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How Do Pathogens Get Into Produce?

Leafy greens, lettuce, cantaloupes, mangoes and strawberries. These are just some of the foods that have sickened or even killed people when they were contaminated with foodborne pathogens such as E. coli, Listeria and Salmonella.

Amidst the confusing swirl of information about these and other produce outbreaks, the question arises: Were some of these pathogens inside the produce? Could it be — in some cases, anyway — that the plant’s roots sucked the pathogens up out of the soil and transferred them through the plant into its edible parts?

Could this happen when uncomposted manure is applied to a field, or when water contaminated with livestock waste is used to irrigate a crop, or when deer wandering through a field or geese flying over it leave behind some fecal droppings? Could some of the pathogens from the manure, polluted irrigation water, or droppings from wildlife soak down into the ground and become available to the roots of the plants?

No idle question, this. In fact, it’s been asked enough times for serious research to be done to try and answer it. The main reason, of course, is the need to come up with information that food producers and handlers can use to prevent their crops from becoming contaminated — without being sidetracked by possibilities that don’t hold water.

Just glancing through the newly proposed food safety rules for fruits and vegetables, it becomes readily apparent that a good deal of attention is paid to preventing the surfaces of fruits and vegetables, especially those that are eaten raw, from being contaminated with foodborne pathogens. Strategies cited in the proposed rules include taking steps to ensure that irrigation and wash water is free from pathogens, that farm and processing equipment doesn’t harbor pathogens and that farmworkers have proper handwashing facilities.

But the question persists: If plants can suck contaminants up out of the soil, what in the world can a producer or processor do if livestock or wildlife pollutes nearby irrigation water or if wandering wildlife contaminates the soil with fecal droppings?

None of this is far-fetched. After all, it was E. coli O157:H7 in droppings from deer wandering through some strawberry fields in Oregon that contaminated berries that would eventually kill an elderly woman and send seven people to the hospital, three of whom suffered kidney failure, according to public health officials.

And it was the same potentially fatal type of E. coli that killed three people and sickened more than 200 in the 2006 outbreak linked to baby spinach grown in California. The likely culprits in that outbreak were wild pigs or livestock that wandered through the field or perhaps nearby irrigation water that had been contaminated by livestock or wildlife. But even with matching DNA samples, the exact way the pathogen actually spread to the spinach remains unknown.

Some mysteries brought to light

It was the 2006 baby spinach E. coli outbreak that led to a research project, funded by Fresh Express, that looked at the question of whether spinach roots could suck pathogens up from soil and transport them through the stems into the leaves.

The research on whether this sort of internalization of E. coli into is possible is also relevant to other salad greens.

The project tracked the pathogen’s journey from the field to harvest. By placing a fluorescence gene at a specific location in the E. coli bacterium, the researchers could use a specialized microscope to see where the pathogen was going.

It turned out that not only could the E. coli survive in the soil for up to 28 days, but the E. coli cells were also able to migrate from the soil into the roots of the spinach plants.

However, after looking at whether any of the E. coli strains traveled past the roots and up into the plant’s interior structures, the researchers concluded that that sort of internalization appeared to be unlikely.

“We wanted to investigate this, because it was one of the questions out there,” USDA microbiologist Manan Sharma told Food Safety News in an earlier interview. “We’ve taken something that has been of concern for eight or nine years and put it to rest.”

He said that thanks to the results of this research project, spinach growers and processors could focus on more likely routes of contamination so they can prevent that from happening.

He also told Food Safety News that if the plants didn’t have a way to keep the pathogens from traveling up into the plants’ leaves, there would probably be a lot more contaminated produce and a lot more sick people.

Even so, Sharma said that the results from this research couldn’t be translated into other crops.

“Each crop system should receive its own evaluation of the risk of the uptake of foodborne pathogens through root systems,” he said.

So, what about other crops?

That’s what scientists wanted to know when they did a review last year of the literature about research projects that focused on whether the edible parts of crops could be contaminated from pathogens or viruses that get into the plants’ roots and then travel up into the edible parts of the plant. Does that happen? they wanted to know.
The paper about this literature review, published May 2012 in Foodborne Pathogens and Disease, starts right out by saying that root uptake of enteric pathogens — those relating to or affecting the intestines — and subsequent internalization into the plants has been a large area of research with results varying due to differences in experimental design, systems tested and pathogens and crops used.

Referring to the 2006 E. coli outbreak linked to baby spinach contaminated with E. coli O157:H7 as the catalyst for more research on whether or how root uptake can contaminate produce, the paper explains that the debate on this topic has led to the need to review the literature. According to the paper, outbreaks of foodborne illnesses have been increasingly linked to the consumption of fruits and vegetables, with the source of some of these outbreaks traced back to the farm. Even so, in many outbreaks, the way the produce was actually contaminated remains unknown.

According to data from the Center for Science in the Public Interest, produce outbreaks accounted for 13 percent of foodborne outbreaks during 1990-2005.

Kalmia E. Kniel, Department of Animal and Food Sciences at the University of Delaware, and one of the project’s researchers, told Food Safety News that, when all is said and done, the results of the literature review show that it’s “very unlikely” that contamination of produce occurs in the field through root uptake.

“There’s enough literature to say that,” she said.

When asked about root crops such as carrots, Kniel said there’s no evidence to show that they’re at risk when it comes to internalizing pathogens from the soil.

That’s not to say, of course, that root crops grown in soil contaminated with pathogens won’t have some pathogens on their surfaces when they’re harvested.

The paper’s conclusion says that “generally, the presence of internalized pathogens in roots of plants does not directly correlate with internalized pathogens in the edible or foliar tissues of crops.”

Even so, the researchers say that any future research about root uptake should include realistic growing conditions, along with realistic pathogen contamination levels.

Some of the research projects used sterilized soil or extremely high levels of pathogens, for example.

Kniel also told Food Safety News that because pathogens are good at exchanging genetic material, especially when under pressure, scientists need to stay one step ahead of how that might affect root uptake and from there internalization into the plant.

Viruses

According to the same research paper, the topic of viral pathogens is critically important to food safety. That’s because from 1973 to 2006, 60 percent of U.S. foodborne outbreaks associated with eating leafy greens were caused by noroviruses, while Salmonella and E. coli only accounted for 10 percent of the outbreaks.

While noroviruses — often referred to as “the stomach flu” because they produce gastrointestinal symptoms — typically involve food contaminated by food handlers, several outbreaks from fresh produce have been linked to environmental contamination (in the field, for example).

Then, too, one of the largest outbreaks of hepatitis A virus in the United States was linked to eating green onions contaminated by the virus. That outbreak sickened about 1,000 people and killed four. And even though polluted irrigation water and farmworkers were among the likely sources for the outbreak, the exact way the onions were contaminated remains unknown.

The research also revealed that while contaminated soil triggered little to no internalization of pathogens from the roots into the plants, that wasn’t always the case with plants grown hydroponically, especially in the case of viruses that can get people sick.

“Following good agricultural practices and using clean water is essential for hydroponics,” Kniel said.

How, then, do pathogens get inside the crops?

“Internalization” happens when pathogens get inside the edible parts of fresh produce. But if not from root uptake, then how?

In a paper titled Internalization of Fresh Produce by Pathogens, which appeared last year in the Annual Review of Food Science and Technology, Marilyn C. Erickson of the Center for Food Safety at the University of Georgia, shared some observations about internalization and root uptake in leafy greens.

She found that while pathogens can get into plants in a number of locations on the plant and in a number of different kinds of produce — both before and after harvest — it is unlikely they enter through roots or seeds when grown in soil under normal growing conditions.

However, some growing, harvesting and processing conditions can open the way for pathogens to get onto and into the produce.

For example, her research showed that a film of moisture on the leaves appears to be a critical factor in a pathogen’s ability to reside on leaf surfaces and then to migrate and infiltrate into the stomata of the plants.

Stomata are tiny openings, typically found on the outer skin of a leaf but also in other parts of the plant. These little “mouths” are made up of two cells, referred to as “guard cells” that surround a tiny pore called a stoma. The stomata’s main job is to allow gases such as carbon dioxide, water vapor and oxygen to quickly move into and out of the leaf.

Erickson said that enteric pathogens can lodge in the stomata or be trapped in crevices of leafy greens that are exposed to contaminated water after harvest.

In addition, surfaces of the greens that have been cut during harvest or during minimal processing furnish sites on the leaves that are especially vulnerable to penetration by the pathogens.

When looking at actual growing conditions, Erickson told Food Safety News that the microflora (organisms that are already in the soil) far outnumber any pathogens that might also be in the soil. In general, the indigenous organisms easily outcompete the pathogens in their search for nutrients, which they need to survive. She said that in “normal soil,” you’d need concentrations of about 10,000 E. coli bacteria per gram for root uptake to happen, and even more in moist soil.

Her research has led her to conjecture that plants have defenses against internalization when they’re growing. “Internalization is more likely to happen after harvest,” she said, referring to cuts in the surfaces of the leaves as an example.

Food safety scientists have pointed out that once a pathogen migrates to a cut surface where nutrients are oozing out, it’s almost impossible to dislodge them. Like any other hungry organism, they’ll hold on tight to a source of food. From there, they can migrate into the plant’s edible parts in search for yet more food.

Cantaloupes

The sweet nutrients inside cantaloupes can lure pathogens on the surface into a melon that has been nicked or cut through these openings. From there, they can travel into the melon itself in search of even more food.

In a research paper about Salmonella contamination in cantaloupes that appeared in the International Journal of Food Microbiology, Trevor Suslow, a food safety scientist at the University of California, Davis, and his colleagues concluded that the outcomes of the project strongly indicated that root uptake and the transportation of Salmonella from the soil due to contaminated irrigation water is “highly unlikely” to occur — even under “exaggerated worst-case” growing conditions.

However, any inputs, such as contaminated irrigation water, which can contain Salmonella, would have the potential to contaminate surfaces of the melons that come into contact with the pathogens — even at low levels.

According to the report’s conclusions, these pathogens, if on the ground’s surface where the cantaloupes are growing, could get onto the melons’ surfaces and from there be transferred to other melons by farmworkers, harvesting equipment or transportation vehicles, for example.

In an earlier interview, Suslow told Food Safety News that as far as he knows, foodborne pathogens can’t penetrate the surface of produce on their own. Generally it takes some kind of opening on the surface to provide a pathway to the subsurface of the produce. But when that happens, he said, even antibacterial solutions won’t be able to rid the produce of pathogens.

The research paper concludes by warning that contamination of the external rind of the melons from irrigation water carrying pathogens remains a concern in melon production. For that reason, it’s important to establish critical limits for melon irrigation in California and other growing regions with similar arid and semi-arid climates, soil texture and crop-management practices.

An industry giant, California provides 70 percent of the cantaloupes sold in this country. During the state’s five-month season, the industry typically packs and ships around 30 million cartons of cantaloupes. A carton contains 12 to 18 cantaloupes.

Cantaloupes stand out in the roll call of recent food poisoning outbreaks. In 2011, Listeria-contaminated cantaloupes from a farm in Colorado sickened more than 140 people and killed 33. And last year, Salmonella-contaminated cantaloupes from a farm in Indiana killed 2 people and sickened more than 175 in 21 states.

© Food Safety News
  • Mike_Mychajlonka_PhD

    I find it hard to understand how one of the authors of the review cited (K. E. Kniel) can state that:  ” . . . its very likely that contamination occurs in the field through root uptake.”  After all, the review written by Kniel and others cites an eleven-year-old paper [Solomon EB, Yaron S and KR Matthews (2002) "Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization," Applied and Environmental Microbiology, Vol., 68, Issue 1, pp. 387-400] claiming just the opposite.  Nowhere in this review have I seen the results of Solomon et al. disputed.  Absent good reason to discount previously published, peer-reviewed, contrary results, I would think that Kniel’s conclusion is unwarranted.  I agree that this matter is a serious issue.  I wonder, though, why it seems to be a recent issue.  Has this issue been there all along and only gained attention now because of better disease reporting or is this route to infection truly something new?

    • http://www.foodsafetynews.com/ Food Safety News Information

      Mike, 

      Thanks for your comment. The article says that Kniel said that it’s very UNlikely that contamination occurs in the field through root uptake. I have a feeling, though, that it was just a typo on your part that caused the “un” to be left off of the word, “likely.” 

      I’ll forward your comment to Kniel. 

      By the way, this isn’t a “recent” issue so much as one that keeps coming up. The researchers wanted to address it so that food producers and processors can put their full attention onto the ways that produce, for the most part, is actually contaminated.

      Cookson

      • Mike_Mychajlonka_PhD

         I checked the rough draft of my original comment copy and found that there I did use the word “unlikely.”  However, while transcribing into the actual comment box, I no doubt made the type you indicated.  Thank you for pointing this out.  Hopefully then, with the proper words tucked away into their proper places, my comment becomes clear:  How can Kniel conclude that contamination in the field through root uptake is “highly unlikely” when the review cites (but does not dispute) papers (such as that of Solomon et al. – 2002), which show that such contamination does indeed take place?

        • http://www.foodsafetynews.com/ Food Safety News Information

          Dr. Kniel provided this response to your comment via email:

          As you allude to by your comment, there are discrepancies between the literature
          findings and as we have developed better systems for studying food safety risks
          to produce and have started to better understand the problem and risks in the
          field, scientists have realized that internalization in the field under
          standard conditions is likely a very low risk. The study you mention here was a
          good one, and used high levels of bacteria and directly provided contact
          between the roots and the pathogen. This situation is unlikely to occur in a
          field. However, this does not mean that it cannot happen, and certainly under
          hydroponic growth, there may be a higher risk, in particular from water
          contaminated with viruses. There are so many systems at play in the field, and
          researchers have shown that under “realistic” contamination it seems that
          bacteria do not readily become internalized through the root into the foliar
          part of the plant. The pre-harvest systems are complex and there are many
          issues at play including microbial competition between pathogens and other
          microflora, and bacterial cell physiology and motility. There are many opportunities
          for contamination and we are all trying to identify areas where we can best
          lower risk. Thank you for pointing out that this is still an interesting area
          where researchers may show varying results depending on the structure of the
          experiment.

  • farmber

    It would be great if our author had some kind of a background in eco-agriculture so that these industrially-oriented pronouncements and distorted goals by industrial-ag scientists could be grounded in the realities of the protective soil food web. 

    Sure, the industrial-ag use of systemic pesticides is specifically engineered so that the applied toxins (as sprayed on the plant, applied to the soil, incorporated into the seed genetics, etc) are taken up by the crop and circulated throughout the plant. For example, the toxin in genetically engineered Bt corn is expressed in the roots (and root exudates out into soil organisms), stem, leaves, corn, pollen, etc. The bottom line for eaters is these systemic pesticides are part and parcel of our food supply.

    But that’s not how healthy soil systems work and this industrial model is constantly up against the living microbe-eats-microbe world of eco-agriculture that thwarts its designs. As an example, the anhydrous ammonia fertilizer applied by conventional chemical farmers works by temporarily killing off and suppressing the natural soil microbes which volatilize nitrogen compounds into the air and water so the crop plant can utilize the N. But the chemical fertilization process is only partially and temporarily effective  – as a major amount of the applied nutrients end up being “lost” to the crop — but “found”  in soil and waterbody contamination, irrigation water contamination and dead zones around the world.

    However, aided by beneficial farming practices (cover cropping, composting, crop rotation, etc) that feed beneficial soil organisms carbonaceous organic matter and promote a healthy tilth structural soil microbe habitat, the living soil foodweb naturally devours soil pathogens. Specific bacteria are used to remediate brownfields and oil spills, for example. And the symbiotic plant-soil microbe relationship — whereby the plant contributes a major portion of its photosynthesized carbohydrate energy to feed and breed up specific beneficial organisms in its rootzone adds even greater protections against plant uptake of soilborne pathogens.

    Eaters concerned about the health of their families and food supply need to demand policies that promote healthy food production practices and support healthy food in the marketplace.

    • Kenkailing

      Thank you farmber. I fear we are moving to treat our food the same way we treat everything else; that is, sanitize everything out of existence…

  • Logiscus

    We are not Scientists and take no issue with the example / potential sources of produce contamination being discussed here. We can only provide confirmation of a very basic method of cross-contamination of produce that continues unabated, uncontrolled, unchecked and ignored year after year, probably  in favour of these more ‘sexy’ or interesting hypotheses. The application of Food Safety disciplines in the UK / European food conveyance and transportation sector is at best very poor. In recent studies food trays, roll-cages, dollies, Home Delivery vehicles, ambient and multi-temp trailers (reefers) have been found to be severely contaminated by pathogens and food spoilage yeasts and moulds. Loading practices alone suggest it is unlikely produce could fail to contact with the contaminated surfaces and therefore cross-contamination of produce with Entero, e.coli, staph, yeasts and molds is highly likely. Until the Retail sector applies the same quality controls throughout their food chain this will continue. The high standards producers and growers constantly strive to achieve are compromised every day by contaminated transportation systems.

  • Oginikwe

     I don’t believe them.  If plants are taking up pathogens through their roots then nothing is safe.

    “If consumers believe they have
    cantaloupe from this farm, they should not try to wash the harmful bacteria off
    the cantaloupe as contamination may be both on the inside and outside of the
    cantaloupe.”

    From: http://www.fda.gov/Food/FoodSafety/CORENetwork/ucm315879.htm

  • http://profile.yahoo.com/7GP2QOKYTPZH4K24MLBYDBLRUY Whrldpz

    I sense that food science has not progressed to the level that will keep us safe because the early goal of providing for a growing population took the focus away from safety and research.  I truly appreciate these articles and comments.  Also, is the cutting of the stem of a melon an entry point for contaminants?  If cutting the stem equals damage to the fruit, then we need to open up research for harvesting techniques.

  • http://profile.yahoo.com/LIFZL3WOPVUVT64ODBHACTXCPQ jmcv02

    Too many generalizations in your comment. You can have the best training and supervision on earth but as soon as you have to turn your back workers may not follow that training. Pretty certain all those farmers in the recalls, were penalized whether they were guilty or not. Our food borne illness rates are lower then they have ever been since we started tracking, the US has the safest food on Earth. If you think you could do better by all means go out and prove it. Talk is cheap….

  • FoodSafetyAllTheWay

    Barry, I agree that humans can vector pathogens; however, water is a known media to support bacterial growth. Water can also transmit pathogens from point A to point B easily and contaminate everything it touches. Hazards can be reduced, not “eliminated” as you say by proper risk assessment. The key to any produce program is regular self-inspection, properly and regularly training your employees, testing water and product, and staying well informed.

  • Dr. D.

    A lot of the most serious food borne illness outbreaks have been due to organically grown vegetables whose producers did exactly what you propose. Contamination with pathogens and food borne illnesses are actually independent of all of the things that you site. Good bugs do not eat bad bugs. Microbial ecology is way more complicated than that. Human pathogens can live in healthy organic soils for long periods of time. Prevention of contamination, whether in conventional or organic agriculture is the key to safety assurance.

    • KenKailing

      Extremely narrow and entirely synthetic view; I challenge that you can’t come close to differentiating even a small part of the natural diversity; that you in fact use an entirely fabricated mechanistic approach to make you limited understanding of nature appear real to the undereducated policy makers; and that of course is what you get paid by industry to do…it isn’t worth the argument. Look at the world around you growing more impoverished — no technical achevement is going to put it back together. There are growing problems everywhere you look and for every bad bug you exterminate, your going to find a dozen more as you destroy the biodiversity holding living systems together until you have nothing. Recall, we live in the only society ever evolved where “sickness” is profitable and health is discouraged through industrial practice.

      Funny how you don’t have a full name?

  • Dr. D

    The water conducting cells in roots (xylem cells) typically have end plates that prevent the movement of bacteria from cell to cell. Years ago we did research on bacterial pugging of cut flowers and found that bacteria moved up each xylem cell to the end plate and no further. Studies is sterile soils using massive amounts of bacteria have sometimes shown that bacteria can move up roots of very young plants whose xylem cells may not have fully matured. But this route seems unlikely in nature. That said, fruits and vegetables have may cracks and crevices where bacteria and viruses can hide and are inaccessible to wash water and sanitizers. So it may not really matter whether these pathogens are internal or external. Once contaminated fruits and vegetables can be hazardous to eat. Prevention of contamination is key.