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Review Article
 

Fresh Farm Produce as a Source of Pathogens: A Review



Sujeet Kumar Mritunjay and Vipin Kumar
 
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ABSTRACT

Salad and fresh produce have become more attractive, because of its nutritional benefits and the fact that it is made in very short time, mostly it is consumed as raw or after minimal processing. Lactuca sativa (Lettuce), Cucumis sativus (cucumber), Lycopersicon esculentum (tomato), Spinach oleracea (spinach), Brassica oleracea (cabbage), Raphanus sativum (radish), Daucus carota (carrot) etc., are the most common vegetable, used in salad. In-spite of its great nutritional value, it’s become harbour of microbes, may be due to untreated irrigation or sewage fertilizer and poor handling after harvesting of these crops. Food-borne pathogen such as Listeria monocytogenes, Salmonella sp., Shigella sp., Campylobacter sp., Staphylococcus aureus, Clostridium botulinum and E. coli O157:H7 has been the main cause of illness during the past decade. Microorganisms that are setters over they are able to survive for several weeks and they could produce diarrhoea, Salmonellosis and Shigellosis etc. The study was conducted to assess the potential hazard of microorganism associated with fresh produce. There is a need to educate the public and farmers in particular on the risk involved in the use of contaminated water and untreated manure during production. Measures to minimize the risk of microbial contamination at all points from the field to the table thorough good agricultural practices, good manufacturing practices would be the most effective strategy to assure that fresh produce is safe for human consumption.

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  How to cite this article:

Sujeet Kumar Mritunjay and Vipin Kumar, 2015. Fresh Farm Produce as a Source of Pathogens: A Review. Research Journal of Environmental Toxicology, 9: 59-70.

DOI: 10.3923/rjet.2015.59.70

URL: https://scialert.net/abstract/?doi=rjet.2015.59.70
 
Received: December 02, 2014; Accepted: March 14, 2015; Published: April 20, 2015



INTRODUCTION

Salad vegetables are important component of nutritional diet, providing vitamins and minerals and phyto-nutrients (Gupta and Rana, 2003; Gupta et al., 2003; Taban and Halkman, 2011; Jabbar et al., 2014). Epidemiological evidence has clearly shown that diets based on fruits and vegetables reduce mortality from cardiovascular and cerebrovascular diseases (Alia et al., 2003). Leafy salad vegetables are Ready-To-Eat (RTE) produce for healthy and convenient meals are considered as safe-to-eat by consumers taken as an appetizer (Lin et al., 1996; Gupta et al., 2003; De Oliveira et al., 2011).

Leafy green vegetables (spinach, cabbage, lettuce and salad leaves of all varieties) were identified as the commodity group of highest concern from a microbiological safety perspective. These vegetables are consumed raw or minimally prepared and most have fewer barriers against microbial growth, such as salt and preservatives, than do the more traditional vehicles of foodborne illness, due to this lack and also because of the survival and growth of microbial pathogens on such foods, fresh produce is expected to continue to cause outbreaks of foodborne illnesses (Stine et al., 2011). Pathogenic Escherichia coli and Salmonella sp. enteric bacteria involved in large food borne outbreaks worldwide, causing symptoms of gastroenteritis and chronic infections. Listeria monocytogenes is a psychrotolerant and ubiquitous microorganism that causes listeriosis, contaminate RTE vegetables (De Oliveira et al., 2011). Pseudomonas aeruginosa, Staphylococcus aureus, Bacillus sp., Proteus sp., Lactobacillus sp., Klebsiella has been found in ready to eat product (Oranusi and Olorunfemi, 2011).

The main objectives of the study were to appraise the potential hazard of microorganism associated with fresh produce and raw eaten salad vegetables and highlighted the importance of proper processing before consumption and also investigate the source of contamination and prevalence of pathogenic microorganisms.

GLOBAL STATUS OF SALAD VEGETABLES AND FRESH PRODUCE

The global production of fruit and vegetables grew by 94% from 1980-2004. In Mumbai, India, with its growing urban population travelling long distances to the place of work, it has become increasingly popular to eat healthy raw salad vegetables, fruits and sprouts preferentially to any other fast food. WHO, street-vended food survey revealed that fruits and vegetables from 86% of the total market. The United States of America being a major provider of fresh produce, approximately 35% of the fresh produce it consumes is imported. Given the role of fresh produce in a healthy diet, it is critical that these foods are as safe as possible. The safety of fresh produce is a global issue covering both the countries that import fresh fruits and vegetables and the countries that supply them. In many instances countries both export and import produce. Consumption of salad vegetables and fresh produce has increased significantly over the past two decades, because of the health benefits of consumers and they are more concerned about their health, due to this demand a large variety of domestic and imported produce has become available in all seasons (Lin et al., 1996; Cordano and Jacquet, 2009; Olaimat and Holley, 2012; Taban and Halkman, 2011). In Nigeria, the consumption of RTE fruits consumption increases, as they are easily accessible, convenient and cheaper than whole fruits. The increased consumption with the associated risk of disease, to which consumers may be exposed is a matter of great concern (Oranusi and Olorunfemi, 2011).

MAIN SOURCE OF PATHOGENS

In the farm-to-table production, important points of contamination of vegetables with disease-causing microorganisms include use of pond and river water to wash vegetable produce, handling of vegetables by workers infected with and carriers of the pathogen(s) and storage of vegetables in contaminated places. Considerable information is available on bacterial load in washing water as well as on vegetables and contamination of plant products by human pathogens is a known fact. Although it is not easy to establish exactly the level of disease risk associated with a given concentration of fecal coliforms or total aerobic plate count or yeast and mould counts, existence of such standards necessitate their observance to exist in international trade of food vegetables. In India, vegetables are washed mostly in readily available water bodies, such as rivers or ponds available in the vicinity of the production site. After the farmers, vegetable vendors are the important handlers of vegetables, selling different kinds on a small platform, all sprinkled frequently (to keep them fresh in the hot and dry summer) with water from the same bucket again and again for days without any disinfection of the bucket. This may lead to a considerable amount of cross-contamination of vegetables on the retailers’ counters (Singh et al., 2006).

Table 1: Main source of pathogens/microbial contamination in fruits and vegetables (Berger et al., 2010; Harris et al., 2003)
Image for - Fresh Farm Produce as a Source of Pathogens: A Review

Type of water source also influence the microbiological quality of produce, wastewater contaminate vegetables with pathogenic microorganisms (Brackett, 1999; Solomon et al., 2002; Kumar, 2012). Salmonella sp., Campylobacter sp. and Shigella sp. contaminate fruits and vegetables through contact with contaminated water or sewage (Oranusi and Olorunfemi, 2011; Kumar, 2012). Contamination with E. coli O157:H7 and Salmonella occurred on farms through the use of contaminated irrigation water and manure (Chang and Fang, 2007). Fields on which livestock or wild animals have grazed are more likely to be contaminated with enteric pathogens. Some bacteria can survive in agriculture soils for many months. Salmonella and Listeria monocytogenes could survive for months in sewage sludge applied to agricultural soils. Many factors comprises of contamination of vegetables. Pathogens may contaminate the vegetables and fruits during washing, peeling, slicing, trimming, packaging and handling (Oranusi and Olorunfemi, 2011). Table 1 summarized the common source of microbial contaminations. Most produce is grown in a natural environment, therefore, vulnerable to contamination with pathogens from multiple sources, including agricultural and post-harvest water, ill workers, the presence of wild or domestic animals or animal waste and unsanitary equipment and facilities (FAO/WHO., 2008).

MICROORGANISMS IN SALAD VEGETABLES

It is now commonly accepted that fruit and vegetable consumption is a risk factor for infection with enteric pathogens (Heaton and Jones, 2008). Escherichia coli, Clostridium botulinum, Salmonella, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus, grow on lettuce, cucumber, carrot, red cabbage, tomatoes and a variety of salad vegetables (Abdul-Raouf et al., 1993; Lin et al., 1996) have been associated with food borne illness for decades (Borch and Arinder, 2002; Velusamy et al., 2010). Listeria monocytogenes, Staphylococcus aureus, Salmonella enterica and Escherichia coli are known as common food borne pathogenic microorganisms (Kim et al., 2013). Most of the pathogens are not newcomers and food-borne outbreaks or infections are not a rare event (Velusamy et al., 2010; Harris et al., 2001). The symptoms of staphylococcal food poisoning had already been described in 1936, one of the earliest food poisoning caused by Bacillus cereus was reported in 1906 (Borch and Arinder, 2002). Cross-contamination is an important factor of food-borne illness. Fruits have been associated with outbreaks in many countries; microorganisms include bacteria, fungi, viruses and parasites. Contamination of norovirus is also reported with salad product. Salmonellosis has been associated with consumption of cut watermelon causes outbreaks in the United States of America (Oranusi and Olorunfemi, 2011). Fruits and vegetables become contaminated with pathogenic microorganisms while growing infields, orchards, vineyards or greenhouses, or during harvesting, post-harvest handling, processing, distribution and preparation. Vegetables and fruits produce have potential to harbor pathogenic microorganisms, but Shigella sp., Salmonella, Enterotoxigenic and Enterohemorrhagic, Escherichia coli, Campylobacter sp., Listeria monocytogenes, Yersinia enterocolitica, Bacillus cereus, Clostridium botulinum and parasites such as Giardia lamblia, Cyclosporacayetanensis and Cryptosporidium parvumare of greatest public health concern (Beuchat, 2002).

Incidence of pathogens: The WHO defines foodborne illnesses as diseases, usually either infectious or toxic in nature, caused by agents that enter the body through the ingestion of food (Velusamy et al., 2010). Over the past few decades foodborne illness outbreaks and cases associated with fresh produce have rapidly increased (Stine et al., 2011). Fresh produce (fresh, cannedor processed) causes 20 million illnesses (24%) costing 38.6 $ billion every year in the US (Olaimat and Holley, 2012). Foodborne pathogenic bacteria are causative agent of illness and death for many people every year, at great economic cost and human suffering (Borch and Arinder, 2002; Olaimat and Holley, 2012). Enterohemorrhagic E. coli infections in the USA incur about $1 billion in costs each year (Boyacioglu et al., 2013). In Taiwan, contamination of fresh cut vegetables with E. coli O157:H7 is reported. In the USA, eight lettuce-associated outbreaks were reported with foodborne pathogens, including E. coli O157:H7 and Salmonella from 1973 through 1997. Salmonellosis caused by many Salmonella serovars has been found in humans and animals. The overall rate of infection ranged from 15 to 20/100,000 population, during each year in the USA. The outbreaks caused by Salmonella sp. were frequent, both in Korea (20.7%) and in Japan (14.2%) S. enteric serovars typhimurium and S. enterica serovars enteritidis are the most frequently isolated serovars from food-borne outbreaks throughout the world (Chang and Fang, 2007). In 2005 alone 1.8 million people died from diarrhoeal diseases (Velusamy et al., 2010).

Incidence of bacterial pathogens in raw eaten salad vegetables and fresh produce are summarized in Table 2. Escherichia coli O157:H7 has caused numerous outbreaks of food-borne illness associated with leafy green vegetables.

Table 2: Incidence of bacterial pathogens in raw eaten salad vegetables and fresh produce
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Abdul-Raouf et al. (1993) were the first to provide evidence of E. coli O157:H7 growth on cut leafy vegetable (McKellar and Delaquis, 2011). In 1995, an outbreak of E. coli O157:H7 infection involving at least 29 people in Montana was epidemiologically linked to consumption of leaf lettuce (De Roever, 1998). The source of contamination was not determined. However, the lettuce was irrigated with surface water and investigations of area grocery stores revealed unsanitary lettuce was irrigated with surface water and investigations of area grocery stores revealed unsanitary leaf lettuce handling methods. In the Same year, in 1995, outbreak of E. coli O157:H7 was reported associated with iceberg lettuce, it was not known how the lettuce was contaminated. However, it is possible that cross-contamination from meat products may have occurred during food preparation or storage (De Roever, 1998). Escherichia coli O157, Salmonella sp. and L. monocytogenes outbreaks have been linked to apple, tomatoes, celery, lettuce, radish, watermelon, orange and other mixed salads (Beuchat, 2002). Eschericha coli O157:H7 causes 20, 000 infections and more than 100 deaths each year in the United States (Michino et al., 1999). From 1982 to 2002, 21% of outbreaks are caused by E. coli O157:H7 in the United States and from 2000 to 2004, fresh produce was the second most identified vehicle causing E. coli O157 foodborne illness outbreaks (Olaimat and Holley, 2012).

Global scenario of bacterial pathogen isolated in salad vegetables: In Japan, July 1996, an outbreak of Escherichia coli O157:H7 infection occurred among school children in Sakai city, Osaka, between May and December 1996, there were 9,451 cases and 12 deaths reported in 16 total outbreaks linked to the consumption of raw radish sprouts (Michino et al., 1999; Olaimat and Holley, 2012). In USA and Canada, October 2006, 199 persons infected with the outbreak strain of E. coli O157:H7 associated with spinach, 3 deaths were reported to Centers for Disease Control and Prevention (CDC) from 26 states. 51% of these cases were hospitalized and 16% developed acute renal failure (CDC., 2006; Olaimat and Holley, 2012). It was estimated that produce (fresh, canned or processed) was responsible for 62, 43 and 65% of parasitic, norovirus and other viral outbreaks, respectively. He also estimated that produce was linked to 43 and 35% of Shigella outbreaks and illnesses, respectively, 27 and 37% of Salmonella outbreaks and cases, respectively and 39 and 54% of E. coli O157:H7 outbreaks and cases, respectively, of those that had a food connection (Olaimat and Holley, 2012). Table 3 showed the common bacterial pathogen isolated from fresh produce.

Enterohemorrhagic E. coli O157:H7 is a causative agent of Hemorrhagic Colitis (HC) and Hemolytic Uremic Syndrome (HUS) (Chang and Fang, 2007). The most recent E. coli outbreak in world linked to contaminated fenugreek sprouts resulted in over 50 deaths and over 4,000 hospitalizations in 16 countries (Boyacioglu et al., 2013).

Interest in healthy diets increases the consumption of ready-to-eat vegetables salad. Apart from the consumption, people had changed their life style due to their busy schedule, results in shortage of time for home cooking that has led many people to buy RTE. A six year study was conducted in Santiago, Chile to estimate the presence of L. monocytogenes in vegetable salad. The finding of the study showed that the raw-eaten-salad vegetables was contaminated with L. monocytogenes and this was the first report on L. monocytogenes contamination of vegetable salads in Chile (Cordano and Jacquet, 2009). Most of the reported outbreaks were caused by pathogenic bacteria, especially Escherichia coli O157:H7 and Salmonella, pathogens E. coli O157:H7 and Salmonella are commonly found in wide variety vegetables (Chang and Fang, 2007).

Table 3: Country vise list of salad vegetables containing bacterial pathogens
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Survival of pathogens: Gastrointestinal illness caused by enteroinvasive, enterotoxigenic and enteropathogenic, Escherichia coli O157:H7 are capable of growing at 8°C. Escherichia coli O157:H7 can grow at 8°C, a temperature below which Ready-To-Eat (RTE) meals and lightly processed salad vegetables may be exposed for several hours during marketing (Chang and Fang, 2007). Fruits and vegetables are an extraordinary source of micronutrients, vitamins and fiber and prevent vitamin C and vitamin A deficiencies, but they are exposed to microbial contamination via contact with soil, dust and water or by post-harvest processing. However, fruits became harbor of wide of pathogenic microbes (Velusamy et al., 2010; Taban and Halkman, 2011). Salad vegetables are mostly contaminated with Escherichia coli, Salmonella sp., S. aureus, Enterobacter sp., Klebsiella sp., S. typhi, Serratia sp., Providencia and P. aeruginosa, Cryptosporidium oocysts and Listeria monocytogenes, that causes several diseases such as diarrhea, kidney failure, typhoid fever, food poisoning, paratyphoid fever, pneumonia, skin infection, respiratory disease (e.g., sinusitis), urinary tract infection, mastitis, phlebitis, meningitis, cryptosporidiosis etc. Washing and rinsing of some type of fruits and vegetables prolong shelf-life by reducing the number of microorganisms on the surfaces. However, only a portion of pathogenic microorganisms may be removed with this simple treatment (Lin et al., 1996; Beuchat, 2002; Kumar, 2012). Contamination with enteric bacterial pathogens like enterohemorrhagic, E. coli or Salmonella sp., leafy greens (spinach and lettuce) will support the survival of enteric bacterial pathogens because currently there is no completely effective killing step during the harvesting, processing and packaging steps (Boyacioglu et al., 2013).

Escherichia coli O157:H7 is a hardy pathogen that can survive long periods of time in water, especially at cold temperatures. Escherichia coli O157:H7 has been considered to be an important pathogen that can cause serious illness with symptoms ranging from bloody diarrhea to hemolytic uremic syndrome. In contrast to other food-borne pathogens, E. coli O157:H7 is more tolerant of some organic acids and it can survive well in acidic food and beverages. Studies determined that it can survive in refrigerated acid foods for weeks (Eribo and Ashenafi, 2003).

Listeria monocytogenes is the pathogen of listeriosis and is transmitted to susceptible individuals by consumption of contaminated foods. Cases of human listeriosis that have been associated with the consumption of raw vegetables are likely, in part, due to contamination by manure from ruminants. Listeria monocytogenes is known to grow on a variety of vegetables at refrigeration temperatures. Pathogens, along with spoilage microorganisms, may contaminate fruits and vegetables via several different routes and at several points throughout the pre and post-harvest system. Potential pre-harvest sources of microorganisms include soil, feces, irrigation water, water used to apply fungicides and insecticides, dust, insects, inadequately composted manure, wild and domestic animals and human handling. Post-harvest sources include feces, human handling, harvesting equipment, transport containers, wild and domestic animals, insects, dust, rinse water, ice, transport vehicles and processing equipments (Beuchat, 2002).

Pathogen Listeria monocytogenes is a ubiquitous bacterium, with high mortality rate and can be present in associated with decaying vegetation and soil (De Roever, 1998). The major population groups at risk for invasive listeriosis are the immune-compromised peoples such as pregnant women, new born babies, elderly people and AIDS patients (Jamali et al., 2013). Escherichia coli and Salmonella sp., are causative agent of foodborne outbreaks in many countries, causing gastroenteritis and even chronic infections (De Oliveira et al., 2011). Epidemiologic evidence suggested that raw celery, tomatoes and lettuce may have been vehicles of L. monocytogenes infection (Beuchat and Brackett, 1991; Jamali et al., 2013). Listeriosis is a relatively rare but serious disease with high fatality rates (30%) compared with other foodborne microbial pathogens and its pathogen have capability to survive under the stress conditions such as high salt concentration, low temperature and low pH (Ponniah et al., 2010; Sant’Ana et al., 2012).

Listeria monocytogenes is widely diffused in the environment on a wide range of vegetation (Beuchat and Brackett, 1991; Farber and Peterkin, 1991) and contaminate the vegetables during cultivation and post-cultivation as well as during handling or distribution; therefore fresh vegetables pose a potent risk of contamination as the eaten raw. Salad has another risk of contamination through preparation, distribution and storage (Olaimat and Holley, 2012). Beuchat and Brackett (1991) also reported the rate of death was slower at 10°C compared with that at 21°C and also observed that death of L. monocytogenes at pH<4.8 in cabbage juice was more rapid at refrigeration (5°C) temperature compared with 30°C. Listeria monocytogenes cells are dies at low pH (4.1) of tomato juice.

REMEDIAL MEASURES OF PATHOGENS

The effectiveness of ozone against microorganisms present in food systems depends on several factors, including the amount of ozone applied, the residual ozone in the medium, various environmental factors such as medium pH, temperature, humidity and additives (surfactants, sugars, etc.) and the amount of organic matter surrounding the cells (Joshi et al., 2013).

Table 4: Remedial measures for pathogens associated with fresh produce
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Inactivation of microbes using various disinfectants and parameters governing for inactivation are given in Table 4.

Olmeza and Akbas (2009) reported the application of 2 ppm ozonized water treatment for 2 min was found to be the optimum processing conditions for ozone disinfection of green leaf lettuce, in terms of reducing the microbial load and maintaining the sensory quality during cold storage. They also observed the studied conditions, 2 ppm ozone treatment was found to be better than the chlorine and organic acid treatments in maintaining the sensory quality of green leaf lettuce during 9 days of storage.

CONCLUSION

The study revealed the potential hazard of raw eaten salad vegetables and indicates the importance of proper lethal treatments before consumption and the need of adoption of hygienic practices by food processors vendors. Proactive and practical education programs are needed in process, i.e., from the field to the consumer’s plate and effective risk assessments of the microbial hazards associated with salad crops which are eaten raw. Mesophilic bacteria, indicator organisms (Coliforms) and pathogens (Salmonella and Listeria monocytogenes) were present in the food. The vegetables and fruits get contaminated with pathogenic microorganisms while growing in fields or orchards or during harvesting, post harvesting handling, processing and distribution. Pre-harvest and post-harvest practices play significant roles as sources of contamination. Street vended food had more microbial contaminants. Vendors and consumers are advised to wash fresh fruits properly before processing, fruits should be handled with sanitized hands. Adaptation and application of Hazard Analysis and Critical Control Point (HACCP) can reduce the chance of contamination and eliminate the pathogenic microorganisms.

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