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Military Preventive Medicine: Mobilization and Deployment, Vol 2 Chapter 37 Diseases Transmitted by Food, Water, and Soil
Diseases Transmitted by Food, Water, and Soil
Chapter 37
DISEASES TRANSMITTED BY FOOD,
WATER, AND SOIL
DAVID N. TAYLOR, MD
SHARON L. LUDWIG, MD, MPH
LEONARD N. BINN, P
H
D
JAMES FLECKENSTEIN, MD
JOSE L. SANCHEZ, MD, MPH
WILLIAM A. PETRI, JR., MD, P
H
D
JOANNA M. SCHAENMAN, P
H
D
CHARLES W. HOGE, MD
JOHN H. CROSS, P
H
D
W. PATRICK CARNEY, MPH, P
H
D
NAOMI E. ARONSON, MD
DUANE R. HOSPENTHAL, MD, P
H
D
MAY-ANN LEE, P
H
D
ERIC P. H. YAP, MBBS, DP
HIL
DIARRHEA CAUSED BY
ESCHERICHIA COLI
CAMPYLOBACTER ENTERITIS
VIRAL GASTROENTERITIS
TYPHOID FEVER
NONTYPHOIDAL SALMONELLOSIS
SHIGELLOSIS
CHOLERA
AMEBIASIS
GIARDIASIS
ENTERIC COCCIDIA INFECTIONS
HELMINTHS
SCHISTOSOMIASIS
COCCIDIOIDOMYCOSIS
HISTOPLASMOSIS
MELIOIDOSIS
999
Military Preventive Medicine: Mobilization and Deployment, Volume 2
D.N. Taylor
, MD, Colonel, Medical Corps, US Army (Retired); Department of International Health, Johns Hopkins University
Bloomberg School of Public Health, 624 North Broadway, Baltimore, MD 21205; Formerly, Research Coordinator for Prevention of
Diarrheal Disease, Division of Communicable Diseases and Immunology, Walter Reed Army Institute of Research, Silver Spring,
Maryland
S.L. Ludwig
, MD, MPH, Commander, US Public Health Service, Operational Preventive Medicine/Epidemiology Staff Officer, US
Coast Guard Commandant (G-WKH-1), 2100 Second Street SW, Washington DC 20593
L.N. Binn
, PhD; Supervisory Research Microbiologist, Department of Virus Diseases, Division of Communicable Diseases and
Immunology, Walter Reed Army Institute of Research, Silver Spring, MD 20910-7500
J. Fleckenstein
, MD; Assistant Professor of Medicine, Departments of Medicine and Molecular Sciences, Infectious Disease Divi-
sion, University of Tennessee Health Science Center and Veterans Affairs, 1030 Jefferson Avenue, Memphis, TN 38104; Formerly:
Lieutenant Colonel, Medical Corps, US Army; Infectious Disease Service, Walter Reed Army Medical Center, Washington, DC
20307
J.L. Sanche
z, MD, MPH, Colonel, Medical Corps, US Army; Medical Epidemiologist and Military Chief, Global Epidemiology and
Threat Assessment, HIV Research Program, Walter Reed Army Institute of Research, 13 Taft Court, Rockville, MD 20850
W.A. Petri, Jr
., MD, PhD; Professor of Medicine, Microbiology, and Pathology, Division of Infectious Diseases, Room 2115, MR4
Building, University of Virginia Health Sciences Center, Charlottesville VA 22908
J.M. Schaenman
, PhD; Chief Resident, Department of Internal Medicine, Stanford University School of Medicine, 300 Pasteur
Drive, Stanford, CA 94305
C.W . Hoge
, MD, Colonel, Medical Corps, US Army; Chief, Department of Psychiatry and Behavioral Sciences, Division of Neurop-
sychiatry, Walter Reed Army Institute of Research, Silver Spring, MD 20910-7500; Formerly, Principal Investigator, Department of
Enteric Infections, Division of Communicable Diseases and Immunology, Walter Reed Army Institute of Research
J.H. Cross
, PhD; Professor of Tropical Public Health, Uniformed Services University of the Health Sciences, 4301 Jones Bridge
Road, Bethesda MD 20814-4799
W.P. Carney
, MPH, PhD, Captain, MSC, US Navy (Ret.); Professor, Department of Preventive Medicine and Biometrics, Uniformed
Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD 20814-4799
N.E. Aronson
, MD, Colonel, Medical Corps, US Army; Director, Infectious Diseases Division, Room A3058, Uniformed Services
University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD 20814
D.R. Hospenthal
, MD, PhD, Lieutenant Colonel, Medical Corps, US Army; Chief, Infectious Disease Service, Brooke Army Medical
Center, 3851 Roger Brooke Drive, Fort Sam Houston, TX 78234-6200
M-A. Lee
, PhD; Programme Head, Defence Medical and Environmental Research Institute, @DSO National Laboratories, 27 Medi-
cal Drive, Singapore 119597
E.P.H. Yap
, MBBS, DPhil; Programme Head, Defence Medical and Environmental Research Institute, @DSO National Laboratories,
27 Medical Drive, Singapore 119597
1000
Diseases Transmitted by Food, Water, and Soil
DIARRHEA CAUSED BY
ESCHERICHIA COLI
Escherichia coli
is a gram-negative, facultatively
anaerobic, rod-shaped bacterium that is generally
a normal, nonpathogenic inhabitant of the intestine
of mammals. It is a member of the large family of
bacteria known as the Enterobacteriaceae, which
also includes salmonellae and shigellae.
E coli
that
compose the normal intestinal flora may become
pathogenic when seeded outside the intestine, as a
cause of sepsis, focal infections, or wound infec-
tions.
E coli
may acquire virulence factors that ren-
der them pathogenic to humans in the gut. These
virulence factors are usually stabile genetic charac-
teristics that are passed on from generation to gen-
eration resulting in a stable clone or strain.
Four general categories of
E coli
have been rec-
ognized as enteric pathogens:
1
Enterotoxigenic
E coli
(ETEC), enterohemorrhagic
E coli
(EHEC), entero-
invasive
E coli
(EIEC), and enteropathogenic
E coli
(EPEC). EPEC organisms are part of a larger group
generally referred to as enteroadherent
E coli
.
disease has accompanied military campaigns for
centuries,
6
but traveler’s diarrhea was only de-
scribed as a clinical syndrome after World War II
when travel to exotic locations by air became more
feasible.
7
It was not until the early 1970s that ETEC
was recognized as an enteric pathogen in both hu-
mans and animals.
8
One of the first known ETEC
outbreaks occurred in British troops stationed in
Aden in the Persian Gulf region in the 1960s.
9
Rowe
identified a single
E coli
serotype (O148:H28) as the
cause of illnesses that occurred in the first few
weeks of the deployment. These strains of
E coli,
as
well as others (O6:H16) from US military forces
serving in Vietnam, were shown to be pathogenic
in volunteers and were subsequently found to pro-
duce enterotoxins.
10
Ever since, ETEC has been
found to be an important cause of diarrhea during
many deployments in the developing world, most
notably the Middle East and Africa (Table 37-1). Di-
arrheal disease was a major problem during the
Persian Gulf War,
11
and ETEC and
Shigella
organisms
caused the majority of these illnesses (Table 37-2).
Enterotoxigenic
Escherichia coli
Introduction and Military Relevance
Description of the Pathogen
ETEC is one of the most common causes of diar-
rheal diseases among children in developing coun-
tries
2,3
and is the most common cause of traveler’s
diarrhea acquired in those countries.
4,5
Diarrheal
ETEC produces either a heat-labile toxin (LT), a
heat-stable toxin (ST), or both toxins (LT/ST). The
isolation rates of ETEC producing these toxins from
persons with diarrhea varies from survey to sur-
TABLE 37-1
ISOLATION RATES OF ENTEROTOXIGENIC
ESCHERICHIA COLI
AMONG PERSONNEL ON
MILITARY DEPLOYMENTS (1987–1993)
Number
Percentage
Exercise (Country)
Year
cultured
ETEC
Reference
Operation Restore Hope (Somalia)
1992-1993
113
16
1
Operation Desert Shield (Saudi Arabia)
1990
432
29
2
Operation Bright Star (Egypt)
1989
104
57
3
USS Kennedy (Alexandria, Egypt
*
)
1988
118
34
4
Operation Bright Star (Egypt)
1987
183
33
5
*
port visit
References: (1) Sharp TW, Thornton SA, Wallace MR, et al. Diarrheal disease among military personnel during Operation Restore
Hope, Somalia, 1992-1993.
Am J Trop Med Hyg
. 1995;52:188–193. (2) Hyams KC, Bourgeois AL, Merrell BR, et al. Diarrheal disease
during Operation Desert Shield.
N Engl J Med
. 1991;325:1423–1428. (3) Taylor DN, Sanchez JL, Candler W, Thornton S, McQueen C,
Echeverria P. Treatment of travelers’ diarrhea: Ciprofloxacin plus loperamide compared with ciprofloxacin alone; a placebo-
controlled, randomized trial.
Ann Intern Med
. 1991;114:731–734. (4) Scott DA, Haberberger RL, Thornton SA, Hyams KC. Norfloxacin
for the prophylaxis of travelers’ diarrhea in U.S. military personnel.
Am J Trop Med
Hyg
. 1990;42:160–164. (5) Haberberger RL Jr,
Mikhail IA, Burans JP, et al. Traveler’s diarrhea during joint American–Egyptian armed forces exercises in Cairo, Egypt.
Mil Med
.
1991;156:27–30.
1001
Military Preventive Medicine: Mobilization and Deployment, Volume 2
TABLE 37-2
nated with human feces used as fertilizer or with
untreated sewage. During the Persian Gulf War,
vegetables acquired from local markets were an
important source of contamination. Decontamina-
tion of salad vegetables in chlorinated water was
unsuccessful because the volume of food required
was too great to allow for the proper contact time.
15
Geographic Distribution
. In tropical climates,
disease caused by ETEC occurs year-round; in more
temperate climates, disease is more common in the
warmer summer months. In the developed world,
ETEC is a rare cause of diarrhea, and almost all of
the epidemiologic data that are available is from
foodborne or waterborne outbreaks.
16–18
Incidence
. Diarrhea caused by ETEC is a major
health problem for infants and children in the de-
veloping world and is the major cause of traveler’s
diarrhea in those traveling to the developing world.
Studies in areas of the developing world where
hygiene is poor suggest that exposure to ETEC is
nearly constant. Under these circumstances, the level
of immunity is the key factor in determining suscep-
tibility to disease. Infants and newly arriving travel-
ers have the least immunity and more frequently
develop severe diarrhea when infected. After repeated
exposure, illnesses become less severe or less symp-
tomatic. Because ETEC is endemic in developing
countries, outbreaks are rare except in new arriv-
als, such as travelers. During the build-up stages
of the Persian Gulf War (August to October 1990),
diarrhea affected as many as 5% of the service mem-
ber strength per week (Figure 37-1).
BACTERIAL ENTEROPATHOGENS IDENTIFIED
IN STOOL SAMPLES FROM 432 US MILITARY
PERSONNEL WITH ACUTE GASTROENTERITIS
DURING OPERATION DESERT SHIELD
Isolation Rate
Enteropathogen
Number Percent
ETEC
*
Heat-labile toxin
15
3.5
Heat-stable toxin
44
10.2
Heat-labile and heat-stable toxin
64
14.8
Mixed ETEC infection
2
0.5
Total of ETEC
125
28.9
Shigella
organisms
S dysenteriae
4
0.9
S flexneri
12
2.8
S boydii
8
1.9
S sonnei
89
20.6
Total of
Shigella
organisms
113
26.2
EIEC
†
3
0.7
Salmonella
7
1.6
Campylobacter
2
0.5
*
Enterotoxigenic
E coli
†
Enteroinvasive
E coli
Reprinted from: Hyams KC, Bourgeois AL, Merrell BR, et al.
Diarrheal disease during Operation Desert Shield.
N Engl J Med
.
1991;325:1423–1425. Copyright © 1991 Massachusetts Medical
Society. All rights reserved.
Pathogenesis and Clinical Findings
vey, but in most studies the isolation rates of each
toxin type are approximately equal.
12
Strains pro-
ducing ST or LT/ST are more pathogenic than
strains producing only LT and belong to a small
number of O:H serotypes; most have recognized
intestinal cell adherence or colonization factors.
1
Strains producing only heat-labile toxin belong to
a much larger number of O:H serotypes and often
do not possess known colonization factors.
12
ETEC can cause a severe watery diarrhea similar
to cholera. ETEC must adhere to the small intesti-
nal mucosa to cause disease. ETEC adherence is
mediated by fimbriae on the surface of the organ-
ism. These fimbriae, called colonization factor an-
tigens, are encoded by plasmids that usually encode
heat stable toxin and often heat labile toxin.
1
The
pathophysiology of diarrhea caused by ETEC is
primarily determined by the production of these
enterotoxins. Similar to cholera toxin, heat labile toxin
is composed of one A subunit and 5 B subunits that
bind to ganglioside GM1 on eucaryotic cell surfaces.
The A subunit undergoes proteolytic cleavage that
produces two fragments designated A1 and A2. The
A1 fragment activates adenylcyclase and increases
cyclic adenosine monophosphate through adenos-
ine diphosphate ribosylation of the cell membrane,
which causes fluid secretion by inhibiting sodium
and chloride absorption and chloride secretion.
Epidemiology
Transmission
.
Most epidemiologic studies have
implicated contaminated foods as the main source
of ETEC. The human reservoir is large, and fecal
spread to food via hands is probably the main
method of contamination.
13,14
ETEC can also be iso-
lated from domestic animals, and contamination of
meats with intestinal contents may be another im-
portant source in food. Vegetables can be contami-
1002
Diseases Transmitted by Food, Water, and Soil
ETEC causes a secretory diarrhea with fluid and
electrolyte loss without evidence of inflammation.
The amount of diarrhea may be mild or massive,
cholera-like purging. Generally, an inoculum of
about 10
8
organisms is required to infect 50% of
persons exposed.
10
Disease severity increases with
inoculum size and may also be associated with the
quantity of toxin produced by the organism. In trav-
elers, disease occurs most commonly in the first
weeks of travel. The incubation period ranges from
12 to 48 hours and shortens with higher inoculum
size. Symptoms that accompany ETEC diarrhea are
malaise, anorexia, abdominal cramping, nausea,
vomiting in 25%, and low-grade fever in 30%. Un-
treated the illness lasts 1 to 5 days but can last as
long as 2 weeks. Stool frequency is usually around
10 episodes per day for 1 or 2 days.
7,19
Complica-
tions are usually associated with dehydration.
These include lethargy, muscle cramping, loss of
consciousness, renal failure, and death. Infants and
children may have a decreased absorptive capacity
of the small bowel for several weeks after the ill-
ness, which can lead to malnutrition.
Diagnostic Approaches
E coli
is a gram-negative rod that grows readily
on routine culture media under aerobic conditions.
E coli
is identified on MacConkey agar as a lactose-
fermenter.
E coli
can be isolated after several days
from fecal specimens preserved in Cary-Blair trans-
port media. There is no biochemical or serological
4.0
Fresh fruits and
vegetables banned
3.0
2.0
1.0
0.0
26 2 9 16 23 30 7 14 21 28 4 11 18 25 2 9 16 23 30 6 13 20 27 3 10 17 24 3 10 17 24 31
Aug Sep
Oct
Nov
Dec
Jan
Feb
Mar
Weekly reporting date
Fig. 37-1
. This graph shows the weekly rates of gastroenteritis among 40,000 Marine Corps ground troops stationed
in northeast Saudi Arabia in 1990 and 1991. The arrow indicates when fresh produce was removed from their diet,
which was followed by a sharp decrease in the diarrheal disease incidence.
Reprinted with permission from: Hyams KC, Hanson K, Wignall FS, Escamilla J, Oldfield EC III. The impact of
infectious diseases on the health of US troops deployed to the Persian Gulf during Operations Desert Shield and
Desert Storm.
Clin Infect Dis
. 1995;20:1497–1504.
1003
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