Microbiological quality of home production of sprouts in Brazil
DOI:
https://doi.org/10.5327/fst.00479Keywords:
bacteria, germination, seed disinfection, total coliforms, chemical decontaminationAbstract
Sprouts are considered foods with high nutritional value, tasty, and easy to produce even in domestic environments. However, their consumption has been linked to various food outbreaks, as they are susceptible to microbial contamination. This work aimed to evaluate the microbiological quality of lentil, wheat, and chia sprouts germinated in a domestic environment and the effectiveness of the sprout and seed sanitization process. Total coliforms, Escherichia coli, mesophilic aerobes, and Bacillus cereus were determined, and the presence of Salmonella spp. and Listeria monocytogenes was investigated. No strains of Salmonella spp., E. coli, and L. monocytogenes were found. However, a high microbial load of total coliforms was found in the sprouts. B. cereus was found only in the wheat and chia sprout samples. The sanitization process with sodium hypochlorite was able to reduce the microbial load of the sprouts, but the load remained high. Seeds should be marketed only when they are suitable for home germination after going through a more efficient decontamination process. In addition, competent authorities are supposed to create and widely disseminate a document of good production practices for safer domestic cultivation of sprouts.
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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
Abdel-Aty, A. M., Elsayed, A. M., Salah, H. A., Bassuiny, R. I., & Mohamed, S. A. (2021). Egyptian chia seeds (Salvia hispanica L.) during germination: upgrading of phenolic profile, antioxidant, antibacterial properties and relevant enzymes activities. Food Science Biotechnology, 30(5), 723–734. https://doi.org/10.1007/s10068-021-00902-2
Andrews, W. H., Wang, H., Jacobson, A., Ge, B., Zhang, G., & Hammack, T. (2023). Salmonella. In Food and Drug Administration (Ed.), Bacteriological Analytical Manual (April 2023 ed.). FDA. https://www.fda.gov/food/laboratory-methods-food/bam-chapter-5-salmonella
Aloo, S. O., Ofosu, F. K., Kilonzi, S. M., Shabbir, U., & Oh, D. H. (2021). Edible Plant Sprouts: Health Benefits, Trends, and Opportunities for Novel Exploration. Nutrients, 13(8), Article 2882. https://doi.org/10.3390/nu13082882.
American Public Health Association. (2015). Compendium of Methods for the Microbiological Examination of Foods (Y. Salfinger & M. L. Tortorello, Ed., 15th ed.). APHA.
Andrews, W. H., & Hamamack, T. (2007). Chapter 5: Salmonella. In United States Food and Drug Administration (Ed.). Bacteriological Analytical Manual (8th ed., pp. 1–21). United States Food and Drug Administration. https://fda.report/media/79991/BAM-Chapter-5--Salmonella-%28version-December-2007%29.pdf
Arnesen, L. P. S., O’Sullivan, K., & Granum, P. E. (2007). Food poisoning potential of Bacillus cereus strains from Norwegian dairies. International Journal of Food Microbiology, 116(2), 292–296. https://doi.org/10.1016/j.ijfoodmicro.2006.12.021
Australia (2013). Eat For Health: Australian Dietary Guidelines Summary. National Health and Medical Research Council.
Barros, D. M., Silva, A. P. F., Moura, D. F., Barros, M. V. C., Pereira, A. B. S., Melo, M. A., Silva, A. L. B., Rocha, T. A., Ferreira, S. A. O., Siqueira, T. T. A., Carvalho, M. F., Freitas, T. S., Leite, D. R. S., Melo, N. S., Alves, T. M., Barbosa, T. S. L., Santos, J. S. S., Costa, M. P., Diniz, M. A., & Fonte, R. A. B. (2021). The influence of food and nutritional transition on the increase in the prevalence of chronic non-communicable diseases. Brazilian Journal of Development, 7(7), 74647–74664. https://doi.org/10.34117/bjdv7n7-579
Brankatschk, K., Kamber, T., Pothier, J. F., Duffy, B., & Smits, T. H. M. (2014). Transcriptional profile of Salmonella enterica subsp. enterica serovar Weltevreden during alfalfa sprout colonization. Microbial Biotechnology, 7(6), 528–544. https://doi.org/10.1111/1751-7915.12104
Brasil (2014). Guia Alimentar para a População Brasileira (2nd ed.). Ministério da Saúde.
Brasil (2022). Instrução normativa n° 161, de 1º de julho de 2022. Estabelece os padrões microbiológicos dos alimentos. Diário Oficial da União. https://www.in.gov.br/en/web/dou/-/instrucao-normativa-in-n-161-de-1-de-julho-de-2022-413366880
Bruker. (2015). Instructions for Use Bruker Guide to MALDI Sample Preparation. Retrieved February 04, 2025, from https://www.bc.edu/content/dam/bc1/top-tier/research/VPR/research-facilities/8702557_IFU_Bruker_Guide_MALDI_Sample_Preparation_Revision_E.pdf
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
Cauchon, K. E., Hitchins, A. D., & Smiley, R. D. (2017). Comparison of Listeria monocytogenes recoveries from spiked mung bean sprouts by the enrichment methods of three regulatory agencies. Food Microbiology, 66, 40–47. https://doi.org/10.1016/j.fm.2017.03.021
Centers for Disease Control and Prevention. (2015). Wholesome Soy Products, Inc. Sprouts and Investigation of Human Listeriosis Cases (Final Update). Retrieved February 04, 2025, from https://www.cdc.gov/listeria/ outbreaks/bean-sprouts-11-14/index.html
Centers for Disease Control and Prevention. (2020). E. coli Outbreak Linked to Clover Sprouts. Retrieved February 04, 2025, from https://www.cdc.gov/ecoli/2020/o103h2-02-20/
Centers for Disease Control and Prevention. (2023). Salmonella. Retrieved February 04, 2025, from https://www.cdc.gov/salmonella/index.html
Choi, W., & Kim, S.-S. (2020). Outbreaks, germination, and inactivation of Bacillus cereus in food products: a review. Journal of Food Protection, 83(9), 1480–1487. https://doi.org/10.4315/0362-028X.JFP-19-429
Dietrich, R., Jessberger, N., Ehling-Schulz, M., Märtlbauer, E., & Granum, P. E. (2021). The food poisoning toxins of Bacillus cereus. Toxins, 13(2), Article 98. https://doi.org/10.3390/toxins13020098
Ding, H., Fu, T.-J., & Smith, M. A. (2013). Microbial contamination in sprouts: how effective is seed disinfection treatment? Journal of Food Science, 78(4), R495–R501. https://doi.org/10.1111/1750-3841.12064
Ebert, A. W. (2022). Sprouts and microgreens—novel food sources for healthy diets. Plants, 11(4), Article 571. https://doi.org/10.3390/plants11040571
European Commission. (2005). Guidance Document on Listeria Monocytogenes shelf-life studies for ready-to-eat foods, under Regulation (EC) (No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. https://food.ec.europa.eu/system/files/2016-10/biosafety_fh_mc_guidance_document_lysteria.pdf
European Food Safety Authority. (2011). Scientific opinion on the risk posed by Shiga toxin-producing Escherichia coli (STEC) and other pathogenic bacteria in seeds and sprouted seeds. EFSA Journal, 9(11), Article 2424. https://doi.org/10.2903/j.efsa.2011.2424
Garner, D., & Kathariou, S. (2016). Fresh produce–associated listeriosis outbreaks, sources of concern, teachable moments, and insights. Journal of Food Protection, 79(2), 337–344. https://doi.org/10.4315/0362-028X.JFP-15-387
Gilbert, G.S., Diaz, A., & Bregoff, H. A. (2023). Seed disinfestation practices to control seed-borne fungi and bacteria in home production of sprouts. Foods, 12(4), Article 747. https://doi.org/10.3390/foods12040747
Glasset, B., Herbin, S., Guillier, L., Cadel-Six, S., Vignaud, M.-L., Grout, J., Pairaud, S., Michel, V., Hennekinne, J.-A., Ramarao, N., & Brisabois, A. (2016). Bacillus cereus-induced food-borne outbreaks in France, 2007 to 2014: epidemiology and genetic characterisation. Eurosurveillance, 21(48), Article 30413. https://doi.org/10.2807/1560-7917.ES.2016.21.48.30413
Harmon, S. M., Kautter, D. A., & Solomon, H. M. (1987). Bacillus cereus contamination of seeds and vegetable sprouts grown in a home sprouting kit. Journal of Food Protection, 50(1), 62–65. https://doi.org/10.4315/0362-028X-50.1.62
Hitchins A. D., Jinneman K., & Chen Y. (2022). Detection of Listeria monocytogenes in Foods and Environmental Samples, and Enumeration of Listeria monocytogenes in Foods. In Food and Drug Administration (Ed.), Bacteriological Analytical Manual (April 2022 ed.). FDA. https://www.fda.gov/food/laboratory-methods-food/bam-chapter-10-detection-listeria-monocytogenes-foods-and-environmental-samples-and-enumeration
Iacumin, L., & Comi, G. (2019). Microbial quality of raw and ready-to-eat mung bean sprouts produced in Italy. Food Microbiology, 82, 371–377. https://doi.org/10.1016/j.fm.2019.03.014
International Organization for Standardization. (2004). International Standard ISO 7932. Microbiology of food and animal feeding stuffs – Horizontal method for the enumeration of presuntive Bacillus cereus - Colony count technique at 30°C (3th ed.). International Organization for Standardization.
Jeddi, M. Z., Yunesian, M., Gorji, M. E., Noori, N., Pourmand, M. R., & Khaniki, G. R. J. (2014). Microbial evaluation of fresh, minimally-processed vegetables and bagged sprouts from chain supermarkets. Journal of Health Population and Nutrition, 32(3), 391–399. https://pubmed.ncbi.nlm.nih.gov/25395902/
Jin, H.-H., & Lee, S.-Y. (2007). Combined effect of aqueous chlorine dioxide and modified atmosphere packaging on inhibiting Salmonella Typhimurium and Listeria monocytogenes in mungbean sprouts. Journal of Food Science, 72(9), M441–M445. https://doi.org/10.1111/j.1750-3841.2007.00555.x
Kim, M.-J., & Cheigh, C.-I. (2021). Microbiological contamination of fresh-cut produce in Korea. Food Science Biotechnology, 31(1), 79–87. https://doi.org/10.1007/s10068-021-01014-7
Lee, S.-Y., Yun, K.-M., Fellman, J., & Kang, D.-H. (2002). Inhibition of Salmonella Typhimurium and Listeria monocytogenes in mung bean sprouts by chemical treatment. Journal of Food Protection, 65(7), 1088–1092. https://doi.org/10.4315/0362-028x-65.7.1088
Menezes, M. F. G., & Maldonado, L. A. (2015). Do nutricionismo à comida: a culinária como estratégia metodológica de educação alimentar e nutricional. Revista Hospital Universitário Pedro Ernesto, 14(3), 82–89. https://doi.org/10.12957/rhupe.2015.19950
Martínez-Villaluenga, C., Frías, J., Gulewicz, P., Gulewicz, K., & Vidal-Valverde, C. (2008). Food safety evaluation of broccoli and radish sprouts. Food and Chemical Toxicology, 46(5), 1635–1634. https://doi.org/10.1016/j.fct.2008.01.004
Miyahira, R. F., & Antunes, A. E. C. (2021). Bacteriological safety of sprouts: a brief review. International Journal of Food Microbiology, 352, Article 109266. https://doi.org/10.1016/j.ijfoodmicro.2021.109266
Miyahira, R. F., Giangiarulo, T., Lopes, J. O., Silva, W. P., Esmerino, E. A., & Antunes, A. E. C. (2023). Sprouts consumption: A correlational study between Brazilian consumers’ perception, motivation to eat new products levels and food choice factors. Journal of Sensory Studies, 38(4), Article e12829. https://doi.org/10.1111/joss.12829
Miyahira, R. F., Lopes, J. O., & Antunes, A. E. C. (2021). The use of sprouts to improve the nutritional value of food products: a brief review. Plant Foods of Human Nutrition, 76(2), 143–152. https://doi.org/10.1007/s11130-021-00888-6
Miyahira, R. F., Pena, F. L., Fabiano, G. A., Lopes, J. O., Ponte, L. G. S., Cunha, D. T., Bezerra, R. M. N., & Antunes, A. E. C. (2022). Changes in phenolic compound and antioxidant activity of germinated broccoli, wheat, and lentils during simulated gastrointestinal digestion. Plant Foods of Human Nutrition, 77(2), 233–240. https://doi.org/10.1007/s11130-022-00970-7
National Advisory Committee on Microbiological Criteria for Foods. (1999). Microbiological safety evaluations and recommendations on sprouted seeds. International Journal of Food Microbiology, 52(3), 123–153. https://doi.org/10.1016/s0168-1605(99)00135-x
Oliveira, M. F. B., & Castro, I. R. R. (2022). Cooking autonomy: a multilevel conceptual model on healthy home cooking. Cadernos de Saúde Pública, 38(4), Article EN178221. https://doi.org/10.1590/0102-311XEN178221
Pao, S., Khalid, M. F., & Kalantari, A. (2005). Microbial profiles of on-line–procured sprouting seeds and potential hazards associated with enterotoxigenic bacillus spp. in homegrown sprouts. Journal of Food Protection, 68(8), 1648–1653. https://doi.org/10.4315/0362-028x-68.8.1648
Peñas, E., & Martínez-Villaluenga, C. (2020). Advances in production, properties and applications of sprouted seeds. Foods, 9(6), Article 790. https://doi.org/10.3390/foods9060790
Portnoy, B. L., Goepfert, J. M., & Harmon, S. M. (1976). An outbreak of Bacillus cereus food poisoning resulting from contaminated vegetable sprouts. American Journal of Epidemiology, 103(6), 589–594. https://doi.org/10.1093/oxfordjournals.aje.a112263
Rahnama, H., Azari, R., Yousefi, M. H., Berizi, E., Mazloomi, S. M., Hosseinzadeh, S., Derakhshan, Z., Ferrante, M., & Conti, G. O. (2023). A systematic review and meta-analysis of the prevalence of Bacillus cereus in foods. Food Control, 143, Article 109250. https://doi.org/10.1016/j.foodcont.2022.109250
Salgado, V. S. C. N., Zago, L., Antunes, A. E. C., & Miyahira, R. F. (2022). Chia (Salvia hispanica L.) Seed Germination: a Brief Review. Plant Foods for Human Nutrition, 77(4), 485–494. https://doi.org/10.1007/s11130-022-01011-z
Santos, C. S., Silva, B., Valente, L. M. P., Gruber, S., & Vasconcelos, M. W. (2020). The effect of sprouting in lentil (Lens culinaris) nutritional and microbiological profile. Foods, 9(4), Article 400. https://doi.org/10.3390/foods9040400
Saroj, S. D., Shashidhar, R., Dhokane, V., Hajare, S., Sharma, A., & Bandekar, J. R. (2006). Microbiological evaluation of sprouts marketed in Mumbai, India, and its suburbs. J Journal of Food Protection, 69(10), 2515–2518. https://doi.org/10.4315/0362-028x-69.10.2515
Seo, Y.-H., Jang, J.-H., & Moon, K.-D. (2010). Microbial evaluation of minimally processed vegetables and sprouts produced in Seoul, Korea. Food Science and Biotechnology, 19(5), 1283–1288. https://doi.org/10.1007/s10068-010-0183-y
Seow, J., Ágoston, R., Phua, L., & Yuk, H.-G. (2012). Microbiological quality of fresh vegetables and fruits sold in Singapore. Food Control, 25(1), 39–44. https://doi.org/10.1016/j.foodcont.2011.10.017
Sikin, A. M., Zoellner, C., & Rizvi, S. S. H. (2013). Current Intervention Strategies for the Microbial Safety of Sprouts. Journal of Food Protection, 76(12), 2099–2123. https://doi.org/10.4315/0362-028x.jfp-12-437
Tango, C. N., Wei, S., Khan, I., Hussain, M. S., Kounkeu, P.-F. N., Park, J.-H., Kim, S.-H., & Oh, D. H. (2018). Microbiological Quality and Safety of Fresh Fruits and Vegetables at Retail Levels in Korea. Journal of Food Science, 83(2), 386–392. https://doi.org/10.1111/1750-3841.13992
Tornuk, F., Ozturk, I., Sagdic, O., & Yetim, H. (2011). Determination and Improvement of Microbial Safety of Wheat Sprouts with Chemical Sanitizers. Foodborne Pathogens and Disease, 8(4), 503–508. https://doi.org/10.1089/fpd.2010.0709
Ultee, A., Kets, E. P., & Smid, E. J. (1999). Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology, 65(10), 4606–4610. https://doi.org/10.1128/AEM.65.10.4606-4610.1999
United States of America (2020). Dietary Guidelines for Americans, 2020–2025 (9th ed.). United State Department of Agriculture; United State Department of Health and Human Services. https://www.dietaryguidelines.gov/resources/2020-2025-dietary-guidelines-online-materials
Zheng, Q., Mikš-Krajnik, M., D’Souza, C., Yang, Y., Heo, D.-J., Kim, S.-K., Lee, S.-C., & Yuk, H.-G. (2015). Growth of healthy and sanitizer-injured Salmonella cells on mung bean sprouts in different commercial enrichment broths. Food Microbiology, 52, 159–168. https://doi.org/10.1016/j.fm.2015.07.013