NIAID - Health Matters

April 2002

Foodborne Diseases

Overview
Preventing Foodborne Diseases
Botulism
Campylobacteriosis
E. coli Infection
Salmonellosis
Shigellosis
NIAID Research
For More Information

Overview

Infectious diseases spread through food or beverages are a common, distressing, and sometimes life-threatening problem for millions of people in the United States and around the world. The U.S. Centers for Disease Control and Prevention (CDC) estimates 76 million people suffer foodborne illnesses each year in the United States, accounting for 325,000 hospitalizations and more than 5,000 deaths.

Foodborne disease is extremely costly. Health experts estimate that the yearly cost of all foodborne diseases in this country is $5 to $6 billion in direct medical expenses and lost productivity. Infections with the bacteria Salmonella alone account for $1 billion yearly in direct and indirect medical costs.

There are more than 250 known foodborne diseases. Bacteria cause most cases, followed by viruses and parasites. Natural and manufactured chemicals in food products also can make people sick. Some diseases are caused by toxins (poisons) from the disease-causing organism, others by bodily reactions to the organism itself. People infected with foodborne germs may have no symptoms or develop symptoms ranging from mild intestinal discomfort to severe dehydration and bloody diarrhea.

Recently, public health, agriculture, and environmental officials have expressed growing concern over keeping the nation's food and water supply safe from terrorist acts. This bioterrorism threat is being studied by a number of U.S. agencies, including the Food and Drug Administration, Department of Agriculture, Centers for Disease Control and Prevention, Environmental Protection Agency, and National Institutes of Health.

This fact sheet will describe five foodborne diseases caused by bacteria.

  • Botulism
  • Campylobacteriosis
  • E. coli infection
  • Salmonellosis
  • Shigellosis

Preventing Foodborne Diseases

Many times, foodborne diseases are easy to avoid. These are some basic ways to prevent being infected by most foodborne germs. Specific ways to avoid getting sick from foodborne organisms are described in the sections on foodborne diseases
  • Wash hands carefully before preparing food.
  • Wash hands, utensils, and kitchen surfaces with hot soapy water after they touch raw meat or poultry.
  • Cook beef and beef products thoroughly, especially hamburger.
  • Cook poultry and eggs thoroughly.
  • Eat cooked food promptly and refrigerate leftovers within 2 hours after cooking.
  • Wash fruits and vegetables thoroughly, especially those that will be eaten raw.
  • Drink only pasteurized milk and juices and treated surface water.
  • Wash hands carefully after using the bathroom, changing infant diapers, or cleaning up animal feces.

Botulism

Botulism is a rare but serious illness caused by botulinum toxin (poison) produced by Clostridium botulinum bacteria. This toxin affects the nerves and if untreated, can cause paralysis and respiratory failure. U.S. health care providers report an average of 110 cases of food, infant, and wound botulism to CDC each year. About 10 to 30 outbreaks of foodborne botulism are reported every year. Although this illness does not occur frequently, it can be fatal if not treated quickly and properly.

How is C. botulinum transmitted?

Often, cases of foodborne botulism come from home-canned foods with low acid content, such as asparagus, green beans, beets, and corn. C. botulinum is anaerobic, which means it can survive and grow with little or no oxygen. Therefore, it can survive very well in sealed containers. Outbreaks of the infection, however, are often from more unusual sources such as chili peppers, tomatoes, and improperly handled baked potatoes wrapped in aluminum foil.

What are the symptoms of foodborne botulism?

  • Double vision and drooping eyelids
  • Slurred speech
  • Dry mouth and difficulty swallowing
  • Weak muscles

Symptoms of foodborne botulism usually begin within 18 to 36 hours after eating contaminated food, but can occur in as few as 6 hours or as much as 10 days afterward.

How is it diagnosed?

A health care provider can use laboratory tests to identify C. botulinum toxin in the blood or stool of an infected person.

How is foodborne botulism treated?

If diagnosed early, health care providers can treat foodborne botulism successfully with an antitoxin that blocks the action of the bacterial toxin circulating in the blood. Although antitoxin keeps the disease from becoming worse, recovery still takes many weeks. Sometimes doctors try to remove contaminated food still in the gut by making the patient vomit or by giving the patient an enema.

Patients who develop severe botulism experience breathing failure and paralysis and need to be put on ventilators (breathing machines).

Can botulism lead to other health problems?

If left untreated, this illness can cause paralysis of the arms, legs, trunk, and muscles that help with breathing. The paralysis usually improves slowly over several weeks.

C. botulinum toxin is one of the most potent toxins known in nature. Exposure to the toxin, particularly in an aerosolized form, can be fatal. It has been weaponized by rogue states and is a focus of current counter-bioterrorism efforts.

Some ways to prevent foodborne botulism.

  • Follow strict hygienic steps when home canning.
  • Refrigerate oils with garlic or herbs.
  • Keep baked potatoes wrapped in aluminum foil hot until served, or refrigerate them.
  • Consider boiling home-canned food before eating it, to kill any bacteria which might lurk in the food.

Can C. botulinum be used for good purposes?

In 1989, the U.S. Food and Drug Administration (FDA) approved Botulinum Toxin Type A, a protein produced by C. botulinum, as a treatment for two eye muscle disorders, and in 2000, to treat cervical dystonia, a neurological movement disorder causing severe neck and shoulder contractions. In April 2002, FDA approved this toxin to temporarily improve the appearance of moderate to severe frown lines between the eyebrows.

Campylobacteriosis

Campylobacteriosis is an infectious disease caused by Campylobacter bacteria. Campylobacter jejuni, C. fetus, and C. coli are the types that usually cause campylobacteriosis in people. C. jejuni causes most cases of the illness.

According to CDC, C. jejuni is the leading cause of bacterial diarrheal illness in the United States, affecting an estimated 2.4 million people every year. The bacteria cause between 5 and 14 percent of all diarrheal illness worldwide. C. jejuni primarily affects children under 5 years old and young adults (15-29 years old). Health care providers report more than 10,000 cases to CDC yearly. In the United States, few people die from Campylobacter infection.

How is Campylobacter transmitted?

Humans can get infected from handling raw poultry, eating undercooked poultry, drinking nonchlorinated water or raw milk, or handling infected animal or human feces. Most frequently, poultry and cattle waste are the sources of the bacteria, but feces from puppies, kittens, and birds also may be contaminated.

What are the symptoms of campylobacteriosis?

  • Diarrhea (often bloody)
  • Abdominal cramping and pain
  • Nausea and vomiting
  • Fever
  • Tiredness

Some infected people have no symptoms. Campylobacteriosis usually lasts for 2 to 5 days, but in some cases as long as 10 days. Rarely, some people have convulsions with fever or meningitis.

How is it diagnosed?

A health care provider can use laboratory tests to identify Campylobacter in the stool of an infected person.

How is it treated?

Most people infected with Campylobacter will get better with no special treatment. If a person needs treatment, a health care provider can prescribe an antibiotic such as ciprofloxacin or azithromycin. Erythromycin helps treat diarrhea caused by Campylobacter. Those with diarrhea should drink plenty of water.

Can campylobacteriosis lead to other health problems?

Some people infected with Campylobacter develop arthritis.

A small number of people with campylobacteriosis may develop Guillain-Barré Syndrome (GBS), the leading cause of acute paralysis in this country. This rare condition develops from 2 to 4 weeks after Campylobacter infection and usually after diarrheal symptoms have disappeared. People with GBS suffer from increasing paralysis of the limbs which lasts for several weeks. In more severe cases, they develop breathing problems requiring very long hospital stays.

Ways to prevent campylobacteriosis.

  • Wash hands before preparing food.
  • Wash hands immediately after handling raw poultry or other meat.
  • Wash all food preparation surfaces and utensils that have come in contact with raw meat thoroughly with soap and hot water.
  • Cook poultry products to an internal temperature of 170 degrees Fahrenheit for breast meat and 180 degrees Fahrenheit for thigh meat.
  • Drink pasteurized milk and chlorinated or boiled water.
  • Wash hands after handling pet feces or visiting zoos and petting zoos.

E. coli Infection

Certain types of Escherichia coli bacteria, commonly called E. coli can cause foodborne illness. Harmless strains of E. coli can be found widely in nature, including the intestinal tracts of humans and warm-blooded animals. Disease-causing strains, however, are a frequent cause of both intestinal and urinary-genital tract infections.

Several different strains of harmful E. coli can cause diarrheal disease. A particularly dangerous type is called enterohemorrhagic E. coli, or EHEC. EHEC often causes bloody diarrhea and can lead to kidney failure in children or people with weakened immune systems.

In 1982, scientists identified the first dangerous strain in the United States. The type of harmful E. coli most commonly found in this country is named O157:H7, which refers to chemical compounds found on the bacterium's surface. This type produces one or more related, powerful toxins which can severely damage the lining of the intestines.

Other types, including O26:H11 and O111:H8, also have been found in this country and can cause human disease.

Cattle are the main sources of E. coli O157:H7, but other domestic and wild mammals also can harbor these bacteria.

How is E. coli transmitted?

E. coli bacteria and its toxins have been found in
  • Undercooked or raw hamburgers
  • Salami
  • Alfalfa sprouts
  • Lettuce
  • Unpasteurized milk, apple juice, and apple cider
  • Contaminated well water

Unsuspecting swimmers have been infected by accidentally swallowing unchlorinated or underchlorinated water in swimming pools contaminated by human feces. People also can get infected by swimming in sewage-contaminated water.

What are the symptoms of E. coli 0157:H7 infection?

E. coli toxin can damage the lining of the intestine and cause other symptoms including
  • Nausea
  • Severe abdominal cramps
  • Watery or very bloody diarrhea
  • Tiredness
  • Vomiting (occasionally)

Occasionally, people develop low-grade fever or vomiting. Symptoms usually begin from 2 to 5 days after eating contaminated food and may last for 8 days.

How is E. coli diagnosed?

A health care provider can use laboratory tests to identify E. coli in the stool of an infected person.

How is E. coli O157:H7 infection treated?

Most people recover from E. coli infection within 5 to 10 days without treatment. Antibiotics are usually not helpful, and health care experts recommend against taking antidiarrheal medicines.

Can E. coli 0157:H7 infection lead to other health problems?

Hemolytic uremic syndrome (HUS), a serious complication of EHEC, can lead to kidney failure. In North America, HUS is the most common cause of acute kidney failure in children, who are particularly prone to this complication. This life-threatening condition is usually treated in an intensive care unit of a hospital, sometimes with blood transfusions and kidney dialysis.

Some ways to prevent E. coli 0157:H7 infection

  • Eat only thoroughly cooked beef and beef products.
  • Cook ground beef patties to an internal temperature of 160 degrees Fahrenheit.
  • Avoid unpasteurized juices.
  • Drink only pasteurized milk.
  • Wash fresh fruits and vegetables thoroughly before eating raw or cooking.

Other types of E. coli can cause diarrheal disease

Enterotoxigenic E. coli (ETEC), which produce a toxin similar to Cholera toxin, can cause diarrhea. These strains typically cause so-called travelers diarrhea because they are prevalent contaminants in food and water in developing countries.

Enteropathogenic E. coli (EPEC) are associated with persistent diarrhea (lasting 2 weeks or more) and are more common in developing countries where they can be transmitted by contaminated water or contact with infected animals. Health experts do not know how much disease some of these other types of E. coli cause in the United States.

Salmonellosis

Salmonellosis, or salmonella, is an infection caused by Salmonella bacteria. Salmonella infections are increasing in the United States. Many types of this bacteria cause disease in animals and people. While the occurrence of different types of Salmonella varies from country to country, Salmonella typhimurium and S. enteritidis are the two most commonly found in the United States.

In 1984, an antibiotic-resistant strain of S. typhimurium, called Definitive Type 104 (DT104), was first found in the United Kingdom and recently in the United States. Now it is the second most common strain (after S. enteritidis) of Salmonella found in humans. This strain poses a major new threat because it is resistant to several antibiotics normally used to treat people with Salmonella infections.

Salmonellosis may occur in small, contained outbreaks in the general population or in large outbreaks in hospitals, restaurants, or institutions for children or the elderly. While the disease is found worldwide, health experts most often report cases in North America and Europe. Every year, CDC receives reports of 40,000 cases of salmonellosis in the United States. The agency estimates that 1.4 million people in this country are infected, however, and that 1,000 people die each year with salmonellosis. Symptoms are most severe in the elderly, infants, and people with chronic conditions. People with AIDS are particularly vulnerable salmonellosis-often suffering from recurring episodes.

How is foodborne Salmonella transmitted?

Salmonella bacteria can be found in food products such as raw poultry, eggs, and beef, and sometimes on unwashed fruit. Food prepared on surfaces that previously contained raw meat or meat products can, in turn, become contaminated with the bacteria. This is called cross-contamination.

In the past few years, CDC has received reports of several cases of salmonellosis from eating raw alfalfa sprouts grown in contaminated soil. Salmonella infection frequently occurs after handling pets, particularly reptiles like snakes, turtles, and lizards.

Salmonellosis can become a chronic infection in some people who may not have symptoms. Though they may have no symptoms, they can spread the disease by not by not washing their hands before preparing food for others. In fact, health care experts recommend that people who know they have salmonellosis not prepare food or pour water for others until a laboratory tests show they no longer carry Salmonella.

What are the symptoms of salmonellosis?

  • Diarrhea
  • Fever
  • Abdominal cramps
  • Headache

In most people, symptoms begin from 12 hours to 3 days after being infected. These symptoms, along with possible nausea, loss of appetite, and vomiting, usually last for 4 to 7 days. Diarrhea can be severe and require hospitalization.

How is it diagnosed?

A health care provider can use laboratory tests to identify Salmonella in the stool of an infected person.

How is salmonellosis treated?

Most cases of salmonellosis clear up within 5 to 7 days and don't require treatment. People with severe diarrhea may need intravenous fluids. If the infection spreads from the intestines into the bloodstream, health care providers can treat it with antibiotics such as ampicillin.

Can salmonellosis cause other health problems?

While most people recover successfully from salmonellosis, a few may develop a chronic condition called Reiter's syndrome. This syndrome can last for months or years and can lead to arthritis. Its symptoms are
  • Painful joints
  • Irritated eyes
  • Painful urination

Unless treated properly, Salmonella can escape from the intestine and spread by blood to other organs, sometimes leading to death.

Typhoid fever, a more serious disease, results from infection with S. typhi. This disease, which can be fatal if untreated, is not common in the United States. It is frequently found in developing countries, usually in contaminated water. It's also a risk in areas where flooding or earthquakes cause sewer systems to overflow.

Appropriate antibiotics are usually effective for treating typhoid fever, although the incidence of antibiotic-resistant S. typhi is increasing is some parts of the world.

Ways to prevent foodborne salmonellosis.

  • Drink only pasteurized milk.
  • Cook poultry and eggs thoroughly.
  • Don't eat foods containing raw eggs, such as homemade caesar salad dressing, cookie dough, and hollandaise sauce or drink homemade eggnog made with raw eggs.
  • Handle raw eggs carefully.
    • Keep eggs refrigerated.
    • Throw away cracked or dirty eggs.
  • Cook eggs thoroughly.
  • Cook poultry products to an internal temperature of 170 degrees Fahrenheit for breast meat and 180 degrees Fahrenheit for thigh meat.
  • Wash all food preparation surfaces and utensils that have come in contact with raw poultry or raw eggs with soap and hot water.
  • Wash hands immediately after handling raw poultry or raw eggs.
  • Wash hands immediately after handling reptiles or contact with pet feces.

Shigellosis

Shigellosis, also called bacillary dysentery, is an infectious disease caused by Shigella bacteria. Four main types of Shigella cause infection: Shigella dysenteriae, S. flexneri, S. boydii, and S. sonnei. CDC estimates that more than 400,000 cases occur every year in the United States. Health care providers report about 18,000 cases to CDC each year. Most cases in this country are caused by S. sonnei.

How are Shigella bacteria transmitted?

People can be infected from foodborne Shigella by
  • Eating food or drinking beverages contaminated by food handlers infected with Shigella who didn't wash their hands properly after using the bathroom.
  • Eating vegetables grown in fields containing sewage.
  • Eating food contaminated by flies which were bred in infected feces.
  • Drinking or swimming in contaminated water.

S. sonnei is the most common type of Shigella in developed countries, including the United States. Outbreaks of shigellosis frequently occur in tropical or temperate climates, especially in areas with severe crowding and/or poor hygiene, which sometimes occur in day care and institutional settings.

Some people have no symptoms but can still pass the bacteria to others. An extremely low number of organisms (10-100) is needed to transmit Shigella. Therefore, it is commonly transmitted by food service workers who are sick or infected, but have no symptoms, and who do not properly wash their hands after using the toilet. Those who know they have shigellosis should not prepare food or pour water for others until laboratory test show they no longer carry Shigella bacteria.

What are the symptoms of shigellosis?

  • Fever
  • Tiredness
  • Watery or bloody diarrhea
  • Nausea and vomiting
  • Abdominal pain

Symptoms usually begin within 2 days after being exposed to Shigella. Symptoms usually are gone within 5 to 7 days.

How is shigellosis treated?

People with mild infections usually get better quickly, without taking medicine. When treatment is necessary, health care providers usually prescribe an antibiotic such as ampicillin or ciprofloxacin. Antidiarrheal medicines may make the illness worse.

Can shigellosis lead to other health problems?

People who had diarrhea symptoms usually recover completely, although their bowel habits may not return to normal until several months later. S. dysenteriae type 1 produces Shiga toxin and can lead to life-threatening hemolytic uremic syndrome (HUS), the same complication that develops in some cases of infection with E. coli (enterohemorrhagic E. coli or EHEC).

S. flexneri infection can progress to Reiter's syndrome which can last for months or years and can lead to chronic arthritis. Its symptoms are

  • Painful joints
  • Irritated eyes
  • Painful urination

Ways to prevent shigellosis.

  • Wash hands thoroughly with soap and water before preparing foods and beverages.
  • Wash hands thoroughly after using the bathroom or changing infant diapers.
  • Disinfect diaper-changing areas after use.
  • Help young children wash their hands carefully after they use the bathroom.
  • Avoid swallowing swimming pool water.

NIAID Research

The National Institute of Allergy and Infectious Diseases (NIAID), is the federal government's lead agency for conducting and funding research on many infectious diseases. Scientists at the Institute and NIAID-supported scientists are using basic, clinical, and applied research to better understand how to detect, treat, and prevent foodborne diseases.

Basic research is helping scientists to better understand how pathogens (germs) spread by contaminated food or water cause disease in humans. NIAID-supported researchers are studying the bacterial genes that help pathogens establish themselves in the human body and cause disease. For example, scientists have identified genes that appear to be involved in signaling certain immune system cells to cause inflammation, and which may contribute to the development of diarrhea.

Other NIAID-sponsored research focuses on methods by which the organism grows and interacts in host cells. Scientists have discovered that some intestinal bacteria recognize when they are in a human host and respond by activating a particular set of powerful genes that enable the organism to live in the host and cause disease. Future studies will define new ways to intervene, whether by prevention or treatment, in the disease process.

NIAID supports several research studies on E. coli 0157:H7 (EHEC).

Researchers have sequenced the genome of E. coli 0157:H7 (EHEC) and compared it with the genome of the harmless E. coli K12. Seventy percent of the two genomes are identical, and the genome of E. coli 0157:H7 is about 30 percent larger than K12. As researchers compare and contrast these and other strains of E. coli, their ability to answer key questions in evolution and disease processes will become easier.

Researchers are working to develop and test monoclonal antibodies to treat EHEC infection, thus preventing hemolytic uremic syndrome (HUS) from developing. (Scientists use monoclonal antibodies as tools for binding to specific protein molecules. As such, they are invaluable in research, medicine, and industry.)

Investigators are further defining the ways by which the toxins produced by EHEC and Shigella result in the kidney damage leading to HUS. The primary goal of this research is to better understand how kidney vascular disease progresses. Researchers are developing antitoxins that may help prevent HUS from developing in infected children.

Researchers also are exploring vaccines to prevent EHEC and Shigella infections in animals or people.

NIAID-supported scientists found that children with bloody diarrhea should not be treated with antibiotics. Antibiotics can lead to the release of more bacterial toxins and further kidney damage, including subsequent HUS.

Cholera is a major source of water- and foodborne sickness and death in the developing countries of Asia, Africa, and South America, particularly during epidemics and in refugee settings. Scientific studies have shown that Vibrio cholerae bacteria, which cause cholera, constantly adapt to changes in the environment.

Individual Cholera bacteria can join together to form large mats called biofilms. NIAID-supported scientists recently have sequenced the genome of V. cholerae and have identified a gene family that allows the bacteria to form biofilms. Biofilms protect the bacteria from environmental stresses and makes the pathogen more resistant to being disinfected by chlorine. When conditions become favorable, other genes allow the bacteria to revert to their original forms. This is one method V. cholerae uses to survive harsh conditions. Better understanding of how the pathogen can shift will help researchers develop new ways to control it during epidemics.

In addition to the genomic studies mentioned above, scientists have determined the complete genome sequences for Salmonella typhi, S. typhimurium, and Campylobacter jejuni. Sequencing studies are underway for Shigella, Yersinia, and other harmful strains of E. coli. Scientists hope this new information will speed the discovery of new targets for treatments and vaccines against foodborne pathogens.

Through preliminary tests of live, attenuated Shigella flexneri vaccine candidates, scientists have discovered two new toxins that may contribute to the diarrhea associated with Shigella species. Studies are under way to find out how these toxins cause fluid loss. The findings will provide crucial information on how to improve attenuated vaccines to prevent shigellosis.

The NIAID enteric diseases program also supports basic and clinical research on other water- and foodborne pathogens including Vibrio cholerae, Helicobacter pylori, Yersinia, Listeria, Clostridia, Bacteroides, Staphylococcus and effects of toxins on the intestinal tract.

NIAID supports an Enteric Pathogens Research Unit to carry out research on the immune response that takes place in the mucous membrane lining of the gut. Because foodborne pathogens universally affect this lining, these studies will give researchers information needed to make vaccines or develop treatment for diseases these pathogens cause. The research includes

  • conducting clinical trials of vaccine candidates
  • using adjuvants, delivery systems, or dosing schedules to help scientists find out how best to increase the immune response to vaccines
  • studying mucosal immunity

In addition to the organisms mentioned above, NIAID conducts research on gastrointestinal viruses that cause diarrhea such as caliciviruses, rotavirus, astrovirus, and hepatitis A virus. Scientists at the NIAID Laboratory of Infectious Diseases in Bethesda, Md., devised the first method for detecting Norwalk virus (a particular calicivirus) particles and for measuring Norwalk virus-specific antibodies (disease-fighting proteins).

Current studies are trying to produce new vaccines including edible vaccines against Norwalk virus and hepatitis A. NIAID scientists developed a recently licensed inactivated vaccine for hepatitis A virus infection.

For More Information

National Institute of Allergy and Infectious Diseases
National Institutes of Health
31 Center Drive, MSC 2520
Bethesda, MD 20892-2520
http://www.niaid.nih.gov

National Library of Medicine
MEDLINEplus
8600 Rockville Pike
Bethesda, MD 20894
1-800-338-7657
http://medlineplus.gov

U.S. Centers for Disease Control and Prevention
National Center for Infectious Diseases
Division of Bacterial and Mycotic Diseases
Atlanta, GA 30333
1-888-232-3228
http://www.cdc.gov

U.S. Department of Agriculture
Food Safety and Inspection Service
1400 Independence Avenue SW, Room 2932-S
Washington, DC 20250-3700
1-800-535-4555 or 202-720-3333
TTY: 1-800-256-7072
http://www.fsis.usda.gov

U.S. Environmental Protection Agency
1200 Pennsylvania Avenue, NW
Washington, DC 20460
202-260-2090
http://www.epa.gov

U.S. Food and Drug Administration
Center for Food Safety and Applied Nutrition
5100 Paint Branch Parkway
College Park, MD 20740-3835
1-888-SAFEFOOD (1-888-723-3663)
http://vm.cfsan.fda.gov/list.html
http://www.cfsan.fda.gov/~dms/fsterrqa.html (food safety and bioterrorism)

Federal, state, and local government information:
http://www.foodsafety.gov

World Health Organization
Avenue Appia 20
1211 Geneva 27
Switzerland
41-22-791-21-11
http://www.who.int


NIAID is a component of the National Institutes of Health (NIH), which is an agency of the Department of Health and Human Services. NIAID supports basic and applied research to prevent, diagnose, and treat infectious and immune-mediated illnesses, including HIV/AIDS and other sexually transmitted diseases, illness from potential agents of bioterrorism, tuberculosis, malaria, autoimmune disorders, asthma and allergies.

News releases, fact sheets and other NIAID-related materials are available on the NIAID Web site at http://www.niaid.nih.gov.

Prepared by:
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National Institute of Allergy and Infectious Diseases
National Institutes of Health
Bethesda, MD 20892


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Last Updated November 20, 2003 (alt)