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Silent VictoriesThe History and Practice of Public Health in Twentieth Century America$

John W. Ward and Christian Warren

Print publication date: 2006

Print ISBN-13: 9780195150698

Published to Oxford Scholarship Online: September 2009

DOI: 10.1093/acprof:oso/9780195150698.001.0001

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Advances in Food Safety to Prevent Foodborne Diseases in the United States

Advances in Food Safety to Prevent Foodborne Diseases in the United States

(p.18) 2 Advances in Food Safety to Prevent Foodborne Diseases in the United States
Silent Victories

Robert V. Tauxe

Emilio J. Esteban

Oxford University Press

Abstract and Keywords

In the United States, the current food supply is broader and far safer than it was 100 years ago. At the start of the 20th century, contaminated foods frequently caused botulism, typhoid fever, septic sore throat, and trichinosis, diseases that now rarely occur. Along with drinking water treatment, sewage sanitation, and pasteurization, food-safety measures have become routine; these measures have been developed and initiated in response to specific public health threats and are continually evolving. The shift of the U.S. food supplies from small local farms to huge global agribusinesses has opened new niches for pathogens, as well as the potential for more systematic disease prevention. The methods public health authorities use to detect, investigate, and understand these public health threats have also advanced over the last century. This chapter, which addresses the progress achieved in the field of food safety, serves to support the continuing effort to make food safer.

Keywords:   public health, 20th century, history, food safety, food regulation, food supply, epidemics, pasteurization, Food and Drug Administration, germ theory

In the United States, the food supply is both broader and far safer than it was 100 years ago. At the start of the twentieth century, contaminated foods frequently caused typhoid fever, septic sore throat, and trichinosis—diseases that now rarely occur. Along with the treatment of drinking water and sewage sanitation, food-safety measures have become routine; these measures have been developed and initiated in response to specific public health threats and are continually evolving. At the same time, the shift of the U.S. food supply from small, local farms to huge, global agribusinesses has opened new niches for pathogens, as well as the potential for more systematic disease prevention. The methods public health authorities use to detect, investigate, and understand these public health threats have also advanced over the last century. This chapter, which addresses the progress achieved in the field of food safety, serves to support the continuing effort to make food safer.

The Social Setting of the Food Supply in 1900

In 1900, the United States was predominantly rural. The census conducted that year found 60% of the population living in rural areas, and another 14% living in towns of fewer than 25,000 persons.1 Farmers constituted 38% of the labor force. Whereas grain milling and meatpacking industries were centralized in the Midwest, most other foods were produced in dairies, truck farms, and other local food industries located near the consumer. Many foods were available only seasonally, and domestic (p.19) iceboxes provided limited refrigeration. Fresh foods were supplemented by canned goods, which had become available after the Civil War, though concerns about their safety and quality limited their general acceptance.2 Kitchen gardens supplied produce, and much food processing occurred in the home, from slaughter and plucking of live fowl to making sausages and preserves. A popular cookbook from 1871, written for a general homemaking audience, gave instructions for making pickles, preserves, catsup, ginger beer, and dehydrated soup at home in addition to providing recipes for the principal meals.3 Because of the substantial effort required to provide food at the household level, middle-class households in that era required a staff. The 1900 census revealed that 9% of the nonagricultural working population reported their occupation as housekeeper or servant.1

Cities with increasing populations were just beginning to appreciate the benefits of treated municipal water supplies and sewage collection systems at the turn of the century,4 ,5 although sewer systems still poured waste into lakes and rivers that served as the water supply. In 1900, only 6% of the population had access to water that was filtered, and 24.5% of the urban population had sewerage.5

The Impact of Foodborne Diseases Early in the Twentieth Century and the Public Health Response

In 1900, American life expectancy at birth was 47 years. In Massachusetts, where vital statistics records were maintained, the infant mortality rate was 141 per 1000 live births.6 Fifteen years later, when national infant mortality was first reported, the rate was 100 per 1000 live births.6 Foodborne and waterborne diseases were substantial contributors to mortality. In 1900, the annual rate for death caused by gastroenteritis was 142 per 100,000 persons and that for typhoid fever was 31.3 per 100,000.6 Contaminated food and water likely were the primary sources of both illnesses. In 1928, the standard public health textbook covered only a fraction of the foodborne diseases discussed in today’s texts; these diseases included typhoid fever, bovine tuberculosis, septic sore throat (a severe streptococcal infection due to Streptococcus zooepidemicus and related strains), scarlet fever, trichinosis, botulism, and salmonellosis (see Table 2.1).7

Severe outbreaks of illness involving substantial numbers of cases captured public attention early in the twentieth century, when the cases were traced to seemingly safe food supplies. For instance, in 1911, one Boston dairy that operated with state-of-the-art cleanliness but without pasteurization caused 2000 cases of septic sore throat and 48 deaths.7 In 1919, a multistate botulism outbreak was recognized in Alliance, Ohio, where a luncheon at a country club made 14 attendees ill, killing seven.18 A detailed investigation implicated a glass jar of olives that had been commercially bottled in California. Though no statistical tests were applied, the link to the olives was clear from the food histories of the cohort of luncheon attendees and was confirmed by feeding laboratory animals the leftover olives. Within a few months, olives from the same bottling plant caused at least eight more deaths in similar outbreaks in Michigan and Tennessee; a botulism outbreak in Montana was traced to similar olives from a second California firm.19 Investigators at the Bureau of Chemistry, (p.20)

Table 2.1. Principal foodborne infectious threats identified in standard textbooks of 1928 and 1939, ranked by number of citations in index.

1928: Rosenau [7]

1939: Shrader [30]

Typhoid fever (Bacillus typhosus,


now Salmonella Typhi)



Bovine tuberculosis

Salmonellosis (Bacillus enteritidis.


now Salmonella)

Typhoid fever (Eberthella


typhosa, now Salmonella

Brucellosis, Malta fever


Tuberculosis (foodborne)


Septic sore throat (Streptococcus


epidemicus, now Streptococcus

Septic sore throat


Staphylococcal food poisoning

Streptococcal scarlet fever



forerunner of today’s Food and Drug Administration, discovered that the jars were not heated sufficiently at the packing plant to kill the botulism spores. However, the Bureau of Chemistry lacked authority to halt a food processor even after it was shown to produce unsafe food. It could only seize batches of processed food that were proved to be contaminated by laboratory testing. The bureau could only warn the public that if they wished to reduce their risk of dying of botulism, they should avoid eating olives packed in glass.19

In 1924, raw oysters caused a nationwide outbreak of typhoid fever. A team of public health officials documented 1500 cases and 150 deaths in 12 cities, from New York to San Francisco. The investigators gathered food-consumption histories from patients, surveyed large numbers of healthy persons about their eating habits, and interviewed cohorts of persons who had eaten the oysters.20 Although no statistics were applied, the investigation exemplified the case-control method. Investigators reported that in New York City, 176 of 246 typhoid fever victims had eaten raw oysters within 30 days of illness, while only 28 of 275 healthy persons living in the same area had done so; both ill and well persons ate tomatoes and lettuce with the same frequency. One New York company was determined to be the source of the implicated oysters; this company stored the harvested oysters in freshwater pens, a practice known as floating. The pens were located near a wharf where boats dumped sewage into the water. As a result of this outbreak, many consumers lost confidence in eating oysters, leading to the formation of the National Shellfish Sanitation Program in 1925. The program encouraged standard regulations and industry practices that would keep oysters away from human sewage by monitoring shellfish-growing waters for sewage contamination and prohibiting the floating of oysters and other dangerous practices.21 This program continues to operate into the twenty-first century as the Interstate Shellfish Sanitation Conference.

(p.21) Microbial Investigations of Foodborne Pathogens

By the start of the twentieth century, European bacteriologists had identified the microbial cause of some foodborne infections by using newly developed laboratory methods. Diagnosis of specific infections replaced the pre-microbiological concept of ptomaines, which were injurious substances believed to form spontaneously in spoiled food. In 1884, Georg Gaffky first cultivated the causative agent of typhoid fever, now called Salmonella Typhi, making possible the bacteriologic diagnosis of that common disease.8 In 1886, August A. H. Gaertner investigated an outbreak of 54 enteric illnesses among people who ate raw ground beef. The meat had come from a cow that died with severe diarrhea and was pronounced safe to eat after visual inspection. Gaertner isolated a bacterial pathogen, now called Salmonella Enteritidis, from the meat itself and from the spleen of a young man who had died following the consumption of the notorious meal, which first linked human salmonellosis to animal infection.9 In 1894, Emile-Pierre van Ermengem first isolated the bacterium Clostridium botulinum from suspect cured meat and from autopsy specimens during an investigation of a botulism outbreak.10 This discovery underlined the need for scientific evaluation of food processing and opened the door to many investigations of the impact of variations in food processing on the safety of food.

In the United States, the first public health laboratories were established at the end of the nineteenth century to perform basic analyses of milk and water and to diagnose typhoid fever and other communicable diseases.11 Massachusetts established a State Hygiene Laboratory in 1886; Providence, Rhode Island, did so in 1888, and California in 1905. State boards of health, initially staffed by volunteers, grew in size and professionalism; by 1915 these boards of health had been established in some form in every state.11 Outbreak investigations were coordinated through these departments. For instance, the first typhoid carrier was identified by the New York City Board of Health through use of epidemiologic and laboratory techniques.12 The carrier, who became known as Typhoid Mary, was a private cook who worked for several families in New York. In 1906, a familial outbreak of typhoid fever brought this cook to the attention of local public health authorities, who documented through bacteriologic testing that she was a chronic carrier. She was detained, but later was allowed to return to work as a cook, causing another outbreak of typhoid fever among hospital staff. Typhoid Mary ultimately was confined for life in a city hospital after causing at least 51 cases in 10 separate outbreaks of typhoid fever.

Local and state public health resources were supplemented by the federal Public Health and Marine Hospital Service (now called the U.S. Public Health Service). Founded in 1798 to provide medical care for sailors as part of the Department of Treasury, this uniformed service had grown in responsibility by the end of the nineteenth century. The Commissioned Corps of the service detected and treated communicable illness in immigrants and prevented interstate spread of epidemic disease. The first bacteriology laboratory of the Public Health and Marine Hospital Service opened on Staten Island in 1887. This laboratory was moved to Washington, D.C., in 1903, then known as the Hygienic Laboratory. Under Dr. Milton Rosenau, it became a premier research institution on milk safety and was the nucleus for the National Institutes of Health.13

(p.22) Food Safety Regulation in the Nineteenth and Twentieth Centuries

From the nineteenth century through the start of the twentieth century, regulatory control of food was driven by consumer health concerns and the partnership of local medical societies with honest businessmen and trade associations. Milk was one of the greatest concerns for regulators and consumers. Cows fed with cheap by-products of other industries (e.g., waste from cotton gins) gave bad-flavored milk. Producers could stretch supplies and improve the look and taste of inferior “swill milk” by adding water of dubious origin, magnesia, and chalk.14 In 1862, after 40 years of effort, the New York State Legislature passed an act that levied a fine on anyone selling impure or adulterated milk.14

The first law applying to food in general was passed by Illinois in 1874, and in 1879, the first federal bill to prevent food adulteration was introduced. By 1895, a total of 27 states had passed some type of food regulation.15 In 1883, because of concern about unsafe substances used to disguise spoiled foods, the Bureau of Chemistry within the Department of Agriculture, led by Harvey W. Wiley, began testing for such contaminants.

In 1906, two new regulations created the current federal food-regulatory system. Upton Sinclair’s novel The Jungle, published earlier that year, highlighted poor working conditions in slaughter plants and focused national attention on the meat supply. The Meat Inspection Act mandated that a federal inspector be present at slaughter to examine each carcass for visible signs of disease and to reject grossly diseased animals.16 The logic behind this law was that disease or carcass contamination that was visible to a trained inspector threatened the consumer. Also in 1906, the Meat Inspection Service was formed as an agency within the U.S. Department of Agriculture’s Bureau of Animal Industry to fulfill the requirements of the Act. Though public confidence was restored, the efficacy of these meat inspections in preventing disease was not established, and doubts were soon expressed. For example, in 1912, Charles Chapin, a public health leader from Rhode Island, voiced the opinion that visual inspection did nothing to prevent trichinosis and thought it “doubtful whether any sickness among consumers has been prevented.”17 The Pure Food and Drug Act, passed on the same day as the Meat Inspection Act, addressed growing concern over toxic food additives and quack patent medicines. The act made the Bureau of Chemistry responsible for testing and regulating foods for the presence of adulterants and for regulating the misbranding of foods, drinks, and drugs transported via interstate commerce.16 The logic behind this law was that laboratory tests would accurately identify unsafe levels of contamination in foods and that the threat of court actions based on these tests would prevent contamination. The Meat Inspection Act and the Pure Food and Drug Act established separate regulatory strategies for meat and for other foods, a duality that continues to this day.

Changes in the Food Supply

Over the course of the twentieth century, food preparation practices changed dramatically, as new technologies transformed the kitchen. The electric refrigerator became (p.23) available during World War I, followed by gas and electric stoves, frozen foods, the precooked convenience dinner, and most recently, the microwave oven.2 As illustrated by a wartime cookbook published in 1942, which included a chapter titled “Entertaining Without a Maid,”22 the family cook was disappearing from middle-class homes. Food became increasingly processed before purchase, and the kitchen changed into a place for food storage and final meal assembly. In addition, more meals were outsourced to restaurants: by 1998, 38% of the family food budget was spent on food prepared and eaten outside the home.23 The art of cooking disappeared from school curricula, and with the increasing popularity and availability of restaurants, cooking became optional for young adults living independently. Restaurants also increasingly provided employment opportunities. In 1997, the growing restaurant industry employed 6% of the nonfarm workers.24

As the United States became more urban and populous, food production became industrialized and involved larger and more centralized food-processing factories. Farms grew larger, crop yields and animal production-efficiency increased, and large agribusinesses replaced small family farms. Interstate transport of perishable foods began with refrigerated railroad cars in the 1870s and later largely switched to refrigerated trucks. Currently, refrigerated cargo jets transport highly perishable foods internationally, making fresh produce available year-round. The supermarket stocked with foods from around the world has become an icon of modern life. Availability of a wide variety of foods has helped spark changes in patterns of eating. U.S. consumers now eat more fruit and chicken than they used to and fewer eggs and less milk.25 Health-conscious consumers seek foods that are lower in fat, salt, and cholesterol. Consumers also are increasingly seeking foods that contain fewer preservatives, and thus have fewer barriers to microbial growth.

Evolving Control of Pesticides and Other Chemicals in Foods

Insecticides and herbicides have increased crop yield, decreased food cost, and enhanced the appearance of food throughout the twentieth century.26 However, residues of these pesticides remaining on foods also create potential health risks. During the 1950s and 1960s, the first pesticide regulations established maximum residue levels allowable on foods (the so-called residue tolerances) and established an approval process for pesticide use. In 1970, the new Environmental Protection Agency (EPA) took over the administration of many environmental regulations, including most of the regulation of pesticides used in food production. Propelled by public concern about the environmental impact of pesticides, the EPA removed dichlorodiphenyl-trichloroethane (DDT) and several other persistent pesticides from the U.S. marketplace, although they continue to be exported for use in other countries. In 1996, the Food Quality Protection Act focused on (1) the protection of children from pesticides, (2) the consumer’s right to know the results of pesticide monitoring, and (3) the use of a single, health-based standard for all pesticide residues in food.

Currently, four agencies play major roles in protecting the public from pesticides and other chemical residues in food. The EPA approves and sets tolerances (p.24) on pesticides used in food production and on other industrial chemicals that could contaminate food. The FDA determines which animal drugs can be used and establishes tolerances for residues of animal drugs in meat. The USDA tests meat and poultry for concentrations of residues that exceed tolerances set by the EPA and FDA. The health impact of pesticide exposure typically is chronic in nature and more difficult to estimate than the health effects of acute infections. However, the actual human exposure to pesticides can be measured with precision. In 1999, the CDC began monitoring this exposure by testing blood samples for residual pesticides.27

Improving Prevention Technologies

During the twentieth century, new prevention technologies were developed by scientists in industry, public health, and regulatory agencies for the most severe food-safety threats. The history of retort canning and of milk pasteurization illustrates the tenacious efforts that translated that research into universal protection.

Retort Food Canning

Canning was widely practiced in the nineteenth century, but was not well standardized at that time. Spores of the bacterium Clostridium botulinum, present in dirt and dust, survive boiling, so they may still be in vegetables that have been simply boiled as they are canned. The spores germinate and grow in conditions that are sufficiently moist and warm and that have minimal amounts of oxygen, such as the interior of a sealed can or jar. As they germinate, the bacteria can produce botulism toxin in the canned food. This potent toxin paralyzes muscles, including the muscles involved in respiration.

Before the development of modern intensive-care medicine, half of the persons affected by botulism died of respiratory paralysis. Even now, botulism often leads to many weeks in the intensive care unit.28 During and after World War I, outbreaks of botulism focused attention on the public health hazard of poorly canned foods. These outbreaks, culminating in the dramatic 1919 multistate olive outbreaks described above, led state health departments to begin surveillance for botulism cases and drove the canning industry to fund research on safe canning methods. From this research evolved the standard botulism retort cook method of 1923. A retort is a large pressure cooker that uses steam under pressure to reach temperatures above 212° F. The new industry standard defined the higher temperature and length of time required to completely eliminate botulinum spores from canned food. This process reliably reduced botulinum spore counts from one trillion per gram—the highest conceivable level of contamination—to zero, a 12-log kill.29 Thereafter, this standard retort cook method was enthusiastically and widely adopted by the canning industry.

In 1930, because of concern that canners were using vegetables of inferior quality, a federal quality standard was developed and titled the McNary-Mapes Amendment to the Pure Food and Drugs Act.30 However, there were still concerns that defective can seams could allow spores to enter a can after heat treatment. In 1973, after an outbreak of botulism was traced to commercially canned vichyssoise soup (p.25) that was adequately heated during canning but apparently became contaminated afterwards because of defects in the can, additional regulation was created to address that gap.31

Pasteurization of Milk

Milk pasteurization, another fundamental foodborne-disease prevention technology, was also slowly adopted in the twentieth century. In the early 1900s, tainted cows’ milk was known to be a source of many infections, including typhoid fever, tuberculosis, diphtheria, and severe streptococcal infections; many families chose to routinely boil milk for infants.7 The first commercial pasteurizing equipment was manufactured in Germany in 1882.32 Pasteurization began in the United States as early as 1893, when private charity milk stations in New York City began to provide pasteurized milk to poor children through the city health department,14 a movement that spread to other cities. In 1902, an estimated 5% of the New York City milk supply underwent heat treatment.32

By 1900, standard pasteurization was defined as 140° F for 20 minutes on the basis of the time and temperature required to inactivate Mycobacterium tuberculosis, the most heat-resistant pathogen known to affect milk at that time. These standards were confirmed by investigations of Dr. Milton Rosenau that were published in 1909.33 Experiments conducted in a dairy plant in Endicott, New York, evaluated the effectiveness of commercial pasteurization equipment in killing M. tuberculosis in milk and led to a public health ordinance that defined pasteurization as heating to 142° F for 30 minutes in approved equipment. However, the technology was slow to be applied. Pasteurization was opposed by some who thought it might be used to market dirtier milk and that it might affect the nutritional value of milk.34 Some persons concerned about recontamination during distribution maintained that the only way to guarantee the safety of milk was to boil it in the home just before drinking it.32 In addition, many thought the best way to prevent milk-associated diseases was through scrupulous attention to animal health and to clean milk production, which could be supported by an on-farm inspection and certification system. While the subsequent certification movement led to substantial improvements in dairy conditions, outbreaks of illness caused by “certified” milk showed that dairy hygiene alone was not enough; pasteurization was also needed as a final processing step to guarantee milk safety.

Despite the evidence suggesting the importance of pasteurization in the milk production process, differing milk-safety strategies were adopted by different jurisdictions. Not until 1923 did a public health expert combine the two processes of pasteurization and certification. This expert, a U.S. Public Health Service officer in Alabama, used both a standard definition for milk that was clean enough to be pasteurized and a standard definition of the pasteurization process itself.13 As other states signed on one by one, this standard became the national Public Health Service Standard Milk Ordinance of 1927. Under this ordinance, milk was first graded on the basis of the sanitation measures used in its production, and then only Grade A milk could be pasteurized.35 By the end of the 1940s, pasteurization was heavily promoted and had become the norm. In 1950, after several cases of Q fever were attributed to (p.26) raw-milk consumption, the issue was raised of whether Coxiella burnetti, the causative organism of Q fever, could survive pasteurization.36 Research showed that this organism was even more resistant to heat than M. tuberculosis, so the temperature for pasteurization was raised to 145° F. Though regulation occurred at the local and state level, the Conference of Interstate Milk Shippers developed reciprocal inspection agreements in 1950, analogous to the function of the Interstate Shellfish Sanitation Conference. This body set standards for dairies of any size.13 As a result, 99% of the fresh milk consumed in the United States is pasteurized Grade A.37

Universal acceptance of the practices of canning and pasteurization was not achieved for decades. For both technologies, time was needed to overcome concerns that these methods were unreliable, that they decreased nutritional value, and that they would mask poor food quality and sanitation. These concerns were ultimately addressed by formal grading processes that helped assure the public that milk would be clean enough to be pasteurized and that vegetables would be of high enough quality to be canned. Concerns about nutrient loss were found to be largely unwarranted, and were countered by fortifying milk with vitamins. Both processes were ultimately defined by clear microbial target endpoints so that milk pasteurization and a botulism retort cook were given standard meanings in all jurisdictions. The concern about equipment reliability was addressed through industry efforts and approval processes. The industry developed quality grading standards and pathogen-reduction processes and these were formally adopted via federal regulation.

As a result of these efforts, outbreaks of botulism caused by commercially canned foods and outbreaks of illness caused by pasteurized milk have become extremely rare. Foodborne botulism now affects approximately 25 persons a year, almost always those who have consumed home-canned vegetables or home-preserved meats and fish.28 Although outbreaks of infections associated with unpasteurized milk still occur with some frequency, outbreaks caused by pasteurized milk are exceedingly rare, and are usually the result of post-pasteurization contamination.37

The Evolution of Surveillance and the Elimination of Other Foodborne Threats

Over the course of the twentieth century, public health surveillance grew from a local process, which was administered by individual counties and cities, to a nationwide network involving all states and the CDC. Since 1951, the Council of State and Territorial Epidemiologists (CSTE) has determined which conditions should be reported nationally; and since 1961, the CDC has published national surveillance data in the Morbidity and Mortality Weekly Report (MMWR). The list of notifiable diseases has changed over time, reflecting public health priorities and the availability of useful data. Notifiable disease surveillance is possible only for those conditions that are routinely diagnosed in clinical practice. Among foodborne diseases, typhoid fever and botulism surveillance data began to be collected early in the twentieth century, and collection of national statistics regarding non-typhoid salmonellosis began in 1942. In 1964, after a large multistate outbreak of Salmonella serotype Derby infections that affected many hospitals, reports of diagnosed cases of salmonellosis (p.27) were supplemented by serotyping data from public health laboratories to create the national Salmonella Surveillance System.38 State public health laboratories began serotyping strains of Salmonella sent to them from clinical laboratories, and the CDC began collecting weekly information on Salmonella that was serotyped. Since then, public health surveillance based on laboratory subtyping of infectious organisms has proved vital in detecting and investigating countless outbreaks of salmonellosis and many other diseases.

The federal regulatory apparatus also has evolved over the last 100 years.16 (See Box 2.1.) The Bureau of Chemistry and the Meat Inspection Service have now become the Food and Drug Administration (FDA) and the Food Safety and Inspection Service (FSIS), respectively. The U.S. Public Health Service was moved from the Department of Treasury to become part of the new Federal Safety Agency, a precursor to the Department of Health and Human Services. In 1938, following a catastrophic outbreak of poisoning from an untested sulfanilamide elixir, passage of the Food, Drug, and Cosmetic Act gave the FDA authority to require pre-market testing of drugs and authority over food labeling and quality control. The act currently serves as the central authority for the FDA. Shortly after the passage of the act, the FDA was moved from the Department of Agriculture to the Federal Safety Agency because of the apparent conflict in mission between promoting the agriculture industry and maintaining food safety. In 1968, the FDA was added to the Public Health Service. As a vestige of its origin, the FDA is still funded through the congressional agriculture committees rather than through the health committees. The FSIS remains an agency within the U.S. Department of Agriculture.

Few statistics on foodborne disease morbidity were collected consistently throughout the twentieth century. However, the food supply is far safer by the twenty-first century than it was at the beginning of the 1900s. One index of the prevalence of food- and waterborne diseases is the infant mortality rate. From 1900 through 1950, this rate decreased rapidly from 141 per 1000 live births (for Massachusetts) to 29.2 per 1000 nationwide; life expectancy at birth increased from 47 to 68.2 years.6 In 1950, deaths caused by gastroenteritis and typhoid fever had fallen to a rate of 5.1 and 0.1 per 100,000 population, respectively. National surveillance data are available for typhoid fever beginning in 1912, making it a useful marker. The incidence of typhoid fever fell precipitously with municipal water treatment, milk pasteurization, and shellfish-bed sanitation long before vaccines or antibiotics were commonly used (Fig. 2.1). Trichinosis, caused by eating pork infested with parasitic cysts, has become exceedingly rare. During the 1940s, an estimated 16% of persons in the United States had trichinosis, most of which was asymptomatic; 3,000–4,000 clinical cases were diagnosed every year, and 10–20 deaths occurred.39 This disease was controlled by improving the safety of the foods consumed by pigs themselves and by breaking the cycle of transmission through garbage and swill. The rate of infection declined markedly as a result of these measures; from 1991 through 1996, only three deaths and an average of 38 cases were reported per year.40 The spread of other serious zoonotic infections among animals also was controlled, virtually eliminating animal anthrax, tuberculosis, and brucellosis in herds. By the 1960s, foodborne infections, like many other infectious diseases, were believed to be under control.



                      Advances in Food Safety to Prevent Foodborne Diseases in the United States

Figure 2.1. The fall of typhoid fever and the rise of nontyphoidal salmonellosis in the United States, 1920–2000. (CDC. National surveillance data.)

Emerging Challenges

An array of newly recognized pathogens illustrates the dynamic nature of foodborne disease. Although some pathogens (e.g., caliciviruses) have a human reservoir, most of these emerging foodborne pathogens are transmitted from animals; modern, industrialized food supply fosters the spread of pathogens through larger, more concentrated animal populations. Unlike typhoid fever, dysentery, and cholera, these infections are not associated with human sewage, but rather with animal manure. They often circulate among food animals without causing illness in them. Many nontyphoidal Salmonella strains have reservoirs in our food animals and serve as indicators of this phenomenon. Reports of these infections increased steadily from 1942, when reporting began, through 1990 (see Fig. 2.1). Healthy animals serve as reservoirs for other pathogens, including Campylobacter (endemic in healthy chickens), E. coli O157 (in cattle), and Vibrio vulnificus (in oysters). These pathogens are not detected by visual inspection of the animal. Because V. vulnificus is found naturally in warm brackish water, monitoring shellfish beds for human sewage contamination does not eliminate the risk of these pathogens. Even Vibrio cholerae O1, the great killer of the nineteenth century, was found to have an established natural niche in the bayous of the Gulf of Mexico, where it persists independent of human sewage contamination.41 For some bacteria, antimicrobial resistance has emerged because of the use of antibiotics in agriculture (causing resistance in the pathogens Salmonella and Campylobacter) and human medicine (causing resistance in Shigella).42

Given the complexity of the U.S. food supply and the growing appetite for diverse cuisines in this country, the emergence of new challenges in the field of foodborne illness is not surprising. At least 13 pathogens have been identified or newly recognized as foodborne challenges since 1976, appearing at the rate of about one every (p.30) 2 years (Table 2.2)45 These emerging infections account for 82% of the estimated 13.8 million cases and 61% of the 1800 deaths attributable to known foodborne pathogens each year in the United States.46 In contrast, five pathogens that were common before 1900 (i.e., Brucella, Clostridium botulinum, Salmonella Typhi, Trichinella, and toxigenic Vibrio cholerae) only caused an estimated 1500 cases and 13 deaths in 1997, many of which were associated with travel abroad. The preponderance of recently identified pathogens in the total burden reflects the progress that occurs in controlling pathogens once they are identified and studied.

Foodborne disease has been linked to an expanding variety of foods. Perishable foods increasingly are being imported into the United States from around the world, sometimes bringing pathogens with them. Immigrants, who tend to retain their native food habits and tastes, also can help introduce novel combinations of pathogens and foods.47 Into the twenty-first century, outbreaks increasingly are being associated with fresh fruits and vegetables and less with foods historically implicated in foodborne disease.48 Produce items are a particular concern because often they are eaten raw. Microbes can move to the interior of fruits and vegetables, where they cannot be washed off or killed by light cooking, as has been demonstrated experimentally with E. coli O157:H7 in apples and alfalfa sprouts.49 51 Even growing vegetables in soil fertilized with manure containing E. coli O157:H7 can lead to internal contamination.52

Safety breakdowns in large, modern food-processing plants can result in outbreaks involving substantial numbers of persons. In 1986, post-pasteurization contamination of milk at a single dairy led to an estimated 150,000 infections with multidrug-resistant salmonellosis in seven states.53 In 1995, a nationwide epidemic of Salmonella Enteritidis infections traced to a nationally distributed brand of ice cream caused illness in an estimated 250,000 persons.54 That epidemic was caused by the use of the same refrigerated trucks to transport contaminated raw eggs and pasteurized ice cream ingredients, leading to post-pasteurization contamination of the ice cream products.

As new pesticides are developed and new food-production uses are authorized for existing compounds, unsuspected chemical contamination of food may occur.

Table 2.2. New and emerging foodborne pathogens identified since 1977, or whose connection with food was established since 1977.

Campylobacter jejuni

Campylobacter fetus ssp fetus

Cryptosporidium parvum

Cyclospora cayetanensis

Escherichia coli O157:H7 and other Shiga-toxin producing E. coli

Listeria monocytogenes

Norwalk-like viruses

Nitzchia pungens (the cause of amnesic shellfish poisoning)

Spongiform encephalopathy prions

Vibrio cholerae O1

Vibrio vulnificus

Vibrio parahaemolyticus

Yersinia enterocolitica

(p.31) Unlike infectious exposures that cause disease quickly, toxic chemical exposures may take many years to be detected. These exposures may affect many persons at once. For example, in January 1999, a total of 500 tons of chicken feed contaminated with polychlorinated biphenyls (PCBs) and dioxins were distributed to farms in Belgium, leading to withdrawal of Belgian chickens from the market for several weeks. Estimates of the total number of human cancer cases that may ultimately result from this incident range between 40 and 8000.55

Three foodborne disease outbreaks in the United States shook the complacency of food safety professionals near the end of the twentieth century. In 1986, an estimated 3200 persons in eight states were infected with Salmonella Enteritidis after they ate a commercially packaged stuffed pasta (CDC, unpublished data). Although the product was labeled “fully cooked,” the stuffing contained raw eggs, and the farm where the eggs originated harbored the same strains of Salmonella Enteritidis as were found in the ill case-patients and the pasta. This outbreak investigation led to the discovery that S. Enteritidis outbreaks were generally associated with egg-containing foods and explained a massive increase in infections caused by this type of Salmonella.56 Eggs had previously been associated with salmonellosis in the 1960s, but contamination at that time occurred on the outside of the shell and therefore could be eliminated by routine disinfection. Following egg-associated outbreaks in the 1960s, egg grading, washing, and disinfection became the standard for the egg industry. However, the eggs in these new S. Enteritidis outbreaks all involved grade A disinfected eggs, suggesting that these Salmonella were on the inside of the shell. Researchers at the Department of Agriculture showed that hens fed Salmonella Enteritidis developed chronic, asymptomatic infections of their reproductive tracts and laid normal-looking eggs that contained Salmonella within their shells.57 The pasta outbreak was the herald event in an epidemic of S. Enteridis infections among egg-laying chickens that began in the Northeast and spread across the nation.58 As the epidemic spread to new states, tracing the eggs implicated in the outbreaks back to their source farms was crucial in showing each local egg industry that they, too, were affected by the epidemic. In response, new control measures are being implemented from farm to table, including better farm-management practices, refrigeration of eggs, education for cooks, and pasteurization of eggs while they are still in the shell.59

In 1993, an outbreak of E. coli O157:H7 infections on the West Coast caused 732 recognized illnesses, 55 cases of hemolytic uremic syndrome, and four deaths.60 ,61 This outbreak, caused by undercooked ground beef from one fast-food chain, had wide-reaching impact. The severity of the illness, the size of the outbreak, and the feeling of helplessness among parents of affected children shifted the prevailing notion that food safety was primarily an issue of consumer education and that consumers were responsible for cooking their food properly. After the hamburger outbreak in 1993, responsibility became redistributed to each link of the food-production chain. This outbreak brought food safety to the top of the nation’s policy agenda, leading to substantial changes in the approach to both meat safety and the safety of food in general.

Following the 1993 outbreak, many states made E. coli O157:H7 infection and hemolytic uremic syndrome notifiable diseases. Molecular methods for characterizing (p.32) strains were pilot-tested in that outbreak and subsequently become the basis for a new surveillance technology called PulseNet (vide infra). Food safety became an issue of public policy, and a new consumer action group (Safe Tables Our Priority, or STOP), consisting of parents of children harmed or killed in the outbreak, lobbied for change. Many restaurants and meat grinders put new emphasis on food-safety measures, and the meat supplier to the implicated fast-food restaurant chain became the industry leader in making meat safer. The Department of Agriculture declared E. coli O157:H7 to be an adulterant in raw ground beef, meaning that raw meat contaminated with E. coli O157:H7 should be withheld from trade. Perhaps most important, the strategy for meat inspections shifted from direct visual and manual carcass inspection, as had been done since 1906, to a new system, called Hazard Analysis and Critical Control Point (HACCP) monitoring. The HACCP monitoring relies on process controls (e.g., more careful slaughter, steam scalding, and more cleansing of equipment to reduce pathogens) and on testing the finished meat for microbial contamination to ensure that the process meets national standards.62

In the spring of 1996, a total of 1465 persons in 20 states, the District of Columbia, and two Canadian provinces became ill with a distinctive combination of recurrent diarrhea and extreme fatigue. The organism implicated in this outbreak was the newly recognized parasite Cyclospora cayetanensis.63 Illnesses were linked to eating fresh raspberries imported from Guatemala, where this crop had been recently introduced; the way in which the berries became contaminated, however, remains unknown. Investigators in Guatemala found that the same organism caused a springtime wave of diarrhea in the children of agricultural workers, who became ill after drinking untreated water.64 After procedural changes on raspberry farms and in the living conditions of Guatemalan workers, limited raspberry imports resumed, though with recurrent outbreaks, production of raspberries for export was greatly reduced.75 The epidemic, which brought the obscure Cyclospora organism to the fore, demonstrates how foodborne pathogens considered to occur only rarely can suddenly appear, and it illustrates the potential hazards associated with growing fresh produce in the developing world, flying it to the developed world, and eating it after only a quick rinse. The incident illustrates the close connection between the poor conditions of workers’ lives in the developing world and the casual treatment of U.S. dinner plates.

Now, at the beginning of the twenty-first century, foodborne disease remains un-conquered. The burden of foodborne diseases in the United States, newly estimated using the most recent and improved surveillance data, is 76 million cases of foodborne infections each year; one in four Americans are affected annually, leading to 323,000 hospitalizations and 5000 deaths.46 An increasing array of pathogens are being recognized as being foodborne (Table 2.3), and much of the foodborne disease burden is not accounted for by known pathogens, indicating that many more are yet to be identified. The previously idiopathic Guillain Barre syndrome and hemolytic uremic syndrome are now known to be postinfectious complications of Campylobacter and E. coli O157:H7 infections, respectively. Other apparently idiopathic syndromes also may prove in the future to follow foodborne infections.


Table 2.3. Principal foodborne infections in 1997, ranked by estimated annual number of cases caused by foodborne transmission, United States [46]. (Values over 1,000 are rounded to the nearest 1000.)

Norwalk-like viruses




Salmonella (nontyphoid)


Clostridium perfringens


Giardia lamblia


Staphylococcus food poisoning


Toxoplasma gondii


E. coli O157:H7 and other

Shiga-toxin producing E. coli




Yersinia enterocolitica


Enterotoxigenic E. coli








Cryptosporidium parvum


Bacillus cereus


Other E. coli


Cyclospora cayetanensis


Vibrio (non cholera)


Hepatitis A


Listeria monocytogenes




Salmonella Typhi (typhoid fever)






Vibrio cholerae, toxigenic


The Lessons of Prevention

Although no vaccine exists for most emerging foodborne pathogens, the progress in food safety in the twentieth century shows that other strategies of prevention can be highly effective, including controlling the pathogens at the food-animal reservoir, preventing the pathogens from contaminating foods, stopping the multiplication of pathogens that get into food, and killing pathogens already present on food (Table 2.4). Success has often depended on understanding the precise mechanisms of transmission well enough to interrupt them with targeted control measures and new technologies.

Early in the twentieth century, the stream of human sewage was separated from the human food and water supplies, controlling many infections for which humans are the primary reservoir. More recent advances have prevented animal manure from contaminating human food and water supplies. Now, control of some foodborne diseases depends on improving the safety of the food and water that the animals themselves consume.


Table 2.4. Generalized schema of foodborne disease prevention.

Production Stage

Sources or Multipliers of Contamination

Control Strategies in

Current Use


Growing or rearing

Contaminated feed and water, manure, wildlife, other animals

Feed sterility, animal disease control, rodent control, biosecurity, competitive exclusion

Water treatment, manure treatment, feed security, vaccination, probiotics

Slaughter or harvest and processing

Water baths and sprays, fecal contamination, cross-contamination

HACCP,* plant sanitation, inspection, microbial testing, water disinfection, steam scalding, pasteurization, irradiation

Irradiation, high pressure, intense light, new additives


Contaminated ice, poor refrigeration, dirty trucks

Ice regulation, refrigeration, vehicle disinfection

Dedicated vehicles


Cross-contamination, time/temperature abuse, ill food handler

Food handler education, handwashing, facility inspection and licensing

Food handler certification, paid sick leave, automated handwashing

(*) Hazard analysis and critical control point programs, which apply safety engineering principles to food production.

Despite recent advances, ill humans still can contaminate the foods they prepare in the kitchen, and the increase in food preparation outside of the home sparks concern for the health and hygiene of restaurant workers. Infections with caliciviruses, Shigella and hepatitis A can easily spread from ill food handlers to consumers via food. The unwary cook also can easily transfer microbes from raw meat to other foods being prepared or make other food-handling errors that can lead to illness in the consumer. Such problems will persist until food handlers are routinely educated in food safety, have clear incentives for hand washing and other hygiene practices, and can take paid leave for illness.

For some foods, especially those that are the pooled products of many animals, even meticulous sanitation may not prevent contamination of the final product, and a definitive pathogen elimination technology is critical. The history of pasteurization is a model for other efforts. The shift in public health strategy for milk from advising homemakers to boil their infant’s milk to requiring the dairy industry to provide pathogen-free milk for all consumers is a model to be followed for other high-risk foods.

Disease prevention is a cyclical process (Fig. 2.2). First, surveillance of an infection is conducted to measure the burden of the problem, track the success or failure (p.35)

                      Advances in Food Safety to Prevent Foodborne Diseases in the United States

Figure 2.2. The cycle of prevention in public health (as proposed by Dr. Paul Mead).

of control measures, and detect outbreaks. Outbreak investigations then are initiated to discover new pathogens, new food sources of infection, and gaps in the food-safety system. These investigations can link a specific pathogen to a particular food, identify the likely point of contamination, and therefore define the point at which better control is needed. The investigation may lead directly to control or may identify the type of applied research needed; applied research conducted by industry, academic scientists, and government researchers can lead to successful prevention measures. New regulatory approaches may be suggested or endorsed by industry, consumer groups, and regulatory agencies. Once short-term control and long-term prevention measures are applied, continued surveillance defines whether they are successful. For major public health threats, ultimate control may require repeated turns of this cycle.

Improving Surveillance, Improving Prevention

Improvements in public health surveillance can propel improved disease prevention. In the United States, several developments made in the last 5 years of the twentieth century are increasing the scope and the sensitivity of public health surveillance. National surveillance was begun for several of the newly recognized conditions, including E. coli O157:H7 in 1993, Cyclospora in 1996, and Listeria monocytogenes in 1998. Salmonella serotype-specific surveillance data sent electronically from state public health laboratories to the CDC began to be routinely analyzed for state, regional, and national surges in the incidence of specific serotypes using the Surveillance Outbreak Detection Algorithm (SODA).65 In addition to enhanced nationwide surveillance, a new active surveillance effort, called FoodNet, began in 1996 in five participating state health departments (www.cdc.gov/foodnet). Growing to eight participating sites by 2000, FoodNet’s active surveillance has provided accurate, detailed information about diagnosed infections with pathogens that are likely (p.36) to be foodborne as well as surveys of laboratory practices and of the general population.76

Standardized subtyping of foodborne pathogens increases the ability of public health surveillance to detect and investigate outbreaks.66 Just as standardized serotyping revolutionized Salmonella surveillance in the 1960s, PulseNet now provides molecular DNA “fingerprints” to enhance surveillance for several bacterial foodborne pathogens. PulseNet is the national network for molecular subtyping of these pathogens, connecting all state public health laboratories, federal food regulatory agency laboratories, and Canadian health authorities. Through PulseNet, participating laboratories use a standardized pulsed-field gel electrophoresis (PFGE) method to produce a molecular DNA fingerprint of bacterial strains isolated from ill persons. Although knowing the fingerprint does not influence patient care, it can be critical for public health surveillance. The fingerprints from various state laboratories can be compared online with each other and with a national database maintained at the CDC. The appearance of a pattern in many states at once may be the first indication of a widespread outbreak, for which a detailed epidemiologic investigation could be implemented to determine the source. Because laboratories at the FDA and FSIS participate in PulseNet, strains of bacteria isolated from foods can be compared with strains that affect humans.

Better surveillance in the twentieth century increasingly unveiled widespread outbreaks involving many jurisdictions. Before modern surveillance technologies were available, recognized foodborne outbreaks typically fit the textbook pattern of a sharp local increase in cases following a local common exposure (e.g., a catered event). Disease-control efforts were handled by local health departments and would commonly entail closure of a restaurant, destruction of a batch of food, and/or education of a food handler. Occasionally, a link would be observed between outbreaks occurring in several places at once, such as the botulism outbreak of 1919 or the typhoid fever outbreak of 1924, but such recognition was rare.

Currently, geographically dispersed outbreaks are being recognized more frequently because of serotyping and the PulseNet system. Dispersed outbreaks do not cause a sharp local increase in cases, but instead cause a few apparently sporadic cases in many jurisdictions concurrently. In addition, they often are caused by foods contaminated at a low level and shipped to many places. The increase in cases in any one place may not be sufficient to attract notice from public health professionals; therefore, widespread outbreaks are detected only when the bacterial strains are sub-typed in public health laboratories and are then compared with strains from many jurisdictions. Subsequent investigation can identify a systematic problem in food production or processing that can have implications for the entire industry.

In recent years, PulseNet has revealed many dispersed outbreaks that follow this new scenario, and the investigations have led to substantial advances in prevention. In 1997, shortly after the state health department in Colorado began testing E. coli O157:H7 isolates with PulseNet, 16 cases of infection with the same unusual pattern were detected in Colorado and in a neighboring state.67 These cases were linked to ground beef produced at a large factory. Because that plant worked leftover beef from one production lot into subsequent days’ production, the volume of potentially contaminated meat was an astounding 25 million pounds of meat. This meat was (p.37) recalled, and the re-work practice was discouraged throughout the industry. In 1998, an increase in apparently sporadic Listeria cases occurred in several states, just as the PulseNet method for Listeria was first being implemented. A total of 101 cases in 22 states were identified as having the same DNA fingerprint and were associated with the consumption of cooked hot dogs from one production plant.68 In response to this finding, the company instituted a recall of the hot dog products. Investigation suggested that further measures were needed to control recontamination of hot dogs after processing. Such measures are now being considered by the entire industry. In 1999, a cluster of 78 Salmonella Newport infections in 13 states was detected by SODA and PFGE subtyping.69 Epidemiologic investigation linked these cases to consumption of fresh imported mangoes. The mangoes had been treated with a new hot-water dip process that had been developed to replace methyl bromide fumigation for the elimination of fruit flies before export. As a result of the investigation, this process is being modified as it is introduced worldwide. In 2000, a cluster of Salmonella Enteritidis infections with the same unusual PFGE pattern was detected by SODA in western states; 88 infections in eight states were associated with drinking unpasteurized orange juice that had been treated with an alternative to pasteurization.70 Following this outbreak, the federal regulations for juice were revised to make contamination less likely to recur.71

Monitoring of the frequency of contamination with pathogens and toxins in foods has been expanded. The new meat safety and inspection rule, published in 1996 by USDA, includes routine monitoring of ground beef for E. coli O157:H7 and of meat and poultry for the prevalence of Salmonella. In addition, limits are set on the frequency with which Salmonella is permitted on raw meat products.62 Since 1967, the FSIS National Residue Program has monitored chemical residues in meat, poultry, and egg products, enforcing the safe limits set by the FDA and EPA and focusing on those residues most likely to have the greatest impact on public health.72 Similarly, since 1991, the Agricultural Marketing Service monitors pesticide residues in fresh produce.73 The systematic monitoring of the food supply for pathogens opens the door for tracking and quantifying the flow of pathogens by comparing the distribution of serotypes and subtypes in both food and case-patients.

The recent focus on the safety of many foods, including meat and poultry, eggs, seafood, and fresh produce, may be leading to fewer infections. In the early 1990s, industry efforts to reduce post-cooking contamination of hot dogs and other ready-to-eat meats were followed by a decline in Listeria infections of approximately 44%.74 Egg safety efforts from farm to table also appear to be working, as the incidence of Salmonella Enteritidis infections has also declined 44% since the peak in 1995.59 Cyclospora appears to have been controlled by Guatemalan raspberry farm sanitation and limitations on Guatemalan raspberry imports.75 From 1996 through 2000, the total incidence of the principal bacterial foodborne infections under surveillance at FoodNet declined 13%.76 These modest but sustained declines indicate some success in recent efforts to reduce Campylobacter, Salmonella, and Listeria infections. However, the incidence of E. coli O157:H7 infections remained stable during this four-year period, indicating a need for further investigations into the spread of this pathogen and for further prevention efforts (e.g., the irradiation of ground beef).

(p.38) Expectations for the Twenty-First Century

We should expect the unexpected in the future.77 More novel pathogens will be recognized, and established pathogens will appear in new food vehicles. In addition, as the population of the United States ages and becomes more subject to immunocompromising conditions and treatments, the number of persons at higher risk for food-borne infections grows. The continued globalization of food production and increasing international travel will result in new food sources, cuisines, and food-processing methods to create more challenges for the control of foodborne diseases. We can meet these challenges with a flexible and responsive public health system and a commitment to the surveillance, investigation, and research needed to find solutions. Collaborative international efforts will be critical to increase cooperation across international borders. The spectre of bioterrorism forces consideration of the security of our food supply as well as its safety. A strong and flexible public health infrastructure with enhanced surveillance and investigative capacity is a critical bulwark against foodborne bioterrorism.78

The philosophic shift that places responsibility for food safety within each link of the food chain will continue. The entire food industry will be increasingly involved in developing food-safety plans and standards, as each link in the chain imposes them on their suppliers. Microbial standards will increasingly be written into purchase contracts. Increasing consumer food-safety education will mean that more consumers demand safer food to begin with. The scope of the shift in food-safety responsibility is illustrated in Europe, where the consumer perspective now governs food-safety policy after the bovine spongiform encephalopathy epidemic led to a collapse in public confidence.

Preventing contamination before food reaches the consumer will be increasingly important. For many zoonotic pathogens, this means bringing elements of the human urban sanitary revolution to animal production, including reliable disinfection of drinking water and disposal of collected feces. For example, Campylobacter in chicken flocks and E. coli O157 in dairy herds may be spread among the animals through contaminated drinking water and perhaps through multiplication in feed-stuffs.79 ,80 Feed and water hygiene on farms may play a key role in the spread of virulent Salmonella strains like Typhimurium DT104 and multidrug-resistant Salmonella Newport. The importance of such hygiene is illustrated by the European epidemic of bovine spongiform encephalopathy that became foodborne in cattle when they were fed brain tissue from cattle with the disease; it subsequently spread to people who presumably consumed beef. Control will depend on complete elimination of unsafe cattle by-products from cattle feed.81 ,82

New regulatory approaches can orchestrate the work of many partners in disease prevention. Pathogen reduction can be achieved by setting specific targets, or food-safety objectives, similar to tolerance limits that are set for pesticides. However, because microbes multiply, the process will not be as simple. Risk-assessment modeling can help account for biologic complexity and can indicate which critical processes must be monitored to achieve the goal.

New prevention technologies are critical to progress in food safety, including vaccinating animals against zoonotic foodborne pathogens and feeding them nonpathogenic (p.39) enteric organisms to prevent the colonization of harmful microbes. Composting treatments that reliably rid animal manure of pathogens have not yet been standardized. Treating foods with ionizing radiation, an important process that is now being adopted, can eliminate many pathogens from foods and would substantially reduce the burden of bacterial foodborne illness.83 Other pathogen elimination technologies may be useful, including high-pressure treatment, ultrasound, and high-intensity light. The successes of the twentieth century and the new challenges faced mean that public health surveillance, scientific investigation of new problems, responsible attention to food safety from farm to table, and partnerships to bring about new control measures will be crucial to the control and prevention of foodborne disease into the foreseeable future.


We gratefully acknowledge the thoughtful reviews of Jose Rigau, Ellen Koch, Balasubramanian Swaminathan, Patricia Griffin, Cynthia Tauxe, and the advice of many others.


Bibliography references:

1. Abstract of the Twelfth Census of the United States, 1900. Washington, DC: Census Office, Government Printing Office, 1902.

2. Ierley M. Open House: A Guided Tour of the American Home, 1637-Present. New York: Henry Holt, 1999.

3. Porter M. Mrs. Porter’s new Southern cookery book. In: Szathmary LI ed. Cookery Americana. Philadelphia: John E Potter, 1871.

4. Sixth Annual Report of the State Board of Health of Ohio. Columbus, OH: State Board of Health, 1890.

5. Melosi M. The Sanitary City: Urban Infrastructure in America from Colonial Times to the Present. Baltimore: Johns Hopkins University Press, 2000.

6. Historical Statistics of the United States. Colonial Times to 1970, Part 1, Bicentennial ed. Washington, DC: Bureau of the Census, U.S. Department of Commerce, 1975.

7. Rosenau MJ. Preventative Medicine and Hygiene, 5th ed. New York: D Appleton, 1928.

8. Gaffky G. Zur aetiologie des abdominal typhus. Mittheilungen aus den Kaiserlichen Gesundheitsamte 1884:2:372–420.

9. Karlinski J. Zur kenntnis des Bacillus enteritidis gaertner. Zentralbl Bakteriol Mikrobiol Hyg[B] 1889:6:289–92.

10. van Ermengem E. Ueber einen neuen anaeroben Bacillus und seine Beziehungen zum Botulismus. Z Hyg Infek 1897:26:1–56.

11. Duffy J. The Sanitarians: A History of American Public Health. Chicago: University of Chicago Press, 1990.

12. Soper G. Typhoid Mary. The Military Surgeon 1919:45:1–15.

13. Williams R. The United States Public Health Service: 1798–1950, vol. 2. Washington, DC: Commissioned Officers Association of the United States Public Health Service, 1951.

14. Duffy J. Public Health in New York City 1866–1966. New York: Russell Sage Foundation, 1974.

15. Okun M. Fair Play in the Marketplace: The First Battle for Pure Food and Drugs. Dekalb, IL: Northern Illinois University Press, 1986.

16. Merrill R, Francer J. Organizing federal food safety regulation. Seton Hall Law Review 2000:31:61–173.

(p.40) 17. Chapin C. Sources and Modes of Infection. New York: John Wiley, 1912.

18. Armstrong C. Botulism from eating canned ripe olives. Public Health Rep 1919:34:2877–905.

19. Botulism: protective measures and cautions from the U.S. Bureau of Chemistry, Department of Agriculture. Public Health Rep 1920:35:327–30.

20. Lumsden L, Hasseltine H, Veldee M. A typhoid fever epidemic caused by oyster-borne infections (1924–1925). Public Health Rep 1925:50(suppl):1–102.

21. History of the National Shellfish Sanitation Program. Interstate Shellfish Sanitation Conference, 2000 Refer to:http://www.issc.org/issc/NSSP/Background/history_nssp.htm. Accessed January 27, 2001.

22. Berolzheimer R. The American Woman’s Cook Book. Chicago: Consolidated Book Publishers, 1942.

23. Manchester A. Food consumption: household food expenditures. U.S. Department of Agriculture, Economic Research Service, 2000. Refer to: www.ers.usda.gov/briefing/consumption/Expenditures.htm. Accessed January 30, 2001.

24. Statistical Abstract of the United States, 1998. Washington, DC: Bureau of the Census, Government Printing Office, 1998.

25. Putnam J. Major trends in the U.S. food supply, 1909–99. Food Rev 2000:23:8–15.

26. History of American agriculture 1776–1990. In: Farm Machinery and Technology 2001. Economic Research Service, U.S. Department of Agriculture. Refer to: www.usda.gov/history2/text4.htm. Accessed June 15, 2001.

27. National Report on Human Exposure to Environmental Chemicals. Atlanta: Centers for Disease Control and Prevention, 2001.

28. Botulism in the United States, 1899–1996. In: Handbook for Epidemiologists, Clinicians and Laboratory Workers. Atlanta: Centers for Disease Control and Prevention, 1998.

29. Esty J, Meyer K. The heat resistance of spores of B. botulinus and allied anaerobes. J Infect Dis 1922:31:434.

30. Shrader JH. Food Control: Its Public Health Aspects. New York: John Wiley, 1939.

31. Thermally-processed low acid foods packaged in hermetically sealed containers. Federal Register 1973:38:2398.

32. Westhoff D. Heating milk for microbial destruction: a historical outline and update. J Food Protect 1978:41:122–30.

33. Rosenau M. The Thermal Death Time of Pathogenic Micro-organisms in Milk. [Hygienic Laboratory Bulletin #56]. Washington, DC: United States Public Health and Marine Hospital Service, 1909.

34. Potter M, Kaufmann A, Blake P, Feldman R. Unpasteurized milk: the hazards of a health fetish. JAMA 1984:252:2048–54.

35. Milk investigations: preparation of a standard milk-control code. In: Annual Report of the Surgeon General of the Public Health Service of the United States for the Fiscal Year 1928. Washington, DC: United States Public Health Service, 1928, 53.

36. Bell J, Beck M, Huebner R. Epidemiological studies of Q fever in southern California. JAMA 1950:142:868–72.

37. Headrick M, Korangy S, Bean N, Angulo F, Altekruse S, Potter M, Klontz K. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health 1998:88:1219–21.

38. Proceedings of the National Conference on Salmonellosis. In: National Conference on Salmonellosis. Atlanta: Centers for Disease Control, 1964.

39. Schantz P. Trichinosis in the United States—1947–1981. Food Tech 1983:83–86.

40. Moorhead A. Trichinellosis in the United States, 1991–1996: declining but not gone. Am J Trop Med Hyg 1999:60:66–9.

(p.41) 41. Blake PA. Endemic cholera in Australia and the United States. In: Wachsmuth IK, Blake PA, Olsvik O eds. Vibrio cholerae and Cholera. Washington, DC: American Society for Microbiology, 1994:309–19.

42. Lee LA, Puhr ND, Maloney EK, Bean NH, Tauxe RV. Increase in antimicrobial-resistant Salmonella infections in the United States. J Infect Dis 1994:170:128–34.

43. Smith K, Besser J, Hedberg C, et al. Quinolone-resistant infections of Campylobacter jejuni in Minnesota, 1992–1998. N Engl J Med 1999:340:1525–32.

44. Tauxe R, Puhr N, Wells JG, Hargrett-Bean N, Blake P. Antimicrobial resistance of Shigella isolates in the USA: The importance of international travelers. J Infect Dis 1990:162:1107–11.

45. Tauxe RV. Emerging foodborne diseases: an evolving public health challenge. Emerg Infect Dis 1997:3:425–34.

46. Mead P, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999:5:607–25.

47. Mead PS, Mintz ED. Ethnic eating: foodborne disease in the global village. Infect Dis Clin Pract 1996:5:319–23.

48. Tauxe RV, Kruse H, Hedberg C, Potter M, Madden J, Wachsmuth. Microbial hazards and emerging issues associated with produce: a preliminary report to the National Advisory Committee on Microbiologic Criteria for Foods. J Food Protect 1997:60:1400–8.

49. Buchanan R, Edelson S, Miller R, Sapers G. Contamination of intact apples after immersion in an aqueous environment containing Escherichia coli O157:H7. J Food Protect 1999:62:444–50.

50. Taormina P, Beuchat L, Slutsker L. Infections associated with eating seed sprouts: an international concern. Emerg Infect Dis 1999:5:626–34.

51. Burnett S, Chen J, Beuchat L. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl Environ Microbiol 2000:66:4679–87.

52. Solomon E, Yaron S, Matthews K. T 31 Transmission and internalization of Escherichia coli O157:H7 from contaminated cow manure into lettuce tissue as monitored by laser scanning confocal microscopy. In: International Association for Food Protection, 88th Annual Meeting. Minneapolis, MN, 2001.

53. Ryan C, Nickels M, Hargrett-Bean N, et al. Massive outbreak of antimicrobial-resistant salmonellosis traced to pasteurized milk. JAMA 1987:258:3269–74.

54. Hennessy TW, Hedberg CW, Slutsker L, et al. A national outbreak of Salmonella Enteritidis infections from ice cream. N Engl J Med 1996:334:1281–86.

55. van Larebeke N, Hens L, Schepens P, et al. The Belgian PCB and dioxin incident of January-June 1999: exposure data and potential impact on health. Environ Health Perspect 2001:109:265–73.

56. St. Louis ME, Morse DL, Potter ME, et al. The emergence of Grade A eggs as a major source of Salmonella Enteritidis infections: implications for the control of salmonellosis. JAMA 1988:259:2103–7.

57. Gast R. Applying experimental infection models to understand the pathogenesis, detection and control of Salmonella enterica serovar Enteritidis in poultry. In: Saeed A, Gast R, Potter M, Wall P, eds. Salmonella enterica serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis, and Control. Ames, IA: Iowa State University Press, 1999, chap. 2, 233–43.

58. Angulo FJ, Swerdlow DL. Epidemiology of human Salmonella enterica Serovar Enteritidis infections in the United States. In: Saeed AM, Gast RK, Potter ME, Wall PG, eds. Salmonella enterica serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis, and Control. Ames, IA: Iowa State University Press, 1999, 33–41.

(p.42) 59. Outbreaks of Salmonella serotype Enteritidis infections associated with eating raw or undercooked shell eggs—United States, 1996–1998. MMWR 2000:49:73–79.

60. Bell BP, Goldoft M, Griffin PM, et al. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: the Washington experience. JAMA 1994:272:1349–53.

61. Griffin P, Bell B, Cieslak P, et al. Large outbreak of Escherichia coli O157:H7 infections in the Western United States: The big picture. In: Karmali M, Goglio A, eds. Recent Advances in Verotoxin-producing Escherichia coli Infections. Amsterdam: Elsevier, 1994:7–12.

62. Pathogen reduction: hazard analysis and critical control point (HACCP) systems; the final rule. Federal Register 1996:61:38805–989.

63. Herwaldt B, Ackers M, the Cyclospora Working Group. An outbreak in 1996 of cyclosporiasis associated with imported raspberries. N Engl J Med 1997:336:1548–56.

64. Bern C, Hernandez B, Lopez M, et al. Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerg Infect Dis 1999:5:766–7 4.

65. Hutwagner LC, Maloney EK, Bean NH, Slutsker L, Martin SM. Using laboratory-based surveillance data for prevention: an algorithm for detecting Salmonella outbreaks. Emerg Infect Dis 1997:3:395–400.

66. Swaminathan B, Barrett T, Hunter S, Tauxe R, and the CDC PulseNet Task Force. PulseNet, the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis 2001:7:382–89.

67. Centers for Disease Control and Prevention. Escherichia coli O157:H7 infections associated with eating a nationally distributed commercial brand of frozen ground beef patties and burgers—Colorado, 1997. MMWR 1997:46:777–78.

68. Centers for Disease Control and Prevention. Update: Multistate outbreak of listeriosis—United States. MMWR 1999:47:1085–86.

69. Sivapalasingam S, Barrett E, Kimura A, et al. A multistate outbreak of Salmonella enterica serotype Newport infections linked to mango consumption: Impact of water-dip disinfestation technology. Clin Infect Dis 2003:37:1585–90.

70. Rangel J, Kimura A, Palumbo M, et al. Multistate outbreak of Salmonella Enteritidis infections linked to consumption of unpasteurized orange juice. Abstract no. 650 In: 38th Annual Meeting, Infectious Diseases Society of America, New Orleans, LA, 2000.

71. Food and Drug Adminstration. FDA publishes final rule to increase safety of fruit and vegetable juices, 2001. Available at: www.fda.gov/bbs/topics/NEWS/2001/NEW00749.html Accessed on June 15, 2001.

72. 2000 FSIS National Residue Program. Washington, DC: Food Safety and Inspection Service, 2000.

73. Pesticide Data Program: Annual Summary, Calendar Year 1999. Washington, DC: Agricultural Marketing Service, Department of Agriculture, 2001.

74. Tappero J, Schuchat A, Deaver K, Mascola L, Wenger J. Reduction in the incidence of human listeriosis in the United States: effectiveness of prevention efforts? JAMA 1995:273:1118–22.

75. Herwaldt B. Cyclospora cayetanensis: a review, focusing on the outbreaks of cyclosporiasis in the 1990s. Clin Infect Dis 2000:31:1040–57.

76. Centers for Disease Control. Preliminary Foodnet data on the incidence of foodborne illnesses—selected sites, United States, 2000. MMWR 2001:50:241–46.

77. Swerdlow D, Altekruse S. Foodborne diseases in the global village: what’s on the plate for the 21st century. In: Scheld W, Craig W, Hughes J, eds. Emerging Infections 2. Washington, DC: ASM Press, 1998,273–94.

78. Sobel J, Khan AS, Swerdlow DL. Threat of a biological terrorist attack on the US food supply. Lancet 2002: 359:874–80.

(p.43) 79. Kapperud G, Skjerve E, Vik L, et al. Epidemiological investigations of risk factors for Campylobacter colonization in Norwegian broiler flocks. Epidemiol Infect 1993:111:245–55.

80. Hancock D, Besser T, Rice D. Ecology of Escherichia coli O157:H7 in cattle and impact of management practices. In: Kaper J, O’Brien A (eds.), Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains. Washington, DC: American Society for Microbiology Press, 1998, 85–91.

81. Taylor D, Woodgate S. Bovine spongiform encephalopathy: the causal role of ruminant-derived protein in cattle diets. RevSciTech 1997:16:187–98.

82. Will R, Ironside J, Zeidler M, et al. A new variant of Creutzfeld-Jakob disease in the UK. Lancet 1996:347:921–25.

83. Tauxe R. Food safety and irradiation: protecting the public health from foodborne infections. Emerg Infect Dis 2001:7:516–21.

84. Ensuring Safe Food, from Production to Consumption. Washington, DC: National Academy Press, 1998.

85. Thacker S. Historical development. In: Teutsch S, Churchill R, eds. Principles and Practice of Public Health Surveillance. New York: Oxford University Press, 1994, 3–17.

Suggested Reading

Bibliography references:

Duffy J. The Sanitarians: A History of American Public Health. Chicago: University of Chicago Press, 1990.

Melosi M. The Sanitary City: Urban Infrastructure in America from Colonial Times to the Present. Baltimore: Johns Hopkins University Press, 2000.

Tauxe RV. Molecular subtyping and the transformation of public health. Foodborne Pathogens and Diseases. 2006:3:4–8.