FDA has announced that it has worked with the Environmental Protection Agency (EPA) to update the protocol for the development and registration of treatments for pre-harvest agricultural water to remove Listeria monocytogenes from the organism test panel.

FDA says that this change is being made because pilot studies have found that sanitizer treatments that will likely be effective for E. coli and Salmonella may be different from those that are most effective for L. monocytogenes. This is likely due to the physical characteristics of E. coli and Salmonella being distinctly different from those of L. monocytogenes. In light of recent outbreaks of Shiga toxin-producing E. coli (STEC) and Salmonella linked to produce, FDA and EPA agreed and decided to move forward with removing this pathogen from the panel.

“We expect that doing so will facilitate the registration of antimicrobial treatments against STECs (and other E. coli) and Salmonella in pre-harvest agricultural water, the availability of which will be a significant resource for farms to protect their crops against these pathogens,” FDA said in a statement. “While we are removing L. monocytogenes from the protocol at this time, companies may opt to continue testing against L. monocytogenes for inclusion in their registration with EPA.

Recent outbreaks of foodborne illness associated with the consumption of romaine lettuce and other leafy greens have highlighted the need for a viable option for treating agricultural water against foodborne pathogens.

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When aiming to achieve pre-harvest agricultural soil safety, the key is to maintain the level of beneficial soil microorganisms while minimizing the potential contamination of foodborne pathogens and plant disease from agricultural inputs used to produce crops, says Achyut Adhikari, PhD, associate professor and extension food safety specialist in the School of Nutrition and Food Sciences at Louisiana State University AgCenter in Baton Rouge.

Soils are often enriched with biological soil amendments of animal origin (BSAAO) to increase nutrient values, enhance water-holding capacity, and support crop growth and yield, says Kali Kniel, PhD, professor in the department of animal and food sciences at the University of Delaware in Newark. Soil amendments can be delivered to soils as raw animal manure, treated or composted manures, and compost teas.

Using animal manure as a fertilizer on agricultural farms is a common practice in the United States because it’s a good source of macro- and micronutrients required for crop production, Dr. Adhikari says. In addition, organic matter present in manure helps improve physical, chemical, and biological properties of soils. It also improves water infiltration, enhances nutrient retention, reduces wind and water erosion, and promotes the growth of beneficial organisms.

According to the Food and Agriculture Organization (FAO) of the United Nations, livestock contributes 40% of the global value of agricultural output and supports the livelihoods and food and nutrition security of almost 1.3 billion people. But, despite their benefits, BSAAOs can also contribute to food safety risks. They can be contaminated with zoonotic pathogens or enhance the growth of zoonotic pathogens in and around the growth of raw agricultural commodities, says Dr. Kniel. “It’s important that growers use soil amendments appropriately to grow healthy, efficient crops, as well as avoid the excessive use of soil amendments that could affect agricultural water if contamination occurs by runoff into produce fields,” she adds.

Potential Pre-Harvest Problems

Poor soil health can cause plants to become diseased, contaminate fruits and vegetables, and ultimately lower food production, says Dr. Adhikari. In addition to the indigenous microflora of soil, pathogens and other microorganisms can be introduced into soil from different inputs such as contaminated irrigation water, runoff water, and unfinished or improperly treated compost or raw manure application, as well as both domestic or wild grazing animals.

The persistence of bacterial and viral pathogens in raw animal manure is based on the manure type, how it’s applied and incorporated into soils, soil type, storage of manure before application onto soils, and the microbial diversity present and nutrient ratios in manure-amended soils, says Dr. Kniel. Persistence and survival of bacterial pathogens in manure-amended soils depend on geographical and environmental factors.

According to Michael Mahovic, PhD, branch chief of the division of produce safety within FDA’s Center for Food Safety and Applied Nutrition in College Park, Md., among the most commonly occurring foodborne pathogens are:

1. Salmonella spp., which can come from domesticated and wild animals and their feces as well as humans and their feces. Some strains have become resident in the environment.
2. Shiga toxin-producing Escherichia coli, which can come from domesticated and wild animals, particularly ruminant animals (e.g., cattle, sheep, goats, and deer), and their feces.
3. Listeria monocytogenes, which can be found in soil, decaying vegetation, water, and domesticated and wild animals and their feces.
4. Cyclospora cayetanensis, which can come from humans and their feces.

Using untreated or partially treated animal manure as a fertilizer in crop production may result in contaminating fresh produce with enteric pathogens, Dr. Adhikari says. Once contamination occurs, it is difficult to remove pathogens completely from fresh produce, even with chemical and physical decontamination treatments. As plants uptake water, soil-borne pathogens can enter the fruit, making it impossible to wash away, leaving heat as the only means of rendering the produce safe.

Furthermore, human exposure to untreated animal manure or insect vectors may put workers at risk of pathogen infection, says Dr. Adhikari. Therefore, it’s essential to adequately treat or compost animal manure before application, and to use proper strategies during application and storage of raw manure to ensure reduced risk of contamination.

Agricultural water can be another vehicle for produce contamination pre-harvest. It can easily become contaminated with rainwater, surface runoffs, wildlife access, animal fecal deposits, and many other things. Surface water that is open to the environment is the most prone to microbial contamination, says Manreet Bhullar, PhD, research assistant professor in the department of horticulture and natural resources at Kansas State University in Olathe. Water can carry pathogens from soil to a plant’s surface through splashing, sprinkling, or other modes of irrigation or crop management practices. Excessive rainfall that causes runoff that can also be a source of contamination from seemingly distant locations. In addition, using contaminated water for irrigation may deposit pathogens that can survive and persist in soil for longer periods of time, depending on several factors.

Water quality is crucial for fresh produce that is consumed raw, says Dr. Adhikari. Water used for irrigation should be routinely tested to ensure its safe to use. Once contaminated, pathogens are difficult or even impossible to remove from fresh produce even after vigorous washing with sanitizers. Municipal waters are potable and safe for agricultural purposes but are not always available. Due to the limited supply and access growers must depend on surface water or well water to meet production requirements.

Mitigating Potential Issues Pre-Harvest

The Food Safety Modernization Act (FSMA) shifted the focus from reacting to problems after they occurred to preventing food safety problems, Dr. Adhikari says. When using BSAAOs per the FSMA Produce Safety Rule (PSR), Dr. Bhullar says the following criteria should be applied:

• To minimize the risk of contamination, soil amendments must be treated to destroy pathogens.
• Aerated compost should be treated at 131°F or 55°C for three days, followed by curing; turned composting should be treated at 131°F or 55°C for 15 days, followed by curing.
• Use a thermometer to check the temperature of the compost pile.

When using and applying soil amendments of animal origin:

• Maximize the time interval between application and harvest.
• Minimize runoff and access by animals.
• Separate raw and finished manure to prevent cross-contamination.
• Designate special tools for treated soil amendments and clean them after use.
• Do not allow manure to contact the edible portion of the plant.

Growers can also mitigate pathogen survival in soils by following guidance from the USDA National Organic Program (NOP) and the California Leafy Greens Handler Marketing Agreement. The NOP recommends that raw (untreated) manure be applied at least 120 days before harvest for crops that are likely to contact the soil and 90 days for crops less likely to contact soils. “This is to provide sufficient time for pathogens to die off in soil and minimize their likelihood of transfer,” says Manan Sharma, PhD, a research microbiologist in the Environmental Microbial and Food Safety Laboratory of USDA’s Agricultural Research Service (ARS) in Beltsville, Md. “Currently, the FDA has ‘no objection’ to the NOP interval for the application of manure and harvest of fruit and vegetable crops, but is evaluating data to determine if the NOP interval is appropriate for produce.”

Research published in 2019 in the journal Applied Environment Microbiology indicated that weather and regionality drive survival of pathogens in soils, more than soil type or manure amendment type, says Dr. Sharma. Rainfall and soil moisture affect pathogen survival duration. Specific amendment types, such as those based on poultry litter, have supported longer survival durations than dairy cattle manure or horse manure in previous studies conducted collaboratively by USDA ARS, the University of Maryland Eastern Shore, and FDA.

A collaboration among USDA ARS, the University of Delaware, and FDA, led by Drs. Kniel and Sharma and published in 2021 in Applied and Environmental Microbiology, showed that the transfer of pathogens to cucumbers from soils occurred at higher levels in seasons with greater rainfall, says Dr. Sharma. Pathogen survival in soils also increased in seasons with more rainfall. Studies are currently underway in different states (e.g., California, Georgia) that examine the survival of pathogens in soils and transfer to specific commodities (e.g., onions, leafy greens), for both untreated (raw) manure amendments and heat-treated amendments. These studies are part of a USDA SCRI-funded grant called CONTACT, a multi-institution produce safety research project.

Despite its benefits, the major concern about using raw manure is that it’s a significant source of human pathogens, says Dr. Adhikari. In fact, growers must avoid using raw manure if they’re growing crops that are consumed raw. Developing practices of using properly composted materials on produce farms will reduce the risks associated with microbial contamination.

Using Good Agricultural Practices

The best way to reduce risks associated with contamination of raw agricultural commodities is to promote the use of USDA’s good agricultural practices (GAPs), says Dr. Kniel. GAPs include good handling practices of soil amendments, which may reduce risks of contamination with zoonotic pathogens (i.e., bacteria, viruses, and protozoa that can cause illness in animals and humans). “Growers should use color-coded tools to reduce the risk of contamination of treated and untreated soil amendments,” Dr. Kniel says. For example, “use tools with ‘green’ handles for untreated soil amendments and don’t use those tools with other soil amendments. Be sure that those tools don’t come into contact with crops at or near harvest time.”

It’s also important for growers to know if the soil amendments they’re using are properly composted, Dr. Kniel says. This requires certification by the retailer or proper monitoring of time and temperatures if a grower does their own composting.

Managing soil amendments can reduce food safety risks. This includes assessing risks from the soil amendment being used, selecting low-risk crops for application (e.g., agronomic), and reviewing the application method (e.g., incorporated, injected, or surface applied) and timing (e.g., days to harvest, season of application) to reduce risks, says Dr. Kniel. For this reason, raw manures are more often applied to agronomic crops rather than to raw agriculture commodities.

Another GAP, according to Amanda Deering, PhD, associate professor in the department of food science at Purdue University in West Lafayette, Ind., is limiting the amount of time that fresh produce touches the soil when possible; however, this is not possible for crops such as cantaloupe, which grow on the ground. Also, fresh produce items that are dropped and touch the ground after harvest should never be sold because they can become damaged when hitting the ground. Cuts and bruises on fruits and vegetables can release nutrients (sugars) from a plant and may be a source of food for any bacteria that are present, which will allow them to grow to high numbers and cause illness in those consuming the fruit or vegetable.

Going Forward

Managing risks in produce production includes addressing potential sources and routes of contamination, such as those described in FSMA. Additionally, if farms aren’t covered by this ruling or face additional distinctive challenges due to their local conditions or practices, they should consider implementing appropriate GAPs, Dr. Mahovic says.

Understanding one’s farming operations is critical to establishing microbially safe practices for safe, fresh produce production. “FSMA’s PSR guidelines don’t fit all farms and only provide scientific recommendations on the common routes of contamination in order to minimize risks,” Dr. Bhullar says. “It’s important to identify all potential concerns of contamination on a farm and to consider them when developing a farm food safety plan.”

Risk-based preventive controls will continue to help minimize risks of contamination; however, there is no such thing as a one-size-fits-all plan. “Microbial food safety risk depends upon pre- and post-harvest practices, agricultural inputs, commodities grown, and environmental factors,” says Dr. Adhikari. “Conducting a risk assessment that is geared toward a particular farm and developing practices to minimize the risk of contamination will help to mitigate specific risks.”

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New research from the Center for Food Safety at the University of Georgia suggests that farmers can reduce foodborne pathogens by applying sanitizers to produce while it is still in the ground. Modern practices for the reduction of foodborne pathogens on produce typically focus on post-harvest washing; however, even though tremendous efforts are performed, outbreaks of foodborne pathogens in this produce still occur.

The researchers examined the bactericidal effects of a food-grade sanitizer and found that it could kill inoculated foodborne pathogens on tomato plants. Additionally, pre-harvest treatment reduced coliform and total bacterial population.

“There was no Listeria detected on all collected tomatoes,” says Tong Zhao, PhD, an associate research scientist at the university and co-author of the study.

According to Dr. Zhao, pre-harvest application of bactericides is not a common practice among vegetable growers. Originally, the researchers planned to study the use of a nonchlorine-based sanitizer made of two FDA-approved food additives—levulinic acid and sodium dodecyl sulfate—as a post-harvest wash solution. However, with advice from Bill Brim, president of Lewis Taylor Farms in Tifton, Ga., the researchers used the solution in a pre-harvest spray instead.

The researchers examined both laboratory and field tests, spraying tomato plants with a solution containing five strains of E. coli, five strains of Salmonella, and five strains of Listeria specially grown in a lab. The plants were then separated into three equal groups and sprayed with the bacteria solution comprised of commercial product Fit-L. One group was treated with acidified chlorine as the positive control, another with a treatment solution containing levulinic acid and sodium dodecyl sulfate, and a third was treated with tap water only as the negative control.

The outcome of the study showed that the combination of levulinic acid and sodium dodecyl was effective in reducing foodborne pathogens on tomato plants contaminated with Salmonella, Shiga toxin-producing E. coli, and Listeria monocytogenes.

“The results reveal that pre-harvest intervention by Fit-L is a practical, easy-to-use, labor-cost-effective, and environmentally friendly approach for control and reduction of foodborne pathogens that may contaminate the surface of the produce and total surface bacterial population at pre-harvest stage,” Zhao says. “Its application at pre-harvest plus post-harvest washing will provide a warranty to secure the safety of fresh produce.”

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Food monitoring procedures are strongly focused on hygiene to avoid microbiological hazards such as bacterial or viral contamination. A general increase in microbiological safety has already been achieved over the past decades through the establishment of various standards (HACCP, IFS/BRC, ISO 22000). Despite greater safety and longer-lasting products, microbiological control must be improved particularly with respect to fresh products. Most foodborne microorganisms that cause illnesses are zoonotic or geonotic but some have human origins, such as the Hepatitis A, Salmonella phi, and Vibrio cholera. These contamination can occur during the food manufacturing process.

A significant increase in diseases stemming from microbiological infections can be expected in the future. The Federal Institute for Risk Assessment stated that foodborne infections will pose a serious problem to the global public health in the coming years. In the last two decades, there has been an  overall increase in foodborne illness outbreaks and cases linked to fresh fruits and vegetables:

• Vegetables, juices, and related products comprised 4.4 percent of all foodborne outbreaks in the EU between 2008 and 2013.
• In the U.S., 13 percent of foodborne outbreaks between 1990 and 2005 have been associated with fresh produce. Green salad, lettuce, seed sprouts, tomatoes and cantaloupes were identified as the main sources of foodborne illness outbreaks.

Frequent combinations are: Salmonella and cantaloupes, sprouts, or tomatoes; E. coli and leaf green vegetables; Cyclospora and raspberries; and Hepatitis A with green onions.

Within the structured approach to food safety management (Risk Analysis framework), Food Safety Objectives (FSO) are essential tools to meet public health goals. FSOs define the maximum level of microbiological hazards permitted in various foods at the point of consumption. Maximum hazard levels at different points along the food chain represent further performance objectives.

Unlike other commodities, such as beef or chicken that is rigorously inspected, microbiology is often neglected when testing fresh fruit and vegetables because adequate strategies are lacking. Fruits and vegetables are foods with generally short shelf life: however, investigations of microbiological risk take some time. A number of different microbiological testing can be used by industry and government actors. Within-lot testing is one of the most common methods when measuring the hazard against a pre-defined limit but the sampling plans are generally time-consuming and resource-inefficient.

Point source contaminations that cause individual consumer illnesses might occur in fresh produce due to bird feces, for example. However, these kinds of risks are difficult to detect once the product is packed and optical control is insufficient. General or nonpoint source contaminations could cause foodborne epidemics because of the effect on a broad range of products. Pre-harvest sources of nonpoint source contamination are most often soil, feces, irrigation water, water used to apply fungicides and insecticides, dust, insects, inadequately composted manure, wild and domestic animals, and human handling.

The earlier a risk is detected, the better the odds for effective measures and lower overall costs.

On the basis of the European Food Safety Authority results and personal experiences with more than 400 microbiological samples and over 2,500 field visits within the last two years, Analytica Alimentaria has developed a new risk analysis process when testing fruit and vegetables:

1. Effective microbiological risk assessment in the field with a new evaluation system, structured questionnaires, and defined approval policies;
2. Synergies via the efficient linking of risk analysis with pre-harvest sampling;
3. Risk-oriented sampling and laboratory analysis of the correct parameters;
4. Clear escalation scheme in the case of positive findings; and
5. Fast decision-making for retailers.

This article describes the complete process of microbiological risk assessment, which can be a general or nonpoint source contamination of the sampled object (field, warehouse) that can cause a foodborne epidemic or individual illness. As the result of the process, the risk can be calculated and mitigated.

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Results and Discussion
The questionnaire developed for the field and warehouse is based on information from scientific literature as well as on the samplers’ own experience. It is also based on the growth of microorganisms along the entire food chain. It is well known that pre- and post-harvest environments are significant sources of pathogens.

Questions and answers are divided into two weighted categories: high-risk questions (HRQ) and low-risk questions (LRQ), as well as additional information on the conditions of the work. The number of “Yes” and “No” votes are summarized separately and taken for a decision on microbiological sampling.

The assessment of microbiological risk is based on the evaluation of the questionnaire, which takes place using Excel spreadsheets.

HRQ specifies the conditions where microbiological contaminations are very likely to occur. Potential sources for microbiological infection in the field are direct sources of living pathogens (past infections, animals, organic fertilizer/manure) and particularly favorable environmental conditions (high water level).

Salmonella, Shigella, and E. coli O157:H7 and other pathogens that can survive for extended periods of time in water. Flood and spray irrigation represent the greatest risk because contamination can be directly deposited onto edible parts of produce. Reconstituted pesticides may also serve as potential sources of pathogens.

LQR collects and evaluates marginal conditions for microbiological contaminations that could be a risk when a common occurrence. The choice of questions was based on respective regulations:

• Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs;
• Regulation (EC) No. 1935/2004 on materials and articles intended to come into contact with food; and
• Guidance for dealing with fruits, vegetables, potatoes.

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Additionally, a monitoring process is included that evaluates the minimum hygiene standards in the field.

The questions should be answered by growers, agricultural technicians, engineers and experienced samplers with “yes,” “no,” or “not known.” Objective criteria is defined to enable correct answering of questions.

The action plan. In case of a positive finding, the main problem often is the absence of an effective plan to restore microbiological safety. The laboratory that has detected the pathogens is responsible for forwarding information to the corresponding grower/producer and to the whole supply chain via the trader. A second sample has to be stored for cross-checking. The laboratory is also responsible for source identification as well as the magnitude of microbiological contamination in the field or warehouse of the grower/producer. The trader has to ensure the grower and all affected goods in the supply chain are temporarily blocked from the market. The trader also contributes to restoring the delivery capacity of the grower.

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The control plan. In case of a detected risk, a microbiological sampling takes place according to the rules of the Questionnaire for Microbiological Risk Assessment (QMRA). A microbiological sample consists of a number of individual subsamples. Each individual subsample is transported and analyzed separately. If any of the subsamples contain pathogens, harvesting is forbidden on the field of origin. A special controlling plan is implemented to identify the source and to decide if point source or nonpoint source contamination exists. Using GPS coordinates and other markers, the affected field is divided into five different, clearly separated areas that adjoin the area where the original sample was found. Control samples from the crop, the soil and the irrigation water have to be taken from each subarea and analyzed to measure the extent of contamination. A nonpoint source contamination exists if two or more control samples are positive. If only one sample is positive a partial contamination of the corresponding subarea exists. A point source contamination exists if all control samples are negative. This implies that only a part of the original sample was contaminated and that contamination could not be detected again. To detect and permanently address the source of microbiological contamination, further microbiological samples from irrigation water and soil must be taken, especially in cases where the same water or fertilizer is used for the subareas.

Examples for averted hazards by QMRA. According to the QMRA, a microbiological risk was found in a Spanish field with cabbage lettuce after strong rainfalls and floods in 2012 (QMRA question No 3). The original sample taken from the lettuce contained Salmonella spp and the action plan was activated. The supply chain was informed and the field was immediately blocked. Further samples were taken according to the control plan (lettuce, soil, and water from five subareas) and all five samples were positive for Salmonella spp: therefore, a nonpoint source contamination existed. The irrigation water from a river nearby was identified as the source of contamination: the river was highly contaminated with waste water and dead animals from neighboring farms.

In 2014, a microbiological risk was found in a Moroccan parsley field. A cow-farming unit existed near the field without an enclosure (QMRA question No 2). The original parsley sample contained STEC (E. coli 0103) but only one sample from the tests and one soil sample was positive. Both positive samples were from the same subarea nearest to the cow-farming unit. The irrigation water sample was negative and a partial contamination was found in the subarea due to animal feces.

In 2015, Listeria monocytogenes was found for Batavia in Italy when an undocumented (date of application, microbiological sampling) use of organic fertilizer had been observed (QMRA Question No 4). After blocking the field, all control samples were negative and a point source contamination of the field was acknowledged. The harvest could be continued.

Conclusions
The microbiological condition of food is one of the most critical elements of food safety, especially for fresh fruits and vegetables. The entire supply chain of fresh fruits and vegetables is highly time sensitive yet microbiological controls take some time for analysis. Unfounded actions could endanger human health and/or the supply chain. This new risk-based evaluation in the field facilitates a safe and convenient risk assessment of the microbiological condition of fresh crops at an early stage in the supply chain. Examples have demonstrated the reliability of the system, which comprises risk evaluation, action and a control plan. The QMRA saves time and cost but should be administered only by well-trained technicians. Sampling must be performed according to standardized and accredited methods.

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Lampe is a geo-ecologist at Analytica Alimentaria GmbH. Reach him at udo.lampe@analytica.international. Hidalgo Palanco is a biologist at the company. Reach him at Isaac.hidalgo@analytica.international. Fernandez Caro is agricultural engineer at Analytics Alimentaria. Reach him at fernando.fernandez@analytica.international. Dr. Krause is a physicist at the company. Reach him at peter.krause@analytica.international.

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