maes, M. y Heyndrickx, M. (2014). Evaluation of an attachment assay on lettuce leaves with temperature and starvation stressed Escherichia coli O157:H7 MB3885. Journal of Food Protection, 77 (4), pp. 549-557. https://doi.org/10.4315/0362-028X.JFP-13-332 PMid:24680065
Van Frankenhuyzen, J. K., Trevors, J. T., Flemming, C. A., Lee, H. y Habash, M. B. (2013). Optimization, validation, and application of a real-time PCR protocol for quantification of viable bacterial cells in municipal sewage sludge and biosolids using reporter genes and Escherichia coli. Journal of Industrial Microbiology and Biotechnology, 40 (11), pp.1251-1261. https://doi.org/10.1007/s10295-013-1319-x PMid:23958912
Wan, C., Yang, Y., Xu, H., Aguilar, Z. P., Liu, C., Lai, W., Xiong, Y., Xu, F. y Wei, H. (2012). Development of a propidium monoazide treatment combined with loop-mediated isothermal amplification (PMA-LAMP) assay for rapid detection of viable Listeria monocytogenes. International Journal of Food Science and Technology. 47 (11), pp. 2460-2467. https://doi.org/10.1111/j.1365-2621.2012.03123.x
Wang, L., Li, P., Zhang, Z., Chen, Q., Aguilar, Z. P. y Xu, H. (2014). Rapid and accurate detection of viable Escherichia coli O157: H7 in milk using a combined IMS, sodium deoxycholate, PMA and real-time quantitative PCR process. Food Control, 36 (1), pp. 119-125. https://doi.org/10.1016/j.foodcont.2013.08.011
Winkelströter, L. K. y De Martinis, E. C. P. (2015). Different methods to quantify Listeria monocytogenes biofilms cells showed different profile in their viability. Brazilian Journal of Microbiology. 46 (1), pp. 231-235. https://doi.org/10.1590/S1517-838220131071 PMid:26221112 PMCid:PMC4512067
Xu, H. S., Roberts, N., Singleton, F. L., Attwell, R. W., Grimes, D. J. y Colwell, R. R. (1982). Survival and viability of nonculturable Escherichia coli and Vibrio cholera in the estuarine and marine environment. Microbial Ecology, 8 (4), pp. 313-323. https://doi.org/10.1007/BF02010671 PMid:24226049
Zhang, S., Ye, C., Lin, H., Lv, L. y Yu, X. (2015). UV disinfection induces a VBNC state in Escherichia coli and Pseudomonas aeruginosa. Environmental Science Technology, 49 (3), pp. 1721-1728. https://doi.org/10.1021/es505211e PMid:25584685
Zhao, X., Wang, J., Forghani, F., Park J. H, Park M. S, Seo, K. H. y Oh, D. H. (2013). Rapid detection of viable Escherichia coli O157 by coupling propidium monoazide with loop-mediated isothermal amplification. Journal of Microbiology and Biotechnology, 23 (12), pp. 1708-1716. https://doi.org/10.4014/jmb.1306.06003 PMid:24002453
Zhao, X., Zhong, J., Wei, C., Lin, C. W. y Ding, T. (2017). Current perspectives on viable but non-culturable state in foodborne pathogens. Frontiers in Microbiology, 8, 580. https://doi.org/10.3389/fmicb.2017.00580
Zhou, B., Liang, T., Zhan, Z., Liu, R., Li, F. y Xu, H. (2017). Rapid and simultaneous quantification of viable Escherichia coli O157:H7 and Salmonella spp. in milk through multiplex real-time PCR. Journal of Dairy Science, 100 (11), 8804-8813. https://doi.org/10.3168/jds.2017-13362 PMid:28865862
Recursos en línea
Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. [En línea]. Disponible en https://eur-lex.europa.eu/legal-content/ES/TXT/?uri=celex:32005R2073
European Commission Notice No. 2017/C 163/01 on Guidance Document on Addressing Microbiological Risks in Fresh Fruit and Vegetables at Primary Production through Good Hygiene. [En línea]. Disponible en https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A52017XC0523%2803%29
FSMA Final Rule on Produce Safety. Standards for the Growing, Harvesting, Packing, and Holding of Produce for Human Consumption. [En línea]. Disponible en https://www.fda.gov/food/food-safety-modernization-act-fsma/fsma-final-rule-produce-safety
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