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The Contamination of Organic Produce by Human Pathogens in Animal Manures

by Hillary Nelson

In October of 1992, public health officials investigated several cases of bloody diarrhea in a small town in Maine; one of the patients, a two year old, developed hemolytic uremic syndrome (HUS) and died of kidney failure. The cause? Escherichia coli 0157:H7, better known as just plain E. coli. E. coli 0157:H7, a bacteria which was only identified in 1982, is one of hundreds of varieties of E. coli found in the guts of mammals. This particular variety, according to the Centers for Disease Control, can be found in anywhere from 1-3% of all cattle in this country and causes them absolutely no harm. However, when E. coli 0157:H7 is picked up by a human host, the effects can be devastating; at the very least it can cause severe, often bloody diarrhea, and in the worst cases, particularly in young children, E. coli can kill. Most often E. coli illnesses are associated with eating undercooked hamburger, but frighteningly, in the Maine case, it turned out the source of the E.coli was a fresh vegetable from an organic garden. In fact, the first victim was a vegetarian, and probably contracted her illness by eating poorly washed raw vegetables that she grew herself using E. coli tainted manure from her own cow and calf as fertilizer (for unknown reasons, calf manure seems to carry the disease more often than adult cow manure). E. coli is spread through contact with contaminated feces. Apparently, through improper handwashing, the first victim then passed the disease on to her own kids and one of their playmates, resulting in the death of one of the children.

This is by no means the only case of E. coli being contracted from vegetables. According to Dr. Jonathan Mermin, an epidemiologist in the Foodborne and Diarrheal Diseases Branch at the Centers for Disease Control and Prevention, the consumption of lettuce was implicated in four separate outbreaks of E. coli during the summer of 1995, one at a restaurant in Idaho, one in Montana where the source seemed to be a supermarket, one involving Boy Scouts in Maine, and one at a hospital in Toronto; only the Montana outbreak was successfully traced back to the source of the lettuce. Then, last summer, outbreaks of E. coli in Illinois and Connecticut were traced to a bagged mesclun mix coming out of California. In both the Montana case and last summers outbreak, the producers of the lettuces were organic growers and the lettuces were probably contaminated by E. coli infected cow manure.

Why are lettuces in particular plagued by E. coli contamination? One reason is that lettuce is not cooked before consumption, a process which generally would kill pathogens. Another is that lettuce is not vigorously washed before consumption or peeled, as are other vegetables. Also, according to Dr. Mermin, there is now some evidence that lettuce juices can actually support E. coli; the process of cutting the head to harvest it, tearing or bruising of the leaves, all make these juices available to the bacteria. And finally, the process of crisping often used in supermarkets and by producers, whereby the heads of lettuce are placed in vats of warm water so that the leaves drink in the moisture and then are placed in the cooler where the leaves become nice and crisp, can cause E. coli contamination of one head of lettuce to spread to every head of lettuce sharing the water bath (this process was implicated in the Montana outbreak).

Dr. Mermin, who flew to California to investigate last summer's outbreak says there are six primary points in the growing-consumption chain where lettuces could become tainted (though in this instance, it was almost certainly on-farm):

  1. Growing. Manures containing E. coli are used to fertilize the crop, or are present in the growing area either because cattle are pastured nearby or deer are present (studies are ongoing regarding E. coli in deer; it is not known if they pick it up from the cows or if perhaps the cattle pick it up from them but it is believed that deer and other ungulates are potentially vectors for E. coli). When the lettuce is cut at harvest, or is bruised or torn, the lettuce juices may become available to support the pathogen.
  2. Processing. The processing area could become contaminated by something as simple as a worker coming in with manure on his shoes.
  3. Boxes and Coolers. The big growers use enormous vats of recycled water to wash and crisp the lettuce; sometimes the same water is used for weeks at a time, during which time a single head of contaminated lettuce could infect thousands of other heads.
  4. Transport. The trucks could be contaminated.
  5. Local distributors. Unsanitary conditions, infected workers who don't carefully wash their hands, the crisping process, all could contribute to contamination.
  6. The consumer. A consumer who handles meat and then tears lettuce, who doesn't scrub a cutting surface between uses, or who is infected already, can readily contaminate lettuce at home.

Lettuce is not the only non-meat food which could be contaminated by human pathogens; last falls Odwalla juice debacle (in which hundreds of people out west were made sick by unpasteurized apple juice - one person died) and an outbreak of E. coli in the United Kingdom associated with the handling of raw potatoes are only two documented examples of produce contamination. And E. coli 0157:H7 is not the only pathogen of concern. Dr. Mermin cited examples of salmonella on tomatoes and cholera on cantaloupe, two good reasons to wash all fruits and vegetables before cutting into them. In Maine, a few hundred school children were made quite ill by cryptosporidium, a protozoan for which there is no primary treatment. The source was apple cider which had been pressed at a school agricultural fair using apples gathered from a cow pasture. Dr. Aaron Margolin, a microbiologist at UNH, listed for me a whole slew of other potentially deadly pathogens carried by animals which could be contracted by humans including tuberculosis, lysteria, campylobacter, rotovirus, and toxoplasmosis. And Dr. Mermin pointed out to me that E. coli 0157:H7 was only recently identified; "Believe me", he said, "there'll be more of these diseases in the future that right now we don't even know exist."

I asked Dr. Margolin what the average small farmer could do to ensure the safety of his/her crops. First, he recommended composting manure before using it as a fertilizer. He also said to be aware of what other animals might be contaminating your garden, noting there are more than fifty animals which can carry cryptosporidium. In fact, several of the experts I spoke with mentioned rats and mice in particular as being vectors for serious illnesses - for example salmonella in the eggs of chickens who eat rat droppings - and suggested being vigilant in their control and extremely cautious around their feces. Dr. Margolin also suggested that deep wells are the best sources of irrigation, and noted that surface water stands a pretty good chance of being contaminated with at least some pathogens which have the potential for being transferred to produce. Thus, if you are washing lettuce mixes before market, it is important you use only drinking quality water to do so. Finally, Dr. Margolin said to be aware of what your neighbors are doing. You can have the most pristine farm in New Hampshire and if someone uphill from you is spreading raw manure or Class B sludge, your soil could be contaminated by run-off.

In the end Dr. Margolin cautioned that any person with a compromised immune system, that is, very young or very old, or a person who is ill, should be following the advice of a physician when it comes to food. He suggested that such individuals should be eating only vegetables which have been washed, peeled and boiled for ten minutes, and should never consume raw foods like salads or unpasteurized products like cider or raw milk. This is an instance where it might be preferrable to get your vitamins out of a bottle rather than to take the risk of contracting a deadly illness. For the rest of us, our body's defenses are truly amazing; a bout of crypto might make me or you well acquainted with our toilets, but it probably wouldn't kill us. But an AIDs patient or an infant, they could be dead.

Clearly, manure handling is of utmost importance in ensuring the safety of what we grow. Most organic growers are composting their manure, but certainly not all. According to Dr. Kathleen Gensheimer, the State Epidemiologist who investigated the Maine case cited at the beginning of this article, the woman who became ill was continuously putting raw manure into her garden all summer. Other experts I spoke with told me about individuals they had seen mulching actively growing food crops with raw manure, and Dr. Mermin, while investigating in California, found the use of raw manure there quite worrisome. Just from a fertilization standpoint, putting raw manure onto food crops that are close to harvest doesn't make sense. From a sanitation standpoint, the practice is reprehensible and in most places is, in fact, illegal. More commonly though, raw manure is not used on actively growing food crops, but spread onto pasture or disked into cropland before it is planted. Though this is a venerable practice, it definitely has problems associated with, most notably run-off polluting water supplies.

I spoke with Will Brinton, PhD. (the director of Woods End Research Lab in Mt. Vernon, ME. and widely regarded as this country's top Compost Wonk) about the issue of raw manure. Over 100 million tons of manure are produced in this country every year and less than seven percent of it is composted. This is a really enormous problem.

Dr. Brinton sees the days of raw manure spreading coming to an end in the not too distant future, mostly because of the degradation of water supplies. I asked him how long pathogens can survive in raw manures which have been spread on cropland, or which have fallen there in the pasturing of animals or using animals such as swine to turn soil. There's a lot of controversy over this issue; he said, it's not well understood but at least partly depends upon conditions such as how wet the soil is. In slightly anaerobic conditions like a very wet field, pathogens will probably survive longer. For this reason, most states have laws regarding how quickly food crops can be harvested from areas where raw manure has been applied. For certified organic growers here in New Hampshire the wait is a minimum of 120 days. However, the Organic Food Protection Act of 1990 (which still has not gone into effect because of the long process of writing rules but which should come on line soon) specifies a minimum of 60 days, a number which could prove to be problematic given that CDC's Dr. Mermin told me there is good evidence that E. coli can survive in manure for seventy days.

Some people use so-called aged manure on their crops, but this term is a hard one to define. Certainly, manure sitting in a pile for a time before it is used will undergo some degree of composting, but again, conditions such as temperature and moisture will affect just how much composting actually happens. Donna Rosenbaum, a food safety consultant with Food Safety Partners told me that freezing has no effect upon E. coli. You put a contaminated hamburger into the freezer, its still contaminated when it comes out. A hamburger has to be evenly heated to 155 degrees for five minutes to kill E. coli. A frozen manure pile contains many microorganisms in suspended animation, just waiting for warm weather to become active. Thus, a manure pile aged for six months in winter has a very different biological profile from one aged six months in spring and summer. Also, keep in mind that every time you add a forkfull of fresh manure to a pile you reinoculate it with pathogens; aging doesn't begin until the day you stop adding fresh waste to the pile. Because of pathogens and run-off pollution problems, Dr. Brinton feels we really should be composting, period before we spread manures. The kind of composting Dr. Brinton is talking about is not the stack-the-manure-in-a-corner-and-hope variety, but proper get-the-manure-hot-and-take-its-temperature variety.

For the complete how-to, buy the On-Farm Composting Handbook available from Northeast Regional Agricultural Engineering Service, 152 Riley-Robb Hall, Cooperative Extension, Ithaca, NY 14853-5701 for $20.00 + $3.95 shipping.

Briefly, proper composting involves balancing the nitrogen in the manure with the carbon in bedding (or leaves or wood chips or whatever you have) at a rate of between 1:20 and 1:40, controlling the moisture, and aerating the pile. Particle size and pH also play a role in composting, but ultimately, if all goes well, the pile should heat to an ideal temperature of between 130 and 140 degrees Fahrenheit for a period of five to fifteen days. Temperatures much lower than these could result in poor pathogen reduction, much higher will kill off many beneficial organisms. This period of heating kills off most of the harmful pathogens in the compost, but according to Dr. Brinton, somewhere between 2-10% of the most heat resistant bacteria survive (though viruses and helminths do not). For this reason, a period of between 60 and 120 days of curing is essential. During this time there is a great bloom of microbial organisms in the manure; this is known as speciation.

Speciation results in most (though not necessarily all) of the harmful pathogens being out-competed and dying. Unfortunately, the federal standards written into the notorious 503 Rule (which you might remember from the great sludge debate) do not require this curing process, so composts can be bagged and sold which sometimes exhibit so-called regrowth, where harmful bacteria briefly bloom before dying out as the compost ages. Though such young composts have the potential to transmit disease, Dr. Brinton, maintains that long curing results in very safe manure. Most of the organic farmers I've talked to are composting their manures for a year and a half, or two years. I think you can be very confident about the safety of these composts.

If you want to be certain your compost is done before using it, there are a couple of tests available from Woods End that are extremely accurate. The more expensive one (in the short-term) is purchasing a Dewar flask, which runs around $300.00. This is the standard technology in Europe, where laws are extremely stringent and flunking the Dewar test can put a compost company out of business. Basically, the flask is a thermos which allows the compost to heat, how fast and how hot determines how done the compost is. A much less expensive test (in the short haul, but if youre going to be doing this a lot, investing in a Dewar flask might be a good idea) is a nifty little set-up developed by Woods End called Solvita. This runs about $14.00 a test and involves sticking a paddle in a jar of compost and waiting for the paddle to change color.

It occured to me that perhaps we could do an end run around the issue of pathogens in manures by making certain the animals who provided our manure did not carry harmful human pathogens. But it turns out testing is expensive and not always particularly helpful. For example, in the Maine case, no E. coli was ever found in the manure of the calf or her mother. However, through complicated procedures it was ascertained that the cow and her calf had antibodies in their blood for E. coli which matched the genetic makeup of the E. coli which was found in the garden soil. Even if such procedures were within the economic means of the average market farmer, they are only a snapshot of a particular moment on the farm. The farmer could buy a pig or a new heifer, a wild animal could enter the farmyard; all these could be carriers and could infect the other animals on the premises. Also, many farmers import manure to their homesteads and have no control over the health of the animals which created it. Countries like Denmark and Sweden have had great success with zero tolerance policies toward Salmonella and E. coli, destroying animals and even whole herds to enforce compliance. Under pressure from consumer groups, President Clinton announced a new food safety initiative; perhaps with enough political will zero tolerance could someday be the norm here, too. Will Brinton, for one, can see a time coming when farms are not only organically certified, but microbially certified as well. But right now these diseases are endemic in agribusinesses where animals are produced in factory conditions. Such businesses would face enormous costs to rid their animals of human pathogens; they just are not interested in doing so, and as long as they don't, it will remain almost impossible for the small farmer to keep these diseases out of his/her operation. For example, most researchers agree that Salmonella is virtually ambient in this country; it can be found in more than 50% of the samples of chicken taken from any supermarket. As Vickie Smith, NH's Organic Certifier told me, You'd have to have completely asceptic conditions to keep all these diseases off a farm. It's just not realistic.

The apple cider industry is still reeling from the Odwalla juice scandal; it may never fully recover. All it would take for organic vegetable producers to suffer a similar disaster would be one well publicized outbreak of organic produce-related E. coli next summer. The greenmarkets would be turned into ghost towns at the height of the season. As stewards of the land, as individuals committed to practices which improve the health of the soil, plants, animals and people, and as responsible business people, it is our duty to see the disaster coming and to keep it from ever arriving. Who are we to shake our fingers at the sludge industry for endangering public safety when we ourselves participate in risky practices? We must recognize the presence of human pathogens in animal manures and do all we can to keep these diseases from reaching our families, friends and customers. Fastidious sanitation cannot be over-emphasized; always, always wash your hands after handling manure, or for that matter farm implements which have come in contact with manure. Take those manure encrusted boots off before entering your house or your vehicle. Wear coveralls to work around manure and then take them off when you're done. Keep your truck bed clean. Don't use poultry to weed any crop you intend to eat in the next year. Plant a green manure crop to precede a vegetable crop on that patch you had the pigs clean up last summer. Never just pull a carrot out of the ground, wipe it off and hand it to your kid for a snack. I could go on forever, but you get the message. And finally, proper composting of manures before they are used is essential to ensuring the safety of the food we grow.

The following individuals were extremely helpful in providing information used in this article:

William F. Brinton, Ph.D.,
Snail-mail: Woods End Research Laboratory, Inc.
PO Box 297
Mt. Vernon, ME 04532
207 293-2457, 207 293-2488 (fax)
Kathleen Gensheimer, M.D.,
State Epidemiologist, Division of Disease Control
Maine Dept. of Human Services
Augusta, ME 04332
207 287-5301, 800 293-7534 (fax)
Associate Professor Aaron Margolin, Ph.D.
Dept. of Microbiology
University of New Hampshire
Durham, NH 03824
603 862-2252
Jonathan Mermin, M.D., Epidemiologist
Foodborne and Diarrheal Diseases Branch
Centers for Disease Control and Prevention
1600 Clifton Road, MS 1-38
Atlanta, Georgia, 30333
404 639-3177, 404 639-2205 (fax)
Donna Rosenbaum
Food Safety Partners
853 Sanders Road, #323
Northbrook, Illinois 60062
847 509-8839

Also, many different individuals at the following organizations were very helpful: The UNH Cooperative Extension, The University of Maine Cooperative Extension, New Hampshire Department of Environmental Services, New Hampshire Department of Agriculture, New Hampshire Dept. of Health and Human Services, USDA National Organic Program, White Mountain Resource Management, Inc.

The following written materials were also used:

Cieslak, Paul R., Gensheimer Kathleen F., et al., Escherichia coli 0157:H7 Infection from a manured garden, The Lancet 1993; 342: 367.

Hay, Jonathan C. Pathogen Destruction and Biosolids Composting, BioCycle 1996; 37,6: 67-76.

Light, Luise. Cleaning Up the Mess, Vegetarian Times 1996; December: 58-69.

Millard, Peter S., Gensheimer, Kathleen F., et al. An Outbreak of Cryptosporidiosis From Fresh-Pressed Apple Cider, JAMA 1994; 272: 1592-6.

Mainely Composting (a series of articles), BioCycle 1996; 37: 46-82

Manual of Best Management Practices For Agriculture in New Hampshire, A Discussion of Nutrient Best Management Practices for Agricultural Nonpoint Source Pollution. New Hampshire Dept. Of Agriculture; Concord, NH: 1995.

New Hampshire Organic Certification Program Production Standards, Part Agr 906 Of Organically Grown Foods. Bureau of Markets, NH Dept. of Agriculture; Concord, NH: 1996.

Organic Food Production Act of 1990, Section 2114. Organic Plan, Part 2 Manuring.

State of New Hampshire Solid Waste Rule on Composting, Env.-Wm 2304.03 Processing Standards.

Rynk, Robert, ed. On Farm Composting Handbook. Ithaca, NY: Northeast Regional Agricultural Engineering Service. 1992.

Copyright 1997--Hillary Nelson. Reprinted with permission. All rights reserved.

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