BW-ch02.pdf

Food, Waterborne, and Agricultural Diseases

Chapter 2

FOOD, WATERBORNE, AND

AGRICULTURAL DISEASES

ZYGMUNT F. DEMBEK, P h D, MS, MPH * ; and EDWIN L. ANDERSON, MD †

INTRODUCTION

FOODBORNE AND WATERBORNE PATHOGENS AND DISEASES

PATHOGEN SUMMARY

WATER SUPPLY CONCERNS

AGRICULTURAL TERRORISM

FOOD AND WATER SECURITY

SUMMARY

* Lieutenant Colonel, Medical Service Corps, US Army Reserve; Chief, Biodefense Epidemiology and Education & Training Programs, Operational Medicine

Department, Division of Medicine, US Army Medical Research Institute of Infectious Diseases, 1425 Porter Street, Fort Detrick, Maryland 21702

† Colonel, Medical Corps, US Army; Physician, Division of Medicine, US Army Medical Research Institute of Infectious Diseases, 1425 Porter Street,

Fort Detrick, Maryland 21702; formerly, Deputy Chief, Division of Medicine, US Army Medical Research Institute of Infectious Diseases, 1425 Porter

Street, Fort Detrick, Maryland

Medical Aspects of Biological Warfare

INTRODUCTION

Food and waterborne pathogens cause a consider-

able amount of disease in the United States. A decade

ago, the US Department of Agriculture (USDA) es-

timated that medical costs and productivity losses

for diseases caused by the five leading foodborne

pathogens are as much as $6.7 billion per year. 1 Many

of the common foodborne pathogens, whether bacte-

ria, viruses, parasites, or toxins, can cause disease if

purposefully introduced into water or food sources.

These pathogens characteristically have the potential

to cause significant morbidity or mortality, have low

infective dose and high virulence, are universally

available, and are stable in food products or potable

water. These agents include ( a ) Clostridium botulinum

toxin, ( b ) the hepatitis A virus, ( c ) Salmonella , ( d ) Shi-

gella , ( e ) enterohemorrhagic Escherichia coli species, ( f )

Cryptosporidium parvum, (g) Campylobacter jejuni , ( h )

Listeria monocytogenes , and ( i ) Vibrio cholerae , among

others. Pathogens in the Centers for Disease Control

and Prevention (CDC) list of biological threat agents

that also may cause food or waterborne disease are

Bacillus anthracis , Brucella species, staphylococcal

enterotoxin B, and ricin. The potential for nonlisted

biological agents such as mycotoxins and parasites

(eg, Taenia sp) to be used in a bioterrorist event also

should be considered.

This chapter provides an introduction to the far-

reaching subjects of food and waterborne diseases, the

potential for terrorist attacks on the food and water

supply, and terrorism directed at the nation’s food-to-

farm continuum (agricultural terrorism). For a more

extensive review of these topics, readers may consult

more specialized texts on food 2 and waterborne 3 dis-

eases and agricultural terrorism. 4,5

FOODBORNE AND WATERBORNE PATHOGENS AND DISEASES

B anthracis is the causative agent of two forms of

foodborne anthrax: (1) oropharyngeal and (2) gas-

trointestinal. Although B anthracis would cause the

most potential harm via an aerosol release, anthrax

is not normally perceived as having bioterrorism po-

tential as a foodborne bacterial contaminant because

the infective dose required for such an attack would

be high. 6 However, given that the early diagnosis of

gastrointestinal anthrax is difficult and problematic for

clinicians who have never treated cases of this disease,

a higher mortality rate than expected may result from

a natural or purposeful outbreak. Anthrax spores are

resistant to disinfection by contact chlorination as used

by water treatment facilities, although higher levels of

chlorination (≥ 100 ppm) for longer contact times (5

minutes) will kill Bacillus spores. 7

C botulinum is the causative agent of botulism

intoxication, of which there are three natural mani-

festations: (1) classic, (2) wound, and (3) infant botu-

lism. A bioterrorism use of botulinum toxin would

possibly occur through inhalational intoxication, as

was considered by the Aum Shinrikyo cult in Japan. 8

C botulinum produces the most potent natural toxin

known; the human lethal dose of type A toxin is ap-

proximately 1.0 µg/kg. 9 There are seven antigenic

types of botulinum toxin, denoted by the letters A

through G. Most human disease is caused by types A,

B, and E. Botulinum toxins A and B are often associ-

ated with home food preparation 10 and home canning 11

and pickling. 12 Botulism-contaminated food cannot be

distinguished by visual examination, and the cook is

often the first to show the toxin’s effects (via sampling

the food during cooking). A 12- to 36-hour incubation

period is common. The incubation period is followed

by blurred vision, speech and swallowing difficulties,

and descending flaccid paralysis. 13

The current mortality rate associated with botulism

intoxication is less than 10%. Foodborne botulism

mortality during the 1950s (before the advent of

modern clinical therapies) was approximately 25%. 14

Little evidence of acquired immunity from botulinum

intoxication exists, even after a severe infection. Suc-

cessful treatment consists of aggressive trivalent (A,

B, E) botulinum antitoxin therapy and ventilatory

support. Early diagnosis is critical for patient survival.

Toxin can be found in food, stool, and serum samples,

which may all be used in the standard mouse model

assay to test for the presence of botulism toxin. 15

A recent controversial paper 16 explored the potential

for botulinum toxin contamination of the milk sup-

ply. A 9-stage cows-to-consumer supply chain was

examined, which accurately reflected a single milk-

processing facility. The release of botulinum toxin was

assumed to have occurred either at a holding tank at

the dairy farm, in a tanker truck transporting milk from

the farm to the processing plant, or at a raw milk silo

at the plant. By the use of this model, it was predicted

that 100,000 individuals could be poisoned with >1

gram of toxin, and 10 grams would affect about 568,000

milk consumers. 16 The National Academy of Sciences

published this information to foster further discussion

and alert authorities to the dangers to the milk supply

from purposeful contamination. 17 The paper describes

interventions that the government and the dairy in-

Food, Waterborne, and Agricultural Diseases

dustry could take to prevent this scenario. Officials

at the US Department of Health and Human Services

requested that this paper not be published. Regardless,

publication ensued because the The National Acad-

emy of Sciences was convinced that this information

would not enable bioterrorists to conduct an attack,

and that the paper itself would stimulate biodefense

efforts. However, whether this information presents a

”roadmap for terrorists” by exposing vulnerabilities in

food processing remains to be determined. 18

Campylobacter , Salmonella , Listeria , and E coli O157:

H7 can be transmitted zoonotically from contaminated

animal food sources. These bacteria species are ubiqui-

tous and cannot be restricted. C jejuni is the most com-

monly reported bacterial cause of foodborne infection

in the United States. Chronic sequelae associated with

C jejuni infections include Guillain-Barre syndrome 19

and arthritis. 20 Infants have the highest age-specific

isolation rate for this pathogen in the United States,

which is attributed to a greater susceptibility upon ini-

tial exposure and a lower threshold of seeking medical

treatment for infants. 21 Reservoirs for C jejuni include

wild fowl and rodents. 22 The intestines of poultry are

easily colonized with C jejuni , 23 and it is a commensal

inhabitant of the intestinal tract of cattle. 24 Antibiotic

resistance of Campylobacter is a growing concern for

poultry. 25 Campylobacter has a 100 to 1,000 cell infec-

tive dose, with poultry being the primary source of

infection in the United States. 26 Insect transmission by

several fly species has also been documented. 27 There

is a 3- to 5-day illness onset for campylobacteriosis and

a 1-week recovery time. Immunity is conferred upon

recovery, which accounts for a significantly higher

incidence rate among individuals younger than 2 years

of age in developing countries. 28

Salmonellosis is the second most common food-

borne illness, 29 and contaminated food is the principal

route of disease transmission. 30 There are over 2,400

Salmonella serotypes, many of which can cause gastro-

enteritis, manifested as diarrhea, abdominal pain, vom-

iting, fever, chills, headache, and dehydration. Other

diseases from Salmonella infections include enteric

fever, septicemia, and localized infections. Poultry is a

principal reservoir of the salmonellae. Water, shellfish,

raw salads, and milk also are commonly implicated as

vehicles for this pathogen. In humans, the most highly

pathogenic Salmonella species is S typhi . This bacte-

rium is the causative agent of typhoid fever, which

comprises about 2.5% of salmonellosis in the United

States. The symptoms of typhoid include septicemia,

high fever, headache, and gastrointestinal illness.

An immense outbreak of milk-borne salmonellosis

from Salmonella enteritica serovar typhimurium occurred

in northern Illinois in 1985, with more than 14,000 peo-

ple reported ill and five deaths. 31,32 A nonpurposeful

outbreak of this magnitude demonstrates what could

be initiated by bioterrorism. Cases also were reported

in the neighboring states of Indiana, Iowa, and Michi-

gan because the contaminated milk was distributed via

supermarket distribution systems. 33 Medical treatment

was complicated because the strain of S typhimurium

was found to be resistant to antibiotics. The cause of

the outbreak was the accidental comingling of raw milk

into the pasteurized product in the milk plant. 34

The earliest use of biological weapons by the Japa-

nese during World War II was the intentional poisoning

of wells with S typhimurium along the Russian border

of Mongolia in 1942. 35 In September and October 1984,

two large groups of salmonellosis cases occurred in

The Dalles, Oregon. Case interviews by health officials

associated patronage of two restaurants in The Dalles

with illness, especially with food items eaten from

salad bars. S typhimurium isolates were then obtained

from clinical specimens. 36 The size and nature of this

outbreak helped to initiate a criminal investigation,

which previously was almost never done in conjunc-

tion with a foodborne disease outbreak. The cause of

the epidemic became known when the Federal Bu-

reau of Investigation investigated a nearby cult (the

Rajneeshees) for additional criminal violations. 37 In

October 1985 authorities found an opened vial hold-

ing the original culture type of S typhimurium in the

Rajneeshee clinic laboratory.

Listeria monocytogenes is often found in silage, water,

and the environs of animal fodder. 38 Soft cheeses, 39 raw

or contaminated milk, 40 and contaminated refrigerated

foods 41 are often sources of this organism. Listeriosis

can result in meningo-encephalitis and septicemia in

neonates and adults, and fever and abortion in preg-

nant women. 42 Fetuses, the newborn, 43 the elderly, 44

and those immunocompromised 45 are at greatest risk

for serious illness. Listeriosis case investigations can

be problematic because of the variable incubation

period for illness (3 to > 90 days). Large outbreaks of

foodborne listeriosis have occurred, including a 1983

Massachusetts epidemic where improperly pasteur-

ized milk was the source of the infection. 46 The milk

originated from a group of farms at which listeriosis

occurred in dairy cows. Of the 49 infections associated

with this outbreak, 14 patients died.

E coli O157:H7 produces two verotoxins and has

emerged as a major cause of serious pediatric illness.

It can result in bloody diarrhea and hemolytic uremic

syndrome, which is defined as the demonstration of

three clinical conditions: (1) microangiopathic hemo-

lytic anemia, (2) acute renal failure, and (3) thrombo-

cytopenia. 47 Children younger than 5 years of age are

at greatest risk for hemolytic uremic syndrome when

Medical Aspects of Biological Warfare

infected with E coli O157:H7 or other enterohemor-

rhagic E coli species, and deaths from these infections

occur most often in the age ranges of 1 to 4 years and

61 to 91 years. 48

A major source of EHEC exposure is from consump-

tion of and contact with beef cattle. 49 About 20% of the

ground beef consumed in the United States is derived

from cull dairy cattle, which may be an important

contributor to this bacterial contamination of the food

supply. 50 For example, during July 2002, the Colorado

Department of Public Health and Environment identi-

fied an outbreak of E coli O157:H7 infections, which

linked 28 illnesses in Colorado and six other states to

the consumption of contaminated ground beef prod-

ucts. Seven patients were hospitalized; five developed

hemolytic uremic syndrome. 51 E coli contaminated food

items commonly result from use of cattle waste for

fertilizer, or coming into contact with cattle products.

Outbreaks have occurred from exposure to various E

coli -tainted food items, including alfafa 52 and radish 53

sprouts, parsley, 54 lettuce, 55 apple cider, 56 unpasteur-

ized gouda cheese, 57 raw milk, 58 recontaminated pas-

teurized milk, 59 and salami, 60 as well as through petting

zoos 61 and environmental transmission. 62,63 Waterborne

outbreaks with E coli O157:H7 also occur, thereby

demonstrating the potential for such contamination

from a purposeful effort. From mid-December 1989 to

mid-January 1990, 243 cases of gastrointestinal illness

from antibiotic-resistant E coli O157:H7 occurred in a

rural Missouri township as a result of an unchlorinated

water supply. 64 Swimming water-associated outbreaks

of E coli O157:H7 also have occurred. 65,66

Humans are the major reservoir for Shigella and the

primary source of subsequent infections. It is thought

that worldwide Shigella -associated illness causes about

165 million cases per year, of which fewer than 1%

occur in industrialized nations. 67 Shigella dysenteriae

produces severe disease, may be associated with life-

threatening complications, and causes about 25,000

cases of illness each year in the United States. Four

serogroups (A through D) cause approximately 80%

of shigellosis cases in the United States. Immunity

is serotype-specific, 68 vaccine development has been

problematic, 69 and the species can easily become re-

sistant to antibiotics. 70 Infants and young children are

most susceptible to shigellosis, attributable in part to

toiletry behaviors and child care practices. Although

not an environmentally hardy organism, Shigella is

highly infectious and can be very persistent in a close

community environment. 71 The infectious dose for

Shigella is from 10 to 100 organisms, and Shigella con-

tamination can cause outbreaks associated with food,

water, and milk. Shigellosis also has been associated

with recreational swimming. 72 Shigellosis is readily

transferred from person-to-person contact and through

fomites; 73 it can also be transmitted by insect vectors

(primarily flies). 74 There is a 1- to 3-day incubation

period for shigellosis. Shigella organisms are shed for 3

to 5 weeks after symptoms cease, ultimately contribut-

ing to a greater person-to-person spread than in other

enteric pathogens such as Salmonella and V cholerae .

Cryptosporidium , a protozoan and an obligate intracel-

lular parasite, can cause food and waterborne illness and

can also be acquired from exposure to contaminated rec-

reational water. 75-79 Seroprevalence surveys indicate that

about 20% of the US population have been infected with

Cryptosporidium by adulthood. 80 The severity and course

of infection can vary considerably, dependent upon the

immune status of the individual. Intestinal cryptospo-

ridiosis is often characterized by severe watery diarrhea

but may, alternatively, be asymptomatic. Pulmonary

and tracheal cryptosporidiosis in humans is associated

with coughing and low-grade fever; these symptoms

are often accompanied by severe intestinal distress. The

duration of illness in one study of 50 healthy individuals

varied from 2 to 26 days, with a mean of 12 days. 81 The

precise infectious dose is unknown; research indicates

that a range of 9 to 1,024 oocysts will initiate infection. 82

The pathobiology is not completely known; however,

the intracellular stages of the parasite can cause severe

tissue alteration. Infected food handlers are a major

contributor to disease transmission. Consequently,

cryptosporidiosis incidence is higher in facilities that

serve uncooked foods, such as restaurants with salad

bars. Child care centers can be a problematic source of

cryptosporidium infection because diarrhea in children

in diapers can be difficult to contain. 83 A significant

reservoir worldwide for Cryptosporidium parvum is do-

mestic livestock, predominately cattle. 84 Drinking-water

outbreaks have affected as many as 403,000 individuals

in a 1993 outbreak in Milwaukee. 85 The water in the

Milwaukee system was both filtered and chlorinated. 86

This organism’s resistance to chlorine treatment ensures

that it will remain a concern in treated potable water, 87

and therefore a risk to immunocompromised individu-

als for whom this organism causes severe and chronic

life-threatening gastroenteritis. 88

Humans are the source of the Hepatovirus hepatitis

A virus. Illness caused by hepatitis A is characterized

by sudden onset of fever, malaise, nausea, anorexia,

and abdominal discomfort, followed by jaundice. The

infectious dose is not precisely known but is thought

to be 10 to 100 virus particles. The virus is hardy, and

it survives on hands and fomites. Because viral par-

ticles are excreted in the feces during clinical illness,

stringent personal hygiene is crucial to prevent disease

transmission. Hepatitis A is commonly transmitted via

personal contact, and fewer than 5% of all hepatitis A

Food, Waterborne, and Agricultural Diseases

cases are demonstrated to have been caused by food

or waterborne transmission. 89 Permanent immunity

to hepatitis A is assumed subsequent to infection 90 or

immunization completion. 91 The advent of nationwide

hepatitis A vaccination programs is gradually causing

a decrease in disease incidence and susceptible popu-

lation. 92 As a result of these successful immunization

programs, hepatitis A may in time cease to be a public

health concern. 93

The potential for hepatitis A virus transmission

in drinking water was demonstrated in the hepatitis

A outbreak among members of the varsity football

team at the College of the Holy Cross in Worcester,

Massachusetts, in 1969. Although 90 of 97 players and

coaches on the team became ill (93% attack rate), sero-

logic testing performed years later revealed that only

33 had IgM anti-hepatitis A virus in serum (34% attack

rate). 94 Because of this discrepancy, the illness may have

been caused by another pathogen present in the water.

The same water supply was used for both irrigation

and potable water. Water used by firefighters to battle

a blaze nearby caused a drop in water pressure, and

back-siphonage brought groundwater into the football

practice field’s irrigation system. The groundwater

had been contaminated by children infected with

hepatitis A in a building immediately adjacent to the

playing field. The football team members became ill

after consuming the water from a faucet hooked up to

this contaminated water source. 95,96

Fungi are plant pathogens that can cause both my-

coses (infections) and mycotoxicoses (exposures to

toxic fungal metabolites that may be dietary, dermal,

or respiratory). Mycotoxins are ubiquitous worldwide

toxic fungal metabolites and contaminants of stored

cereal grains. 97,98 Although they are not on the CDC

threat list, mycotoxins (including aflatoxin B1, ochra-

toxin, T-2 toxin, deoxynivalenol [DON], and nivalenol

[NIV], and others), often have oncogenic properties

from chronic exposure, and may also have potential

for use as small-scale biological weapons. The fact that

these toxins are found naturally in commercially avail-

able cereal-based foods, including bread and related

products, noodles, breakfast cereals, baby and infant

foods, and rice, indicates that a ready substrate for

growth is available and purposeful contamination of

these foodstuffs is possible. Mycotoxicoses are often

undiagnosed and hence unrecognized by public health

authorities, except when large numbers of people are

affected. 99 The symptoms of mycotoxicosis depend

on the type of mycotoxin; the amount and duration

of exposure; the age, health, and sex of the exposed

individual; and many unknown synergistic effects

including genetics, dietary status, and interactions

with other toxic insults. 100

Large naturally occurring outbreaks of trichothecene

intoxications have occurred, including an outbreak af-

fecting 130,000 people in the Anhui province in China

in 1991 caused by moldy wheat and barley. Fusarium

mycotoxins including DON and NIV have also been

discovered in corn samples in Linxian, China, in posi-

tive correlation with the incidence of esophageal can-

cer. 101,102 A large exposure of trichothecene mycotoxin

from moldy grain and bread in Orenburg, Russia, in

1944 caused alimentary toxic aleukia and subsequent

mortality in at least 10% of the population. 103 Although

outbreaks of mycotoxicoses have decreased greatly as

a result of increases in hygiene measures, they still oc-

cur in developing countries, 104 are considered a serious

international health problem, 105 and are also a risk for

domestic animals. 105-107

The history of mycotoxin use as a biological weapon

includes efforts by Iraq’s biological weapon program to

develop and use aflatoxins during the 1980s. Strains of

Aspergillus flavus and A parasiticus were cultured, and

2,300 liters of concentrated toxin were extracted. This

aflatoxin was used mostly to fill missile warheads, and

the remainder was kept stockpiled. 108,109 The Soviet

Union is suspected of deploying trichothecene toxins

(NIV, DON, and T-2) in the “yellow rain” incidents in

Laos and Cambodia during the 1980s. Whether the

toxin exposures that occurred at that time were the

result of purposeful 110 or natural 111 events has never

been completely resolved. These events indicate the

potential for mycotoxin use as a biological weapon or

bioterrorism agent.

Parasites such as tapeworms (eg, Taenia sp) may

have the potential for use as agents of bioterrorism.

It is conceivable that, for example, a culture of Taenia

solium eggs be poured onto a salad bar or into water,

and be ingested and cause illness. Symptoms of taeniasis

from ingestion of the eggs would include cysticercosis,

which would not appear for weeks to years following

infection. However, this infection timeline should not

eliminate parasites from consideration as having the

potential for bioterrorist use. In their novel The Eleventh

Plague , Marr and Baldwin present just such a scenario,

with devastating effects. 112 T solium has the potential

to be transmitted from person-to-person through food

handlers with poor personal hygiene, adding to the

spread of the outbreak. 113 Such an outbreak may go

undiagnosed for an additional period, during which

ill persons are seen by healthcare providers unfamiliar

with tapeworm infections. A purposeful outbreak of

giardiasis that occurred in Edinburgh, Scotland, in 1990

demonstrates that parasites can be used for bioterrorism.

Nine individuals living in the same apartment complex

developed giardiasis subsequent to the purposeful fecal

contamination of an unsecured water supply. 114

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