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Food and waterborne disease threats.

The developed world enjoys the most varied, affordable, safe, wholesome and affordable food supply in the history of civilization. This is not by accident; the safety of the food chain is ensured through a complex, integrated network of local, county, state, federal, and Department of Defense organizations dedicated to mitigating the threat of unintentional contamination of our food supply from production through transportation and distribution to the consumer (Figure 1). From local and county health departments through federal agencies, including the Food and Drug Administration and the US Department of Agriculture Food Safety and Inspection Service and Veterinary Services, each link along the food chain is monitored and regulated with the goal of achieving healthy herds, flocks, crops, and communities, and a safe food supply. Yet even with this system in place, food and waterborne disease continues to be a significant health risk in populations throughout the world, including the United States. (1) A majority of the foodborne disease agents are zoonotic, that is, maintained in vertebrate animal reservoirs and incidentally infective to humans. We are intimately connected to animal populations through shared, or zoonotic diseases, the food chain, and the human-animal bond--our innate desire to surround ourselves with animals. In an era where many US citizens believe steak comes from the local supermarket, it is essential to remember that it is impossible to separate agriculture from food, and it is equally inadvisable to separate animal health from human health. (2)

The resurgence of the One Health Concept* has fueled improved connectivity in integrated surveillance and reporting for humans and animal diseases both within the United States and abroad. The risk for food and waterborne disease is greatest in regions with fractured public health and veterinary infrastructure, lack of a functioning national health surveillance system, and unknown incidence of endemic disease, factors present in many locations around the world where the US military is deployed. The risk of foodborne disease is further increased in concentrated military populations composed of immunologically naive Soldiers largely unaware of the host of disease agents present in local fare. Protecting our deployed Soldiers, Marines, Sailors, and Airmen from food and waterborne disease is the primary focus of the US Army Veterinary Service.

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It is impossible to overstate the importance of a safe and secure food supply, not only to the individual but also to nations. Public confidence in the food chain is essential; a loss of public trust carries significant social, economic, and political weight. Even the perception of an unsafe food supply creates serious social and economic consequences (Figure 2). The 1999 dioxin contamination of the Belgian poultry, meat, and dairy industries caused $1.5 billion in lost revenues and was directly responsible for the peaceful ouster of the Belgian coalition government in general elections 6 weeks following release of the discovery. The full effects of potential chronic disorders such as teratogenesis, carcinogenesis, immunosuppression, and liver or kidney failure is yet to be seen. (4) One positive effect of the Belgian dioxin scare was that the removal of poultry products from the shelves resulted in an astounding 40% decrease in the incidence of Campylobacter infections, a bacterial agent ubiquitous in the poultry industry. (5) The cause of dioxin contamination was determined to be intentional, criminal contamination of recycled cooking oil destined for animal feed. The use of dioxin in subsistence as an intentional politically motivated attack surfaced in 2004 with the alleged poisoning of Viktor Yushchenko, the Ukrainian opposition presidential candidate.

The agriculture-food industry is a highly complex, integrated, just-in-time system of massive concentrated production, transportation, processing, national and international distribution and retail. There are numerous critical control points uniquely susceptible to unintentional adulteration throughout the food chain. Similarly, the industry is an open "soft" target for intentional contamination for social, political, economic, or religious motivations. The January 2001 Department of Defense report, Proliferation: Threat and Response, (6) was the first official document which identified that attacks on US food supplies could affect the economic stability of the country and erode military readiness. As outgoing Secretary of Health and Human Services, Tommy Thompson said in a 2004 interview that he worries "every single night" about "food poisoning" on a massive scale. He continued, "I for the life of me cannot understand why the terrorists have not attacked our food supply, because it is so easy to do." (7) Ensuring the safety of the food chain from intentional adulteration, termed food defense, is an emerging role of the US Army Veterinary Service.

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Food and waterborne disease due to unintentional contamination remains a significant health threat, even in the United States. We are no further away from the great endemic diseases of the underdeveloped world than an air transport of fresh vegetables destined for our grocery stores and restaurants. A typical restaurant meal contains ingredients from 30 countries and is handled by food service workers from no fewer than 4 countries. US citizens believe food safety is the responsibility of the vendor and regulatory agencies. In stark contrast, the entire developing world believes the responsibility for food safety lies with the consumer--caveat emptor. With this perception in the US, perhaps it is not surprising that 74% of US households failed to meet minimum sanitary standards in a recent Audits International survey. (8) The risk lies not just with meats, but equally with fresh fruits and vegetables. For the first time, the incidence of foodborne disease due to consumption of produce equaled that due to contaminated meat, poultry, eggs, and seafood in 2000. Reports of large-scale outbreaks traced to spinach or lettuce have become as commonplace as ground beef recalls. (9)

Food and waterborne disease is responsible for an estimated 76 million cases of gastroenteritis annually in the United States alone, with 325,000 hospitalized patients and 5,000 deaths. Worldwide, food and waterborne diseases represent the most commonly reported outbreaks to the World Health Organization. This is a staggering fact given the extent of infectious diseases abroad such as malaria, leishmaniasis, and tuberculosis. No doubt the incidence has always been high in the underdeveloped world. The increase in recognized outbreaks likely represents improved surveillance and reporting. (10)

The primary route of exposure is fecal-oral contamination of food and water due to poor food handler hygiene and the use of contaminated water and ice in processing. Raw and undercooked meat, poultry, eggs, dairy products, shellfish, and produce are the highest risk food items commonly consumed. Unpasteurized milk was responsible for 45 outbreaks in the United States from 1998 through 2005. Other means of infection are person-to-person via asymptomatic carriers and episodes of public vomiting, through fomites or aerosolization. A review of 348 outbreaks of acute gastroenteritis reported to the Centers for Disease Control and Prevention revealed 39% were foodborne, 12% were person-to-person, 3% were due to contaminated water, and 46% were from undetermined sources. (11) Control of disease outbreaks is usually restricted to the identification and removal of the point source, and minimizing person-to-person transmission. Critical to the process is rapid, sensitive, and specific diagnostics. Agent detection in food and water systems poses unique diagnostic challenges. Water detection requires a large sample size and sophisticated concentration technologies. Many food items contain enzymatic inhibitors that reduce the effectiveness of assays. Development of new validated detection assays is an ongoing focus in the food and water diagnostic community. (12)

Many kinds of infectious agents are responsible for causing food and waterborne diseases, including viruses like Norovirus and Rotavirus, bacteria including Salmonella, Campylobacter and Shigella, metazoan parasites like trichinosis, and protozoal infections such as cryptosporidiosis. Many outbreaks are multifactoral, further complicating the diagnosis and tracing the origin of outbreaks. The majority of cases present as acute gastroenteritis: nausea and vomiting, cramps, fever, diarrhea, headache, and myalgia. Many diverse disease agents present with similar signs and symptoms, although the presence of blood in the stool should always raise concerns about a bacterial agent and inspire the attending health care worker to collect stool specimens for culture. Of interest, less than 60% of cases of acute gastroenteritis presented to physicians in the US are actually cultured for disease agents. While most cases of acute gastroenteritis resolve within a matter of days, a low percentage of cases develop serious complications, including hemolytic-uremic syndrome, thrombotic thrombocytopenic purpura, Reiter's Syndrome (consisting of arthritis, urethritis, and conjunctivitis), septicemia, dehydration, and electrolyte and acid-base derangement, shock and death. (13,14)

SHIGA-TOXIN PRODUCING ESCHERICIA COLI

The enteric coliform organism, E. coli, is ubiquitous in animals and farm environments. Most strains exist as innocuous intestinal flora and serve as a useful indicator of fecal contamination. Some strains including O157:H7 and 0153 produce a Shiga-like toxin and are capable of causing severe gastroenteritis. The primary source is the mammalian intestinal tract. While many mammals carry this organism, human exposure is primarily from ruminants and contaminated environments. Products at greatest risk include raw milk, fresh produce, water sources, unpasteurized cider, and undercooked ground beef. The incidence of disease in the US is 2.8 per 100,000, with an estimated 73,000 cases per year. Disease outbreaks are commonly associated with large-scale recalls of regionally, nationally, or internationally distributed ground beef. Following a 2- to 5-day incubation period, affected patients develop a 6 to 10 day course of severe cramps, fever, and watery diarrhea that becomes bloody with time. Many recovered patients become silent carriers, capable of shedding organisms for protracted periods. Up to 4% of infected juveniles develop hemolytic-uremic syndrome, while a smaller proportion of adults develop thrombotic thrombocytopenic purpura. The cardinal signs of cramping and blood diarrhea always warrant a stool culture and strain typing. A typical isolation media is Sorbitol-McConkey agar. Shiga-like toxin is detected using a verotoxin assay. Treatment consists of supportive fluid and electrolyte therapy. Antibiotics appear to predispose for hemolytic-uremic syndrome. Antidiarrheal products like Imodium are contraindicated. Shiga-like E. coli is a reportable disease. (15,16)

NOROVIRUS

Norovirus is a nonenveloped, single-strand RNA virus of the family Caliciviridae. It is resistant to drying, freezing, steam, and chlorination, and is the number one cause of acute gastroenteritis, responsible for over 50% of outbreaks in the United States. Detection was restricted to a few specialized research laboratories until recently, thus explaining the large proportion of historic foodborne disease outbreaks with undetermined etiology. This is a disease of high-density encampments, including everything from Naval vessels and cruise ships to military and youth training camps, and even a recent outbreak at a marathon dance contest. Oysters in contaminated waters filter and concentrate the virus in high titers. Transmission is primarily through contaminated food and water supplies, although the hardy nature of this virus explains many cases of person-to-person transmission and exposure via aerosolization following episodes of public vomiting. Diagnosis is made by reverse transcriptase polymerase chain reaction technology. (17)

The symptoms are that of a typical case of gastroenteritis, with up to 30% of recovered patients becoming asymptomatic shedding carriers of the disease. A notable exception was the Norovirus outbreak in the British field hospital in Afghanistan in 2002. Twenty-nine patients and staff were affected by an unusually severe, acute disease characterized by headache, stiff neck, photophobia, listlessness, disseminated intravascular coagulation, and mild gastrointestinal symptoms. The disease presentation resembled a hemorrhagic viral disease like Rift Valley Fever more than a typical intestinal agent. Diagnosis was delayed for several days, resulting in a palpable operational paralysis in the sector. (18) This outbreak speaks loudly for the need for forward-deployed, rapid, sensitive, and specific diagnostics to support military operations.

CRYPTOCOCCUS NEOFORMANS

Cryptococcus neoformans, the etiology of cryptosporidioisis is a minute, intracellular apicomplexan protozoal parasite (Figure 3). Reservoirs include humans, ruminants (especially calves), and even birds. Transmission is fecal-oral, and can be human-to-human, animal-to-human, foodborne, or waterborne. The most common source of outbreaks is a failure of solid waste management. The disease is self-limiting in the immunocompetent patient, with nausea, cramps, and an explosive watery diarrhea of 3 to 4 days duration following a 1- to 12-day incubation period. In immunosuppressed patients, cryptosporidiosis becomes a chronic diarrhea with persistent shedding of myriad organisms. Up to 20% of acquired immunodeficiency syndrome patients are affected by chronic cryptosporidiosis. (19) While some outbreaks are truly due to a zoonotic strain spread from livestock to humans, the majority of cases are actually caused by genotype I, a strictly anthroponotic variant. Outbreaks have been reported from swimming pools and water parks and from the food service industry, including an interesting case in Spokane, Washington, traced to contaminated green onions. (20) The most spectacular outbreaks are due to solid waste failures. The 1993 outbreak in Milwaukee, Wisconsin, affected 403,000 residents, and stands today as the largest public health outbreak in US history. (21) At the time, diary farms located along 2 rivers upstream from Milwaukee were blamed. However subsequent study of the causative organism revealed its nonzoonotic nature, thus implicating human fecal contamination of the drinking water supply as the likely source of infection. (22)

[FIGURE 3 OMITTED]

Control and prevention must thus follow a 2-pronged approach, both directed at limiting the ingestion of food and water contaminated by ruminant fecal material, but also aimed at prevention and early detection of large-scale community waste management failures.

TRICHINOSIS

Trichinosis is cause by the nematode parasite, Trichinella spiralis, a member of the Class Adenophorea. Transmission is entirely from ingesting raw or undercooked meat. This nematode parasite is unique in that the infected human or animal serves as both the intermediate and definitive host. Reservoirs include rats, pigs, dogs and cats, horses, wildlife, and even marine mammals. The US commercial swine industry is likely free of the disease, however, backyard and foreign pork products should be considered contaminated. (23)

After 5 to 15 days incubation, the patient presents with a triad of signs: myalgia, fever and fatigue, edema of the upper eyelids, and a stunning peripheral eosinophilia. Diagnosis is made via history of exposure, clinical examination, hematology, assays to detect elevated muscle enzymes such as lactate dehydrogenase and creatine phosphokinase, and muscle biopsy. Biopsies reveal coiled nonencapsulated nematode larvae eliciting minimal local tissue reaction (Figure 4). Suspect animal muscle tissue can be evaluated by histopathology or a larvae per gram (LPG) digestion assay. (24)

Outbreaks in the United States are most often due to ingestion of wild game jerky, including cougar and bear. A Montana outbreak was traced to bear jerky prepared following 6 months of freezing.

The LPG assay revealed 212 larvae per gram! (23) Outbreaks in France and Belgium have been traced to consumption of raw horse flesh, and outbreaks throughout Germany are typically due to smoked pork sausage. A 2007 outbreak in Pomerania affected over 200 people, and was traced to raw pork from a single producer. Other outbreaks around the world were caused by ingestion of barbequed badger (Russia and Korea); dog meat (Russia, Kazakhstan, Slovakia, Thailand, and China); fox sausage (Italy); and barbequed leg of jackal (Algeria). (25,26)

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Prevention requires cooking all meat to 160[degrees, or until it turns from pink to brown. Historically, freeze-resistant strains were restricted to the Arctic; however, the past 2 decades have seen increasing numbers of freeze-resistant strains responsible for outbreaks in the lower 48 states. (27) Judicious rodent control on farming operations is essential, as is sanitary disposal of garbage.

Food and waterborne diseases are easily preventable by following basic hygiene practices and having complete knowledge of the processing and products consumed. The US Army Veterinary Service maintains a worldwide directory of sanitarily approved food sources (28) to ensure that our Soldiers, Marines, Sailors, and Airmen are protected against incursions of food and waterborne disease. Food safety spans the entire food chain, from farm production through consumption in the dining facility. Unfortunately, the finest food safety network can be rendered ineffective through poor hygiene and high risk behavior. As Field-Marshall Sir William Slim wrote in his memoirs of command of the 14th Army in Burma in 1942, Good doctors are no use without good discipline. More than half the battle against disease is fought, not by the doctors, but by the regimental officers. (29)

REFERENCES

(1.) Mead P, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis. 1999;5 (5):607-625.

(2.) Marano N, Pappaioanou M. Historical, new, and reemerging links between human and animal health. Emerg Infect Dis. 2004; 10(12):2065-2066.

(3.) King LJ, Anderson LR, Blackmore CG, et al. Executive summary of the AVMA One Health Initiative Task Force report. J Am Vet Med Assoc. 2008;233(2):259-261.

(4.) Bernard A, Fierens S. The Belgian PCB/dioxin incident: a critical review of health risks evaluations. Int J Toxicol. 2002; 21(5):333-340.

(5.) Vellinga A, Van Looke F. The dioxin crisis as experiment to determine poultry-related Campylobacter enteritis. Emerg Infect Dis. 2002; 8(1):19-22.

(6.) Proliferation: Threat and Response. Washington, DC: US Dept of Defense; January 2001.

(7.) Allen M. Rumsfeld To Remain At Pentagon, Thompson Quits at HHS, Warns of Vulnerabilities. Washington Post. December 4, 2004; A01. Available at: http://www.washingtonpost.com/ac2/wp-dyn/A33767-2004Dec3? language=printer. Accessed January 6, 2009.

(8.) Saelens M. Results of 1999 home food safety survey by Audits International to be announced. PR Newswire, 1999.

(9.) DeWaal C, Barlow K. Outbreak alert! Closing the gaps in our Federal food-safety net. Washington, DC: Center for Science in the Public Interest; 2002.

(10.) Grein T, Kamara K, Rodier G, et al. Rumors of disease in the global village: outbreak verification. Emerg Infect Dis. 2000; 6(2):97-102.

(11.) Lynch M, Painter J, Woodruff R, Braden C. Surveillance for foodborne-disease outbreaks--United States, 19982002. MMWR. Morb Mortal WklyRep. 2006; 55(SS10):1-34.

(12.) Jaykus L. Epidemiology and detection as options for control of viral and parasitic foodborne disease. Emerg Infect Dis. 1997; 3(4):529-539.

(13.) Petersen K, James W. Agents, vehicles, and causal inference in bacterial foodborne disease outbreaks: 82 reports (1986-1995). J Amer Vet Med Assoc. 1998; 212(12):1874-1881.

(14.) LeBaron C, Furutan N, Lew J, et al. Viral agents of gastroenteritis public health importance and outbreak management. MMWR. Morb Mortal WklyRep. 1990;39(RR-5):1-24.

(15.) Rangel J, Sparling P, Crowe C, Griffin P, Swerdlow D. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis. 2005;11(4):603-609.

(16.) Solomon E, Yaron S, Matthews K. Transmission of Escherichia coli O157:H7 from contaminated manure irrigation water to lettuce tissue and its subsequent internalization. Appl Environ Microbiol. 2002;68(1):397-400.

(17.) WiddowsonM, Sulka A, Bulens S, et al. Norovirus and foodborne disease, United States, 1991-2000. Emerg Infect Dis. 2005; 11(1):95-102.

(18.) Brown D, Gray J, MacDonald P, Green A, Morgan D. Outbreak of acute gastroenteritis associated with Norwalk-like viruses among British military personnel--Afghanistan, May 2002. MMWR. Morb Mortal Wkly Rep. 2002;51 (22):477-479.

(19.) Yoder J, Beach M. Cryptosporidiosis surveillance--United States, 2003-2005. MMWR. 2007; 56(SS-7):1-10.

(20.) Foodborne Outbreak of Cryptosporidiosis-Spokane, Washington, 1997. MMWR Morb Mortal Wkly Rep. 1998; 47:565-567.

(21.) Mackenzie WR, Hoxie NJ, Proctor ME, et al. A massive outbreak in Milwaukee of cryptosporidium infection transmitted through the public water supply. New Eng J Med. 1994; 331:161-167.

(22.) Peng M, Xiao L, Freeman A, Arrowood M, Escalante A, Weltman A. Genetic polymorphism among Cryptosporidium parvum isolates: evidence of two distinct human transmission cycles. Emerg Infect Dis. 1997;3 (4):567-573.

(23.) Roy S, Lopez A, Schantz P. Trichinellosis surveillance--United States, 1997-2001. MMWR. Morb Mortal WklyRep. 2003; 52(SS-6):1-8.

(24.) Clausen M, Meyer C, Krantz T, et al. Trichinella infection and clinical disease. QJM. 1996;89(8):631-636.

(25.) Laurichesse H, et al. Outbreak of trichinosis in France associated with eating horse meat. Commun Dis Rep CDR Rev. 1997; 7(5):R69-R73.

(26.) Trichinellosis Outbreaks-Northrhine-Westfalia, Germany, 1998-1999. MMWR. Morb Mortal Wkly Rep. 1999;48:488492.

(27.) Worley D, Seesee F, Espinosa B, Sterner M. Survival of sylvatic Trichinella spiralis isolates in frozen tissue and processed meat products. J Amer Vet Med Assoc. 1986; 189(9):1047-1049.

(28.) Worldwide Directory of Sanitarily Approved Food Establishments for Armed Forces Procurement. Fort Sam Houston, Texas: US Army Veterinary Command; June 4, 2008. Available at: http://vets.amedd .army.mil/VETSVCS/approved.nsf/a33b0b8376c838f586256f82007bf7b7/a981a3522fa3217e86256f 960052191f?OpenDocument.

(29.) Slim W. Defeat Into Victory. 2nd ed. London: Cassell and Company LTD; 1956:180.

COL Marc E. Mattix, VC, USAR

* The One Health Concept, first articulated by early scientists such as Rudolph Virchow, recognizes the intimate relationship between human health, animal health and the environment, and calls for an integrative, collaborative approach to health by encouraging the collaboration between experts of diverse fields of study. (3)

AUTHOR

COL Mattix is Assistant Chief, US Army Veterinary Corps for Mobilization and Reserve Affairs, Falls Church, Virginia.
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Date:Jan 1, 2009
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