This report is being reprinted with the permission of the American Medical
Association; the Center for Food Safety and Nutrition, Food and Drug Administration; and the
Food Safety and Inspection Service, U.S. Department of Agriculture. It is reprinted as
a courtesy to the MMWR readership.
PREFACE
Foodborne illness is a serious public health problem. The Centers for Disease Control
and Prevention (CDC) estimates that each year 76 million people get sick, more than 300,000
are hospitalized, and 5,000 Americans die as a result of foodborne illnesses, primarily the
very young, elderly, and the immunocompromised. Recent changes in human demographics
and food preferences, changes in food production and distribution systems, microbial
adaptation, and lack of support for public health resources and infrastructure have led to the
emergence of novel as well as traditional foodborne diseases. With increasing travel and
trade opportunities, it is not surprising that the risk of contracting and spreading a
foodborne illness now exists locally, regionally, and even globally.
Physicians have a critical role in the prevention and control of
food-related disease
outbreaks. This primer is intended to help physicians in this role by providing them with
practical and concise information on the diagnosis, treatment, and reporting of foodborne illnesses.
It was developed collaboratively by the American Medical Association, the Centers for
Disease Control and Prevention, the Food and Drug Administration's Center for Food Safety
and Applied Nutrition, and the US Department of Agriculture's Food Safety and Inspection
Service as part of President Clinton's National Food Safety Initiative.
We encourage you to review this information and participate in the attached
continuing medical education (CME) program. Even if you choose not to participate in the CME
component, please take time to complete and return the "Program Evaluation Form." Your
feedback is valuable for updating this primer and for planning future physician education programs.
E. Ratcliffe Anderson, Jr., MD Executive Vice President, CEO
American Medical Association
Jeffrey Koplan, MD, MPH Director
Centers for Disease Control and Prevention
Jane E. Henney, MD Commissioner
Food and Drug Administration
Thomas J. Billy Administrator
Food Safety and Inspection Service
US Department of Agriculture
Writers, Reviewers, Contributors
Writing/Working Group
American Medical Association L J Tan, PhD (Working Group Chair)
Jim Lyznicki, MS, MPH
Centers for Disease Control and Prevention Penny M. Adcock, MD
Eileen Dunne, MD, MPH
Julia Smith, MPH
Center for Food Safety and Applied Nutrition
Food and Drug Administration Eileen Parish, MD
Arthur Miller, PhD
Howard Seltzer
Food Safety and Inspection Service
US Department of Agriculture Ruth Etzel, MD, PhD
Reviewers/Contributors
The following organizations and individuals reviewed drafts of this document and
provided valuable comments:
American Academy of Family Physicians
American Academy of Pediatrics
American Association of Public Health Physicians
American College of Emergency Physicians
American College of Preventive Medicine
Association of State and Territorial Health Officials
Council of State and Territorial Epidemiologists
Infectious Diseases Society of America
Peter Chien, Jr.
American Medical Association
Student Section
AdHoc Committee on Scientific Issues
Chicago, IL
Michael Crutcher, MD, MPH
Oklahoma State Department of Health
Oklahoma City, OK
Jeffrey Davis, MD, MPH
Wisconsin Department of Health and Family Services
Madison, WI
Roy Dehart, MD
Center for Occupational and Environmental Medicine
Nashville, TN
B. Clair Eliason, MD
University of Illinois
School of Medicine at Rockford
Rockford, IL
Richard Guerrant, MD
Health Sciences Center
University of Virginia
Charlottesville, VA
Bennett Lorber, MD
Temple University School of Medicine
Philadelphia, PA
Dale Morse, MD
New York State Department of Health
Albany, NY
Michael Moser, MD, MPH
Kansas Department of Health and Environment
Topeka, KS
Margaret Neill, MD
Memorial Hospital of Rhode Island
Pawtucket, RI
Michael Osterholm, PhD, MPH
ican, Inc.
Eden Prairie, MN
Louis Pickering, MD
National Immunization Program
Centers for Disease Control and Prevention
Atlanta, GA
Christopher Shearer, MD
Phoenix Baptist Hospital
Family Medicine Center
Phoenix, AZ
Melvyn Sterling, MD, FACP
University of California
Irvine, CA
Made Sutjita, MD, PhD
Morehouse School of Medicine
Atlanta, GA
Philip Tarr, MD
Children's Hospital and Regional
Medical Center
University of Washington
Seattle, WA
James Walker, DVM
Oklahoma State Department of Health
Oklahoma City, OK
William Weil, MD
Michigan State University
East Lansing, MI
Diagnosis and Management of Foodborne Illnesses:
A
Primer for Physicians
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
This activity has been planned and implemented in accordance with the Essential
Areas and Policies of the Accreditation Council for Continuing Medical Education (ACCME)
through the joint sponsorship of the Centers for Disease Control and Prevention (CDC), the Food
Safety and Inspection Services, US Department of Agriculture, and the Center for Food Safety
and Applied Nutrition, Food and Drug Association. CDC is accredited by the ACCME to
provide continuing medical education for physicians.
CDC designates this educational activity for a maximum of 3 hours in category 1
credit towards the AMA Physician's Recognition Award. Each physician should claim only
those hours of credit that he/she actually spent in the educational activity.
DIAGNOSIS AND MANAGEMENT
OF FOODBORNE ILLNESSES:
A PRIMER FOR PHYSICIANS
BACKGROUND
This primer is directed to primary care physicians, who are more likely to see
the index case of a potential food-related disease outbreak. It is a teaching tool to
update primary care physicians about foodborne illness and remind them of their
important role in recognizing suspicious symptoms, disease clusters, and etiologic agents,
and reporting cases of foodborne illness to public health authorities.
Specifically, this guide urges physicians to:
Recognize the potential for a foodborne etiology in a patient's illness;
Realize that many but not all cases of foodborne illness have
gastrointestinal tract symptoms;
Obtain stool cultures in appropriate settings, and recognize that testing for
some specific pathogens, e.g. E. coli O157:H7, Vibrio spp., must be requested;
Report suspect cases to appropriate public health officials;
Talk with patients about ways to prevent food-related diseases; and
Appreciate that any patient with foodborne illness may represent the
sentinel case of a more widespread outbreak.
Foodborne illness is considered to be any illness that is related to food
ingestion; gastrointestinal tract symptoms are the most common clinical manifestations
of foodborne illnesses. This document provides detailed summary tables and
charts, references, and resources for healthcare professionals. Patient scenarios and
clinical vignettes are included for self-evaluation and to reinforce information presented in
this primer. Also included is a CME component worth 3 credit hours.
This primer is not a clinical guideline or definitive resource for the diagnosis
and treatment of foodborne illness. Safe food handling practices and technologies
(e.g. irradiation, food processing and storage) also are not addressed. More
detailed information on these topics is available in the references and resources listed in
this document, as well as from medical specialists and medical specialty societies,
state and local public health authorities, and federal government agencies.
For additional copies, please contact:
L J Tan, PhD
American Medical Association
515 North State Street
Chicago, Illinois 60610
312 464-4147
312 464-5841 (fax) [email protected] (Email)
food-related disease threats are numerous and varied, involving biological
and nonbiological agents. Foodborne illnesses can be caused by microorganisms and
their toxins, marine organisms and their toxins, fungi and their related toxins, and
chemical contaminants. During the last 20 years, some foods that have been linked to
outbreaks include: milk (Campylobacter); shellfish (Norwalk-like viruses); unpasteurized
apple cider (Escherichia coli O157:H7), eggs
(Salmonella); fish (ciguatera poisoning); raspberries
(Cyclospora); strawberries (hepatitis A virus); and ready-to-eat
meats (Listeria).
While physicians have a critical role in surveillance for and prevention of
potential disease outbreaks, only a fraction of the people who experience gastrointestinal
tract symptoms from foodborne illness seek medical care. In those who do seek care
and submit specimens, bacteria are more likely than other pathogens to be identified
as causative agents. Bacterial agents most often identified in patients with
foodborne illness in the United States are
Campylobacter, Salmonella, and
Shigella species, with substantial variation occurring by geographic area and season. Testing for
viral etiologies of diarrheal disease is rarely done, but viruses are considered the
most common cause of foodborne illness.
This section and the Foodborne Illnesses
Tables summarize diagnostic features and laboratory testing for bacterial, viral, parasitic, and noninfectious causes of
foodborne illness. For more specific guidance, consult an appropriate medical specialist
or medical specialty society, as well as various resources listed in other sections of
this document. Also refer to this section and the
Foodborne Illnesses Tables when working through the
Patient Scenarios and Clinical
Vignettes of this primer.
RECOGNIZING FOODBORNE ILLNESSES
Patients with foodborne illnesses typically present with gastrointestinal
tract symptoms (e.g. vomiting, diarrhea, and abdominal pain); however,
nonspecific symptoms and neurologic symptoms may also occur. Every outbreak begins with
an index case who may not be severely ill. A physician who encounters this person
may be the only one with the opportunity to make an early and expeditious diagnosis.
Thus, the physician must have a high index of suspicion and ask appropriate questions
to recognize that an illness may have a foodborne etiology.
Important clues to determining the etiology of a foodborne disease are the:
Incubation period;
Duration of the resultant illness;
Predominant clinical symptoms; and
Population involved in the outbreak.
Additional clues may be derived by asking whether the patient has consumed
raw or poorly cooked foods (e.g. raw or undercooked eggs, meats, shellfish,
fish), unpasteurized milk or juices, home canned goods, fresh produce, or soft cheeses
made from unpasteurized milk. Inquire whether any of the patient's family members or
close friends has similar symptoms. Inquiries about living on or visiting a farm, pet
contact, day care attendance, occupation, foreign travel, travel to coastal areas,
camping excursions to mountains or other areas where untreated water is consumed,
and attendance at group picnics or similar outings also may provide clues for
determining the etiology of the illness.
If a foodborne illness is suspected, submit appropriate specimens for
laboratory testing and contact the state or local health department for advice about
epidemiologic investigation. For the physician, implication of a specific source in disease
transmission is difficult from a single patient encounter. Attempts to identify the source of
the outbreak are best left to public health authorities.
Because infectious diarrhea can be contagious and is easily spread, rapid
and definitive identification of an etiologic agent may help control a disease outbreak.
An individual physician who obtains testing can contribute the necessary piece of
data that ultimately leads to identification of the source of an outbreak.
DIAGNOSING FOODBORNE ILLNESSES
Differential Diagnosis
As shown in Table 1 and the Foodborne Illnesses
Tables a variety of infectious and noninfectious agents must be considered in patients suspected of having a
foodborne illness. Establishing a diagnosis can be difficult, however, particularly in patients
with persistent or chronic diarrhea, those with severe abdominal pain, and when there is
an underlying disease process. The extent of diagnostic evaluation depends on the
clinical picture, the differential diagnosis considered, and clinical judgment.
If any of the following signs and symptoms occur, alone or in
combination, laboratory testing may provide important diagnostic clues (particular attention
should be given to very young and elderly patients and to immunocompromised patients,
all of whom are more vulnerable):
Bloody diarrhea
Weight loss
Diarrhea leading to dehydration
Fever
Prolonged diarrhea (3 or more unformed stools per day, persisting several days)
Neurologic involvement such as paresthesias, motor weakness, cranial
nerve palsies
Sudden onset of nausea, vomiting, diarrhea
Severe abdominal pain
In addition to foodborne causes, a differential diagnosis of gastrointestinal
tract disease should include underlying medical conditions such as irritable
bowel syndrome; inflammatory bowel diseases such as Crohn's disease or ulcerative
colitis; malignancy; medication use (including antibiotic-related
Clostridium difficile toxin colitis); gastrointestinal tract surgery or radiation; malabsorption syndromes;
immune deficiencies; Brainerd diarrhea; and numerous other structural, functional,
and metabolic etiologies. Consideration also should be given to exogenous factors such
as the association of the illness with travel, occupation, emotional stress,
sexual practices, exposure to other ill persons, recent hospitalization, child care
center attendance, and nursing home residence.
The differential diagnosis of patients presenting with neurological symptoms due
to a foodborne illness is also complex. Possible food-related causes to consider
include recent ingestion of contaminated seafood, mushroom poisoning, and
chemical poisoning. Because the ingestion of certain toxins (e.g. botulinum toxin,
tetrodotoxin) and chemicals (e.g. organophosphates) can be life-threatening, a differential
diagnosis must be made quickly with concern for aggressive therapy and life support
measures (e.g. respiratory support, administration of antitoxin or atropine), and possible
hospital admission.
Clinical Microbiology Testing
When submitting specimens for microbiologic testing, it is important to realize
that clinical microbiology laboratories differ in protocols used for the detection
of pathogens. To optimize recovery of an etiologic agent, physicians should
understand routine specimen collection and testing procedures as well as circumstances
and procedures for making special test requests. Some complex tests (e.g. toxin
testing, serotyping, molecular techniques) may only be available from large commercial
and public health laboratories. Contact your microbiology laboratory for more information.
Stool cultures are indicated if the patient is immunocompromised, febrile,
has bloody diarrhea, has severe abdominal pain, or if the illness is clinically severe
or persistent. Stool cultures are also indicated if many fecal leukocytes are
present, which indicates diffuse colonic inflammation and is suggestive of invasive
bacterial pathogens such as Shigella,
Salmonella, and Campylobacter species, and invasive
E. coli. In most laboratories, routine stool cultures are limited to screening for
Salmonella and Shigella species, and
Campylobacter jejuni/coli. Cultures for
Vibrio and Yersinia species, E.
coli O157:H7, and Campylobacter species other than
jejuni/coli require additional media or incubation conditions and therefore require advance notification
or communication with laboratory and infectious disease personnel.
Stool examination for parasites generally is indicated for patients with
suggestive travel histories, who are immunocompromised, who suffer chronic or
persistent diarrhea, or when the diarrheal illness is unresponsive to appropriate
antimicrobial therapy. Stool examination for parasites is also indicated for gastrointestinal
tract illnesses that appear to have a long incubation period. Requests for ova and
parasite examination of a stool specimen will often enable identification of
Giardia lamblia and Entamoeba
histolytica, but a special request may be needed for detection
of Cryptosporidium parvum and Cyclospora
cayetanensis. Each laboratory may vary in
its routine procedures for detecting parasites so it is important to contact
your laboratory.
Blood cultures should be obtained when bacteremia or systemic infection
are suspected.
Direct antigen detection tests and molecular biology techniques are available
for rapid identification of certain bacterial, viral, and parasitic agents in clinical
specimens. In some circumstances, microbiologic and chemical laboratory testing of vomitus
or implicated food items also is warranted. For more information on
laboratory procedures for the detection of foodborne pathogens, consult an appropriate
medical specialist, clinical microbiologist, or state public health laboratory.
TREATING FOODBORNE ILLNESSES
Selection of appropriate treatment depends on identification of the
responsible pathogen (if possible) and determining if specific therapy is available. Many
episodes of acute gastroenteritis are self limiting and require fluid replacement and
supportive care. Oral rehydration is indicated for patients who are mildly to
moderately dehydrated; intravenous therapy may be required for more severe
dehydration. Because many antidiarrheal agents have potentially serious adverse effects in
infants and young children, their routine use is not recommended in this age group.
Choice of antimicrobial therapy should be based on:
Clinical signs and symptoms;
Organism detected in clinical specimens;
Antimicrobial susceptibility tests; and
Appropriateness of treating with an antibiotic (some enteric bacterial
infections are best not treated).
Knowledge of the infectious agent and its antimicrobial susceptibility pattern
allows the physician to initiate, change, or discontinue antimicrobial therapy. Such
information also can support public health surveillance of infectious disease and
antimicrobial resistance trends in the community. Antimicrobial resistance has increased for
some enteric pathogens, which requires judicious use of this therapy.
SURVEILLANCE AND REPORTING OF FOODBORNE ILLNESSES
Reporting of foodborne illnesses in the United States began more than 50
years ago when state health officers, concerned about the high morbidity and
mortality caused by typhoid fever and infantile diarrhea, recommended that cases of
"enteric fever" be investigated and reported. The intent of investigating and reporting
these cases was to obtain information about the role of food, milk, and water in outbreaks
of gastrointestinal tract illness as the basis for public health actions. These
early reporting efforts led to the enactment of important public health measures (e.g.
the Pasteurized Milk Ordinance) that profoundly decreased the incidence of
foodborne illnesses.
Often health care professionals may suspect foodborne illness either because
of the organism involved or because of other available information, such as several
ill patients who have eaten the same food. Health care professionals can serve as
the
eyes and ears for the health department by providing such information to the local
or state public health authorities. Foodborne disease reporting is not only important
for disease prevention and control, but more accurate assessments of the burden
of foodborne illness in the community occur when physicians report foodborne
illnesses to the local or state health department. In addition, reporting of cases of
foodborne illness by practicing physicians to the local health department may help the
health officer identify a foodborne disease outbreak in the community. This may lead to
early identification and removal of contaminated products from the commercial market. If
a restaurant or other food service establishment is identified as the source of
the outbreak, health officers will work to correct inadequate food preparation practices,
if necessary. If the home is the likely source of the contamination, health officers
can institute public education about proper food handling practices. Occasionally,
reporting may lead to the identification of a previously unrecognized agent of foodborne
illness. Reporting also may lead to identification and appropriate management of
human carriers of known foodborne pathogens, especially those with high-risk occupations
for disease transmission such as foodworkers.
Table 2 lists current reporting requirements for foodborne diseases and
conditions in the United States. National reporting requirements are determined
collaboratively by the Council of State and Territorial Epidemiologists and the Centers for
Disease Control and Prevention (CDC).
Typically, the appropriate procedure for physicians to follow in reporting
foodborne illnesses is to contact the local or state health department whenever they identify
a specific notifiable disease. However, it is often unclear if a patient has a
foodborne illness prior to diagnostic tests, so physicians should also report potential
foodborne illnesses, such as when two or more patients present with a similar illness that
may have resulted from the ingestion of a common food. Local health departments
then report the illnesses to the state health department and determine if
further investigation is warranted.
Each state health department reports foodborne illnesses to the CDC. The
CDC compiles this data nationally and disseminates information to the public
through annual summary reports. The CDC assists state and local public health authorities
with epidemiologic investigations and the design of interventions to prevent and
control food-related outbreaks. The CDC also coordinates a national network of public
health laboratories, called PulseNet, which perform "molecular fingerprinting" of bacteria
(by pulsed-field gel electrophoresis) to support epidemiolgic investigations.
Thus, in addition to reporting cases of potential foodborne illnesses, it is
important for physicians to report noticeable increases in unusual illnesses, symptom
complexes, or disease patterns (even without definitive diagnosis) to public health
authorities. Prompt reporting of unusual patterns of diarrheal/gastrointestinal tract illness,
for example, can allow public health officials to initiate an epidemiologic
investigation earlier than would be possible if the report awaited definitive etiologic diagnosis.
Finally, new information on food safety is constantly emerging.
Recommendations and precautions for people at high risk are updated whenever new data
about preventing foodborne illnesses become available. Physicians and other health
care professionals need to be aware of and follow the most current information on
food safety.
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
Foodborne Illnesses Table: Bacterial Agents
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
Foodborne Diseases and Conditions Designated as
Notifiable at the National Level -- United States 2000
In the United States, requirements for reporting diseases and conditions
are mandated by state and territorial laws and/or regulations. However, physicians
are highly encouraged to report foodborne illness that they may encounter in the
event that an outbreak situation may be present. Reporting will facilitate the tracking of
the outbreak and in fact, the case identified may even be the sentinel case!
Differences exist between states and territories as to which diseases
and conditions are reportable. The Council of State and Territorial Epidemiologists
(CSTE) and the Centers for Disease Control and Prevention (CDC) collaborate on
which diseases and conditions are designated as nationally notifiable. Details on
specific state requirements are located at http://www.cste.org/reporting%20requirements.htm. This information is also available by contacting CSTE at:
The Council of State and Territorial Epidemiologists (CSTE)
Suite 303; 2872 Woodcock Boulevard
Atlanta, Georgia 30341
Phone: 770 458-3811
Notifiable Bacterial Foodborne Diseases and Conditions
Toll-free Information Phone Numbers
USDA Meat and Poultry Hotline: 800 535-4555
FDA Safe Food Hotline: 888 SAFE-FOOD (723-3366)
CDC Voice Information System: 888 CDC-FAXX (232-3299)
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
Foodborne Illnesses Table: Viral Agents
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
Foodborne Diseases and Conditions Designated as
Notifiable at the National Level -- United States 2000
In the United States, requirements for reporting diseases and conditions
are mandated by state and territorial laws and/or regulations. However, physicians
are highly encouraged to report foodborne illness that they may encounter in the
event that an outbreak situation may be present. Reporting will facilitate the tracking of
the outbreak and in fact, the case identified may even be the sentinel case!
Differences exist between states and territories as to which diseases
and conditions are reportable. The Council of State and Territorial Epidemiologists
(CSTE) and the Centers for Disease Control and Prevention (CDC) collaborate on
which diseases and conditions are designated as nationally notifiable. Details on
specific state requirements are located at http://www.cste.org/reporting%20requirements.htm. This information is also available by contacting CSTE at:
The Council of State and Territorial Epidemiologists (CSTE)
Suite 303; 2872 Woodcock Boulevard
Atlanta, Georgia 30341
Phone: 770 458-3811
Notifiable Bacterial Foodborne Diseases and Conditions
Toll-free Information Phone Numbers
USDA Meat and Poultry Hotline: 800 535-4555
FDA Safe Food Hotline: 888 SAFE-FOOD (723-3366)
CDC Voice Information System: 888 CDC-FAXX (232-3299)
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
Foodborne Illnesses Table: Parasitic Agents
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
Foodborne Diseases and Conditions Designated as
Notifiable at the National Level -- United States 2000
In the United States, requirements for reporting diseases and conditions
are mandated by state and territorial laws and/or regulations. However, physicians
are highly encouraged to report foodborne illness that they may encounter in the
event that an outbreak situation may be present. Reporting will facilitate the tracking of
the outbreak and in fact, the case identified may even be the sentinel case!
Differences exist between states and territories as to which diseases
and conditions are reportable. The Council of State and Territorial Epidemiologists
(CSTE) and the Centers for Disease Control and Prevention (CDC) collaborate on
which diseases and conditions are designated as nationally notifiable. Details on
specific state requirements are located at http://www.cste.org/reporting%20requirements.htm. This information is also available by contacting CSTE at:
The Council of State and Territorial Epidemiologists (CSTE)
Suite 303; 2872 Woodcock Boulevard
Atlanta, Georgia 30341
Phone: 770 458-3811
Notifiable Bacterial Foodborne Diseases and Conditions
Toll-free Information Phone Numbers
USDA Meat and Poultry Hotline: 800 535-4555
FDA Safe Food Hotline: 888 SAFE-FOOD (723-3366)
CDC Voice Information System: 888 CDC-FAXX (232-3299)
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
Foodborne Illnesses Table: Non-Infectious Agents
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
Foodborne Diseases and Conditions Designated as
Notifiable at the National Level -- United States 2000
In the United States, requirements for reporting diseases and conditions
are mandated by state and territorial laws and/or regulations. However, physicians
are highly encouraged to report foodborne illness that they may encounter in the
event that an outbreak situation may be present. Reporting will facilitate the tracking of
the outbreak and in fact, the case identified may even be the sentinel case!
Differences exist between states and territories as to which diseases
and conditions are reportable. The Council of State and Territorial Epidemiologists
(CSTE) and the Centers for Disease Control and Prevention (CDC) collaborate on
which diseases and conditions are designated as nationally notifiable. Details on
specific state requirements are located at http://www.cste.org/reporting%20requirements.htm. This information is also available by contacting CSTE at:
The Council of State and Territorial Epidemiologists (CSTE)
Suite 303; 2872 Woodcock Boulevard
Atlanta, Georgia 30341
Phone: 770 458-3811
Notifiable Bacterial Foodborne Diseases and Conditions
Toll-free Information Phone Numbers
USDA Meat and Poultry Hotline: 800 535-4555
FDA Safe Food Hotline: 888 SAFE-FOOD (723-3366)
CDC Voice Information System: 888 CDC-FAXX (232-3299)
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
BOTULISM POISONING: PATIENT SCENARIO
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
This learning scenario can be used to reinforce medical management
information pertaining to foodborne illnesses, such as that provided from the other booklets of
this primer. This case study provides questions that need to be considered when
dealing with a potential case of foodborne illness. Answers are provided
immediately following the questions to enhance the learning process.
Similar learning scenarios are also available for other foodborne pathogens.
BOTULISM POISONING: A PATIENT SCENARIO
On Sunday morning at 6am, you receive a call from the wife of a 35-year-old
man who awoke complaining of dry mouth and blurred vision. His symptoms
rapidly progressed over the next 2 hours to include diplopia, dysphagia, and weakness in
his arms. You ask to talk with him directly, but he is having difficulty speaking. He
was previously healthy.
You meet them in the local emergency department. On physical examination, he
is afebrile with a heart rate of 80 beats per minute, a blood pressure of 120/80 mm
Hg, and a respiratory rate of 12 breaths per minute. His pulse oximetry is 98%
oxygen saturation. He has a hoarse voice, bilateral ptosis, a weak gag reflex, and
bilateral proximal upper extremity weakness. He has no lower extremity weakness.
Sensation is intact in all extremities. His mental status is normal.
What is the possible differential diagnosis for his
chief complaint?
Guillain-Barré Syndrome
Myasthenia gravis
Tick paralysis
Cerebral vascular accident
Botulism intoxication
Heavy metal (thallium, arsenic, lead) or organophosphate toxicity
What additional information would assist in the diagnosis?
Has he had a recent flu-like illness?
Has he had a recent gastrointestinal tract illness?
Has he had similar symptoms before?
Is there a family history of hypertension, stroke, or other neurological disorders?
Has he found any ticks on himself or recently been in a
tick-infested area?
Had he had any occupational or recreational exposure to heavy metals
or organophosphates?
Has he eaten any home-canned foods? What foods has he consumed in the last
72 hours?
Has anyone else in the home been ill?
The patient denies having a flu-like illness within the last month. Neither he nor
his family members have had similar symptoms. There is no family history of stroke
or other neurological disorders, and he does not have hypertension
or hypercholesterolemia. He has not discovered any ticks on himself or in
his
environment, and he has not been camping, hiking, or in any tick-infested area
within the last week. He has had no occupational or recreational exposures to heavy
metals or organophosphates. He denies eating any home-canned foods. He cannot
remember everything he ate during the last
72 hours, but recalls eating lunch at a coffee shop near his office. He and his
wife hosted a barbeque one evening at which they served grilled chicken, vegetables,
and homemade ice cream. The night before onset of his symptoms, they ate at
their favorite Italian restaurant where they shared a calamari appetizer, had salad
prepared by the waiter at the table, and shared an entree of Fettuccine Fra Diablo. They
finished the meal with a cappuccino and tiramisu.
How does this information assist with the diagnosis?
Guillain-Barré Syndrome (GBS) is usually preceded by a diarrheal or flu-like
illness within 5 days to 3 weeks before onset of symptoms. It characteristically presents
with an ascending pattern of muscle weakness; however, the Miller-Fisher variant of
GBS may present with a descending pattern of muscle weakness. Myasthenia gravis
is characterized by muscle fatigue after exercise, and the symptoms fluctuate over
time. Tick-borne paralysis should be ruled out by a thorough examination for a tick; it
also usually presents with an ascending pattern of muscle paralysis. Heavy
metal poisoning may cause gastrointestinal tract symptoms, alopecia, mental
disturbances (irritability, concentration difficulties, and somnolence) and peripheral
neuropathy. Organophosphate toxicity causes a cholinergic syndrome. Botulism is a
probable diagnosis despite the absence of a history of consumption of home-canned
foods; bilateral cranial nerve palsies and a descending pattern of weakness are
classic symptoms of botulism. The incubation period for this illness is typically 18 to 36
hours; therefore, it is important to obtain as complete a dietary history as possible for
this time period. It is important that the local or state health department be
contacted immediately when botulism is suspected.
What diagnostic tests are needed?
Five diagnostic tests may help pinpoint the diagnosis:
Electromyelogram (EMG) with rapid repetitive stimulation of the affected
area at 2050 Hertz
Tensilon test
Lumbar puncture -- Cerebrospinal fluid (CSF) protein
Computerized tomography (CT) scan of the head
Magnetic resonance imaging (MRI)
In cases of botulism intoxication, an EMG of the affected muscles done with
rapid repetitive stimulation at 2050 Hertz will usually demonstrate a potentiated
response in muscle action potentials; whereas in GBS and myasthenia gravis rapid
repetitive stimulation yields flat and decremental responses, respectively. Administration
of Tensilon (edrophonium) will help confirm the diagnosis of myasthenia gravis
by showing improved muscle strength after injection of this compound. CSF protein
levels are normal in botulism but are almost always elevated in GBS except early in
the course of the illness. A CT scan of the head with and without contrast may help rule
out
a significant cerebrovascular accident or encephalitis. An MRI may be helpful
to distinguish soft tissue abnormalities or midbrain lesions. If the history suggests
heavy metal or organophosphate toxicity, special tests including evaluation of hair or
blood can be done.
You order the EMG, Tensilon test, CSF studies, and the CT scan of the head.
The EMG shows a potentiated muscle action potential with rapid repetitive stimulation
at 20 Hertz, consistent with botulism intoxication. The Tensilon test is negative
(no improvement with Tensilon) and the CSF protein, glucose, and cell counts are
normal. CT scan of the head shows no meningeal enhancement or evidence of
intracranial hemorrhage.
What diagnostic test(s) will confirm the diagnosis of botulism?
To confirm the diagnosis of botulism, serum, stool, and any leftover suspect
food should be tested for the presence of botulinum toxin. The test is a mouse
bioassay. Mice are given injections of dilutions of sera, stool, and food extract followed
by injections of monovalent antitoxins A, B, and E and polyvalent antitoxin ABCEF,
and observed for signs of botulism and death. Stool and food also can be cultured for
the bacterium Clostridium botulinum, which produces the toxins.
To order tests for botulinum toxin and C. botulinum
culture, the state health department should be contacted. It can provide information about what
specimens should be collected and how they should be stored, and will forward the specimens
to the state public health laboratory or to the Centers for Disease Control and
Prevention (CDC) if the state does not have the capacity to test for botulism.
What treatment is needed?
The most important treatment for botulism is supportive care. The
patient's cardiorespiratory status should be monitored continuously in an intensive care
unit. His respiratory function as measured by forced vital capacity should be
monitored frequently, and he should be placed on assisted ventilation at the first sign
of respiratory decompensation. Induced vomiting or gastric lavage are
sometimes recommended to eliminate unabsorbed toxin from the stomach. These therapies
are only done with a protected airway when the risk of aspiration is low. Cathartic
agents or enemas are sometimes recommended to remove unabsorbed toxin from
the gastrointestinal tract.
The only pharmacological treatment for botulism is antitoxin. The
currently available licensed antitoxins are equine antibodies to toxin; one product has
antibodies to toxin types A and B, the most common causes of botulism, and the other
product has antibodies to toxin types A, B, and E. Use of the product containing antibodies
to type E toxin is reserved for patients at high risk of type E botulism
intoxication including those patients who were exposed to botulinum toxin in Alaska, or those
who have a history of consumption of preserved fish, fish eggs, seal, walrus, whale,
or beaver tail.
Antitoxin is most effective in preventing progression of the illness and
shortening the duration of ventilatory failure if administered early (24-48 hours) after the onset
of neurologic symptoms. If a diagnosis of botulism intoxication is strongly
suspected, antitoxin should be administered promptly and should not be delayed until
the
diagnosis is confirmed. Hypersensitivity reactions have been reported in up to 9%
of patients who receive antitoxin; therefore, skin testing is recommended prior
to administration of antitoxin. Antimicrobials have not been of benefit in the treatment
of foodborne botulism intoxication.
Botulinum antitoxin is obtained from quarantine stations with permission
for release from the CDC and some state health departments; this should be
arranged through the state health department. Epidemiologists within the Foodborne
and Diarrheal Diseases branch are available 24 hours a day through the CDC; you
can contact the on-call epidemiologist at CDC by calling the security desk at 404
639-2888 or at 404 639-2206 during business hours (8:30am _ 4:30pm EST).
Should this case be reported to the local health department?
All suspected cases of botulism intoxication should be reported
immediately to the local health department. It will then notify the state health department, which
will notify the CDC. In collaboration with state health departments, the CDC will assist
with laboratory tests, arrange for treatment with botulinum antitoxin, and notify the
Food and Drug Administration (FDA). The FDA is responsible for investigating
commercial products possibly contaminated with botulinum toxin and assessing the need for
a recall. In the present scenario, the patient denied consuming home-canned foods, suggesting the source of botulinum toxin was a commercial product. A
contaminated, widely distributed commercial product could be a potential hazard to many
people. State and local health officials with the assistance of the FDA will begin a
more thorough investigation, searching for other cases and identifying suspect
food exposures.
What was the most likely source of botulism intoxication in
this patient? What commercial foods are potential sources
of botulism intoxication?
home-canned foods are responsible for over 90% of all cases of
foodborne botulism. However, commercial products have also occasionally been implicated.
A product with an anaerobic environment allows for the growth
of C. botulinum spores and toxin production. The toxins are resistant to digestion by gastric enzymes. In
the present scenario, the salad dressing was contaminated. The patient's wife had
the house Dijon on her salad, but the patient had garlicinfused olive oil. The oil created
an anaerobic environment, which allowed C. botulinum
spores that were on the garlic to germinate and produce toxin. The oil was not acidified or refrigerated;
these procedures could have prevented C. botulinum
spore growth and toxin production.
How can botulism be prevented?
C. botulinum spores are highly heat-resistant; commercial and home-canning
procedures should be done at the appropriate temperature and pressure to kill
these spores. A pressure cooker must be used to can vegetables at home safely because
it can reach temperatures above boiling (>212°F or >100°C). Information on
safe home-canning procedures is available from local county extension home
economists. Botulinum toxin is readily inactivated by heat; nevertheless, the FDA recommends
that any food suspected to contain botulinum toxin be destroyed. Proper acidification
and
refrigeration of commercial products such as herb-infused oils will inhibit spore
growth and toxin production.
Growth of C. botulinum in food may cause container lids to bulge and cause
foods to have a bad odor. Commercial or home-canned food products with bulging lids or
a bad odor should not be eaten. However, botulism has also been associated with
foods that smell and taste normally; therefore, the smell and taste of food should not be
used to determine if it is contaminated.
The patient's serum and stool contained type A botulinum toxin. An investigation
by the state and local health department found four other cases of intoxication
associated with the garlic-infused oil at the restaurant. Two of the patients had been
hospitalized with a diagnosis of stroke, one had been hospitalized with a diagnosis of
myasthenia gravis, and one had been hospitalized with an unknown diagnosis. The patient in
this scenario required assisted ventilation, but his respiratory muscle function
improved after he received antitoxin. He fully recovered within 3 weeks of the onset of
his symptoms.
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
This learning scenario can be used to reinforce medical management
information pertaining to foodborne illnesses, such as that provided from the other booklets of
this primer. This case study provides questions that need to be considered when
dealing with a potential case of foodborne illness. Answers are provided
immediately following the questions to enhance the learning process.
Similar learning scenarios are also available for other foodborne pathogens.
ESCHERICHIA COLI O157:H7 INFECTION:
A PATIENT SCENARIO
Pierre is a 3-year-old who was brought to the outpatient clinic by his mother.
He had a 2-day history of severe abdominal cramps and diarrhea (5 to 7 watery
stools daily). He has had no fever or vomiting. His mother was especially alarmed
this morning when she noticed blood in his diarrheal stools. He refuses to eat, but has
been drinking a few ounces of liquids every 2 to 3 hours. She has been unable to assess
his urine output because of his diarrhea. Pierre previously has been healthy, and has
had no significant weight loss or other symptoms.
On physical examination, he is afebrile with normal blood pressure,
respirations and capillary refill. His oral mucosa and skin are dry, but his skin turgor is normal.
His abdomen has hyperactive bowel sounds, mild distension, and diffuse tenderness,
but is soft with no rebound or guarding. He has loose stool in the rectal vault, which
is grossly bloody.
What is the possible differential diagnosis for his
chief complaint?
Inflammatory bowel disease
Polyps
Meckel's diverticulum
Intussusception
Coagulopathy
Infectious enteritis
What additional information would assist with the diagnosis?
Has he had similar symptoms before?
Is there a family history of inflammatory bowel disease?
Is there a family history of bleeding disorders?
Do other household members or close acquaintances have diarrhea or
bloody diarrhea?
Does he attend child care? If "yes," have there been reports of diarrhea
or bloody diarrhea in other children attending the child care facility?
There is no family history of inflammatory bowel disease or bleeding
disorders. Pierre's mother reports that he usually has 1 to 2 episodes of
self-limited diarrhea
each year, but has never had bloody diarrhea. No other household members have
had diarrhea or bloody diarrhea; however, his grandmother and 15-year-old sister
have had mild abdominal cramps. He does not attend child care; his mother has not
heard that any of his playmates have been ill.
How does this information assist with the diagnosis?
Inflammatory bowel disease is an unlikely diagnosis because of his young age,
the acute onset of diarrhea, and the absence of a history of recurrent diarrhea and
other symptoms such as weight loss, fever, and arthritis. Even if inflammatory bowel
disease is suspected, it would be appropriate to rule out an infectious etiology
before proceeding with further workup. Polyps and Meckel's diverticulum usually
cause painless hematochezia. They can be complicated by intussusception, which
is characterized by a tense abdomen and absent bowel sounds. If intussusception
is suspected, evaluation with abdominal radiography and therapeutic enema may
be performed. There is no family history of coagulopathic disorders and Pierre has
not had a history of abnormal hemostasis. The symptoms of abdominal pain in
other household members suggest an infectious etiology.
The most likely diagnosis is infectious enteritis.
What additional historical information could assist with
the identification of the etiologic agent?
What foods has he consumed within the last week? Specifically, has
he consumed undercooked ground beef, unpasteurized juices, or alfalfa sprouts?
Has he traveled to a foreign country within the last month?
Does he have any pets, specifically reptiles such as an iguana or turtle?
What is the family's source of drinking water?
Have there been any outbreaks of diarrhea in the community, at church, or at
his sibling's school?
Has he recently visited a petting zoo?
The most worrisome diagnosis in a child with bloody diarrhea is infection
with Shiga toxinproducing E. coli, the most common being
E. coli O157:H7. E. coli O157:H7 is associated with serious complications including the hemolytic uremic
syndrome (HUS). Campylobacter,
Salmonella, and Shigella infections also may cause
bloody stools. The incubation periods for these four bacterial infections are 1 to 8 days, 2 to
5 days, 1 to 3 days, and 1 to 2 days, respectively. Therefore, any contaminated food
that he consumed within the prior week could have contributed to his illness.
Pierre's favorite and most frequently consumed foods are hot dogs and spaghetti. He
usually has cereal for breakfast, although he occasionally eats an egg, which he
prefers sunnysideup. He has hot dogs or spaghetti with cheese or fruit for lunch, and
has dinner with other family members. During the last week, his mother recalls that
dinner has included baked chicken, meatloaf, hamburgers, and pizza from the local
pizzeria. She reports the meatloaf was well cooked to 165°C; she checked the
internal temperature with a meat thermometer before serving. The burger appeared to be
well cooked; it was brown in the middle. The family doesn't eat alfalfa sprouts.
The family vacationed at a United States resort but has not traveled to a
foreign country for 2 years. They have a menagerie of pets including a dog, a cat,
two hamsters, a parrot, a Sicilian worm, and a new iguana. Pierre has not visited a
petting zoo nor had contact with other animals. They live on a vegetable farm; they have
no cows, pigs, or sheep. Their main source of water is from a well, but they use
bottled water for drinking. They know of no other outbreaks of diarrhea or bloody diarrhea
in
the community, church, or school. The local health department has not had
other reports of bloody diarrhea or
E. coli O157:H7 infection from the community.
Just as you are about to leave the room, the mother recalls that the nanny, who is
a vegetarian and loves to introduce Pierre to various "veggie delights," related a
story last week about how she prepared for Pierre a veggie sandwich with cucumber,
cream cheese, and alfalfa sprouts. The nanny said he ate only one bite of the sandwich
and refused the rest, begging for spaghetti instead.
Are diagnostic tests needed?
Identification of the cause of Pierre's diarrhea is important because it will
influence antimicrobial therapy, follow-up, and prognosis, and may obviate the need for
invasive diagnostic procedures such as laparotomy or colonoscopy. The child's
dietary, environmental, and travel history suggest he is at high risk for three of the
infectious agents discussed above (i.e., Salmonella, Campylobacter, and E. coli O157:H7).
For example,
E. coli O157:H7 infection has been associated with undercooked ground beef.
Although the hamburger he consumed appeared to be wellcooked (brown in the middle),
recent studies have shown that a significant proportion of ground beef patties are brown
in the middle before they have reached an internal temperature high enough to
kill E. coli O157:H7 (160°F).
Recently, E. coli O157:H7 outbreaks have also been
associated with fresh produce such as unpasteurized apple juice, cabbage, and alfalfa
sprouts. The infectious dose of E. coli O157:H7
is low; ground beef patties with less than 700 organisms per uncooked patty have been associated with illness.
Pierre also could have Campylobacter infection. Transmission
of Campylobacter infection has been associated with the preparation or consumption of raw
or undercooked chicken, and consumption of contaminated water and unpasteurized
milk. Campylobacter can crosscontaminate fruits and vegetables when they
contact surfaces that may have touched raw chicken such as knives and cutting
boards. Campylobacter also has a low infectious dose.
Finally, Pierre is at risk for Salmonella
infection. Children living in households with reptiles, such as iguanas, are at increased risk. Since
1985, Salmonella serotype Enteritidis has emerged as a pathogen in raw shell eggs. Chickens may
become bacteremic with Salmonella Enteritidis,
which seeds the eggs transovarially. Therefore, an egg that is clean and has a normal appearance may be
contaminated. Many outbreaks of Salmonella infection have been associated with foods that
contain raw or undercooked eggs. Salmonella
infections also have been associated with undercooked meat and poultry and fresh fruits and
vegetables.
Shigella is a less likely cause of his illness; it usually causes outbreaks in child
care settings where persontoperson transmission is common. However, food
products such as raw produce can be contaminated
with Shigella and lead to illness.
What diagnostic tests are needed?
Routine stool cultures will detect common enteric bacterial enteropathogens
such as Campylobacter and Salmonella. However, many clinical laboratories do not
screen stools routinely for E. coli O157:H7;
it is incumbent upon the clinician to request
such testing when E. coli O157:H7 infection is suspected, especially for patients with
bloody
diarrhea. Bloody diarrhea is very common in patients
with E. coli O157:H7 infection, although the absence of bloody diarrhea does not rule out the diagnosis. Culturing
for E. coli O157:H7 is relatively simple and inexpensive; this bacteria does not
ferment sorbitol and, therefore, appears as a colorless colony on sorbitolMacConkey
(SMAC) agar. Colorless colonies on SMAC agar are selected and assayed for O157
antigen using a commercial kit. All strains of E. coli
that agglutinate with the O157 antibody are presumed to
be E. coli O157:H7 and should be reported to the local public
health authorities. Confirmation of the H flagellar antigen is usually done by a
reference laboratory. Recently, rapid diagnostic kits that test for the presence of Shiga toxin
have become available for use in clinical laboratories. Specimens that test positive
should be forwarded to the public health laboratory for further
evaluation.
The lab calls you with the results of the stool culture. Pierre's stool
grew E. coli O157:H7.
What treatment is needed?
The treatment of E. coli O157:H7 infection is largely supportive.
Dehydration should be treated with liberal oral or intravenous rehydration to reduce the stress
of volume depletion on the kidneys. This is often best accomplished in the hospital
with intravenous fluids and close monitoring.
The use of antimicrobial therapy is controversial. Data suggest that
antimicrobial agents may be harmful. Antimicrobial agents may kill or disrupt
intracolonic E. coli O157:H7 organisms, allowing them to release toxin that is absorbed systemically,
and may increase the risk of hemolytic uremic syndrome (HUS). Antimicrobials also
have not been shown to decrease illness severity.
Antidiarrheal medications, especially those that slow intestinal motility, should
be avoided. They may delay clearance of the organism, increase the time for
toxin absorption, and increase the risk and severity of
HUS.
What are the complications of E. coli O157:H7 infection?
What follow-up is needed?
Within one week after the onset of diarrhea, 10% of children <10 years of age
with
E. coli O157:H7 infection develop HUS, which is characterized by hemolytic
anemia, thrombocytopenia, oliguriaanuria, and rarely seizures. Children with visible blood
in their stools are at increased risk of developing HUS. If HUS has not developed within
2 to 3 days after the diarrhea has resolved, this complication is unlikely to occur.
Pierre's parents should be instructed to watch for signs and symptoms of HUS, and he
should be evaluated by a clinician if he develops these. Regardless of other symptoms, if
his diarrhea continues longer than 4 to 5 days, a complete blood count, platelet count,
and blood smear analysis should be considered.
Adults with E. coli O157:H7 infection may develop HUS or
thrombotic thrombocytopenic purpura (TTP), a microangiopathic disorder that resembles HUS
but is accompanied by neurologic abnormalities. The mortality rate
with E. coli O157:H7associated HUS is approximately 3% to 5% in children, but may be higher
in elderly patients who develop TTP.
Should this case be reported to the local health department?
All cases of E. coli O157:H7 infection, postdiarrheal HUS, and postdiarrheal
TTP should be reported to the local public health department. The ease with
which person-to-person transmission occurs, especially from children who are
not toilet-trained, makes diagnosis and reporting very important. The health
department can use this information to identify clusters of infection, discover common sources
of exposure, and take measures to remove the source of the infection (i.e., remove
the contaminated food) and prevent transmission of the organism to others.
In addition to reporting cases of E. coli O157:H7
infection, it also is helpful to send
E. coli O157:H7 isolates to the local health department. Isolates can be subtyped
by pulsed-field gel electrophoresis (PFGE) to determine if other reported cases
of E. coli O157:H7 infection are related. Many state public health laboratories now have
the capacity to do molecular subtyping. In 1995, the Centers for Disease Control
and Prevention (CDC) initiated PulseNet, a national computer network of public
health laboratories that employs standard methods to
subtype E. coli O157:H7 strains. As of May 2000, there were 34 public health laboratories from various states participating
in PulseNet, as well as laboratories from the US Department of Agriculture Food
Safety and Inspection Service (USDAFSIS), and the Food and Drug Administration
(FDA). Laboratories within the network can transmit PFGE patterns electronically to
a databank at the CDC where they are automatically compared to patterns of
other isolates. If the patterns submitted by laboratories in different locations during a
defined time period are found to match, the CDC computer will alert PulseNet participants of
a possible multistate outbreak. The information can be used by the CDC, the
USDAFSIS, the FDA, and the state health departments to rapidly initiate outbreak
investigations and preventive actions.
How can E. coli O157:H7 infection be prevented?
Consumers should avoid eating undercooked ground beef. The most reliable
way to determine whether ground beef is cooked to a temperature high enough to
destroy
E. coli O157:H7 is to use a meat thermometer and cook to an internal temperature
of 160°F. Use of meat thermometers when cooking ground beef is especially
important for children, older persons, and the immunocompromised who are at highest risk
of contracting foodborne diseases, of developing severe foodborne illness, and of
dying from foodborne diseases. If a meat thermometer is not available, consumers
should not eat ground beef that is pink in the middle. If served an undercooked
(pink) hamburger at a restaurant, consumers should send it back and have it cooked longer.
Consumers should avoid unpasteurized juices and milk, and should wash all
fresh produce thoroughly before consumption. Children under 5 years of age,
immunocompromised persons, and the elderly should avoid eating alfalfa sprouts. Infected
persons, especially children, should be encouraged to wash their hands carefully
and frequently with soap and water to reduce the risk of spreading the infection.
Preventive measures to reduce the number of cattle that
carry E. coli O157:H7 and to reduce contamination of meat during slaughter and grinding are also underway.
Pierre continued to have bloody diarrhea. On the fifth day of illness, a
complete blood count showed a hemoglobin of 9g/dL and a platelet count of 79 x
109/L. A peripheral blood smear revealed evidence of hemolysis. Despite hydration
and appropriate supportive care, he developed renal insufficiency, which required
dialysis. His renal function improved after 4 weeks of dialysis, and he eventually recovered
with no other complications.
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
This learning scenario can be used to reinforce medical management
information pertaining to foodborne illnesses, such as that provided from the other booklets of
this primer. This case study provides questions that need to be considered when
dealing with a potential case of foodborne illness. Answers are provided
immediately following the questions to enhance the learning process.
Similar learning scenarios are also available for other foodborne pathogens.
ENTEROTOXIGENIC ESCHERICHIA COLI INFECTION:
A PATIENT SCENARIO
Stephanie is a 35-year-old who presents to your office with a 4day history
of abdominal cramps, headache, and 810 episodes/day of watery diarrhea. She has
had a few episodes of vomiting but denies fever or bloody diarrhea. She has no
complaints of dysuria or back pain. She was previously healthy.
Physical examination reveals she is afebrile with a blood pressure of 120/80
mm Hg and normal capillary refill. She has a soft and diffusely tender abdomen
with hyperactive bowel sounds but no rebound or guarding. She has no
costovertebral angle (CVA) tenderness and stool examination is negative for occult blood.
What is the possible differential diagnosis for her
chief complaint?
What additional information would assist with the diagnosis?
Has she ever had similar symptoms before?
Is there a family history of malabsorption syndromes or endocrinopathies?
Does she have other signs or symptoms such as weight loss, bloating, history
of milk intolerance, flushing, tachycardia, or weight loss?
What is her occupation?
Has she traveled to a foreign country within the last month?
Do other household members or close acquaintances have gastrointestinal
tract symptoms or diarrhea?
Stephanie reports she rarely has diarrhea, usually less than one episode a
year. She denies a family history of malabsorptive or endocrine disorders, and has had
none of the other symptoms listed above. She is an art therapist for a local children's
mental health clinic, and is not aware that any of her patients have had gastrointestinal
tract symptoms or diarrhea. Other household members are well; however, several of
her extended family members and friends who attended her younger sibling's high
school graduation picnic last weekend also have diarrhea. In fact, her aunt (the hostess of
the party) called the local health department because she was concerned that the
illnesses might be associated with food that was served at the event from a local
restaurant
(Restaurant A). Stephanie is uncertain what her aunt learned from the
health department.
How does this information assist with the diagnosis?
This information suggests that Stephanie's case of diarrhea may be part of a
larger outbreak. The most appropriate next step in her management is to contact the
local health department and ask if it is aware of an outbreak of foodborne disease, or if
it has had reports of diarrheal illness from other patrons or partygoers who
consumed food from Restaurant A. The health department also may provide information
about the etiologic agent or suspected etiologic agent, and provide recommendations
for treatment.
You call the health department and learn that there is an outbreak of
foodborne illness associated with consumption of food from Restaurant A. Similar to
Stephanie, most patients have had abdominal cramps and watery diarrhea, few have had
fever, and no one has reported bloody diarrhea. The median incubation period is 42
hours and the diarrhea lasts 3 to 7 days. At this time, neither the vehicle of transmission
nor the etiologic agent has been identified. The health department officials request
that you obtain a stool culture and report the results back to them.
What are the possible etiologic agents of this outbreak
of foodborne illness?
Based on its investigation, the health department suspects the vehicle for
this outbreak was a food item consumed at Restaurant A, 42 hours before the illness. If
this is so, the most likely etiologic agent is a bacterial pathogen as suggested by
the moderate incubation period, the lack of vomiting, and the significant duration of
illness. Foodborne illness caused by the most common enteric viral pathogens typically has
a shorter incubation period, more vomiting, less diarrhea, and a shorter duration
of symptoms. By contrast, parasitic infections usually have a longer incubation period
(1 to 2 weeks) and a longer duration of illness (>2 to 3 weeks).
The bacterial enteric pathogens that should be considered as possible sources
of the outbreak are Campylobacter and Salmonella,
the two most common causes of bacterial foodborne diseases in the United States. Typically these infections
are characterized by fever in addition to abdominal cramps and diarrhea, and
bloody stools are possible but not common. E. coli O157:H7
infection should also be considered, although bloody stools frequently are reported with this
infection. Vibrios and enterotoxigenic E. coli
rarely are diagnosed causes of foodborne illness in
the United States but should remain in the differential diagnosis given the profuse
watery diarrhea that characterizes this outbreak.
A stool culture for bacterial enteropathogens including
Salmonella, Shigella, Campylobacter,
Yersinia, and E. coli O157:H7 is negative. You report this
information to the health department and learn that the routine stool cultures from other
patients in the outbreak are also negative. The state public health laboratory examined
stools for common viral enteric pathogens; those preliminary studies are negative.
What other pathogen(s) should be considered? How are
they identified?
The most likely etiologic agent of this outbreak is
enterotoxigenic E. coli (ETEC). ETEC is a common cause of traveler's diarrhea and is an increasingly recognized
cause of foodborne illness in the United States. This bacterium elaborates one or
more enterotoxins that cause intestinal secretion and diarrhea. The incubation
period, symptoms, and duration of diarrhea described for persons involved in this
outbreak are characteristic of ETEC infection. Furthermore, clinical laboratories and most
state and territorial public health laboratories do not have the capacity to test for ETEC
in stool; the identification process requires a complex procedure with
expensive reagents. Therefore, if the characteristics of a diarrheal illness are suggestive of
a bacterial etiology but routine stool cultures are negative for common bacterial
and viral enteropathogens, ETEC should be strongly suspected as the etiologic agent.
Local health departments can arrange to have stools tested for ETEC at the state
public health laboratory or at the Centers for Disease Control and Prevention.
What should the patient know about ETEC infections? What
is the next step in management?
ETEC is the most common cause of "traveler's diarrhea" and is becoming a
more frequently recognized cause of foodborne illness in the United States. The illness
is self-limited; the diarrhea usually lasts fewer than 5 days.
Because the duration of illness is short, ETEC infections generally do not
require antibiotic therapy. Treatment is mainly supportive including oral or intravenous
fluids for rehydration. Occasionally antibiotics, such as ciprofloxacin for adults
and trimethoprim/sulfamethoxazole for children, are given if the patient has an
underlying illness or if the diarrhea is severe. ETEC infection may cause dehydration but there
are generally no serious complications or long-term sequelae from this infection.
Patients should be reminded to wash their hands with warm running water
and soap after using the bathroom and before and after eating to avoid transmitting
the infection to others. They should tell friends who might have attended other parties
at which food from Restaurant A was served to call the local health department to
report cases of illness.
How can ETEC infections be prevented?
Human and animal wastes are the ultimate source of ETEC
contamination. Travelers in developing countries should avoid foods that could be contaminated
with bacteria. They should eat thoroughly cooked foods prepared in facilities that
practice proper food handling techniques. They should avoid unpasteurized juices and milk,
and drink bottled beverages, or water that has been boiled or adequately chlorinated.
They should avoid raw foods (e.g. salads, peeled fruit or vegetables, raw
seafood, undercooked meat or poultry) and foods from street vendors.
In the United States, proper food preparation and handling practices will reduce
the risk of ETEC infections. This should include careful handwashing with warm water
and soap after using the bathroom and before and after preparing or consuming food.
Stephanie's watery diarrhea resolved after 5 days. She was mildly dehydrated
and missed 3 days of work, but recovered completely with no long-term complications.
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
This learning scenario can be used to reinforce medical management
information pertaining to foodborne illnesses, such as that provided from the other booklets of
this primer. This case study provides questions that need to be considered when
dealing with a potential case of foodborne illness. Answers are provided
immediately following the questions to enhance the learning process.
Similar learning scenarios are also available for other foodborne pathogens.
LISTERIA MONOCYTOGENES INFECTION:
A PATIENT SCENARIO
Sandy, the pregnant mother of a 2-year-old boy presents to your office at
28 weeks' gestation complaining of fever, chills, headache, myalgias, and sore throat.
She has previously been healthy and has had an uncomplicated pregnancy. She
is somewhat concerned about the illness because she just returned from Kenya a
few weeks earlier.
Physical examination reveals a temperature of 102°F, pulse of 100 beats
per minute, respirations of 20 breaths per minute, and a blood pressure of 100/60 mm
Hg. Her posterior pharynx is nonerythematous with no tonsillar enlargement or
exudates. She has no remarkable cervical lymphadenopathy. Breath sounds are clear and
equal bilaterally, and her abdomen is remarkable only for her gravid uterus. She has
normal capillary refill and no petechiae or rashes.
What should be included in the differential diagnosis?
Viral illness
Influenza
Adenovirus
Coxsackie virus
Primary herpes
Primary Human Immunodeficiency
Virus (HIV)
Infectious Mononucleosis
(EpsteinBarr Virus [EBV])
Cytomegalovirus (CMV)
Parvovirus
Mycoplasma
Group A Streptococcus pharyngitis
Gonococcal pharyngitis
Bacteremia (Listeria monocytogenes,
Group B Streptococcus,
Salmonella typhi)
Parasitic diseases
Malaria
What additional information would assist with the diagnosis?
What season of the year is it?
Do other household members have similar symptoms?
What is her occupation?
Has she been around ill children or adolescents?
Has she been camping, hiking, or exposed to ticks?
When did she travel to Kenya; where did she visit?
Did she take malaria prophylaxis, and what medication?
Has she been sexually active with more than one partner during the last
6 months?
Is she on any medications currently?
Has she had any animal exposures?
It is early autumn and no other household members are ill. She is a legal
secretary; none of the clients with whom she has worked have been ill, and she has not
been around ill children or adolescents. Her 2-year-old son attends day care; he has
been well and there have been no reports of ill children from the center director.
She traveled to Nairobi, Kenya, at 15 weeks' gestation, and was well throughout the
trip. She took mefloquine for malaria prophylaxis once weekly, and did not forget
any doses. She has not been camping or hiking, and is unaware of tick exposure.
She recalls only one day of mild illness during her pregnancy, which occurred about
5 weeks earlier and was characterized by
2 or 3 episodes of vomiting and a few loose stools. She attributed the symptoms to
a change in diet; she increased milk and fruit consumption in an attempt to be
"healthy for the baby." She and her husband have been happily married for 5 years; she
denies having any other sexual partners. She is currently taking no medications, and she
has had no animal exposures except for her pet dog.
How does this information assist with the diagnosis?
Influenza is an unlikely diagnosis; it is early autumn and Sandy has not
been exposed to other ill persons at home or work. Her sexual history indicates her risk
for HIV, herpes, and gonorrhea infection is low. Her recreational history
suggests tickborne disease is improbable. Malaria is a possible diagnosis but she has had
no fever in the 12 weeks since she returned from Nairobi, a city over 5,000 feet
above sea level where the risk of contracting malaria is low. Mycoplasma,
adenovirus, coxsackie virus, group A Streptococcus,
CMV, EBV, parvovirus, and other viral
agents could account for her symptoms. She could also be bacteremic, but has no
symptoms to indicate she is septic.
What diagnostic tests are needed?
Consider rapid antigen screen for group A Streptococcus
Consider rapid test for infectious mononucleosis
Consider urinalysis and thick and thin blood smear
The rapid tests for group A
Streptococcus and infectious mononucleosis
are negative. Urinalysis is negative for bacteria and thick and thin blood smear shows
no evidence of malaria parasites. One hour after an appropriate dose of
acetaminophen, her temperature is 101°F, and she continues to have flu-like
symptoms. Her
blood pressure, capillary refill, and the rest of her physical examination are normal.
She returns home with instructions to call you if she develops new symptoms,
her symptoms worsen, or her symptoms do not abate in the next 24 hours.
Four weeks later, you receive another call from Sandy. She reports her water
just broke. She has otherwise been well; the flu-like symptoms she had at her last
visit resolved within 48 hours. You meet her in the labor and delivery suite, and confirm
by physical examination that her membranes are prematurely ruptured. Despite
tocolytic therapy, her labor progresses and she delivers an infant girl at 32 weeks'
gestation. After delivery, Sandy has a normal postpartum course. The infant is admitted to
the neonatal intensive care unit and requires supplemental oxygen for the first few
hours of life, but soon after is weaned off oxygen and tolerates her first feeding
without difficulty. At 22 hours of age, the infant's nurse notes she is tachypneic with
intercostal retractions. The infant's blood pressure is in the low range of normal. The nurse
is repeating the blood pressure measurement when the infant becomes bradycardic
with delayed capillary refill. Despite full resuscitation efforts including intubation
and inotropic support, the infant dies. The next morning you receive a report from
the microbiology laboratory that blood cultures drawn just before the infant's death
are growing grampositive short
rods/cocci.
What were the most likely causes of the infant's sepsis?
Group B Streptococcus
Staphylococcus aureus
Coagulasenegative Staphylococcus
Enterococcus
ahemolytic Streptococcus
Listeria monocytogenes
Group B Streptococcus and Escherichia coli (a gramnegative rod) are
responsible for up to 75% of cases of earlyonset neonatal sepsis. Listeria monocytogenes, a
less common cause of earlyonset neonatal sepsis, also causes an illness that
clinically parallels that of group B Streptococcus; infants are infected in utero and
develop illness at birth or shortly
thereafter.
The following morning, the microbiology laboratory calls to report it has
identified the grampositive short rods/cocci in the blood as
Listeria monocytogenes.
What, if anything, could have been done to prevent this
infant's death?
Listeriosis is an uncommon disease; approximately 1,200 cases
of Listeria monocytogenes infection are reported each year in the United States. Up to one
third of these infections occur in pregnant women, and can be complicated by
maternal
bacteremia, fetal loss, or infant bacteremia and meningitis. The symptoms
associated with listeriosis during pregnancy are often nonspecific and may imitate those
of influenza. These flu-like symptoms coincide with the bacteremic phase of infection.
In pregnant women with a febrile illness, appropriate clinical management may
include obtaining blood cultures to rule out listeriosis.
Fetal infection most likely results from transplacental transmission of
maternal bacteremia. Neonatal infection can be prevented if
maternal Listeria monocytogenes is treated with the appropriate antibiotics during pregnancy.
Listeria has been epidemiologically linked to such foods as fresh soft
cheeses, readytoeat deli meats, hot dogs, and unpasteurized and inadequately
pasteurized milk. Its ability to grow at temperatures as low as 3°C permits multiplication
in refrigerated foods. Any one of these could have been the vector for this case.
All pregnant women should receive dietary counseling to avoid foods that
increase the risk of Listeria monocytogenes
infection. They should be advised to avoid unpasteurized milk and cheeses made from unpasteurized milk (particularly fresh
soft cheeses) during pregnancy. All pregnant women should cook (until steaming
hot) leftover foods or ready-to-eat foods such as hot dogs, before eating, and wash
their hands carefully to avoid cross-contamination if preparing these foods for others.
Other groups at high risk for listeriosis are elderly and
immunocompromised patients. They frequently present with sepsis or meningitis. People in these
highrisk groups should also receive dietary counseling to avoid high-risk foods.
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
CLINICAL VIGNETTES: WHAT'S YOUR CALL?
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
January 2001
PATIENT VIGNETTES -- WHAT'S YOUR CALL?
The following clinical vignettes are provided for your self-evaluation. All
are possible situations that may present at your practice. The Clinical
Considerations booklet and the Foodborne Illnesses Tables that are also part of this primer will
provide the information necessary for you to adequately address these clinical situations.
Note that these vignettes include both infectious and noninfectious forms of
foodborne illness.
For the following clinical vignettes, choose the best answer from the choices
listed at the end of the vignettes:
A -- likely diagnosis; choose the best possible answer listed on
"answer selections" page under A selections.
B -- most appropriate choice to confirm the diagnosis (there may be more than
one correct answer -- list all of them). Choose from the possible answers listed
on "answer selections" page under the
B section.
Finally, decide whether the situation warrants reporting to the local or state
health department.
Clinical Vignettes
I. You receive a long-distance call from a patient who is an outdoorsman. He
is with a group that collected and ate some wild mushrooms less than 2 hours
ago. Several members of the group have since developed vomiting, diarrhea, and
some mental confusion.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
II. A newborn child has symptoms of sepsis. Cerebrospinal fluid studies
are consistent with meningitis. The mother had a flu-like syndrome prior to delivery.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
III. This patient has just returned today from Latin America following a
2day business trip where he reports eating several meals of fish that he bought from
street venders around his hotel. He feels very ill with profuse, watery diarrhea and vomiting.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
IV. An 18month child is brought to your office with fever, bloody diarrhea,
and some vomiting. She has been drinking unpasteurized milk in the last 48 hours. No
other family members are ill.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
V. A patient calls and states that he and several family members are ill
with severe vomiting. They ate at a church picnic 4 hours earlier.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up
action:
Report to the health department? Yes No
VI. A patient calls and states that most family members have developed
severe vomiting, about 1 hour after eating at a picnic. They ate barbecued beef, chips,
potato salad, and homemade root beer. Some are complaining of a metallic taste.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
VII. A patient has had chronic intermittent diarrhea for about 3 weeks. There is
no fever or vomiting and no blood in the stool. The patient travels to Latin America
and Eastern Europe frequently, most recently 2 weeks ago.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
VIII. The parents of a 6month old infant are concerned because she is listless
and weak. The infant is feeding poorly, has poor head control, and is constipated. There
is no fever or vomiting.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
IX. A businessman who travels frequently is ill with fatigue, jaundice,
abdominal pain and diarrhea. About 1 month ago, he returned from an international trip
during which he consumed raw oysters.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department Yes No
X. Several members of a single family are ill with abdominal cramps and
watery diarrhea. They just returned from visiting friends on the East Coast of the
United States where they consumed raw oysters 48 hours ago.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up
action:
Report to the health department? Yes No
XI. A minister at a local church calls to report that many members
began developing watery diarrhea on the morning after the annual ham dinner
fundraiser. Some people also reported nausea and abdominal cramps, but no one has fever
or bloody stools.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
XII. You receive a long-distance call from a patient on a fishing vacation off
the coast of Belize. Her family has been eating a variety of local fish and shellfish that
they caught. She reports that several family members developed abdominal pain,
severe diarrhea, and weakness the morning after they consumed the seafood for dinner.
One family member began having difficulty speaking later on that same night.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up action:
Report to the health department? Yes No
XIII. A family in a rural community is worried that their father may be having
a stroke. He is complaining of double vision and is having trouble swallowing. They
have a large garden and eat home-canned vegetables.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up
action:
Report to the health department? Yes No
XIV. A 2-year-old child who attends day care presents with abdominal cramps
and severe bloody diarrhea, which has been present for 2 days. He has no fever.
A -- likely diagnosis:
B -- most appropriate test to confirm etiology/follow-up
action:
Report to the health department? Yes No
ANSWER CHOICES
A: Choose from any of these possible etiologies:
Intoxication from preformed toxins of
Staphylococcus aureus or Bacillus cereus
Intoxication from toxins produced in
vivo by Clostridium perfringens
Salmonella or
Campylobacter are possible.
E. coli O157:H7
Norwalklike viruses, Vibrio
parahemolyticus, and other Vibrio infections
Vibrio cholerae infection
Botulism must be ruled out
Listeria monocytogenes sepsis
Cryptosporidium parvum
Cyclospora cayetanensis
A form of metal poisoning
A form of mushroom poisoning
Likely fish/shellfish toxin
Giardia lamblia
Trichinella spiralis
Hepatitis A virus
B: Choose from any of these following tests/actions
Clinical diagnosis; laboratory tests may not always be indicated.
Generally detected on routine stool cultures.
Generally, a reference laboratory is needed to identify the toxin from
food, stool, or vomitus.
Important to identify causative organism for public health reasons.
Send stool samples to health department
(Vibrio cholerae, other Vibrios,
E. coli O157:H7, special toxin tests,
Clostridium perfringens, Clostridium
botulinum).
Not detected by routine stool cultures
(E. coli O157:H7, Vibrio cholerae, other
Vibrios).
Should test for viral agents.
For cysts, ova, and parasite detection, at least 3 stool samples must
be collected. Sometimes the organism may still be missed; thus
sampling via endoscopy may be necessary.
Test for appropriate metal.
Special test needed to identify a fish toxin.
Consult a mycologist to identify the mushroom.
Blood culture is the best source for diagnosis.
Blood test helpful to identify the agent.
May need acute and convalescent serum or viral cultures.
Answers
Question number
Choice for A
Choice(s) for B
Report to health department?
I
12
11
Yes
II
8
12
Yes
III
6
5, 6
Yes
IV
3
2
Yes
V
1
1, 3
Yes
VI
11
9
Yes
VII
14
8
Yes
VIII
7
5
Yes
IX
16
7, 13, 14
Yes
X
5
5, 6, 7
Yes
XI
2
1, 5
Yes
XII
13
10
Yes
XIII
7
5
Yes
XIV
4
5, 6
Yes
Diagnosis and Management of Foodborne Illnesses:
A Primer for Physicians
SUGGESTED FOOD SAFETY RESOURCES AND READING LIST
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition
Food and Drug Administration
Food Safety and Inspection Service
US Department of Agriculture
CDC Voice Information System: 888 CDC-FAXX (232-3299)
SUGGESTED READING LIST
General Reading
Mead PS, Slutsker L, Dietz V, et al. food-related illness and death in the United
States. Emerg Infect Dis [serial online]. 1999;5(5):607-625. Available from: URL:
http://www.cdc.gov/ncidod/eid/vol5no5/mead.htm.
Centers for Disease Control and Prevention. Surveillance for foodborne-disease
outbreaks--United States, 1993-1997. MMWR. 2000;49(SS01):1-66.
Swerdlow DL, Altekruse SF. Foodborne diseases in the global village: what's on
the plate for the 21st century. In: Scheld WM, Craig WA, Hughes JM, eds.
Emerging Infections 2. Washington, DC: ASM Press; 1998:273-293.
Tauxe RV, Hughes JM. Foodborne disease. In: Mandell GL, Bennett JE, Dolin R,
eds. Principles and Practice of Infectious Diseases, 4th Ed. New York: Churchill
Livingstone; 1997:1012-1024.
Tauxe RV. Emerging foodborne disease: an evolving public health challenge.
Emerg Infect Dis. 1997;3:425-434.
ANTHRAX
Turnbull PCB, Bohm R, et al. Guidelines for the Surveillance and Control of Anthrax
in Humans and Animals. Geneva: WHO/Zoon/93.170. 1993.
Inglesby TV, Henderson DA, Bartlett JG et al. Anthrax as a biological weapon:
medical and public health management. Working Group on Civilian Biodefense. JAMA.
1999; 281:1735-1745.
BOTULISM
Shapiro RL, Hatheway C, Becher J, Swerdlow DL. Botulism surveillance
and emergency response: a public health strategy for a global challenge.
JAMA. 1997;278:433-435.
Shapiro RL, Hatheway C, Swerdlow DL. Botulism in the United States: A clinical
and epidemiologic review. Ann Intern Med. 1998;129:221-8
Angulo FJ, Getz J, Taylor JP, et al. A large outbreak of botulism: the hazardous
baked potato. J Infect Dis. 1998;178:172-177.
Angulo FJ, St. Louis ME. Botulism. In: Evans AS, Brachman PS, eds. Bacterial
Infections of Humans. New York: Plenum; 1998:13153.
BRAINERD DIARRHEA
Parsonnet J, Wanke C, Hack H. Idiopathic chronic diarrhea. In: Infections of
the Gastrointestinal Tract. MJ Blaser, PD Smith, JI Ravdin, HB Greenberg, RL
Guerrant, editors. Raven Press, Ltd. New York 1995;311-323.
Mintz ED, Weber JT, Tauxe RV, et al. An outbreak of brainerd diarrhea among
travelers to the Galapagos Islands. J Infect Dis. 1998;177:1041-1045.
Osterholm MT, MacDonald KL, White KE, et al. An outbreak of newly
recognized chronic diarrhea syndrome associated with raw milk consumption.
JAMA. 1986;256:484-490.
BRUCELLOSIS
Baldi PC, Miguel SE, Fossati, CA, Wallach JC. Serological follow-up of
human brucellosis by measuring IgG Antibodies to lipopolysaccharide and
cytoplasmic proteins of Brucella species. Clin Infect Dis.
1996;22:446-455.
Martin-Mazuelos E, Nogales MC, Florez C, Gomez-Mateos M, Lozano F, Sanchez
A. Outbreak of Brucella melitensis among microbiology laboratory workers. J
Clin Microbiol. 1994;32:2035-2036.
Khuri-bulos NA, Doud AH, Azab SM. Treatment of childhood brucellosis: results of
a prospective trial on 113 children. Pediatr Infect Dis J. 1993;12:377-381.
Chomel BB, DeBess EE, Mangiamele DM, Reilly KF, Farver TB, Sun RK, Barrett
LR. Changing trends in the epidemiology of human brucellosis in California from 1973
to 1992: a shift toward foodborne transmission. J Infect Dis.
1994;170:1216-1223.
CAMPYLOBACTER
Roels TH, Wickus HH, Bostrum JJ, et al. A foodborne outbreak of
Campylobacter jejuni (0:33) infection associated with tuna salad: a rare strain in an unusual
vehicle. Epidemol Infect. 1998;121:281-287.
Smith, KE, Besser, JM, Hedberg, CW, et al. Quinolone-resistant Campylobacter
jejuni infections in Minnesota, 1992-1998. N Engl J Med. 1999;340:1525-1532.
Allos BM, Taylor DN. Campylobacter infections. In: Evans AS, Brachman PS,
eds. Bacterial Infections of Humans. New York: Plenum Medical; 1998:169-190.
CHOLERA
Mahon BE, Mintz ED, Greene KD, et al. Reported cholera in the United
States, 1992-1994: a reflection of global changes in cholera epidemiology.
JAMA. 1996;276:307-312.
Wachsmuth IK, Blake PA, Olsvik O, eds. Vibrio
cholerae and Cholera: Molecular to Global Perspectives. Washington, DC: American Society for Microbiology; 1994.
Mintz ED, Tauxe, RT, Levine MM. The global resurgence of cholera. In: Noah
N, O'Mahoney M, eds. Communicable Disease Epidemiology and Control. New York:
John Wiley & Sons, Inc., 1998.
Centers for Disease Control and Prevention. Foodborne outbreak of diarrheal
illness associated with Cryptosporidium
parvum -- Minnesota, 1995. MMWR. 1996;45:783-784.
Millard PS, Gensheimer KF, Addiss DG, et. al. An outbreak of cryptosporidiosis
from fresh-pressed apple cider. JAMA. 1994;272:1592-1596
Mac Kenzie WR, Hoxie NJ, Proctor ME, et al. A massive outbreak in Milwaukee
of Cryptosporidium infection transmitted through the public water supply. N Engl J
Med. 1994;331:161-7.
Smith JL. Cryptosporidium and Giardia as agents of foodborne disease. J
Food Protection. 1993;56:451-461.
CYCLOSPORA
Herwaldt BL, et al. An outbreak in 1996 of cyclosporiasis associated with
imported raspberries. N Engl J Med. 1997;336:1548-1556.
Herwaldt BL, et al. The return of
Cyclospora in 1997: another outbreak of cyclosporiasis in North America associated with imported raspberries. Ann
Intern Med. 1999; 130:21-0220.
Soave R, et al. Cyclospora. Infect Dis Clin North Am.
1998;12:1-12.
Dalton CB; Mintz ED; Wells JG; Bopp CA; Tauxe RV. Outbreaks of
enterotoxigenic Escherichia coli infection in American adults: a clinical and epidemiologic
profile. Epidemiol Infect. 1999;123:9-16.
Moyenuddin M, Wachsmuth IK, Moseley SL et al. Serotype, antimicrobial
resistance, and adherence properties of Escherichia
coli strains associated with outbreaks of diarrheal illness in children in the United States. J Clin Microbiol.
1989;27:2234-2239.
Centers for Disease Control and Prevention. Foodborne outbreaks of
enterotoxigenic Escherichia coli Rhode Island and New Hampshire, 1993. MMWR.
1994;43:81-89.
Altekruse SF, Street DA, Fein SB, Levy AS. Consumer knowledge of
foodborne microbial hazards and food-handling practices. J Food Prot.
1996;59:287-294.
Reid DS, Harris LJ. Microorganisms and microbial toxins. Adv Exp Med Biol.
1999; 459:9-21.
Blaha T. Epidemiology and quality assurance application to food safety. Prev Vet
Med. 1999;39(2):81-92.
ESCHERICHIA COLI O157:H7
Bender JB, Hedberg CW, Besser JM, et al. Surveillance for
Escherichia coli O157:H7 infections in Minnesota by molecular subtyping. N Engl J. Med.
1997;337:388-394.
Mahon BE, Griffin PM, Mead PS, Tauxe RV. Hemolytic uremic syndrome surveillance
to monitor trends in infection with Escherichia
coli O157:H7 and other shiga toxin-producing
E. coli. Emerg Infect Dis [serial online]. 1997;3(3):409-412.
Available from: URL:
http://www.cdc.gov/ncidod/eid/vol3no3/letters.htm#mahon.
Slutsker L, Ries AA, Greene KD, et al. Escherichia
coli O157:H7 diarrhea in the United States: clinical and epidemiologic features. Ann Intern Med.
1997;126:505-513.
Mead PS and Griffin PM. Escherichia coli O157:H7. Lancet.
1998;352:1207-12.
Wong CS, Jelacic S, Habeed RL, Watkins, SL, and Tarr, PI. The risk of
the hemolyticuremic syndrome after antibiotic treatment of Escherichia coli
O157:H7 infections. N Engl J Med. 2000;342:1930-6.
GIARDIA
Hardie RM, Wall PG, Gott P, et al. Infectious Diarrhea in Tourists Staying in a
Resort Hotel. Emerg Infect Dis [serial online]. 1999;5(1):168-171. Available from: URL:
http://www.cdc.gov/ncidod/eid/vol5no1/hardie.htm
.
Mintz ED, et al. Foodborne giardiasis in a corporate office setting. J Infect Dis.
1993; 167:250-253.
Hill D. Giardiasis: issues in diagnosis and management. Inf Dis Clin North Am.
1993; 7:503-25.
Petersen LR, Cartter ML, Hadler JL. A foodborne outbreak of
Giardia lamblia. J Infect Dis. 1988;157:846-848.
HEPATITIS A
Centers for Disease Control and Prevention. Prevention of hepatitis A through
active or passive immunization: recommendations of the Advisory Committee
on Immunization Practices (ACIP). MMWR. 1999;48(No. RR-12).
LISTERIOSIS
Salamina G, Donne ED, Niccolini A, et al. A foodborne outbreak of
gastroenteritis involving Listeria
monocytogenes. Epidemiol Infect. 1996;117:429-436.
Schuchat A. Listeriosis and pregnancy: food for thought. Obstet Gynecol
Surv. 1997;52:721-722.
Centers for Disease Control and Prevention. Multistate outbreak of listeriosis --
United States, 1998. MMWR. 1998;47:1085-1086.
Slutsker L, Schuchat A. Listeriosis in humans. In: Ryser ET, Marth EH, eds.
Listeria, Listeriosis, and Food Safety. New York: Marcel Dekker; 1999;75-95.
NORWALK-LIKE VIRUSES
Kapikian AZ, Estes MK, Chanock RM. Norwalk group of viruses. In: Fields BN,
Knipe DM, Howley PM, et al, eds. Fields Virology. 3rd ed. Philadelphia,
Pennsylvania: LippincottRaven Publishers; 1996:783-810.
Fankhauser RL, Noel JS, Monroe SS, Ando TA, Glass RI. Molecular epidemiology
of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J Infect
Dis. 1998;178:1571-1578.
Centers for Disease Control and Prevention. Norwalk-like viral gastroenteritis in
US army trainees -- Texas, 1998. MMWR. 1999;48:225-227.
Hedberg CW, Osterholm MT. Outbreaks of foodborne and waterborne
viral gastroenteritis. Clin Microbiol Rev. 1993;6:199-210.
Parashar UD, Dow L, Fankhauser RL, et al. An outbreak of viral
gastroenteritis associated with consumption of sandwiches: implications for the control
of transmission by food handlers. Epidemiol Infect. 1998;121:615-621.
SALMONELLOSIS
Mahon BE, Ponka A, Hall WN, et al. An international outbreak of
Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J Infect
Dis. 1997;175:876-82.
Mermin J, Hoar B, Angulo FJ. Iguanas and Salmonella
marina infection in children: a reflection of the incidence of
reptile-associated salmonellosis in the United
States. Pediatrics. 1997;99:399-402.
Centers for Disease Control and Prevention. Multidrug-resistant
Salmonella serotype enteritidis infection associated with consumption of raw shell eggs, United
States, 1994-1995. MMWR. 1996;45:737-742.
SHIGELLOSIS
Sobel J, Cameron DN, Ismail J, et al. A prolonged outbreak of
Shigella sonnei infections in traditionally observant Jewish communities in North America caused by
a molecularly distinct bacterial subtype. J Infect Dis. 1998;177:1405-1408.
Mohle-Boetani JC, Stapleton M, Finger R, et al. Community-wide shigellosis: control
of an outbreak and risk factors in child day-care centers. Am J Public
Health. 1995;85:812-816.
Ries AA, Wells JG, Olivola D, et al. Epidemic
Shigella dysenteriae type 1 in Burundi: panresistance and implications for prevention. J Infect Dis.
1994;169:1035-1041.
Lee LA, Shapiro CN, Hargrett-Bean N, Tauxe RV. Hyperedemic shigellosis in the
United States: a review of surveillance data for 1967-1988. J Infect Dis.
1991;164:894-900.
Townes JM, Quick R, Gonzales O, et al. Etiology of bloody diarrhea in Bolivian
children: implications for empiric therapy. J Infect Dis. 1997;175:1527-1530.
TOXOPLASMOSIS
Centers for Disease Control and Prevention. CDC recommendations
regarding selected conditions affecting women's health. MMWR. 2000;49(No.
RR-2):57-75.
Centers for Disease Control and Prevention. Preventing congenital
toxoplasmosis. MMWR. 2000;49(No. RR-2):57-75.
Centers for Disease Control and Prevention. 1999 USPHS/IDSA guidelines for
the prevention of opportunistic infections in persons infected with
human immunodeficiency virus: US Public Health Service (USPHS) and Infectious
Diseases Society of America (IDSA). MMWR. 1999;48(No. RR-10):7-9.
TRICHINOSIS
Capo V, Dickson DD. Clinical aspects of infections with
Trichinella spp. Clin Microbiol. 1996;9:47-54.
Laurichesse H, Cambon M, Perre D, et al. Outbreak of trichinellosis in
France associated with eating horse meat. Com Dis Rep. 1997;7(5):R69-73.
MacLean JD, Viallet J, Law C, Staudt M: Trichinosis in the Canadian Arctic: Report
of five outbreaks and a new clinical syndrome. J Infect Dis. 1989;160:513.
TYPHOID FEVER
Mermin JH, Townes JM, Gerber M, et al. Typhoid fever in the United
States, 1985-1994: changing risks of international travel and increasing
antimicrobial resistance. Arch Intern Med. 1998;158:633-638.
Centers for Disease Control and Prevention. Typhoid immunization:
recommendations of the Advisory Committee on Immunization Practices. MMWR. 1994;43(No.
RR-14).
Ackers ML; Puhr ND; Tauxe RV; Mintz ED. Laboratory-based surveillance of
Salmonella serotype typhi infections in the United States: antimicrobial resistance on the
rise. JAMA. 2000;283:2668-73.
REFERENCES USED TO COMPILE FOODBORNE
ILLNESSES TABLES
Askew GL, Finelli L, Genese CA, Sorhage FE, Sosin DM, Spitalny KC. Boilerbasse:
an outbreak of methemoglobinemia in New Jersey in 1992. Pediatrics. 1994;94:381.
Bhat RV, Beedu SR, Ramakrishna Y, Munshi KL. Outbreak of
trichothecene mycotoxicosis associated with consumption of moulddamaged wheat products
in Kashmir Valley, India. Lancet. 1989;1:35.
Cartwright CP. Utility of Multiple-Stool-Specimen Ova and Parasite Examinations in
a High-Prevalence Setting. J Clin Microbiol. 1999;37:2408-2411.
Centers for Disease Control and Prevention. Prevention of hepatitis A through
active and passive immunization: Recommendations of the Advisory Committee
on Immunization Practices (ACIP). MMWR. 1999;48(No. RR-12).
Chien L, Robertson H, Gerrard JW. Infantile gastroenteritis due to water with
high sulfate content. Can Med Assoc J. 1968;99:102.
DuPont HL and The Practice Parameters Committee of the American College
of Gastroenterology. Guidelines on acute infectious diarrhea in adults. Am
J Gastroenterol. 1997;92:1962.
Eliason BC, Lewan RB. Gastroenteritis in children: principles of diagnosis
and treatment. Am Fam Physician. 1998;58:1769.
Fleming CA, Caron D, Gunn JE, Barry MA. A food borne outbreak of
Cyclospora cayetanensis at a wedding: clinical features and risk factors for illness. Arch
Intern Med. 1998;158:1121.
Guidelines for confirmation of foodborne-disease outbreaks. MMWR Appendix
B. 1996;45(SS-5):58.
Morgan MRA, Fenwick GR. Foodborne Illness: natural foodborne toxicants.
Lancet. 1990;336:1492.
Neill MA, Osterholm MT, Swerdlow DL. New threats from food borne
infections. Patient Care. July 15, 1994;47-71.
Rodrigue DC, Etzel RA, de Porras E, Velasquez OH, Tauxe RV, Kilbourne, EM, Blake
PA. Lethal paralytic shellfish poisoning in Guatemala. Am J Trop Med Hyg. 1990;42:267.
Schlech WF III. Listeria gastroenteritis: old syndrome, new pathogen. N Engl J
Med. 1997;336(2):130-132.
Seamens CM, Schwartz G. Foodborne illnesses: differential diagnosis and
targeted management. Emerg Med Ref. 1998;19:120.
Tangermann RH, Etzel RA, Mortimer L, Renner GD, Paschal DC. An outbreak of
a food-related illness resembling boric acid poisoning. Arch Environ Contm
Toxicol. 1992;90:228.
Tauxe RV, Hughes JM. Foodborne disease. In: Mandel GF, Bennett JE, Dohr R,
eds. Principles and Practices of Infectious Diseases, 4th ed. Churchill Livingstone: New
York; 1997;1012.
Wong CS, Jelacic S, Habeed RL, Watkins, SL, and Tarr, PI. The risk of
the hemolyticuremic syndrome after antibiotic treatment of Escherichia coli
O157:H7 infections. N Engl J Med. 2000;342:1930-6.
AVOID FOODBORNE ILLNESS: FIGHT BAC!™
The US food supply is among the safest in the world, but organisms that you
can't see, smell, or taste -- bacteria, viruses and tiny parasites -- are everywhere in
the environment. These microorganisms -- called pathogens -- can invade food
and cause illness, sometimes severe and even life-threatening illness, especially in
young children, older adults, and persons with weakened immune systems. In
pregnant women, foodborne illness can endanger their unborn babies.
The most common symptoms of foodborne illness are diarrhea, abdominal
cramps, vomiting, head or muscleaches, and fever. Symptoms usually appear 12 to 72
hours after eating contaminated food but may occur between 30 minutes and 4 weeks
later. Most people recover within 4 to 7 days without needing antibiotic treatment.
If symptoms are severe or the ill person is very young, very old, pregnant,
or already ill, call your doctor immediately.
Who Is At Risk
If you are among those at high risk, you need to be aware of and follow the
most current information on food safety. Young children, pregnant women, older
adults, and persons with weakened immune systems are at a higher risk for
foodborne illness. Immune systems may be weakened by medical treatments, such
as steroids or chemotherapy, or by conditions, such as AIDS, cancer, or diabetes.
You are also at increased risk if you suffer from liver disease or alcoholism or if
you have decreased stomach acidity (due to gastric surgery or the regular use
of antacids).
If You Are At Risk
If you face a higher risk of foodborne illness, you are advised not to eat:
Raw fish or shellfish, including oysters, clams, mussels, and scallops
Raw or unpasteurized milk or cheeses
Soft cheeses, such as feta, Brie, Camembert, blueveined,
and Mexicanstyle cheese (Hard cheeses, processed cheeses, cream
cheese, cottage cheese, and yogurt need not be avoided)
Raw or undercooked eggs or foods containing raw or lightly cooked
eggs, including certain salad dressings, cookie and cake batters, sauces,
and beverages such as unpasteurized egg nog (Foods made from
commercially pasteurized eggs are safe to eat)
Raw or undercooked meat or poultry
Raw sprouts (Alfalfa, clover, and radish)
Unpasteurized fruit or vegetable juices (These juices will carry a
warning label)
It is also important to reheat some foods that are bought precooked, because
they can become contaminated with pathogens after they have been processed
and packaged. These foods include: hot dogs, luncheon meats (cold cuts),
fermented and dry sausage, and other deli-style meat and poultry products. New
information on food safety is constantly emerging. Recommendations and precautions
for people at high risk are updated as scientists learn more about
preventing foodborne illness.
EVERYONE SHOULD FOLLOW THESE FOUR SIMPLE STEPS TO FOOD SAFETY
1. Clean: Wash hands and surfaces often.
Bacteria, viruses, and parasites can be spread throughout the kitchen and get
onto cutting boards, utensils, and countertops. Here's how to Fight
BAC!™:
Wash your hands with hot, soapy water before and after handling food and
after using the bathroom, changing diapers, and handling pets.
Wash your cutting boards, dishes, utensils, and countertops with hot,
soapy water after preparing each food item and before you go on to the next food.
Important: Rinse raw produce in water. Don't use soap or detergents.
If necessary, use a small vegetable brush to remove surface dirt.
2. Separate: Don't cross-contaminate.
Cross-contamination is the word for how bacteria, viruses, and parasites can
be spread from one food product to another. This is especially true when handling
raw meat, poultry, seafood, and eggs, so keep these foods and their juices away
from ready-to-eat foods. Here's how to Fight
BAC!™:
Separate raw meat, poultry, and seafood from other foods in your grocery
shop-ping cart and in your refrigerator.
If possible, use a different cutting board for raw meat, poultry and
seafood products.
Always wash hands, cutting boards, dishes, and utensils with hot, soapy
water after they come in contact with raw meat, poultry, seafood, and eggs.
Use separate plates for cooked food and raw foods.
3. Cook: Cook to proper temperatures.
Food safety experts agree that foods are properly cooked when they are
heated for a long enough time and at a high enough temperature to kill the harmful
pathogens that cause foodborne illness. The best way to Fight
BAC!™ is to:
Use a clean thermometer that measures the internal temperature of cooked
food to make sure meat, poultry, and casseroles are cooked to the temperatures
in the chart at right.
Cook eggs until the yolk and white are firm. If you use recipes in which
eggs remain raw or only partially cooked, use pasteurized eggs.
Fish should be opaque and flake easily with a fork.
When cooking in a microwave oven, make sure there are no cold spots
where pathogens can survive. For best results, cover food, stir, and rotate for
even cooking. If there is no turntable, rotate the dish by hand once or twice
during cooking.
Bring sauces, soups, and gravy to a boil when reheating. Heat other
leftovers thoroughly to at least 165°F.
4. Chill: Refrigerate promptly.
Refrigerate foods quickly because cold temperatures keep harmful pathogens
from growing and multiplying. So, set your refrigerator no higher than 40°F and the
freezer at 0°F. Check these temperatures occasionally with an appliance thermometer.
Then, Fight BAC!™ by following these steps:
Refrigerate or freeze perishables, prepared foods, and leftovers within two
hours or sooner.
Never defrost food at room temperature. Thaw food in the refrigerator,
under cold running water, or in the microwave.
Marinate foods in the refrigerator.
Divide large amounts of leftovers into shallow containers for quick cooling in
the refrigerator.
Don't pack the refrigerator. Cool air must circulate to keep food safe.
US Department of Agriculture, Meat and Poultry
Hotline --- 800 535-4555, TTY: 800 2567076
US Food and Drug Administration, Food Information
Hotline --- 888 SAFEFOOD www.foodsafety.gov
Safe Cooking Temperatures
Raw food
Internal temperature
Ground Products
Hamburger
Beef, veal, lamb, pork
160° F
160° F
Beef, Veal, Lamb
Roasts & steaks medium-rare
medium
well-done
145° F
160° F
170° F
Pork
Chops, roasts, ribs medium
well-done
Ham, fresh
Sausage, fresh
160° F
170° F
160° F
160° F
Poultry
Chicken, whole & pieces
Duck
Turkey (unstuffed)
Whole
Breast
Dark meat
Stuffing (cooked separately)
180° F
180° F
180° F
180° F
170° F
180° F
165° F
Eggs
Fried, poached
Casseroles
Sauces, custards
Yolk & white are firm 160° F
160° F
Seafood
Fin Fish
Flesh opaque & flakes
easily with fork
Shrimp, Lobster &
Crabs
Shells red and flesh pearly & opaque
Clams, Oysters &
Mussels
Shells are open
PROGRAM EVALUATION FORM
Please circle your answers and add comments as desired. Please fax this
form back to: L J Tan, PhD at 312 4645841, or see back side for mailing instructions.
1. The primer increased my ability to recognize foodborne illnesses and increased
the likelihood that I will consider such illnesses in my patients.
1. Strongly agree 2. Agree 3. Undecided
4. Disagree 5. Strongly disagree
Comment:
2. The primer increased my knowledge and skills in the diagnosis and management
of foodborne illnesses.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
3. This primer increased my knowledge of the role of public health authorities in
the prevention and control of foodborne disease outbreaks.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
4. It is important to talk to my patients about food safety.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
5. As formatted, this primer is a useful physician education tool. 1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
6. The amount of information presented was appropriate for my needs.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
7. I will recommend this primer to my colleagues. 1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
8. I would like to receive regular updates of this primer.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
9. I would like to see a similar physician education program for other clinical issues.
1. Strongly agree 2. Agree 3. Undecided 4. Disagree 5. Strongly disagree
Comment:
10. How long did it take you to work through this primer?
Provide any additional comments about this primer, your experiences
with foodborne illnesses, and suggestions for future physician education efforts:
Please fax the completed survey to: L J Tan, PhD at 312 464-5841 or fold on
the dotted lines with the mailing side out, tape, and mail this form back with first
class postage. Thank you.
Diagnosis and Management of Foodborne Illnesses: A Primer for Physicians is produced by
American Medical Association
Centers for Disease Control and Prevention
Center for Food Safety and Applied Nutrition, Food and Drug Administration
Food Safety and Inspection Service, US Department of Agriculture
First class postage required
Diagnosis and Management of Foodborne Illnesses
Program Evaluation (c/o L J Tan)
American Medical Association
515 N. State Street
Chicago, Illinois 60610
All MMWR HTML versions of articles are electronic conversions from ASCII text
into HTML. This conversion may have resulted in character translation or format errors in the HTML version.
Users should not rely on this HTML document, but are referred to the electronic PDF version and/or
the original MMWR paper copy for the official text, figures, and tables.
An original paper copy of this issue can be obtained from the Superintendent of Documents,
U.S. Government Printing Office (GPO), Washington, DC 20402-9371; telephone: (202) 512-1800.
Contact GPO for current prices.
**Questions or messages regarding errors in formatting should be addressed to
[email protected].
