Microbiology of carrot, tomato and cabbage from organic and conventional agriculture in Costa Rica

Authors

DOI:

https://doi.org/10.15517/am.v34i2.52743

Keywords:

vegetables, Escherichia coli, Listeria monocytogenes, bacteria, moulds

Abstract

Introduction. Interest in consuming fresh products such as vegetables has been increasing over the years. Different cultivation methods to produce vegetables such as carrots, tomatoes, and cabbages are available. Conventional and organic farming systems are the most common. Objective. To compare the microbiology of carrot, tomato and cabbage from farms with organic or conventional agricultural production systems in Costa Rica. Materials and methods. Sampling was carried out in Cartago, Heredia and Alajuela, Costa Rica, from September 2020 to November 2021, during the rainy season in all cases. Vegetables from model farms of carrot, tomato and cabbage, one of organic production and three of conventional production, were sampled. Microbial counts of total aerobic mesophilic, total coliforms, Escherichia coli, yeasts and molds, and the absence/presence of Listeria monocytogenes were determined. Results. Total aerobic, yeast and mold and total coliform counts for conventionally and organically grown carrots, cabbages, and tomatoes did not differ from each other. In the vegetables studied, E. coli counts were <1 log CFU/g and Listeria monocytogenes was absent. Presence of Listeria sp. in carrot samples from conventional cultivation was found in contrast to its absence in carrots from organic cultivation. Conclusions. L. monocytogenes was absent in the vegetables studied, which in general had acceptable microbial loads according to regulations and similar to studies reported worldwide. Under controlled conditions, when compared to those obtained from conventional production systems, it is possible to obtain vegetables from organic farming without detriment to their microbiological quality and with the derived benefits for the health of the consumer and the environment.

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References

Abadias, M., Usall, J., Anguera, M., Solsona, C., & Viñas, I. (2008). Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. International Journal of Food Microbiology, 123(1–2), 121–129. https://doi.org/10.1016/j.ijfoodmicro.2007.12.013

Adams, M. R., Moss, M. O., & McClure, P. (2016). Food microbiology (4th ed.). The Royal Society of Chemistry.

Aftab Uddin, M., Wali Ullah, M., & Noor, R. (2012). Prevalence of Vibrio cholerae in human-, poultry-, animal excreta and compost samples. Stamford Journal of Microbiology, 2(1), 38–41. https://doi.org/10.3329/sjm.v2i1.15213

Ajayeoba, T. A., Atanda, O. O., Obadina, A. O., Bankole, M. O., & Adelowo, O. O. (2015). The incidence and distribution of Listeria monocytogenes in ready-to-eat vegetables in South-Western Nigeria. Food Science & Nutrition, 4(1), 59–66. https://doi.org/10.1002/fsn3.263

AL-Zenki, S. F., AL-Mazeedi, H. M., AL-Hooti, S. N., AL-Ati, T., AL-Matawah, Q., Alomirah, H. F., & Sidhu, J. (2008). Characterization of quality and safety of tomatoes sold in the state of Kuwait. International Journal of Postharvest Technology and Innovation, 1(3), 298–311. https://doi.org/10.1504/IJPTI.2008.021464

Association of Official Agricultural Chemists. (2005). Microbiological methods. Coliforms. Escherichia coli. In W. Horwitz, & G. W. Latimer (Eds.), Official Methods of Analysis of AOAC International (AOAC official method 991.14, 18th ed.). AOAC International.

Bolaños Alfaro, S. E. (2002). Recuento microbiológico y presencia de enteropatógenos en vegetales cultivados y comercializados en el Área Metropolitana [Tesis de licenciatura, Universidad de Costa Rica]. Repositorio Kerwa. https://hdl.handle.net/10669/16783

Bosona, T., & Gebresenbet, G. (2018). Life cycle analysis of organic tomato production and supply in Sweden. Journal of Cleaner Production, 196, 635–643. https://doi.org/10.1016/j.jclepro.2018.06.087

Campuzano, F. S., Mejía Flórez, D., Madero Ibarra, C., & Pabón Sánchez, P. (2015). Determinación de la calidad microbiológica y sanitaria de alimentos preparados vendidos en la vía pública de la ciudad de Bogotá DC. Nova, 13(23), 81–92. https://doi.org/10.22490/24629448.1708

Consejo Nacional de Producción. (2016). Análisis y monitoreo de mercados: Tomate. https://www.cnp.go.cr/sim/sector_agricola/Hortalizas/tomate/Analisis_de_Mercado/2016/M_tomate_01_08-11-16.pdf

Chaturvedi, M., Kumar, V., Singh, D., & Kumar, S. (2013). Assessment of microbial load of some common vegetables among two different socioeconomic groups. International Food Research Journal, 20(5), 2927–2931. http://www.ifrj.upm.edu.my/20%20(05)%202013/52%20IFRJ%2020%20(05)%202013%20Chaturvedi%20131.pdf

da Silva, N., Taniwaki, M., Junqueira, V., Silveira, N., Okazaki, M., & Gomes, R., (2019). Microbiological examination methods of food and water (2nd ed.). CRC Press.

Dávila-Aviña, J. E., Ríos-López, A., Aguayo-Acosta, A., & Solís-Soto, L. Y. (2020). Probiotics in fresh-cut produce. In M. Wasim Siddiqui (Ed.), Fresh-cut fruits and vegetables (pp. 205–223). Academic Press. https://doi.org/10.1016/B978-0-12-816184-5.00010-0

do Prado Vilarin, S., Rocha Teixeira, T. M., Gonçalves Lima, C. M., Pamplona Pagnossa, J., Mendoça de Figueiredo, R., Cardoso Medeiros, U. B., & Ferreira Santana, R. (2020). Effect of sanitization on minimally processed cabbage (Brassica oleracea L.). Research, Society and Development, 9(6), Article e59963467. https://doi.org/10.33448/rsd-v9i6.3467

El-Hage Scialabba, N., & Hattam, C. (Eds.) (2003). Agricultura Orgánica, Ambiente y Seguridad Alimentaria. Organización de las Naciones Unidas para la Agricultura y la Alimentación. https://www.fao.org/3/y4137s/y4137s00.htm#Contents

Erickson, M. C. (2010). Microbial risks associated with cabbage, carrots, celery, onions, and deli salads made with these produce items. Comprehensive Reviews in Food Science and Food Safety, 9(6), 602–619. https://doi.org/10.1111/j.1541-4337.2010.00129.x

Erkmen, O., & T. F. Bozoglu. (Eds.). (2016). Food microbiology: Principles into practice. John Wiley & Sons, Ltd.

García-Barquero, M. E. (2015). Análisis del comportamiento de mercado en las ferias del agricultor de la Gran Área Metropolitana. Tecnología en Marcha, 29(1), 83–95. https://doi.org/10.18845/tm.v29i1.2541

Garro Alfaro, J. E. (2016). El suelo y los abonos orgánicos. Instituto Nacional de Innovación y Transferencia en Tecnología Agropecuaria. http://www.mag.go.cr/bibliotecavirtual/F04-10872.pdf

Gosh, M., Ganguli, A., & Mudgil, S. (2004). Microbiological quality of carrots used for preparation of fresh squeezed street vended carrot juices in India. Journal of Food, Agriculture & Environment, 2(2), 143–145. https://www.wflpublisher.com/Abstract/181

Hasibur, R., Farahnaaz, F., Md. Sajjad, A., Kamal, K. D., & Rashed, N. (2016). Demonstration of the source of microbial contamination of freshly cultivated cabbage, cauliflower, potato and squash collected from rural farms of Bangladesh. International Food Research Journal, 23(3), 1289–1295. http://www.ifrj.upm.edu.my/23%20(03)%202016/(52).pdf

Hernández Yépez, J. N. (2013). Caracterización físico-química y microbiológica del tomate margariteño (Lycopersicum esculentum var. España) y evaluación de la efectividad de tratamientos de pre-envasado para el incremento de su vida comercial a temperatura ambiente [Tesis de doctorado, Universidad de Córdoba]. Helvia: repositorio institucional de la Universidad de Córdoba. http://hdl.handle.net/10396/9925

Hirotani, H., Naranjo, J., Moroyoqui, P. G., & Gerba, C. P. (2006). Demonstration of indicator microorganisms on the surface of vegetables on the market in the United States and Mexico. Journal of Food Science, 67(5), 1847–1850. https://doi.org/10.1111/j.1365-2621.2002.tb08733.x

Instituto Nacional de Estadística y Censos. (2015). Resultados generales. VI Censo Nacional Agropecuario. https://www.inec.cr/censos/censo-agropecuario-2014

Instituto Nacional de Estadística y Censos. (2018). Encuesta Nacional Agropecuaria 2018. http://sistemas.inec.cr/pad5/index.php/catalog/243

Jaramillo, J., Rodríguez, V. P. Guzmán, M., Zapata, M., & Rengifo, T. (2007). Producción de tomate bajos condiciones protegidas (Manual Técnico). Organización de las Naciones Unidas para la Agricultura y la Alimentación. http://www.fao.org/3/a1374s/a1374s00.htm

Johnston, L. M., Jaykus, L. -A., Moll, D., Anciso, J., Mora, B., & Moe, C. L. (2006). A field study of the microbiological quality of fresh produce of domestic and Mexican origin. International Journal of Food Microbiology, 112(2), 83–95. https://doi.org/10.1016/j.ijfoodmicro.2006.05.002

Khadka, R. B., Marasini, M., Rawal, R., Gautam, D. M., & Acedo, A. L. (2017). Effects of variety and postharvest handling practices on microbial population at different stages of the value chain of fresh tomato (Solanum lycopersicum) in Western Terai of Nepal. BioMed Research International, 2017, Article 7148076. https://doi.org/10.1155/2017/7148076

Kayode, A. J., & Okoh, A. I. (2022). Incidence and genetic diversity of multi-drug resistant Listeria monocytogenes isolates recovered from fruits and vegetables in the Eastern Cape Province, South Africa. International Journal of Food Microbiology, 363, Article 109513. https://doi.org/10.1016/j.ijfoodmicro.2021.109513

Kim, M. -J., & Cheigh, C. -I. (2022). Microbiological contamination of fresh-cut produce in Korea. Food Science Biotechnology, 31, 79–87. https://doi.org/10.1007/s10068-021-01014-7

Kuan, C. -H., Rukayadi, Y., Ahmad, S. H., Wan Mohamed Radzi, C. W. J., Thung, T. -Y., Premarathne, J. M. K. J. K., Chang, W. -S., Loo, Y. -Y., Tan, C. -W., Ramzi, O. B., Mohd Fadzil, S. N., Kuan, C. -S., Yeo, S. -K., Nishibuchi, M., & Radu, S. (2017). Comparison of the microbiological quality and safety between conventional and organic vegetables sold in Malaysia. Frontiers in Microbiology, 8, Article 1433. https://doi.org/10.3389/fmicb.2017.01433

Kyanko, M. V., Russo, M. L., Fernández, M., & Pose, G. (2010). Efectividad del ácido peracético sobre la reducción de la carga de esporas de mohos causantes de pudrición poscosecha de frutas y hortalizas. Información Tecnológica, 21(4), 125–130. http://doi.org/10.4067/S0718-07642010000400016

León, J. S., Jaykus, L. -A., & Moe, C. L. (2009). Food safety issues and the microbiology of fruits and vegetables. In N. Heredia, I. Wesley, & S. García (Eds.), Microbiologically safe foods (pp. 255–290). John Wiley & Sons, Inc. https://doi.org/10.1002/9780470439074.ch12

López Marín, L. M. (2012, setiembre 14-16). Actualidad de la agrocadena del cultivo de tomate (Solanum lycopersicum) [Presentación en congreso]. Segundo Congreso Nacional del Cultivo de Tomate, Pérez Zeledón, Costa Rica. http://www.mag.go.cr/bibliotecavirtual/A50-5910.pdf

Lotter, D. (2015). Facing food insecurity in Africa: why, after 30 years of work in organic agriculture, I am promoting the use of synthetic fertilizers and herbicides in small-scale staple crop production. Agriculture and Human Values, 32, 111–118. https://doi.org/10.1007/s10460-014-9547-x

Madigan, M. T., Martinko, J. M., Dunlap, P. V., & Clark, D. P. (2009). Brock. Biología de los microorganismos (12th ed.). Pearson.

Marín Céspedes, S. (2015). Comparación de un Andisol manejado convencional y orgánicamente mediante la respuesta de la papa en invernadero a prácticas de fertilización convencional, orgánica y de aplicación de solubilizadores de fósforo [Tesis de licenciatura, Universidad de Costa Rica]. Repositorio Kerwa. https://hdl.handle.net/10669/76801

Martín Alva, E. A. (2007). Listeria monocytogenes en repollo y lechuga como vehículos de transmisión de listeriosis humana. Mercados La Hermelinda, Central y Palermo de Trujillo, Perú [Tesis de doctorado, Universidad Nacional de Trujillo]. Repositorio de la Universidad Nacional de Trujillo. http://dspace.unitru.edu.pe/handle/UNITRU/5786

Miceli, A., & Settanni, L. (2019). Influence of agronomic practices and pre-harvest conditions on the attachment and development of Listeria monocytogenes in vegetables. Annals of Microbiology, 69, 185–199. https://doi.org/10.1007/s13213-019-1435-6

Ministerio de Agricultura y Ganadería. (2008). Buenas prácticas agropecuarias. http://www.mag.go.cr/bibliotecavirtual/P01-4955.PDF

Ocaña-de Jesús, R. L., Gutiérrez-Ibáñez, A. T., Sánchez-Pale, J. R., Mariezcurrena-Berasain, M. D., Velázquez-Garduño, G., Laguna Cerda, A., & Rojas Puebla, I. (2015). Calidad microbiológica del tomate (Solanum lycopersicum L.) producido bajo condiciones de invernáculo en 5 municipios del Estado de México. Phyton, 84(1), 45–50. http://www.revistaphyton.fund-romuloraggio.org.ar/vol84-1/Ocania_De_Jesus.pdf

Okushima, L., Saito, M., Ikeguchi, A., Ishii, M., & Sase, S. (2004). An evaluation of floating dust particles and molds in commercial greenhouses. Acta Horticulturae, 639, 359–366. https://doi.org/10.17660/ActaHortic.2004.639.48

Olaimat A. N., & Holley R. A. (2012) Factors influencing the microbial safety of fresh produce: a review. Food Microbiology, 32(1), 1–19. https://doi.org/10.1016/j.fm.2012.04.016

Pang, H., McEgan, R., Mishra, A., Micallef, S. A., & Pradhan, A. K. (2017). Identifying and modeling meteorological risk factors associated with pre-harvest contamination of Listeria species in a mixed produce and dairy farm. Food Research International, 102, 355–363. https://doi.org/10.1016/j.foodres.2017.09.029

Pérez Rodríguez, E. G., & Chávez Castillo, M. (2012). Frecuencia de Listeria monocytogenes en tomate, zanahoria, espinaca, lechuga y rabanito, expendidos en mercados de Trujillo, Perú. Revista Ciencia y Tecnología, 8(22), 11–21. https://revistas.unitru.edu.pe/index.php/PGM/article/view/183

Poder Ejecutivo Federal. (1995, octubre 10). Norma oficial mexicana NOM-093-SSA1-1994, bienes y servicios. Prácticas de higiene y sanidad en la preparación de alimentos que se ofrecen en establecimientos fijos. Secretaría de Gobernación. https://bit.ly/3yH1xSH

Pomareda, F. (2022, mayo 18). PNUD: Costa Rica usa hasta 8 veces más plaguicidas que los demás países OCDE de América. Semanario Universidad. https://semanariouniversidad.com/pais/pnud-costa-rica-usa-hasta-8-veces-mas-plaguicidas-que-los-demas-paises-ocde-de-america/

Presidencia de la República, & Ministerio de Agricultura y Ganadería. (2001, octubre 9). Reglamento sobre la agricultura orgánica (N°25834-MAG). Sistema Costarricense de Información Jurídica. https://bit.ly/3MlnoVy

Presidencia de la República, Ministerio de Comercio Exterior, Ministerio de Salud, Ministerio de Agricultura y Ganadería, & Ministerio de Economía Industria y Comercio. (2018, julio 16). Reglamento técnico centroamericano Criterios microbiológicos para la inocuidad de los alimentos (N° 41420 – COMEX – S – MAG – MEIC). Sistema Costarricense de Información Jurídica. https://bit.ly/3epJqKe

Prazak, A. N., Murano, E. A., Mercado, I., & Acuff, G. R. (2002). Prevalence of Listeria monocytogenes during production and postharvest processing of cabbage. Journal of Food Protection, 65(11), 1728–1734. https://doi.org/10.4315/0362-028X-65.11.1728

Programa Integral de Mercadeo Agropecuario. (2016, noviembre). Análisis del consumo de frutas, hortalizas, pescado y mariscos en los hogares costarricenses. http://www.pima.go.cr/wp-content/uploads/2017/07/Analisis-Consumo.pdf

Ramírez Mérida, L. G., Morón de Salim, A., Alfieri Graterol, A. Y., & Gamboa, O. (2009). Frecuencia de Listeria monocytogenes en muestras de tomates (Lycopersicum esculentum) y cilantro (Coriandrum sativum) frescos en tres supermercados de Valencia. Archivos Latinoamericanos de Nutrición, 59(3), 318–324. https://www.alanrevista.org/ediciones/2009/3/art-13/

Ramírez Vargas, C., & Nienhuis, J. (2012). Evaluación del crecimiento y productividad del tomate (Lycopersicon esculentum Mill) bajo cultivo protegido en tres localidades de Costa Rica. Revista Tecnología En Marcha, 25(1), 3–15. https://doi.org/10.18845/tm.v25i1.172

Red Nacional de Laboratorios Oficiales de Análisis de Alimentos. (2014). Análisis microbiológico de los alimentos. Metodología analítica Oficial. Microorganismos indicadores (Vol. 3). https://bit.ly/3CCcCWe

Reganold, J., & Wachter, J. (2020). Agriculture. Organic. In Y. Wang (Ed.), Terrestrial ecosystem and biodiversity (2nd ed., Chapter 29, pp. 251–259). CRC Press. https://doi.org/10.1201/9780429445651

Ronga, D., Biazzi, E., Parati, K., Carminati, D., Carminati, E., & Tava, A. (2019). Microalgal biostimulants and biofertilisers in crop productions. Agronomy, 9(4), Article 192. https://doi.org/10.3390/agronomy9040192

Sair, A.T., Masud, T., Sohail, A., & Rafique, A. (2017). Microbiological variation amongst fresh and minimally processed vegetables from retail establishers - a public health study in Pakistan. Food Research, 1(6), 249–255. http://doi.org/10.26656/fr.2017.6.060

Salfinger, Y., & Tortorello, M. L. (2015). Compendium of methods for the microbiological examination of foods. American Public Health Association. https://doi.org/10.2105/MBEF.0222

Sánchez López, J. (2017). Generación de líneas T-DNA de tomate (Solanum lycopersicum) para la identificación de mutantes de inserción alterados en la morfogénesis y el desarrollo vegetal [Tesis de doctorado, Universitat Politècnica de València]. RiuNet. https://doi.org/10.4995/Thesis/10251/78617

Smith, A., Moorhouse, E., Monaghan, J., Taylor, C., & Singleton, I. (2018). Sources and survival of Listeria monocytogenes on fresh, leafy produce. Journal of Applied Microbiology, 125(4), 930–942. https://doi.org/10.1111/jam.14025

Smoot, L. M., & Pierson, M. D. (2001). Microorganismos indicadores y criterios microbiológicos. In M. P. Doyle, L. R. Beuchat, & T. J. Montville, (Eds.), Microbiología de los alimentos. Fundamentos y fronteras (pp. 69–83). Acribia.

Song, W. -J., Chung, H. -Y., Kang, D. -H., & Ha, J. -W. (2019). Microbial quality of reduced-sodium napa cabbage kimchi and its processing. Food Science and Nutrition, 7(2), 628–635. https://doi.org/10.1002/fsn3.898

Tal, A. (2018). Making conventional agriculture environmentally friendly: moving beyond the glorification of organic agriculture and the demonization of conventional agriculture. Sustainability, 10(4), Article 1078. https://doi.org/10.3390/su10041078

Townsend, A., Strawn, L. K., Chapman, B. J., & Dunn, L. L. (2021). A systematic review of Listeria species and Listeria monocytogenes prevalence, persistence, and diversity throughout the fresh produce supply chain. Foods, 10(6), Article 1427. https://doi.org/10.3390/foods10061427

United States Food and Drug Administration. (2017). Draft guidande for industry: Control of Listeria monocytogenes in ready-to-eat foods (Document FDA-2008-D-0096). https://bit.ly/3exwCSa

United States Food and Drug Administration. (2022). Bacteriological analytical manual (BAM). https://bit.ly/3MwMgtq

Zarb, J., Ghorbani, R., Koocheki, A., & Leifert, C. (2005). The importance of microorganisms in organic agriculture. Outlooks on Pest Management, 16(2), 52–55. https://doi.org/10.1564/16apl02

Zarkani, A. A., Schierstaedt, J., Becker, M., J Krumwiede, J., Grimm, M., Grosch, R., Jechalke, S., & Schikora, A. (2019). Salmonella adapts to plants and their environment during colonization of tomatoes. FEMS Microbiology Ecology, 95(11), Article fiz152. https://doi.org/10.1093/femsec/fiz152

Published

2023-04-27

How to Cite

Castro-Urbina, F., Wittmann-Vega, V., Davidovich-Young, G., & Wong-González, E. (2023). Microbiology of carrot, tomato and cabbage from organic and conventional agriculture in Costa Rica. Agronomía Mesoamericana, 34(2), 52743. https://doi.org/10.15517/am.v34i2.52743