Microbiology of organic and conventionally grown fresh produce

Daniele F. Maffei Erika Y. Batalha Mariza Landgraf Donald W. Schaffner Bernadette D.G.M. Franco About the authors

ABSTRACT

Fresh produce is a generalized term for a group of farm-produced crops, including fruits and vegetables. Organic agriculture has been on the rise and attracting the attention of the food production sector, since it uses eco-agricultural principles that are ostensibly environmentally-friendly and provides products potentially free from the residues of agrochemicals. Organic farming practices such as the use of animal manure can however increase the risk of contamination by enteric pathogenic microorganisms and may consequently pose health risks. A number of scientific studies conducted in different countries have compared the microbiological quality of produce samples from organic and conventional production and results are contradictory. While some have reported greater microbial counts in fresh produce from organic production, other studies do not. This manuscript provides a brief review of the current knowledge and summarizes data on the occurrence of pathogenic microorganisms in vegetables from organic production.

Keywords:
Fresh produce; Foodborne diseases; Organic agriculture; Pathogens

Introduction

Fresh produce is a generalized term for a group of farm-produced crops, including fruits and vegetables. These foods are an important component of a healthy diet. Consumption of fresh produce is widely promoted by governmental health agencies since it supplies essential nutrients such as vitamins, minerals, dietary fiber and phytochemical compounds at a relatively low calorie density. Furthermore, the consumption of fruits and vegetables has been strongly associated with reduced chronic diseases, risk of heart disease and cancer.11 Dias JS. Nutritional quality and health benefits of vegetables: a review. Food Nutr Sci. 2012;3:1354-1374.

2 Liu RH. Health-promoting components of fruits and vegetables in the diet. Adv Nutr. 2013;4:384-392.
-33 Slavin JL, Lloyd B. Health benefits of fruits and vegetables. Adv Nutr. 2012;3:506-516. Alternative cropping systems have been developed because of society's increasing concerns about the sustainability of conventional agriculture, intensive use of chemical products and their potential risk to human health and the environment.44 Bettiol W, Ghini R, Galvão JAH, Siloto RC. Organic and conventional tomato cropping systems. Sci Agric. 2004;61:253-259.,55 Crowder DW, Reganold JP. Financial competitiveness of organic agriculture on a global scale. Proc Natl Acad Sci U S A. 2015;112:7611-7616. Organic agriculture has been on the rise and is attracting the attention of the food production sector in many parts of the world, since it revives eco-agricultural principles that are potentially more environmentally friendly and may provide products with few agrochemical residues.66 Azadi H, Schoonbeek S, Mahmoudi H, Derudder B, De Maeyer P, Witloxa F. Organic agriculture and sustainable food production system: main potentials. Agric Ecosyst Environ. 2011;144:92-94.,77 Willer H, Lernoud J, eds. The World of Organic Agriculture. Statistics and Emerging Trends. Bonn: Research Institute of Organic Agriculture (FiBL), Frick, and IFOAM - Organics International; 2016. Organic farming practices which use animal manure as fertilizer can increase the risk of contamination by enteric pathogenic microorganisms and, consequently, pose health risks becoming a major concern for consumers and governments. Furthermore, these foods are often consumed raw, increasing risk of infection if pathogens are present.88 Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010;12:2385-2397.

Despite the growing demand for organic fresh produce and its health benefits, a number of foodborne disease outbreaks have been associated with the consumption of these foods.88 Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010;12:2385-2397.

9 Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis. 2015;12:32-38.

10 Doyle MP, Erickson MC. Summer meeting 2007 - the problems with fresh produce: an overview. J Appl Microbiol. 2008;105:317-330.

11 Harris LJ, Farber JN, Beuchat LR, et al. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf. 2003;2:78-141.

12 Jung Y, Jang H, Matthews KR. Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb Biotechnol. 2014;7:517-527.

13 Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect. 2009;137:307-315.
-1414 Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot. 2004;67:2342-2353. However, the number of studies focusing on microbial safety of organically produced foods is low. This manuscript provides a brief review of the current knowledge and summarizes data on the risk of pathogenic microorganisms in vegetables from organic production.

Organic farming

The organic sector has expanded recently worldwide, due to policy support and a growing market demand for these products. Organic farming can be defined as an ecological production system that promotes and enhances biodiversity and biological cycle in soil, crop and livestock. It is based on minimal use of off-farm inputs and on management practices that restore, maintain and enhance ecological harmony.1515 Winter CK, Davis SF. Organic foods. J Food Sci. 2006;71:117-124. The process of certification is also important in organic farming. Certification is intended to assure the consumers that a product marketed as organic was in fact produced according to organic production standards, which vary from country to country, based on their certifying bodies.1616 Vijayan G. Organic Food Certification and Marketing Strategies. Agrihortico; 2014.

Organic farming is regulated internationally by Codex Alimentarius Guidelines [established by the Food and Agricultural Organization of the United Nations (FAO) and the World Health Organization (WHO)] and by the International Federation of Organic Agriculture Movements (IFOAM) Basic Standards.1717 Tuomisto HL, Hodge ID, Riordan P, Macdonald DW. Does organic farming reduce environmental impacts? A meta-analysis of European research. J Environ Manag. 2012;112:309-320. According to the IFOAM,1818 International Federation of Organic Agriculture Movements (IFOAM). The Principles of Organic Agriculture. Bonn, Germany: Preamble. IFOAM; 2005. Available at http://www.ifoam.org/sites/default/files/ifoam_poa.pdf Accessed 06.09.16.
http://www.ifoam.org/sites/default/files...
the principles of organic agriculture are: (i) health: organic agriculture should sustain and enhance the health of soil, plant, animal, human and planet as one and indivisible; (ii) ecology: organic agriculture should be based on living ecological systems and cycles, work with them, emulate them and help sustain them; (iii) fairness: organic agriculture should be built on relationships that ensure fairness with regard to the common environment and life opportunities and (iv) care: organic agriculture should be managed in a precautionary and responsible manner to protect the health and well-being of current and future generations and the environment.

Main sources of contamination of fresh produce by foodborne pathogens

Fresh produce can become contaminated with pathogenic microorganisms during pre-harvest (in the field) and post-harvest stages and this contamination can arise from environmental, animal or human sources. Pre-harvest sources include soil, irrigation water, inadequately composted or raw animal manure, dust, insects, presence of wild and domestic animals and human handling. Post-harvest sources include human handling, harvesting equipment, transport containers/vehicles, rinse water, improper storage and packaging.88 Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010;12:2385-2397.,1111 Harris LJ, Farber JN, Beuchat LR, et al. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf. 2003;2:78-141.,1919 Beuchat LR. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 2002;4:413-423.,2020 Sant'Ana AS, Silva FFP, Maffei DF, Franco BDGM. Fruits and vegetables: introduction. In: Batt CA, Tortorello ML, eds. Encyclopedia of Food Microbiology. 2nd ed. Amsterdam: Academic Press; 2014:972-982. Fig. 1 illustrates the main routes of fresh produce contamination in the field.

Fig. 1
The sources and routes of contamination of fruits and vegetables.

The soil is a habitat for many organisms, including human pathogens, which can contaminate plants through the seeds, roots or surface. Both conventional and organic produce can be fertilized with natural sources of nutrients such as animal manure and plant debris. Since animal manure is the main fertilizer type in organic farming, where no chemical treatment against bacteria is allowed, it gives rise to concern about the possible contamination of produce with microbial pathogens such as Escherichia coli O157:H7, Salmonella spp., and Listeria monocytogenes.2121 Oliveira M, Usall J, Viñas I, Anguera M, Gatius F, Abadias M. Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol. 2010;27:679-684.,2222 Wießner S, Thiel B, Krämer J, Köpke U. Hygienic quality of head lettuce: effects of organic and mineral fertilizers. Food Control. 2009;20:881-886. A key strategy used to reduce the concentration of enteric pathogens in manure is composting, the biological decomposition of organic matter by microorganisms under controlled conditions.2323 Moreno J, López MJ, Vargas-García MC, Suárez-Estrella F. Recent advances in microbial aspects of compost production and use. Acta Hort (ISHS). 2013;1013:443-457. Compost can provide certain benefits to plants when applied to the soil. If composting is done incorrectly (i.e. for too short a time or at too low a temperature), the result can increase microbial proliferation and risk of pathogen contamination.2424 Maffei DF, Silveira NFA, Catanozi MPLM. Microbiological quality of organic and conventional vegetables sold in Brazil. Food Control. 2013;29:226-230.,2525 Suárez-Estrella F, Vargas-García MC, Elorrieta MA, López MJ, Moreno J. Temperature effect on Fusarium oxysporum f.sp. melonis survival during horticultural waste composting. J Appl Microbiol. 2003;94:475-482.

The irrigation water can also be a source of contamination. The most common sources of water for irrigation include wells, rivers, reservoirs and lakes, all of which are susceptible to contamination by human pathogens. The presence of pathogenic microorganisms in irrigation water and their transfer to vegetables has been reported.2626 Chigor VN, Umoh VJ, Smith SI. Occurrence of Escherichia coli O157 in a river used for fresh produce irrigation in Nigeria. Afr J Biotechnol. 2010;9:178-182.

27 Ijabadeniyi OA, Debusho LK, Vanderlinde M, Buys EM. Irrigation water as a potential preharvest source of bacterial contamination of vegetables. J Food Saf. 2011;31:452-461.
-2828 Okafo CN, Umoh VJ, Galadima M. Occurrence of pathogens on vegetables harvested from soils irrigated with contaminated streams. Sci Total Environ. 2003;311:49-56. Moreover, vegetable cultivation in open areas allows the access of animals (birds, insects, rodents, domestic and wild animals), which can defecate in the fields and, therefore, be a source of contamination. Studies conducted by Islam et al.2929 Islam M, Doyle MP, Phatak SC, Millner P, Jiang X. Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. J Food Prot. 2004;67:1365-1370.,3030 Islam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang X. Persistence of Salmonella enterica serovar Typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog Dis. 2004;1:27-35. showed that pathogens such as S. Typhimurium and E. coli O157:H7 can survive for a long period in soil (>150 days) and vegetables (>60 days) grown after experimental contamination using contaminated fertilizer (manure) or irrigation water.

Contaminated equipment, poor hygiene and improper post-harvest handling can compromise the microbial safety of a product. Proper storage conditions, including temperature, air circulation and relative humidity may be needed for pathogen control. The storage of fresh produce under refrigeration (≤4 ºC) is an important strategy to reduce the metabolic rate of the plant and prevent or limit the growth of pathogens.3131 Matthews KR. Sources of enteric pathogen contamination of fruits and vegetables: future directions of research. Stewart Postharvest Rev. 2013;9:1-5.

Pathogens isolated from or associated with organic produce

An increased number of foodborne disease outbreaks have been associated with the consumption of fresh produce recently.88 Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010;12:2385-2397.

9 Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis. 2015;12:32-38.

10 Doyle MP, Erickson MC. Summer meeting 2007 - the problems with fresh produce: an overview. J Appl Microbiol. 2008;105:317-330.

11 Harris LJ, Farber JN, Beuchat LR, et al. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf. 2003;2:78-141.

12 Jung Y, Jang H, Matthews KR. Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb Biotechnol. 2014;7:517-527.

13 Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect. 2009;137:307-315.
-1414 Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot. 2004;67:2342-2353.,3232 Sagoo SK, Little CL, Ward L, Gillespie IA, Mitchell RT. Microbiological study of ready-to-eat salad vegetables from retail establishments uncovers a national outbreak of salmonellosis. J Food Prot. 2003;66:403-409. According to a report by the Center for Science in the Public Interest (CSPI), fresh produce was the cause of most foodborne illnesses occurred in the U.S. between 2004 and 2013, including 193,754 illnesses from 9,625 outbreaks.3333 Center for Science in the Public Interest. Outbreak Alert! 2015: A Review of Foodborne Illness in the U.S. from 2004-2013; 2015. Available at: https://cspinet.org/reports/outbreak-alert-2015.pdf. Accessed 25 August 2016.
https://cspinet.org/reports/outbreak-ale...
Studies have isolated pathogens including Salmonella spp., L. monocytogenes and pathogenic E. coli from fresh and fresh-cut vegetable samples in many countries.3434 Abadias M, Usall J, Anguera M, Solsona C, Viñas I. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol. 2008;123:121-129.

35 Arthur L, Jones S, Fabri M, Odumeru J. Microbial survey of selected Ontario-grown fresh fruits and vegetables. J Food Prot. 2007;70:2864-2867.

36 De Léon HB, Gómez-Aldapa CA, Rangel-Vargas E, Vázquez-Barrios E, Castro-Rosas J. Frequency of indicator bacteria, Salmonella and diarrhoeagenic Escherichia coli pathotypes on ready-to-eat cooked vegetable salads from Mexican restaurants. Lett Appl Microbiol. 2013;56:414-420.

37 Froder H, Martins CG, Souza KLO, Landgraf M, Franco BDGM, Destro MT. Minimally processed vegetable salads: microbial quality evaluation. J Food Prot. 2007;70:1277-1280.

38 Giusti M, Aurigemma C, Marinelli L, et al. The evaluation of the microbial safety of fresh ready-to-eat vegetables produced by different technologies in Italy. J Appl Microbiol. 2010;109:996-1006.

39 Jeddi MZ, Yunesian M, Gorji ME, Noori N, Pourmand MR, Khaniki GRJ. Microbial evaluation of fresh, minimally-processed vegetables and bagged sprouts from chain supermarkets. J Health Popul Nutr. 2014;32:391-399.

40 Kovacevic M, Burazin J, Pavlovic H, Kopjar M, Pilizota V. Prevalence and level of Listeria monocytogenes and other Listeria sp. in ready-to-eat minimally processed and refrigerated vegetables. World J Microb Biotechnol. 2013;29:707-712.

41 Maistro LC, Miya NTN, Sant’Ana AS, Pereira JL. Microbiological quality and safety of minimally processed vegetables marketed in Campinas, SP - Brazil, as assessed by traditional and alternative methods. Food Control. 2012;28:258-264.

42 Mora A, León SL, Blanco M, et al. Phage types, virulence genes and PFGE profiles of Shiga toxin-producing Escherichia coli O157:H7 isolated from raw beef, soft cheese and vegetables in Lima (Peru). Int J Food Microbiol. 2007;114:204-210.

43 Moreno Y, Sánchez-Contreras J, Montes RM, García-Hernández J, Ballesteros L, Ferrús MA. Detection and enumeration of viable Listeria monocytogenes cells from ready-to-eat and processed vegetable foods by culture and DVC-FISH. Food Control. 2012;27:374-379.

44 Oliveira MA, Souza VM, Bergamini AMM, Martinis ECP. Microbiological quality of ready-to-eat minimally processed vegetables consumed in Brazil. Food Control. 2011;22:1400-1403.

45 Quiroz-Santiago C, Rodas-Suárez OR, Vázquez QCR, Fernández FJ, Quiñones-Ramírez EI, Vázquez-Salinas C. Prevalence of Salmonella in vegetables from Mexico. J Food Prot. 2009;72:1279-1282.

46 Rúgeles LC, Bai J, Martínez AJ, Vanegas MC, Gómez-Duarte OG. Molecular characterization of diarrheagenic Escherichia coli strains from stools samples and food products in Colombia. Int J Food Microbiol. 2010;138:282-286.

47 Sant’Ana AS, Igarashi MC, Landgraf M, Destro MT, Franco BDGM. Prevalence, populations and pheno- and genotypic characteristics of Listeria monocytogenes isolated from ready-to-eat vegetables marketed in São Paulo, Brazil. Int J Food Microbiol. 2012;155:1-9.

48 Sant’Ana AS, Landgraf M, Destro MT, Franco BDGM. Prevalence and counts of Salmonella spp. in minimally processed vegetables in São Paulo, Brazil. Food Microbiol. 2011;28:1235-1237.
-4949 Seo Y, Jang J, Moon K. Microbial evaluation of minimally processed vegetables and sprouts produced in Seoul, Korea. Food Sci Biotechnol. 2010;19:1283-1288. Other studies have compared the microbiological quality of vegetables from organic and conventional production.2121 Oliveira M, Usall J, Viñas I, Anguera M, Gatius F, Abadias M. Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol. 2010;27:679-684.,2222 Wießner S, Thiel B, Krämer J, Köpke U. Hygienic quality of head lettuce: effects of organic and mineral fertilizers. Food Control. 2009;20:881-886.,2424 Maffei DF, Silveira NFA, Catanozi MPLM. Microbiological quality of organic and conventional vegetables sold in Brazil. Food Control. 2013;29:226-230.,5050 Bohaychuk VM, Bradbury RW, Dimock R, et al. A microbiological survey of selected Alberta-grown fresh produce from farmers’ markets in Alberta, Canada. J Food Prot. 2009;72:415-420.

51 Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S, Tondo EC, Uyttendaelea M. Microbiological quality and safety assessment of lettuce production in Brazil. Int J Food Microbiol. 2014;181:67-76.

52 Gomes Neto NJ, Pessoa RML, Queiroga IMBN, et al. Bacterial counts and the occurrence of parasites in lettuce (Lactuca sativa) from different cropping systems in Brazil. Food Control. 2012;28:47-51.

53 Khalil R, Gomaa M. Evaluation of the microbiological quality of conventional and organic leafy greens at the time of purchase from retail markets in Alexandria, Egypt. Pol J Microbiol. 2014;63:237-243.

54 Marine SC, Pagadala S, Wang F, et al. The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microb. 2015;8:2395-2407.

55 Mukherjee A, Speh D, Dyck E, Diez-Gonzales F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot. 2004;67:894-900.

56 Mukherjee A, Speh D, Jones AT, Buesing KM, Diez-Gonzalez F. Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. J Food Prot. 2006;69:1928-1936.

57 Phillips CA, Harrison MA. Comparison of the microflora on organically and conventionally grown spring mix from a California processor. J Food Prot. 2005;68:1143-1146.

58 Ry JH, Kim M, Kim EG, Beuchat LR, Kim H. Comparison of the microbiological quality of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea. J Food Sci. 2014;79:M1739-M1744.
-5959 Tango CN, Choi NJ, Chung MS, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014;77:1411-1417. Ceuppens et al.5151 Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S, Tondo EC, Uyttendaelea M. Microbiological quality and safety assessment of lettuce production in Brazil. Int J Food Microbiol. 2014;181:67-76. assessed the microbiological quality of lettuce production in Brazil and detected generic E. coli more frequently and at higher average concentrations in lettuce samples from organic farms (23.1% and 3.22 log CFU/g) vs. conventional farms (16.7% and 2.27 log CFU/g). Gomes Neto et al.5252 Gomes Neto NJ, Pessoa RML, Queiroga IMBN, et al. Bacterial counts and the occurrence of parasites in lettuce (Lactuca sativa) from different cropping systems in Brazil. Food Control. 2012;28:47-51. evaluated the microbiological quality of 180 iceberg lettuce samples from conventional (n = 60), organic (n = 60) and hydroponic (n = 60) cropping systems in Brazil and observed that samples from organic systems were the most contaminated both by bacteria and intestinal parasites, while the lowest contamination level was observed in hydroponically grown lettuce. Maffei et al.2424 Maffei DF, Silveira NFA, Catanozi MPLM. Microbiological quality of organic and conventional vegetables sold in Brazil. Food Control. 2013;29:226-230. analyzed 130 samples of different organic (n = 65) and conventional (n = 65) vegetable varieties (also in Brazil), and observed that some organic varieties had greater microbial counts with the highest incidence of generic E. coli in organic loose-leaf lettuce (90% of samples positive).

Mukherjee et al.5555 Mukherjee A, Speh D, Dyck E, Diez-Gonzales F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot. 2004;67:894-900. analyzed 476 organic and 129 conventional produce samples from farms in Minnesota, USA, and found greater prevalence of E. coli in organic vs. conventional samples. The largest prevalence of E. coli was in organic lettuce (22.4% of samples). Oliveira et al.2121 Oliveira M, Usall J, Viñas I, Anguera M, Gatius F, Abadias M. Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol. 2010;27:679-684. analyzed 72 lettuce samples of organic and conventional agriculture in Spain and found similar results, with a greater prevalence of E. coli in lettuce samples from organic (22.2%) than conventional (12.5%) agriculture. Wießner et al.2222 Wießner S, Thiel B, Krämer J, Köpke U. Hygienic quality of head lettuce: effects of organic and mineral fertilizers. Food Control. 2009;20:881-886. investigated the effect of different organic manures in comparison with mineral fertilizer on the risk of pathogen transfer in lettuce plants in Germany and observed that microbial counts tended to be slightly higher after organic fertilization, although the differences were not statistically significant (p < 0.05). Although these studies show that organic produce generally seems to be more contaminated than conventional produce, this effect was not seen in every study.

Bohaychuk et al.5050 Bohaychuk VM, Bradbury RW, Dimock R, et al. A microbiological survey of selected Alberta-grown fresh produce from farmers’ markets in Alberta, Canada. J Food Prot. 2009;72:415-420. analyzed 673 fresh produce samples collected from Alberta public and farmer's markets in Canada (including organic produce) and observed that the levels of E. coli in organically and conventionally grown produce was not significantly different (p < 0.05). Khalil and Gomaa5353 Khalil R, Gomaa M. Evaluation of the microbiological quality of conventional and organic leafy greens at the time of purchase from retail markets in Alexandria, Egypt. Pol J Microbiol. 2014;63:237-243. analyzed 380 samples of unpackaged whole conventional and 84 packaged whole organic leafy greens collected from retail markets in Alexandria, Egypt, and observed the mean total bacterial count for organic samples were statistically significantly less (p < 0.05) than those of the corresponding conventional samples and E. coli was detected in 100% of all leafy greens. Marine et al.5454 Marine SC, Pagadala S, Wang F, et al. The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microb. 2015;8:2395-2407. evaluated leafy greens from organic (n = 178) and conventional (n = 191) farms in the Mid-Atlantic Region of the United States. They observed that the farming system was not a significant factor for E. coli, aerobic mesophiles or Salmonella, but with (non-statistically significant) higher total coliform counts from organic farm samples.

Mukherjee et al.5656 Mukherjee A, Speh D, Jones AT, Buesing KM, Diez-Gonzalez F. Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. J Food Prot. 2006;69:1928-1936. conducted a 2-year study to evaluated 2029 preharvest produce samples (473 organic, 911 semiorganic, and 645 conventional) in Minnesota and Wisconsin, USA, and concluded that the microbiological quality of preharvest produce from the three types of farms was very similar. Phillips and Harrison5757 Phillips CA, Harrison MA. Comparison of the microflora on organically and conventionally grown spring mix from a California processor. J Food Prot. 2005;68:1143-1146. evaluated the microflora of organic (n = 108) and conventional (n = 108) spring mix samples obtained from a commercial California (USA) fresh-cut produce where manure is not used in the cultivation practices. The authors observed that the mean microbial population for conventional samples was not statistically different (p > 0.05) from the corresponding mean populations for organic samples. The mean population of each microbial group was significantly higher in unwashed vs. washed product. Ryu et al.5858 Ry JH, Kim M, Kim EG, Beuchat LR, Kim H. Comparison of the microbiological quality of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea. J Food Sci. 2014;79:M1739-M1744. analyzed the microbiological quality of 11 types of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea and did not observe significant difference (p > 0.05) in the overall microbiological quality among samples. Tango et al.5959 Tango CN, Choi NJ, Chung MS, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014;77:1411-1417. analyzed the microbiological quality of 354 Korean leafy vegetable samples (165 conventional and 189 organic) and their results did not support the hypothesis that organic produce poses a greater risk of pathogen contamination vs. conventional produce.

Only Ceuppens et al.,5151 Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S, Tondo EC, Uyttendaelea M. Microbiological quality and safety assessment of lettuce production in Brazil. Int J Food Microbiol. 2014;181:67-76. Marine et al.,5454 Marine SC, Pagadala S, Wang F, et al. The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microb. 2015;8:2395-2407. Mukherjee et al.5555 Mukherjee A, Speh D, Dyck E, Diez-Gonzales F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot. 2004;67:894-900. and Tango et al.5959 Tango CN, Choi NJ, Chung MS, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014;77:1411-1417. detected pathogenic bacteria in the fresh produce samples analyzed above. Ceuppens et al.5151 Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S, Tondo EC, Uyttendaelea M. Microbiological quality and safety assessment of lettuce production in Brazil. Int J Food Microbiol. 2014;181:67-76. isolated Salmonella from one organic lettuce sample. Marine et al.5454 Marine SC, Pagadala S, Wang F, et al. The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microb. 2015;8:2395-2407. isolated Salmonella from eight (2.16%) of 369 leafy greens [four organic (2.24%) and four conventional (2.09%) samples]. Mukherjee et al.5555 Mukherjee A, Speh D, Dyck E, Diez-Gonzales F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot. 2004;67:894-900. isolated Salmonella from one organic lettuce and one organic green pepper sample. Tango et al.5959 Tango CN, Choi NJ, Chung MS, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014;77:1411-1417. reported positive results for Bacillus cereus (n = 17), Staphylococcus aureus (n = 13) and L. monocytogenes (n = 10) in 63 organic samples, vs. 3, 8 and 6, respectively for conventional samples. These authors also detected E. coli O157:H7 in 1 out of 55 conventional samples.

Some scientific studies have been conducted to determine the presence of pathogenic bacteria exclusively in organic produce.6060 Batalha EY [M. Sc. Dissertation] Escherichia coli produtora de toxina de Shiga em vegetais orgânicos cultivados na região metropolitana de SP. São Paulo, Brasil: Faculdade de Ciências Farmacêuticas. USP, São Paulo; 2015, 64 pp.

61 Chang WS, Afsah-Hejri L, Rukayadi Y, et al. Quantification of Escherichia coli O157:H7 in organic vegetables and chickens. Int Food Res J. 2013;20:1023-1029.

62 Loncarevic S, Johannessen GS, Rorvik LM. Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol. 2005;41:186-189.

63 Machado DC, Maia CM, Carvalho ID, da Silva NF, Serafini AB. Microbiological quality of organic vegetables produced in soil treated with different types of manure and mineral fertilizer. Braz J Microbiol. 2006;37:538-544.

64 McMahon MAS, Wilson IG. The occurrence of enteric pathogens and Aeromonas species in organic vegetables. Int J Food Microbiol. 2001;70:155-162.

65 Nguz K, Shindano J, Samapundo S, Huyghebaert A. Microbiological evaluation of fresh cut organic vegetables produced in Zambia. Food Control. 2005;16:623-628.

66 Rodrigues RQ, Loiko MR, de Paula CMD, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control. 2014;42:152-164.
-6767 Sagoo SK, Little CL, Mitchell RT. The microbiological examination of ready-to-eat organic vegetables from retail establishments in the United Kingdom. Lett Appl Microbiol. 2001;33:434-439. Among these, only Chang et al.,6161 Chang WS, Afsah-Hejri L, Rukayadi Y, et al. Quantification of Escherichia coli O157:H7 in organic vegetables and chickens. Int Food Res J. 2013;20:1023-1029. Loncarevic et al.,6262 Loncarevic S, Johannessen GS, Rorvik LM. Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol. 2005;41:186-189. McMahon and Wilson,6464 McMahon MAS, Wilson IG. The occurrence of enteric pathogens and Aeromonas species in organic vegetables. Int J Food Microbiol. 2001;70:155-162. Nguz et al.6565 Nguz K, Shindano J, Samapundo S, Huyghebaert A. Microbiological evaluation of fresh cut organic vegetables produced in Zambia. Food Control. 2005;16:623-628. and Rodrigues et al.6666 Rodrigues RQ, Loiko MR, de Paula CMD, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control. 2014;42:152-164. detected the presence of pathogenic bacteria. Chang et al.6161 Chang WS, Afsah-Hejri L, Rukayadi Y, et al. Quantification of Escherichia coli O157:H7 in organic vegetables and chickens. Int Food Res J. 2013;20:1023-1029. reported the presence of E. coli O157:H7 in four out of 210 organic vegetables collected in supermarket and groceries in Selangor, Malaysia. Loncarevic et al.6262 Loncarevic S, Johannessen GS, Rorvik LM. Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol. 2005;41:186-189. isolated L. monocytogenes serogroups 1 and 4 from two of 179 organically grown leaf lettuce samples in Norway. McMahon and Wilson6464 McMahon MAS, Wilson IG. The occurrence of enteric pathogens and Aeromonas species in organic vegetables. Int J Food Microbiol. 2001;70:155-162. investigated the occurrence of selected enteric pathogens and Aeromonas species in organic vegetables in Northern Ireland. They found Aeromonas spp only (34% of the samples) including A. schubertii (21%), A. hydrophila (5.8%), A. trota (5.8%), A. caviae (3.5%) and A. veronii biovar veronii (2.3%). These Aeromonas species were previously reported to be potentially pathogenic and responsible for gastrointestinal infections in humans.6868 Igbinosa IH, Igumbor EU, Aghdasi F, Tom M, Okoh A. Emerging Aeromonas species infections and their significance in public health. Sci World J. 2012;:1-13.,6969 Merino S, Rubines X, Knichel S, Tomás JM. Emerging pathogens: Aeromonas spp. Int J Food Microbiol. 1995;28:157-168. Nguz et al.6565 Nguz K, Shindano J, Samapundo S, Huyghebaert A. Microbiological evaluation of fresh cut organic vegetables produced in Zambia. Food Control. 2005;16:623-628. assessed the microbiological quality of fresh-cut organic vegetables (washed with chlorine solution at 150 µg mL−1) produced in Zambia and detected the presence of L. monocytogenes, Salmonella and S. aureus in 20%, 23.1% and 80.0% of samples, respectively. Rodrigues et al.6666 Rodrigues RQ, Loiko MR, de Paula CMD, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control. 2014;42:152-164. isolated Salmonella from only one of 36 Brazilian organic lettuce samples.

The incidence of pathogens in organic vegetables varies according to the study (Table 1). Salmonella spp prevalence varies between 0.4 and 23.1%, L. monocytogenes between 1.1 and 20% and S. aureus between 20.6 and 80%. B. cereus prevalence can be as high as 26.9% and as high as 34% for Aeromonas spp. E. coli O157:H7 prevalence can be as high as 1.9%. Since fresh produce is often consumed raw even low prevalence rates may mean increased risk of foodborne disease from these foods.

Table 1
Incidence of pathogenic bacteria on organic vegetables.

Information on foodborne outbreaks from organic produce is limited. However, some cases involving Shiga toxin-producing E. coli (STEC) and organic produce have been reported in the past few years. An outbreak involving STEC O157:H7 linked to organic spinach and spring mix blend occurred in the U.S. in 2012 and affected 33 persons from five states: 46% were hospitalized and two developed hemolytic uremic syndrome (HUS).7070 Centers for Disease Control and Prevention. Multistate Outbreak of Shiga Toxin-Producing Escherichia coli O157:H7 Infections Linked to Organic Spinach and Spring Mix Blend (Final Update); 2012. Available at http://www.cdc.gov/ecoli/2012/O157H7-11-12/index.html Accessed 25.08.16.
http://www.cdc.gov/ecoli/2012/O157H7-11-...
STEC O104:H4 was responsible for an outbreak linked to organic raw sprouts in Germany, with thousands of infections.7171 Frank C, Werber D, Cramer JP, et al. Epidemic profile of shiga-toxin-producing Escherichia coli O104:H4 Outbreak in Germany. N Engl J Med. 2011;365:1771-1780.,7272 King LA, Nogareda F, Weill FX, et al. Outbreak of shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis. 2012;54:1588-1594.

Control measures

Current strategies to control microbial contamination during the production of fresh produce (regardless of cultivation method) are based on the implementation of Good Agricultural Practices (GAP). A GAP framework considers the implementation of best practices regarding worker's health and hygiene, soil and water quality, sewage treatment, wildlife and livestock management, manure and biosolids management, field sanitation and hygiene, and harvest and transportation.2020 Sant'Ana AS, Silva FFP, Maffei DF, Franco BDGM. Fruits and vegetables: introduction. In: Batt CA, Tortorello ML, eds. Encyclopedia of Food Microbiology. 2nd ed. Amsterdam: Academic Press; 2014:972-982. The implementation of food safety management tools such as Good Hygienic Practices (GHP) and Hazard Analysis and Critical Control Points (HACCP) at postharvest steps also helps to reduce, eliminate or prevent the occurrence of hazards. The washing step before consumption is also important as it may reduce microbial load on vegetables surfaces. Washing with sanitizer may also reduce contamination and prevent cross-contamination by pathogenic microorganisms.7373 López-Gálvez F, Allende A, Selma MV, Gil MI. Prevention of Escherichia coli cross contamination by different commercial sanitizers during washing of fresh-cut lettuce. Int J Food Microbiol. 2009;133:167-171.

74 Maffei DF, Sant’Ana AS, Monteiro G, Schaffner DW, Franco BDGM. Assessing the effect of sodium dichloroisocyanurate concentration on transfer of Salmonella enterica serotype Typhimurium in wash water for production of minimally processed iceberg lettuce (Lactuca sativa L). Lett Appl Microbiol. 2016;62:444-451.

75 Tomás-Callejas A, López-Gálvez F, Sbodio A, Artés F, Artés-Hernández F, Suslow TV. Chlorine dioxide and chlorine effectiveness to prevent Escherichia coli O157:H7 and Salmonella cross contamination on fresh-cut Red Chard. Food Control. 2012;23:325-332.
-7676 Zhang G, Ma L, Phelan VH, Doyle MP. Efficacy of antimicrobial agents in lettuce leaf processing water for control of Escherichia coli O157:H7. J Food Prot. 2009;72:1392-1397.

Concluding remarks

Data summarized above from a variety of studies focusing on different crops and different countries highlight the potential risks of pathogenic microorganisms in fresh produce, including organic products. Although a number of studies have indicated that organic produce may pose a greater risk than conventional grown produce, this trend is not universal across all studies. Further efforts are needed to understand and control the disease risk associated with organic produce from harvest through consumption.

Acknowledgements

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for scholarship (830642/1999-4) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for scholarship (2016/09601-5) and financial support (2013/07914-8).

REFERENCES

  • 1
    Dias JS. Nutritional quality and health benefits of vegetables: a review. Food Nutr Sci 2012;3:1354-1374.
  • 2
    Liu RH. Health-promoting components of fruits and vegetables in the diet. Adv Nutr 2013;4:384-392.
  • 3
    Slavin JL, Lloyd B. Health benefits of fruits and vegetables. Adv Nutr 2012;3:506-516.
  • 4
    Bettiol W, Ghini R, Galvão JAH, Siloto RC. Organic and conventional tomato cropping systems. Sci Agric 2004;61:253-259.
  • 5
    Crowder DW, Reganold JP. Financial competitiveness of organic agriculture on a global scale. Proc Natl Acad Sci U S A 2015;112:7611-7616.
  • 6
    Azadi H, Schoonbeek S, Mahmoudi H, Derudder B, De Maeyer P, Witloxa F. Organic agriculture and sustainable food production system: main potentials. Agric Ecosyst Environ 2011;144:92-94.
  • 7
    Willer H, Lernoud J, eds. The World of Organic Agriculture. Statistics and Emerging Trends Bonn: Research Institute of Organic Agriculture (FiBL), Frick, and IFOAM - Organics International; 2016.
  • 8
    Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 2010;12:2385-2397.
  • 9
    Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis 2015;12:32-38.
  • 10
    Doyle MP, Erickson MC. Summer meeting 2007 - the problems with fresh produce: an overview. J Appl Microbiol 2008;105:317-330.
  • 11
    Harris LJ, Farber JN, Beuchat LR, et al. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2003;2:78-141.
  • 12
    Jung Y, Jang H, Matthews KR. Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb Biotechnol 2014;7:517-527.
  • 13
    Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 2009;137:307-315.
  • 14
    Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 2004;67:2342-2353.
  • 15
    Winter CK, Davis SF. Organic foods. J Food Sci 2006;71:117-124.
  • 16
    Vijayan G. Organic Food Certification and Marketing Strategies Agrihortico; 2014.
  • 17
    Tuomisto HL, Hodge ID, Riordan P, Macdonald DW. Does organic farming reduce environmental impacts? A meta-analysis of European research. J Environ Manag 2012;112:309-320.
  • 18
    International Federation of Organic Agriculture Movements (IFOAM). The Principles of Organic Agriculture Bonn, Germany: Preamble. IFOAM; 2005. Available at http://www.ifoam.org/sites/default/files/ifoam_poa.pdf Accessed 06.09.16.
    » http://www.ifoam.org/sites/default/files/ifoam_poa.pdf
  • 19
    Beuchat LR. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect 2002;4:413-423.
  • 20
    Sant'Ana AS, Silva FFP, Maffei DF, Franco BDGM. Fruits and vegetables: introduction. In: Batt CA, Tortorello ML, eds. Encyclopedia of Food Microbiology 2nd ed. Amsterdam: Academic Press; 2014:972-982.
  • 21
    Oliveira M, Usall J, Viñas I, Anguera M, Gatius F, Abadias M. Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol 2010;27:679-684.
  • 22
    Wießner S, Thiel B, Krämer J, Köpke U. Hygienic quality of head lettuce: effects of organic and mineral fertilizers. Food Control 2009;20:881-886.
  • 23
    Moreno J, López MJ, Vargas-García MC, Suárez-Estrella F. Recent advances in microbial aspects of compost production and use. Acta Hort (ISHS) 2013;1013:443-457.
  • 24
    Maffei DF, Silveira NFA, Catanozi MPLM. Microbiological quality of organic and conventional vegetables sold in Brazil. Food Control 2013;29:226-230.
  • 25
    Suárez-Estrella F, Vargas-García MC, Elorrieta MA, López MJ, Moreno J. Temperature effect on Fusarium oxysporum f.sp. melonis survival during horticultural waste composting. J Appl Microbiol 2003;94:475-482.
  • 26
    Chigor VN, Umoh VJ, Smith SI. Occurrence of Escherichia coli O157 in a river used for fresh produce irrigation in Nigeria. Afr J Biotechnol 2010;9:178-182.
  • 27
    Ijabadeniyi OA, Debusho LK, Vanderlinde M, Buys EM. Irrigation water as a potential preharvest source of bacterial contamination of vegetables. J Food Saf 2011;31:452-461.
  • 28
    Okafo CN, Umoh VJ, Galadima M. Occurrence of pathogens on vegetables harvested from soils irrigated with contaminated streams. Sci Total Environ 2003;311:49-56.
  • 29
    Islam M, Doyle MP, Phatak SC, Millner P, Jiang X. Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. J Food Prot 2004;67:1365-1370.
  • 30
    Islam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang X. Persistence of Salmonella enterica serovar Typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog Dis 2004;1:27-35.
  • 31
    Matthews KR. Sources of enteric pathogen contamination of fruits and vegetables: future directions of research. Stewart Postharvest Rev 2013;9:1-5.
  • 32
    Sagoo SK, Little CL, Ward L, Gillespie IA, Mitchell RT. Microbiological study of ready-to-eat salad vegetables from retail establishments uncovers a national outbreak of salmonellosis. J Food Prot 2003;66:403-409.
  • 33
    Center for Science in the Public Interest. Outbreak Alert! 2015: A Review of Foodborne Illness in the U.S. from 2004-2013; 2015. Available at: https://cspinet.org/reports/outbreak-alert-2015.pdf Accessed 25 August 2016.
    » https://cspinet.org/reports/outbreak-alert-2015.pdf
  • 34
    Abadias M, Usall J, Anguera M, Solsona C, Viñas I. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 2008;123:121-129.
  • 35
    Arthur L, Jones S, Fabri M, Odumeru J. Microbial survey of selected Ontario-grown fresh fruits and vegetables. J Food Prot 2007;70:2864-2867.
  • 36
    De Léon HB, Gómez-Aldapa CA, Rangel-Vargas E, Vázquez-Barrios E, Castro-Rosas J. Frequency of indicator bacteria, Salmonella and diarrhoeagenic Escherichia coli pathotypes on ready-to-eat cooked vegetable salads from Mexican restaurants. Lett Appl Microbiol 2013;56:414-420.
  • 37
    Froder H, Martins CG, Souza KLO, Landgraf M, Franco BDGM, Destro MT. Minimally processed vegetable salads: microbial quality evaluation. J Food Prot 2007;70:1277-1280.
  • 38
    Giusti M, Aurigemma C, Marinelli L, et al. The evaluation of the microbial safety of fresh ready-to-eat vegetables produced by different technologies in Italy. J Appl Microbiol 2010;109:996-1006.
  • 39
    Jeddi MZ, Yunesian M, Gorji ME, Noori N, Pourmand MR, Khaniki GRJ. Microbial evaluation of fresh, minimally-processed vegetables and bagged sprouts from chain supermarkets. J Health Popul Nutr 2014;32:391-399.
  • 40
    Kovacevic M, Burazin J, Pavlovic H, Kopjar M, Pilizota V. Prevalence and level of Listeria monocytogenes and other Listeria sp. in ready-to-eat minimally processed and refrigerated vegetables. World J Microb Biotechnol 2013;29:707-712.
  • 41
    Maistro LC, Miya NTN, Sant’Ana AS, Pereira JL. Microbiological quality and safety of minimally processed vegetables marketed in Campinas, SP - Brazil, as assessed by traditional and alternative methods. Food Control 2012;28:258-264.
  • 42
    Mora A, León SL, Blanco M, et al. Phage types, virulence genes and PFGE profiles of Shiga toxin-producing Escherichia coli O157:H7 isolated from raw beef, soft cheese and vegetables in Lima (Peru). Int J Food Microbiol 2007;114:204-210.
  • 43
    Moreno Y, Sánchez-Contreras J, Montes RM, García-Hernández J, Ballesteros L, Ferrús MA. Detection and enumeration of viable Listeria monocytogenes cells from ready-to-eat and processed vegetable foods by culture and DVC-FISH. Food Control 2012;27:374-379.
  • 44
    Oliveira MA, Souza VM, Bergamini AMM, Martinis ECP. Microbiological quality of ready-to-eat minimally processed vegetables consumed in Brazil. Food Control 2011;22:1400-1403.
  • 45
    Quiroz-Santiago C, Rodas-Suárez OR, Vázquez QCR, Fernández FJ, Quiñones-Ramírez EI, Vázquez-Salinas C. Prevalence of Salmonella in vegetables from Mexico. J Food Prot 2009;72:1279-1282.
  • 46
    Rúgeles LC, Bai J, Martínez AJ, Vanegas MC, Gómez-Duarte OG. Molecular characterization of diarrheagenic Escherichia coli strains from stools samples and food products in Colombia. Int J Food Microbiol 2010;138:282-286.
  • 47
    Sant’Ana AS, Igarashi MC, Landgraf M, Destro MT, Franco BDGM. Prevalence, populations and pheno- and genotypic characteristics of Listeria monocytogenes isolated from ready-to-eat vegetables marketed in São Paulo, Brazil. Int J Food Microbiol 2012;155:1-9.
  • 48
    Sant’Ana AS, Landgraf M, Destro MT, Franco BDGM. Prevalence and counts of Salmonella spp. in minimally processed vegetables in São Paulo, Brazil. Food Microbiol 2011;28:1235-1237.
  • 49
    Seo Y, Jang J, Moon K. Microbial evaluation of minimally processed vegetables and sprouts produced in Seoul, Korea. Food Sci Biotechnol 2010;19:1283-1288.
  • 50
    Bohaychuk VM, Bradbury RW, Dimock R, et al. A microbiological survey of selected Alberta-grown fresh produce from farmers’ markets in Alberta, Canada. J Food Prot 2009;72:415-420.
  • 51
    Ceuppens S, Hessel CT, Rodrigues RQ, Bartz S, Tondo EC, Uyttendaelea M. Microbiological quality and safety assessment of lettuce production in Brazil. Int J Food Microbiol 2014;181:67-76.
  • 52
    Gomes Neto NJ, Pessoa RML, Queiroga IMBN, et al. Bacterial counts and the occurrence of parasites in lettuce (Lactuca sativa) from different cropping systems in Brazil. Food Control 2012;28:47-51.
  • 53
    Khalil R, Gomaa M. Evaluation of the microbiological quality of conventional and organic leafy greens at the time of purchase from retail markets in Alexandria, Egypt. Pol J Microbiol 2014;63:237-243.
  • 54
    Marine SC, Pagadala S, Wang F, et al. The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microb 2015;8:2395-2407.
  • 55
    Mukherjee A, Speh D, Dyck E, Diez-Gonzales F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot 2004;67:894-900.
  • 56
    Mukherjee A, Speh D, Jones AT, Buesing KM, Diez-Gonzalez F. Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. J Food Prot 2006;69:1928-1936.
  • 57
    Phillips CA, Harrison MA. Comparison of the microflora on organically and conventionally grown spring mix from a California processor. J Food Prot 2005;68:1143-1146.
  • 58
    Ry JH, Kim M, Kim EG, Beuchat LR, Kim H. Comparison of the microbiological quality of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea. J Food Sci 2014;79:M1739-M1744.
  • 59
    Tango CN, Choi NJ, Chung MS, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot 2014;77:1411-1417.
  • 60
    Batalha EY [M. Sc. Dissertation] Escherichia coli produtora de toxina de Shiga em vegetais orgânicos cultivados na região metropolitana de SP São Paulo, Brasil: Faculdade de Ciências Farmacêuticas. USP, São Paulo; 2015, 64 pp.
  • 61
    Chang WS, Afsah-Hejri L, Rukayadi Y, et al. Quantification of Escherichia coli O157:H7 in organic vegetables and chickens. Int Food Res J 2013;20:1023-1029.
  • 62
    Loncarevic S, Johannessen GS, Rorvik LM. Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol 2005;41:186-189.
  • 63
    Machado DC, Maia CM, Carvalho ID, da Silva NF, Serafini AB. Microbiological quality of organic vegetables produced in soil treated with different types of manure and mineral fertilizer. Braz J Microbiol 2006;37:538-544.
  • 64
    McMahon MAS, Wilson IG. The occurrence of enteric pathogens and Aeromonas species in organic vegetables. Int J Food Microbiol 2001;70:155-162.
  • 65
    Nguz K, Shindano J, Samapundo S, Huyghebaert A. Microbiological evaluation of fresh cut organic vegetables produced in Zambia. Food Control 2005;16:623-628.
  • 66
    Rodrigues RQ, Loiko MR, de Paula CMD, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control 2014;42:152-164.
  • 67
    Sagoo SK, Little CL, Mitchell RT. The microbiological examination of ready-to-eat organic vegetables from retail establishments in the United Kingdom. Lett Appl Microbiol 2001;33:434-439.
  • 68
    Igbinosa IH, Igumbor EU, Aghdasi F, Tom M, Okoh A. Emerging Aeromonas species infections and their significance in public health. Sci World J 2012;:1-13.
  • 69
    Merino S, Rubines X, Knichel S, Tomás JM. Emerging pathogens: Aeromonas spp. Int J Food Microbiol 1995;28:157-168.
  • 70
    Centers for Disease Control and Prevention. Multistate Outbreak of Shiga Toxin-Producing Escherichia coli O157:H7 Infections Linked to Organic Spinach and Spring Mix Blend (Final Update); 2012. Available at http://www.cdc.gov/ecoli/2012/O157H7-11-12/index.html Accessed 25.08.16.
    » http://www.cdc.gov/ecoli/2012/O157H7-11-12/index.html
  • 71
    Frank C, Werber D, Cramer JP, et al. Epidemic profile of shiga-toxin-producing Escherichia coli O104:H4 Outbreak in Germany. N Engl J Med 2011;365:1771-1780.
  • 72
    King LA, Nogareda F, Weill FX, et al. Outbreak of shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis 2012;54:1588-1594.
  • 73
    López-Gálvez F, Allende A, Selma MV, Gil MI. Prevention of Escherichia coli cross contamination by different commercial sanitizers during washing of fresh-cut lettuce. Int J Food Microbiol 2009;133:167-171.
  • 74
    Maffei DF, Sant’Ana AS, Monteiro G, Schaffner DW, Franco BDGM. Assessing the effect of sodium dichloroisocyanurate concentration on transfer of Salmonella enterica serotype Typhimurium in wash water for production of minimally processed iceberg lettuce (Lactuca sativa L). Lett Appl Microbiol 2016;62:444-451.
  • 75
    Tomás-Callejas A, López-Gálvez F, Sbodio A, Artés F, Artés-Hernández F, Suslow TV. Chlorine dioxide and chlorine effectiveness to prevent Escherichia coli O157:H7 and Salmonella cross contamination on fresh-cut Red Chard. Food Control 2012;23:325-332.
  • 76
    Zhang G, Ma L, Phelan VH, Doyle MP. Efficacy of antimicrobial agents in lettuce leaf processing water for control of Escherichia coli O157:H7. J Food Prot 2009;72:1392-1397.

Publication Dates

  • Publication in this collection
    Dec 2016

History

  • Received
    21 Sept 2016
  • Accepted
    05 Oct 2016
Sociedade Brasileira de Microbiologia USP - ICB III - Dep. de Microbiologia, Sociedade Brasileira de Microbiologia, Av. Prof. Lineu Prestes, 2415, Cidade Universitária, 05508-900 São Paulo, SP - Brasil, Ramal USP 7979, Tel. / Fax: (55 11) 3813-9647 ou 3037-7095 - São Paulo - SP - Brazil
E-mail: bjm@sbmicrobiologia.org.br