Abstract

Foodborne illness is a serious public health threat. The Centers for Disease Control and Prevention (CDC) estimates that 76 million foodborne illnesses, including 325,000 hospitalizations and 5,000 deaths, occur in the United States each year. Two recently published Foodborne Diseases Active Surveillance Network (FoodNet) reports showed that Salmonella, Campylobacter, Shigella, Cryptosporidium, and Shiga toxin Escherichia coli (STEC) O157 continue to be leading causes of both the number and incidence of laboratory-confirmed foodborne infections in the United States. According to the United States Department of Agriculture (USDA), foodborne illness costs the US economy $10–83 billion per year. Recent large foodborne outbreaks have led to claims that the number of foodborne disease outbreaks and concomitant illnesses has increased in recent years. However, a comparison of data from the CDC showed very little change in the incidence of foodborne illness caused by common pathogens between 2008 and the preceding 3 years (2005–2007). Nevertheless, despite intensified prevention efforts, foodborne illness remains a persistent problem in the United States. Food can become contaminated at any point in the farm-to-table continuum, as well as in consumers' own kitchens. Therefore, foodborne illness risk reduction and control interventions must be implemented at every step throughout the food preparation process, from farm to table. In addition, more effective food safety education programs for foodhandlers and consumers are needed. Strategies should take into account food safety-related trends including large-scale production and wide distribution of food, globalization of the food supply, eating outside of the home, emergence of new pathogens, and growing population of at-risk consumers.

INTRODUCTION

Over the past few decades, the United States Department of Agriculture–Food Safety and Inspection Service (USDA–FSIS), the US Food and Drug Administration–Center for Food Safety and Applied Nutrition (FDA–CFSAN), and state/city/county departments of health have intensified food safety regulation and enforcement as well as inspection of food production and distribution systems. During this period of time, the USDA–FSIS and FDA–CFSAN have also launched and prescribed many food safety management systems, including the Hazard Analysis Critical Control Points (HACCP) system.1,2 HACCP is a logical and verifiable approach towards identifying biological, chemical, and physical hazards in food production and putting safety measures in place to prevent, eliminate, or reduce the hazards to safe levels. By instituting preventive controls, food safety hazards are less likely to occur. The effectiveness of HACCP has led USDA–FSIS to publish its final rule on the HACCP system in 1999, making it a requirement for meat and poultry plants.3 In 2001, the FDA–CFSAN followed suit, announcing its final rule, requiring juice processors to use HACCP principles for juice processing.4 Seafood processors also are now required to have HACCP plans.5 In addition to these regulations, the FDA–CFSAN, USDA–FSIS, other federal agencies such as the Centers for Disease Control and Prevention (CDC) and the US Environmental Protection Agency (EPA), and state/city/county departments of health have published many foodborne illness-prevention guidance documents for food handlers. Furthermore, federal agencies and state/city/county departments of health provide educational information (for different audiences) through printed materials and online for the safe handling of food and reducing the risks associated with foodborne illness. Many public and private organizations such as the Cooperative Extension System, the Partnership for Food Safety Education, the National Restaurant Association Educational Foundation, and the National Registry of Food Safety Professionals have also implemented education programs that address the control of foodborne pathogens from farm to table.

To preserve food and to prevent spoilage as well as the growth of pathogenic microorganisms, food processing companies use a variety of the numerous food processing methods that are currently available. Some of the most effective methods for preserving food include pasteurization, canning, refrigeration, freezing, drying, reduced oxygen packaging, the addition of food preservatives, curing, and food irradiation. As technology advances, newer and more sophisticated techniques (geared toward lengthening food shelf life and destroying or preventing spoilage and/or growth of pathogenic microorganisms) will continue to be developed.

In recent years there has been a growing trend toward the sale of prewashed bagged produce. In 2004, a study by Nielsen found that bagged salads had become the second-fastest-selling item in US grocery stores after bottled water.6 They called this rise “dramatic” and attributed it to convenience. There is consensus among members of the scientific community that thorough washing of fruits and vegetables (particularly those consumed raw) is the key to minimizing the risk of foodborne illness associated with fresh produce. Similarly, it is now widely accepted that washing cannot eliminate contamination. Nevertheless, nutrition educators and healthcare professionals believe that the benefits of eating fresh fruits and vegetables outweigh the risk of contracting a foodborne illness by consuming fresh produce.

Despite the foodborne illness prevention efforts noted above, foodborne outbreaks (defined as the occurrence of two or more cases of similar illness resulting from the ingestion of a common food) continue to occur and claim lives in the United States. Although numerous foodborne disease outbreaks occur every year in the United States, only a small fraction of them are recognized and reported to the CDC. Some of the large outbreaks published or reported to the CDC since 1988 are summarized in Table 1.7,31

Table 1

Notable outbreaks of human infection due to foodborne pathogens in the United States, 1980–2009.

YearState(s)PathogenVehicle of transmissionNumber of illnessesNumber of deathsReference
2009MultistateSalmonella TyphimuriumPeanut butter71497
2008Multistate, District of Columbia, and CanadaSaintpaul serotype of Salmonella entericaMexican-grown peppers1,01728
2007MultistateSalmonellaChicken and turkey pot pies4019
2007MultistateSalmonellaConAgra27210
2007MultistateSalmonellaPeter Pan and Great Value Peanut Butter42511
2007MultistateE. coli O157:H7Topp's Brand frozen ground beef patties4012
2008MultistateE. coli O157:H7Ground beef sold at Kroger® stores in Michigan and Ohio4513
2007MassachusettsListeria monocytogenesFarm milk or milk-related products5314
2006South Plainfield, New Jersey, and Long IslandE. coli O157:H7Green onions6715
2006Multistate and CanadaE. coli O157:H7Bagged spinach packaged by Natural Selection Foods199316
2002MultistateE. coli O157:H7Hamburger1817
2002MultistateListeria monocytogenesProcessed chicken46718
2000MultistateSalmonellaBean sprouts2319
2000Pennsylvania, WashingtonE. coli O157:H7Dairy farms5620
200011 statesListeria monocytogenesDelicatessen turkey304 deaths, 3 miscarriages21
2000North CarolinaListeria monocytogenesHomemade Mexican-style cheese120 deaths, 5 miscarriages22
199915 States, 2 Canadian provincesSalmonellaUnpasteurized orange juice9123
1999Connecticut, Maryland, New YorkListeria monocytogenesPaté1124
199822 statesListeria monocytogenesProcessed meats10115 deaths25
1997ColoradoE. coli O157:H7Ground beef1526
1996California, Colorado, Washington and British ColumbiaE. coli O157:H7Unpasteurized apple juice4527
1994Minnesota, South Dakota, WisconsinSalmonellaIce cream>3,000028
1994Illinois Michigan, Wisconsin,Listeria monocytogenesPasteurized chocolate milk69029
1993Washington, Idaho, California, NevadaE. coli O157:H7Hamburgers>500430
1989ConnecticutListeria monocytogenesShrimp1031
YearState(s)PathogenVehicle of transmissionNumber of illnessesNumber of deathsReference
2009MultistateSalmonella TyphimuriumPeanut butter71497
2008Multistate, District of Columbia, and CanadaSaintpaul serotype of Salmonella entericaMexican-grown peppers1,01728
2007MultistateSalmonellaChicken and turkey pot pies4019
2007MultistateSalmonellaConAgra27210
2007MultistateSalmonellaPeter Pan and Great Value Peanut Butter42511
2007MultistateE. coli O157:H7Topp's Brand frozen ground beef patties4012
2008MultistateE. coli O157:H7Ground beef sold at Kroger® stores in Michigan and Ohio4513
2007MassachusettsListeria monocytogenesFarm milk or milk-related products5314
2006South Plainfield, New Jersey, and Long IslandE. coli O157:H7Green onions6715
2006Multistate and CanadaE. coli O157:H7Bagged spinach packaged by Natural Selection Foods199316
2002MultistateE. coli O157:H7Hamburger1817
2002MultistateListeria monocytogenesProcessed chicken46718
2000MultistateSalmonellaBean sprouts2319
2000Pennsylvania, WashingtonE. coli O157:H7Dairy farms5620
200011 statesListeria monocytogenesDelicatessen turkey304 deaths, 3 miscarriages21
2000North CarolinaListeria monocytogenesHomemade Mexican-style cheese120 deaths, 5 miscarriages22
199915 States, 2 Canadian provincesSalmonellaUnpasteurized orange juice9123
1999Connecticut, Maryland, New YorkListeria monocytogenesPaté1124
199822 statesListeria monocytogenesProcessed meats10115 deaths25
1997ColoradoE. coli O157:H7Ground beef1526
1996California, Colorado, Washington and British ColumbiaE. coli O157:H7Unpasteurized apple juice4527
1994Minnesota, South Dakota, WisconsinSalmonellaIce cream>3,000028
1994Illinois Michigan, Wisconsin,Listeria monocytogenesPasteurized chocolate milk69029
1993Washington, Idaho, California, NevadaE. coli O157:H7Hamburgers>500430
1989ConnecticutListeria monocytogenesShrimp1031
Table 1

Notable outbreaks of human infection due to foodborne pathogens in the United States, 1980–2009.

YearState(s)PathogenVehicle of transmissionNumber of illnessesNumber of deathsReference
2009MultistateSalmonella TyphimuriumPeanut butter71497
2008Multistate, District of Columbia, and CanadaSaintpaul serotype of Salmonella entericaMexican-grown peppers1,01728
2007MultistateSalmonellaChicken and turkey pot pies4019
2007MultistateSalmonellaConAgra27210
2007MultistateSalmonellaPeter Pan and Great Value Peanut Butter42511
2007MultistateE. coli O157:H7Topp's Brand frozen ground beef patties4012
2008MultistateE. coli O157:H7Ground beef sold at Kroger® stores in Michigan and Ohio4513
2007MassachusettsListeria monocytogenesFarm milk or milk-related products5314
2006South Plainfield, New Jersey, and Long IslandE. coli O157:H7Green onions6715
2006Multistate and CanadaE. coli O157:H7Bagged spinach packaged by Natural Selection Foods199316
2002MultistateE. coli O157:H7Hamburger1817
2002MultistateListeria monocytogenesProcessed chicken46718
2000MultistateSalmonellaBean sprouts2319
2000Pennsylvania, WashingtonE. coli O157:H7Dairy farms5620
200011 statesListeria monocytogenesDelicatessen turkey304 deaths, 3 miscarriages21
2000North CarolinaListeria monocytogenesHomemade Mexican-style cheese120 deaths, 5 miscarriages22
199915 States, 2 Canadian provincesSalmonellaUnpasteurized orange juice9123
1999Connecticut, Maryland, New YorkListeria monocytogenesPaté1124
199822 statesListeria monocytogenesProcessed meats10115 deaths25
1997ColoradoE. coli O157:H7Ground beef1526
1996California, Colorado, Washington and British ColumbiaE. coli O157:H7Unpasteurized apple juice4527
1994Minnesota, South Dakota, WisconsinSalmonellaIce cream>3,000028
1994Illinois Michigan, Wisconsin,Listeria monocytogenesPasteurized chocolate milk69029
1993Washington, Idaho, California, NevadaE. coli O157:H7Hamburgers>500430
1989ConnecticutListeria monocytogenesShrimp1031
YearState(s)PathogenVehicle of transmissionNumber of illnessesNumber of deathsReference
2009MultistateSalmonella TyphimuriumPeanut butter71497
2008Multistate, District of Columbia, and CanadaSaintpaul serotype of Salmonella entericaMexican-grown peppers1,01728
2007MultistateSalmonellaChicken and turkey pot pies4019
2007MultistateSalmonellaConAgra27210
2007MultistateSalmonellaPeter Pan and Great Value Peanut Butter42511
2007MultistateE. coli O157:H7Topp's Brand frozen ground beef patties4012
2008MultistateE. coli O157:H7Ground beef sold at Kroger® stores in Michigan and Ohio4513
2007MassachusettsListeria monocytogenesFarm milk or milk-related products5314
2006South Plainfield, New Jersey, and Long IslandE. coli O157:H7Green onions6715
2006Multistate and CanadaE. coli O157:H7Bagged spinach packaged by Natural Selection Foods199316
2002MultistateE. coli O157:H7Hamburger1817
2002MultistateListeria monocytogenesProcessed chicken46718
2000MultistateSalmonellaBean sprouts2319
2000Pennsylvania, WashingtonE. coli O157:H7Dairy farms5620
200011 statesListeria monocytogenesDelicatessen turkey304 deaths, 3 miscarriages21
2000North CarolinaListeria monocytogenesHomemade Mexican-style cheese120 deaths, 5 miscarriages22
199915 States, 2 Canadian provincesSalmonellaUnpasteurized orange juice9123
1999Connecticut, Maryland, New YorkListeria monocytogenesPaté1124
199822 statesListeria monocytogenesProcessed meats10115 deaths25
1997ColoradoE. coli O157:H7Ground beef1526
1996California, Colorado, Washington and British ColumbiaE. coli O157:H7Unpasteurized apple juice4527
1994Minnesota, South Dakota, WisconsinSalmonellaIce cream>3,000028
1994Illinois Michigan, Wisconsin,Listeria monocytogenesPasteurized chocolate milk69029
1993Washington, Idaho, California, NevadaE. coli O157:H7Hamburgers>500430
1989ConnecticutListeria monocytogenesShrimp1031

Two recently published Foodborne Diseases Active Surveillance Network (FoodNet) reports showed that Salmonella, Campylobacter, Shigella, Cryptosporidium, and Shiga toxin Escherichia coli (STEC) O157 continue to be the leading causes of both the number and incidence of laboratory-confirmed foodborne infections in the United States (Tables 1, 2 and 3).32,33 According to the CDC, smaller outbreaks, especially those occurring within one state, are unlikely to be reported to public health officials.34 Outbreaks not causing serious illness, hospitalization, or death, or those not resulting in patients showing symptoms quickly are also unlikely to be reported to public health officials.34 Other factors that can determine whether or not an outbreak is recognized include consumer awareness and healthcare providers' ability to diagnose foodborne illness; interest and motivation of the consumer and healthcare provider to report the illness; and the capacity of state and local (city or county) health departments and environmental agencies to conduct foodborne illness surveillance.34

Table 2

Comparison of the numbers of laboratory-confirmed infections caused by specific bacterial pathogens in 200833 and 2005,32 as reported at 10 FoodNet Sites in the states of CA, CO, CT, GA, MD, MN, NM, NY, OR, and TN).

Pathogen20082005
PercentCases reportedPercentCases reported
Salmonella38.957,44444.576,505
Campylobacter34.075,82538.445,690
Shigella12.543,02918.142,095
Cryptosporidium7.941,0366.201,326
STEC O1572.835133.07473
STEC non-O1570.772051.23128
Yersinia0.981640.98163
Listeria0.811350.81136
Vibrio0.721310.78121
Cyclospora0.39170.1065
Total10018,49910016,702
Pathogen20082005
PercentCases reportedPercentCases reported
Salmonella38.957,44444.576,505
Campylobacter34.075,82538.445,690
Shigella12.543,02918.142,095
Cryptosporidium7.941,0366.201,326
STEC O1572.835133.07473
STEC non-O1570.772051.23128
Yersinia0.981640.98163
Listeria0.811350.81136
Vibrio0.721310.78121
Cyclospora0.39170.1065
Total10018,49910016,702

Parasitic pathogen.

Table 2

Comparison of the numbers of laboratory-confirmed infections caused by specific bacterial pathogens in 200833 and 2005,32 as reported at 10 FoodNet Sites in the states of CA, CO, CT, GA, MD, MN, NM, NY, OR, and TN).

Pathogen20082005
PercentCases reportedPercentCases reported
Salmonella38.957,44444.576,505
Campylobacter34.075,82538.445,690
Shigella12.543,02918.142,095
Cryptosporidium7.941,0366.201,326
STEC O1572.835133.07473
STEC non-O1570.772051.23128
Yersinia0.981640.98163
Listeria0.811350.81136
Vibrio0.721310.78121
Cyclospora0.39170.1065
Total10018,49910016,702
Pathogen20082005
PercentCases reportedPercentCases reported
Salmonella38.957,44444.576,505
Campylobacter34.075,82538.445,690
Shigella12.543,02918.142,095
Cryptosporidium7.941,0366.201,326
STEC O1572.835133.07473
STEC non-O1570.772051.23128
Yersinia0.981640.98163
Listeria0.811350.81136
Vibrio0.721310.78121
Cyclospora0.39170.1065
Total10018,49910016,702

Parasitic pathogen.

Table 3

Comparison of the incidence of laboratory-confirmed infections caused by specific bacterial pathogens in 200833 and 2005,32 as reported at 10 FoodNet sites in the states of CA, CO, CT, GA, MD, MN, NM, NY, OR, and TN.

PathogenIncidence
20082005
Salmonella16.2014.47
Campylobacter12.6812.66
Shigella6.594.66
Cryptosporidium2.252.95
STEC O1571.121.05
STEC non-O1570.450.28
Yersinia0.360.36
Listeria0.290.30
Vibrio0.290.27
Cyclospora0.040.14
PathogenIncidence
20082005
Salmonella16.2014.47
Campylobacter12.6812.66
Shigella6.594.66
Cryptosporidium2.252.95
STEC O1571.121.05
STEC non-O1570.450.28
Yersinia0.360.36
Listeria0.290.30
Vibrio0.290.27
Cyclospora0.040.14

Cases per 100,000 population.

Parasitic pathogen.

Table 3

Comparison of the incidence of laboratory-confirmed infections caused by specific bacterial pathogens in 200833 and 2005,32 as reported at 10 FoodNet sites in the states of CA, CO, CT, GA, MD, MN, NM, NY, OR, and TN.

PathogenIncidence
20082005
Salmonella16.2014.47
Campylobacter12.6812.66
Shigella6.594.66
Cryptosporidium2.252.95
STEC O1571.121.05
STEC non-O1570.450.28
Yersinia0.360.36
Listeria0.290.30
Vibrio0.290.27
Cyclospora0.040.14
PathogenIncidence
20082005
Salmonella16.2014.47
Campylobacter12.6812.66
Shigella6.594.66
Cryptosporidium2.252.95
STEC O1571.121.05
STEC non-O1570.450.28
Yersinia0.360.36
Listeria0.290.30
Vibrio0.290.27
Cyclospora0.040.14

Cases per 100,000 population.

Parasitic pathogen.

The occurrence of several small and large foodborne outbreaks in recent years and the accompanying broad media coverage, have led to a widespread perception that the numbers of foodborne disease outbreaks and cases are increasing in the United States. In reality, however, there is little evidence that the actual overall prevalence of foodborne illness is increasing.

FACTORS CONTRIBUTING TO THE OCCURRENCE OF FOODBORNE ILLNESS

The trends affecting the occurrence of foodborne illness include, but are not limited to the following: 1) large-scale production and wide distribution of food; 2) globalization of the food supply; 3) eating outside of the home; 4) microbial genomic diversification/emergence of new pathogens; and 5) growing population of at-risk consumers.

Large-scale production and wide distribution of food

In order to meet the increased demand for food due to growing human population worldwide, industrial-scale and centralized production systems including large-scale farming, intensified animal production, and large-scale food processing and distribution have drastically increased over the past several decades. Nearly all food consumed in the United States today is produced using modern intensive farming.35 Although such intensive food production systems are needed in order to meet the increasing demand for food, they have been blamed for the evolution of new pathogens. For example, the emergence of certain Salmonella serotypes over the past several decades is believed to have been caused by intensive animal farming.36

In an effort to combat the obesity epidemic in the United States, nutrition educators and healthcare professionals are encouraging consumers to eat more fruits and vegetables. At the same time as this effort is being made, however, the number of foodborne illness outbreaks linked to fresh produce (especially those eaten without cooking) is rising.37 This increase is likely being offset by a decrease in the number of outbreaks from other sources, since the overall prevalence of foodborne illness is not increasing.

Although food processing, especially that involving large-scale production, increases product value, lengthens product shelf life, and controls hazards, it is thought to also be responsible for food contamination and the spread of foodborne pathogens. The pooling of raw materials, for example, can result in a single adulterated component contaminating the rest and, potentially, the final product. The fact that food or food ingredients are often handled by several people using different equipment in diverse food processing settings can also increase the opportunities for contamination unless there are effective controls. Also, a continuous food production operation provides the conditions microorganisms need to grow. Such conditions include food, moisture, and temperature. Foodborne microorganisms need nutrients (e.g., carbohydrates and proteins) for their growth. Although the majority of foodborne microorganisms grow well between 41°F and 135°F,38 others can grow at refrigeration temperatures (≤41°F) or survive freezing temperatures (≤32°F). The growth of many foodborne microorganisms is significantly slowed down if water activity (aw), which is defined as the amount of moisture available for microbial growth, is 0.85 or lower.38 The aw scale ranges from 0 (driest) to 1.00 (wettest).

Failure to monitor and control pathogenic microorganisms such as Listeria monocytogenes in the food processing environment can result in them forming biofilms and thus colonizing certain food and non-food contact surfaces. Consequently, L. monocytogenes can persist in a food processing plant for a long time. For example, a specific outbreak L. monocytogenes subtype has been shown to persist for at least 12 years in a plant processing turkey frankfurters and delicatessen turkey meat in the US state of Oklahoma.39,40 Once a microbial population forms a biofilm and establishes a colony, it becomes extremely difficult to eliminate.41 In fact, at that point, the cleaning and sanitizing of colonized surfaces is often counterproductive. Rather than eliminating the microorganism, activities aimed at cleaning and sanitizing may loosen and release the cells from the biofilm, thereby increasing the likelihood of product contamination.42 Contamination can be controlled through continuous surveillance (i.e., collection and analysis of environmental samples on a regular basis).43 In this way, contaminated areas, surfaces, or spots can be detected and appropriate control actions can be taken before biofilms or colonies become established.

The impact of food processing on environmental contamination with foodborne pathogens is well known. In a food processing setting, a contaminated food-contact surface or food ingredient can result in contamination of several batches of final product and wide distribution of contaminated products within a short period of time. The recent Salmonella Typhimurium outbreak7 linked to a peanut butter plant in the US state of Georgia is a typical example of the severe consequences of a contaminated food processing environment. As of April 29, 2009, this multistate outbreak had sickened 714 people and possibly contributed to 9 deaths.7 The Salmonella contamination not only impacted the incriminated plant, it also resulted in the contamination and recall of other manufacturers' products that contained the contaminated peanut butter or paste.35 Cookies, crackers, cereal, candy, ice cream, and pet foods are among the products of other manufacturers that had peanut butter originating from the GA facility as an ingredient and have consequently been recalled due to possible contamination with Salmonella Typhimurium. Although the CDC and the FDA warned consumers to not eat recalled products as soon as the outbreak was detected, more outbreak-related illnesses continued to be reported by consumers who ate recalled products for the next several months, partly because many of the implicated products have a long shelf life. The CDC's consumer advice and recommendations are available at http://www.cdc.gov/salmonella/typhimurium/update.html#recommendations

Dirty food-contact surfaces and cross-contamination are the most common avenues of contamination both on farms and in food processing environments. Cross-contamination is defined as the transfer of microorganisms from one food or surface to another. Food producers can deny pathogens sites for harbor and thus prevent product contamination by developing and implementing standard operating procedures (SOPs) for cleaning and sanitizing equipment and food-contact surfaces. Preventing cross-contamination is another important way to reduce product contamination. Training employees to properly clean and sanitize equipment and food-contact surfaces, as well as to prevent cross-contamination, is important for ensuring food safety.

Globalization of the food supply

According to the USDA's Economic Research Service (USDA–ERS), imported food accounted for 15% (based on volume) of food consumed in the United States in 2005.44 When based on value, the proportion of food consumed in the United States that originated from foreign countries was 7% in 2005. Data from the USDA–ERS show that the average annual import share (when based on both volume and value) of food consumed in the United States has increased since 1980. Fresh produce, tree nuts, and fish and shellfish are the most common food imports. Data also indicate that the demand for ethnic food among consumers in the United States is rising.35

If contaminated with pathogens, imported food (especially fresh produce) can result in spread of the pathogens.45,46 Therefore, the importation of food from other countries (particularly those with inferior food safety standards) can increase the risk of foodborne illness in the United States. Water contamination is a significant public health issue in many developing countries47,48 and contaminated water is one of the most common sources of contamination in fresh produce.49,50 Products typically become adulterated when washed with contaminated water. Other unsafe agricultural practices, such as the possible use of untreated human waste and animal manure as fertilizers, can also result in the contamination of fresh produce.49,51

Eating food outside of the home

The number of Americans eating food prepared away from home has risen between 1977 and 1996.52 Nearly 50% of household expenditure on food in the United States goes towards the purchase of food from full-service and fast-food restaurants.52 Lifestyle, social, and economic changes, as well as increased travel and tourism, have all contributed to an increase in the number of American consumers eating food prepared in restaurants. Demand for food from street vendors is also on the rise. Eating food prepared away from home has implications for public health. A considerable number of foodborne illnesses occur in food service establishments. For example, according to the CDC, 50% of foodborne outbreaks reported through its surveillance system occurred in restaurants during 1998–2002.34 Based on these data, the risk of foodborne illness associated with eating out is greater than that of eating food prepared at home.

Further, changes in shopping habits in recent years have led to rising demand for ready-to-eat and refrigerated or frozen food products among consumers in the United States.53 Processed foods involve multiple stages of handling compared to unprocessed foods. Since frequent handling increases the chance of product contamination, such products may present a greater risk of foodborne illness. But the increase observed in recent years in both the number and frequency of foodborne illness outbreaks linked to unprocessed foods, such as fresh produce,37,45 has called this premise into question.

Numerous cases of foodborne illness also occur in the home.54,55 Practices leading to such cases include poor time-temperature control (e.g., allowing food to remain too long at room temperature), cross-contamination, and poor personal hygiene. Consumers can avoid foodborne illness by handling food safely, following food preparation recommendations, and avoiding foods commonly associated with foodborne illness (e.g., raw or undercooked meat, poultry, and seafood; raw or undercooked eggs; raw sprouts; unpasteurized fruit and vegetable juices; and unpasteurized milk and soft cheese).56 Many educational resources for consumers that focus on preventing foodborne illness in home kitchens are available at http://www.foodsafety.gov and http://www.fightbac.org.

Genetic variability and emergence of new pathogens

The ability of microorganisms to adapt to different environmental conditions and to frequently survive unfavorable environmental conditions and changes has been attributed to their large genetic variability.57 Researchers are just beginning to understand the mechanisms underlying the evolution and emergence of new bacterial pathogens. Many studies have revealed that organisms can undergo changes in their physiology in a short period of time, resulting in the emergence of new pathogens.58 The emergence of new pathogens can have serious implications for public health, especially if the strains can evolve or mutate to become more virulent or drug resistant.36 For example, multidrug-resistant (MDR) strains of Salmonella have recently emerged, which represent a significant threat to food safety. MDR Salmonella strains that are resistant to the antimicrobial agents designed to eradicate typical Salmonella strains render those drugs ineffective for treating MDR Salmonella-related infections.36 The emergence of MDR Salmonella has been blamed on the administration of antimicrobial agents to food animals.36 The emergence of new pathogens is assisted by a variety of factors including environmental changes, changes in food production or processing methods, changes in populations affected by the pathogens, and changes in microbial characteristics and distribution.58

Increasing proportion of at-risk consumers

The highest rates of foodborne illness are among young children, adults who have a weakened immune system, older adults, and pregnant women.

According to projections of the United States Census Bureau, the proportion of individuals aged 65 years and older is increasing in the United States.59 These projections estimate that approximately 20% of US residents will be aged 65 and older in 2030. In 2050, this subpopulation is expected to rise to 88.5 million, reflecting more than a twofold change from 38.7 million in 2008.

The immunocompromised group is composed of individuals who are chronically ill, such as AIDS patients or persons who take medications that adversely affect their immune system.53 The latter category includes cancer patients on immunosuppressive drugs, people who take antibiotics, and patients treated for transplants and diabetes.

Due to better healthcare and advances in the field of medicine, older adults and people with weakened immune systems, who would otherwise die prematurely, are living longer; hence, these subpopulations are growing in the United States. It is difficult to determine the impact this increase may be having on the overall incidence of foodborne illness in the United States as any increase in the incidence of foodborne illness among these subpopulations is being mitigated by improved healthcare and advances in medical technologies.

THE BURDEN OF FOODBORNE ILLNESS IN THE UNITED STATES

The CDC estimates that foodborne infections cause 76 million illnesses, including 325,000 hospitalizations and 5,000 deaths, each year in the United States.60 Further, the cost of foodborne illness to the US economy is $10–83 billion per year.61 The costs of foodborne illness include lost productivity, medical costs, loss of customers and sales, and lawsuits resulting in compensation for loss of income, medical expenses, legal fees, and other damages.62 Other hidden costs include the pain and suffering associated with foodborne illness, time spent by family members caring for ill relatives, and the cost of treatment-related travel for patients and their relatives.

Bacteria and viruses pose the greatest threat to food safety. During 1998–2002, bacteria caused more than half of all reported foodborne disease outbreaks (55%) and cases (55%).34 During this same period, viruses caused 33% of outbreaks and 41% of foodborne illness cases. Other common causes of foodborne illness include chemical agents, parasites, fungi (yeasts and molds), and physical hazards (e.g., bones or bone fragments; stones, leaves, or stalks; and shell fragments from nuts, shellfish, and eggs).38 Although any food can be contaminated and become potentially hazardous, certain foods pose a greater threat to public health than others. High-risk foods include raw or undercooked foods of animal origin (e.g., meat and poultry, eggs, fish, and unpasteurized milk).56 Fresh produce, particularly raw fruits and vegetables, have been responsible for many foodborne outbreaks in recent years and, consequently, are currently considered to be high-risk foods. Unpasteurized fruit juices and alfalfa sprouts/other raw sprouts are also regarded as high-risk foods.56

FOODBORNE ILLNESS OUTBREAKS REPORTED IN THE UNITED STATES, 1988–2006

The annual numbers of foodborne disease outbreaks (FBDOs) and foodborne illnesses reported to the CDC between 1988 and 2006 are shown in Figures 1 and 2, respectively. However, the numbers of outbreaks reported annually to the CDC34,65 represent only a portion of the actual number of outbreaks that occur. According to the CDC, each year, many foodborne outbreaks and illnesses go unreported.34,60 For example, it has been estimated that for every case of outbreak-associated cases of salmonellosis (foodborne illness caused by Salmonella infection), reported through the Foodborne Disease Outbreak Surveillance System (PulseNet), an extra 38 go undetected or unreported.66 PulseNet is a national network designed to help detect foodborne disease outbreaks.67,69 The program was launched in four states in 1996 and by 2001 all 50 states and several large cities were participating. PulseNet is comprised of the CDC and state health departments in the United States. Since its launch in 1996, PulseNet's utility for increasing the number of recognized outbreaks (including those caused by STEC O157, Salmonella enterica, Listeria monocytogenes, Shigella spp., and Campylobacter spp.) has been noted by many authors. In PulseNet laboratories, foodborne pathogens are characterized using the pulsed-field gel electrophoresis (PFGE) subtyping technique. Using standardized protocols, PFGE DNA “fingerprints” of isolates of foodborne pathogens are generated67,69 and rapidly exchanged among the CDC and participating laboratories through electronic submission of the PFGE “fingerprints” to a CDC database; the database is configured to allow for rapid comparison of the patterns as well as real-time communication among participating laboratories. A close relationship among PFGE banding patterns points to a common source of an outbreak pathogen subtype. PFGE data from the FDA and USDA–FSIS laboratories are also entered into the CDC FoodNet database.

Figure 1

Foodborne disease outbreaks (FBDOs) in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

Figure 2

Foodborne illnesses in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

The number of cases of foodborne illness increased in 1998 compared to previous years (1988–1997). In 1998, 1,314 FBDOs resulted in 27,257 cases of illness. Prior to 1998, the number of illnesses per year ranged from 11,015 to 22,607 (Figures 1 and 2). The CDC has attributed this increase to the enhanced surveillance made possible through implementation of the National Molecular Subtyping Network for Foodborne Disease Surveillance (PulseNet) program in 1996.34,69 The number of foodborne disease outbreaks per year (Figure 1) and the number of illnesses per year (Figure 2) remained relatively constant between 1998 and 2006.

Figure 3 shows the average number of foodborne illness cases per outbreak during 1988–2006. Between 1988 and 1995, the average number of illnesses per outbreak per year was generally high, indicating the outbreaks in those years were relatively large. In 1996, the average number of foodborne illness cases per outbreak peaked at approximately 47. One year later, the average number of illnesses per outbreak decreased to approximately 24 and in 1998 it decreased again to approximately 21. The annual average size of outbreaks was smaller between 1998 and 2006 compared to the years 1988–1997 (Figure 3). According to the CDC, this decrease in the average size of reported outbreaks following implementation of enhanced surveillance in 1996 was largely a result of the increased ability of investigators to detect smaller outbreaks that would not otherwise have been reported.64

Figure 3

Foodborne illnesses per foodborne disease outbreak (FBDO) in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

Figure 4 depicts the proportion of reported outbreaks and illnesses of known etiology per year between 1988 and 2006. During 1999–2006, the proportion of outbreaks with a known etiology steadily and consistently increased each year, from 27.6% in 1999 to 50.0% in 2006 (Fig. 4).

Figure 4

Proportion of foodborne disease outbreaks (FBDOs) and illnesses of known etiology in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
 FBDOs (◆), illnesses (graphic)
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

During 1988–2006, bacteria caused the majority of foodborne outbreaks and illnesses (Figures 5 and 6). The number of outbreaks and the number illnesses caused by viruses remained low between 1988 and 1997, but they sharply increased during 1997 and 2000, and they remained high during 2000–2006. It is noteworthy that the number of outbreaks caused by viruses was higher than that caused by bacteria in 2004 and 2006 (Figure 6). Likewise, viruses caused more illnesses compared to bacteria during 2004–2006 (Figure 6). The CDC has largely attributed the changes in the proportion of outbreaks and illnesses caused by viral pathogens noted above to better specimen collection and diagnostic/detection protocols for viral infections.34 Chemical hazards and parasites generally caused only a small proportion of outbreaks and illnesses (Figures 5 and 6).

Figure 5

Foodborne disease outbreaks (FBDOs) by etiology in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
 Bacterial (◆), viral (graphic), chemical (▴), and parasitic (●)
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

Figure 6

Foodborne illnesses by etiology in the United States, 1988–2006. Data from the CDC (1996),63, (2000),64, (2006),34, and (2009).65 
 Bacterial (◆), viral (graphic), chemical (▴), and parasitic (●)
*All data for 2001–2006 were collected electronically through the Electronic Foodborne Outbreak Reporting System (eFORS) without confirmation of etiology by CDC staff; all etiologies are as reported by the state. Etiologies of outbreaks prior to 2001 were confirmed by CDC staff, so some differences may exist between 2001–2006 data and data from prior years.

CONCLUSION

Foodborne illness continues to be a significant public health threat in the United States despite intensified efforts to prevent it. Several trends including large-scale production and wide distribution of food, globalization of the food supply, eating outside of the home, emergence of new pathogens, and increasing proportion of at-risk consumers are facilitating outbreaks of foodborne illness and making it difficult to control foodborne pathogens and decrease the incidence of the infections they cause.

Despite the occurrence of many large outbreaks of foodborne illness in recent years, there is insufficient evidence to support claims that the numbers of actual foodborne illness outbreaks and cases are climbing. According to the CDC, the increase in both reported outbreaks and foodborne illness cases in recent years is likely a reflection of enhanced surveillance rather than a true increase in incidence.34 The media's coverage of some recent outbreaks, especially those linked to peanut butter,7 Mexican-grown peppers,8 and bagged spinach,16 has also increased awareness, which may help explain the widespread notion that the numbers of foodborne disease outbreaks and concomitant illnesses have increased in recent years. Furthermore, increased awareness of foodborne illness and its symptoms has likely resulted in increased reporting and better diagnosing of foodborne illnesses by patients and physicians, respectively.

In a recently published report, the Foodborne Diseases Active Surveillance Network (FoodNet), a partnership surveillance project of the CDC, the USDA-FSIS, the FDA, and 10 US states, found there was very little change in the incidence of foodborne illness caused by common pathogens when the 2008 data was compared to the preceding 3 years (2005–2007).33 While there has been little change in the overall incidence of foodborne illness, a recent HealthyPeople 201070 progress review indicates that the numbers of certain specific foodborne infections have, in fact, gone down. For example, during 1997–2005, the incidence of infections caused by Campylobacter spp., E. coli O157:H7, and L. monocytogenes decreased from 24.6 to 12.7 cases per 100,000 population, 2.1 to 1.1 per 100,000, and 0.47 to 0.30 per 100,000, respectively.71 The 2010 targets for Campylobacter spp., E. coli O157:H7, and L. monocytogenes are 12.3 cases per 100,000, 1.0 per 100,000, and 0.24 per 100,000, respectively.71

The continued occurrence of food-related infections calls for better foodborne illness risk reduction and control interventions. Since food can become contaminated at any point during the food processing and preparation chain, including in the consumers' own kitchens, interventions must be implemented at every step, from farm to table.

In order to meet the increased demand for food associated with the growing human population worldwide, industrial-scale and centralized production systems, including large-scale farming, intensified animal production, and large-scale food processing and distribution, have drastically increased over the past several decades. The fact that these systems are needed in order to meet the demand for food is undisputable. However, these kinds of systems have also been blamed for increasing the risk of foodborne illness. Strategies for controlling potential microbial food safety hazards include the use of good agricultural practices; the HACCP program; good manufacturing practices, and standard operating procedures for sanitation. Training employees to avoid food contamination by properly cleaning and sanitizing equipment and food-contact surfaces, preventing cross-contamination, and practicing good personal hygiene is also important for ensuring food safety.

In the home, consumers can avoid foodborne illness by handling food safely, following food preparation recommendations, and avoiding foods commonly associated with foodborne illness (e.g., raw or undercooked meat, poultry, and seafood; raw or undercooked eggs; raw sprouts; unpasteurized fruit and vegetable juices; and unpasteurized milk and soft cheese).56 Many educational resources for consumers that focus on preventing foodborne illness in home kitchens are available at http://www.foodsafety.gov and http://www.fightbac.org. To further improve education of the general public about food safety, closer ties between food safety educators and the media are encouraged.

Finally, more research into understanding the biology, ecology, and spread of foodborne pathogens is necessary in order to identify better pathogen-control strategies. To more effectively control foodborne pathogens, more research on the mechanisms underlying the evolution and emergence of new bacterial pathogens is needed.

Declaration of interest

The author has no relevant interests to declare.

REFERENCES

1

National Advisory Committee on Microbiological Criteria for Foods
.
Hazard analysis and critical control point principles and application guidelines
.
J Food Prot
.
1998
;
61
:
1246
1259
.

2

Codex Alimentarius Commission
.
Recommended International Code of Practice General Principles of Food Hygiene, CAC/RCP 1-1969, Rev. 4-2003
. Rome, Italy:
Food and Agriculture Organization and World Health Organization
;
2003
.

3

United States Department of Agriculture
Food and Inspection Service
.
Title 9 Code of Federal Regulation (CFR) Part 417—“Hazard Analysis and Critical Control Point (HACCP) Systems” for Meat and Poultry Products 1996
. U.S. Government Printing Office via GPO Access. Washington DC, USA.
2009
: Available at: http://www.access.gpo.gov/nara/cfr/waisidx_07/9cfr417-07.html. Accessed 18 May 2009.

4

US Food and Drug Administration
.
Title 21 Code of Federal Regulation (CFR) Part 120—“Hazard Analysis and Critical Control Point (HACCP) Systems,” Procedures for the Safe and Sanitary Processing and Importing of Juice 2001
. U.S. Government Printing Office via GPO Access. Washington DC, USA.
2009
: Available at: http://www.access.gpo.gov/nara/cfr/waisidx_06/21cfr120-06.html. Accessed 18 May 2009.

5

US Food and Drug Administration
.
Title 21 Code of Federal Regulation (CFR) Part 123—“Hazard Analysis and Critical Control Point (HACCP) Systems,” Procedures for the Safe and Sanitary Processing and Importing of Fish and Fishery Products 1995
. U.S. Government Printing Office via GPO Access. Washington DC, USA.
2009
: Available at: http://www.access.gpo.gov/nara/cfr/waisidx_06/21cfr123-06.html. Accessed 18 May 2009.

6

Nielsen
.
“Fresh” Alternatives at Retail. The Nielsen Company
. September
2004
: New York, NY. Available at: http://il.nielsen.com/Archive/Insight/sheet1_eng.pdf. Accessed 5 February 2010.

7

Centers for Disease Control and Prevention
.
Investigation Update: Outbreak of Salmonella typhimurium Infections, 2008–2009
.
2010
: Available at: http://www.cdc.gov/salmonella/typhimurium/update.html. Accessed 4 February 2010.

8

Centers for Disease Control and Prevention
.
Investigation of Outbreak of Infections Caused by Salmonella Saintpaul
.
2009
: Available at: http://www.cdc.gov/salmonella/saintpaul/. Accessed 7 April 2009.

9

Centers for Disease Control and Prevention
.
Multistate Outbreak of Salmonella Infections Associated with Frozen Pot Pies – United States
.
2007
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5747a3.htm. Accessed 7 April 2009.

10

Centers for Disease Control and Prevention
.
Investigation of Outbreak of Human Infections Caused by Salmonella I 4,[5],12:i:-.
2009
: Available at: http://www.cdc.gov/salmonella/4512eyeminus.html. Accessed 7 April 2009.

11

Centers for Disease Control and Prevention
.
Salmonellosis – Outbreak Investigation
.
2007
: Available at: http://www.cdc.gov/ncidod/dbmd/diseaseinfo/salmonellosis_2007/030707_outbreak_notice.htm. Accessed 7 April 2009.

12

Centers for Disease Control and Prevention
.
Multistate Outbreak of E. coli O157 Infections Linked to Topp's Brand Ground Beef Patties
.
2009
: Available at: http://www.cdc.gov/ecoli/2007/october/100207.html. Accessed 7 April 2009.

13

Centers for Disease Control and Prevention
.
Investigation of Multistate Outbreak of E. coli O157:H7 Infections
.
2009
: Available at: http://www.cdc.gov/ecoli/june2008outbreak/index_071608.html. Accessed 8 April 2009.

14

Centers for Disease Control and Prevention
.
Outbreak of Listeria monocytogenes Infections Associated with Pasteurized Milk from a Local Dairy – Massachusetts
.
2007
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5740a1.htm. Accessed 7 April 2009.

15

Centers for Disease Control and Prevention
.
Multistate Outbreak of E. coli O157 Infections
.
2006
: Available at: http://www.cdc.gov/ecoli/2006/december/121206.htm. Accessed 7 April 2009.

16

Centers for Disease Control and Prevention
.
Update on Multi-State Outbreak of E. coli O157:H7 Infections from Fresh Spinach
. October 6,
2006
: Available at: http://www.cdc.gov/foodborne/ecolispinach/100606.htm. Accessed 7 April 2009.

17

Centers for Disease Control and Prevention
.
Multistate Outbreak of Escherichia coli O157:H7 Infections Associated with Eating Ground Beef – United States
. June–July
2002
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5129a1.htm. Accessed 7 April 2009.

18

Centers for Disease Control and Prevention
.
Public Health Dispatch: Outbreak of Listeriosis – Northeastern United States
.
2002
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5142a3.htm. Accessed 7 April 2009.

19

Centers for Disease Control and Prevention
.
Outbreak of Salmonella serotype Kottbus Infections Associated with Eating Alfalfa Sprouts – Arizona, California, Colorado, and New Mexico
. February–April
2001
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5101a3.htm. Accessed 7 April 2009.

20

Centers for Disease Control and Prevention (CDC)
.
Outbreaks of Escherichia coli O157:H7 Infections Among Children Associated With Farm Visits – Pennsylvania and Washington
.
2000
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5015a5.htm. Accessed 7 April 2009.

21

Olsen
SJ
Patrick
M
Hunter
SB
, et al.
Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat
.
Clin Infect Dis
.
2005
;
40
:
962
967
. Available at:http://www.cdc.gov/enterics/publications/438-Olsen2005.pdf. Accessed 7 April 2009.

22

Centers for Disease Control and Prevention
.
Outbreak of Listeriosis Associated with Homemade Mexican-style Cheese – North Carolina, October 2000–January 2001
.
2009
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5026a3.htm. Accessed 7 April 2009.

23

Centers for Disease Control and Prevention
.
Outbreak of Salmonella Serotype Muenchen Infections Associated with Unpasteurized Orange Juice – United States and Canada
. June
1999
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm4827a2.htm. Accessed 7 April 2009.

24

Centers for Disease Control and Prevention
.
US Foodborne Disease Outbreaks
.
2003
: Available at: http://www.cdc.gov/foodborneoutbreaks/outbreak_data.htm. Accessed 3 June 2009.

25

Centers for Disease Control and Prevention
.
Update: Multistate Outbreak of Listeriosis – United States, 1998–1999
.
2009
: Available at: http://www.cdc.gov/media/pressrel/r990114.htm. Accessed 7 April 2009.

26

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
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/00049079.htm. Accessed 7 April 2009.

27

Centers for Disease Control and Prevention
.
Outbreak of Escherichia coli O157:H7 Infections Associated with Drinking Unpasteurized Commercial Apple Juice – British Columbia, California, Colorado, and Washington
. October
1996
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/00044358.htm. Accessed 7 April 2009.

28

Vought
KJ
Tatini
SR
.
Salmonella enteritidis contamination of ice cream associated with a 1994 multistate outbreak
.
J Food Prot
.
1998
;
61
:
5
10
.

29

Dalton
CB
Austin
CC
Sobel
J
, et al.
An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk
.
N Engl J Med
.
1997
;
336
:
100
105
.

30

Centers for Disease Control and Prevention
.
Update: Multistate Outbreak of Escherichia coli O157:H7 Infections from Hamburgers – Western United States, 1992–1993
.
2009
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/00020219.htm. Accessed 8 April 2009.

31

Riedo
FX
Pinner
RW
Tosca
ML
, et al.
A point-source foodborne listeriosis outbreak: documented incubation period and possible mild illness
.
J Infect Dis
.
1994
;
170
:
693
696
.

32

Centers for Disease Control and Prevention
.
FoodNet Annual Report. Atlanta, USA
.
2005
: Available at: http://www.cdc.gov/foodnet/annual/2005/2005_AR_Report.pdf. Accessed 5 February 2010.

33

Centers for Disease Control and Prevention
.
Preliminary FoodNet Data on the Incidence of Infection with Pathogens Transmitted Commonly Through Food – 10 States, 2008. Atlanta, USA
.
2009
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5813a2.htm. Accessed 1 June 2009.

34

Centers for Disease Control and Prevention
.
Surveillance for Foodborne-disease Outbreaks – United States, 1998–2002
. In: Surveillance Summaries, MMWR 2006; 55(No. SS-11). Atlanta, USA.
2009
: Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/ss5510a1.htm. Accessed 18 May 2009.

35

Maki
DG
.
Coming to grips with foodborne infection — peanut butter, peppers, and nationwide Salmonella outbreaks
.
N Engl J Med
.
2009
;
360
:
10
.

36

World Health Organization
.
Drug-resistant Salmonella. Fact Sheet N°139
.
2005
: Available at: http://www.who.int/mediacentre/factsheets/fs139/en/. Accessed 30 April 2009.

37

Lynch
MF
Tauxe
RV
Hedberg
CW
.
The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities
.
Epidemiol Infect
.
2009
;
137
:
307
315
.

38

National Restaurant Association
.
ServSafe Coursebook
, 5th edn. Chicago, IL:
Prentice Hall
;
2008
.

39

Wiedmann
M
Nightingale
K
.
DNA-based subtyping methods facilitate identification of foodborne pathogens
.
Food Technol Mag
.
2009
;
63
:
44
49
.

40

Orsi
RH
Borowsky
M
Lauer
P
, et al.
Shortterm genome evolution of Listeria monocytogenes in a non-controlled environment
.
BMC Genomics
.
2008
;
9
:
539
.

41

Gamble
R
Muriana
PM
.
Microplate fluorescence assay for measurement of the ability of strains of Listeria monocytogenes from meat and meat-processing plants to adhere to abiotic surfaces
.
Appl Environ Microbiol
.
2007
;
73
:
5235
5244
.

42

Folsom
JP
Frank
JF
.
Chlorine resistance of Listeria monocytogenes biofilms and relationship to subtype, cell density, and planktonic cell chlorine resistance
.
J Food Prot
.
2006
;
69
:
1292
1296
.

43

Nyachuba
DG
Donnelly
CW
.
Comparison of 3MTMPetrifilmTM Environmental Listeria Plates versus standard enrichment methods for the detection of Listeria monocytogenes of epidemiological significance from environmental surfaces
.
J Food Sci
.
2007
;
72
:
M356
M354
.

44

United States Department of Agriculture–Economic Research Service
.
AmberWaves Statistics – Data Feature. What Share of U.S. Consumed Food Is Imported?
2008
, Volume 6,
36
37
. Available at: http://www.ers.usda.gov/AmberWaves/February08/PDF/Datafeature.pdf. Accessed 28 February 2010.

45

Johnston
LM
Jaykus
LA
Moll
D
Anciso
J
Mora
B
Moe
CL
.
A field study of the microbiological quality of fresh produce of domestic and Mexican origin
.
Int J Food Microbiol
.
2006
;
112
:
83
95
.

46

Herwaldt
BL
Ackers
M-L
,
the Cyclospora Working Group
.
An outbreak in 1996 of cyclosporiasis associated with imported raspberries
.
N Engl J Med
.
1997
;
336
:
1548
1556
.

47

Ortega
YR
Sanchez
R
.
Update on Cyclospora cayetanensis, a food-borne and waterborne parasite
.
Clin Microbiol Rev
.
2010
;
23
:
218
234
.

48

World Health Organization
.
Safety Water, Safer Health – Costs, Benefits, and Sustainability of Interventions to Protect and Promote Health
.
2010
: Geneva, Switzerland; WHO. Available at: http://whqlibdoc.who.int/publications/2008/9789241596435_eng.pdf. Accessed 5 February 2010.

49

U.S. Department of Health and Human Services / Food and Drug Administration Guidance for Industry
.
Guide to Minimize Microbial Food Safety Hazards of Fresh-cut Fruits and Vegetables
.
2010
: Available at: http://www.fda.gov/food/guidancecomplianceregulatoryinformation/guidancedocuments/produceandplanproducts/ucm064458.htm. Accessed 5 February 2010.

50

Gerba
CP
.
The role of water and water testing in produce safety
. In:
Fan
X
Niemira
BA
Doona
CJ
Feeherry
FE
Gravani
RB
, eds.
Microbial Safety of Fresh Produce?
Ames, IA:
Wiley-Blackwell
;
2009
.

51

Jiang
X
Shepherd
M
.
The role of manure and compost in produce safety
. In:
Fan
X
Niemira
BA
Doona
CJ
Feeherry
FE
Gravani
RB
, eds.
Microbial Safety of Fresh Produce?
Ames, IA:
Wiley-Blackwell
;
2009
.

52

Creel
JS
Sharkey
JR
McIntosh
A
Anding
J
Huber
JC
Jr
.
Availability of healthier options in traditional and nontraditional rural fast-food outlets
.
BMC Public Health
.
2008
;
8
:
395
.

53

Gandhi
M
Chikindas
ML
.
Listeria: a foodborne pathogen that knows how to survive
.
Int J Food Microbiol
.
2007
;
113
:
1
15
.

54

Scott
E
.
Food safety and foodborne disease in 21st century homes
.
Can J Infect Dis
.
2003
;
14
:
277
280
. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2094945/pdf/JID14277.pdf/?tool=pmcentrez. Accessed 5 February 2010.

55

Scott
E
.
A review of foodborne disease and other hygiene issues in the home
.
J Appl Bacteriol
.
1996
;
80
:
5
9
.

56

Centers for Disease Control and Prevention
.
Foodborne Illness, Frequently Asked Questions
.
2005
: Atlanta, USA. Available at: http://www.cdc.gov/ncidod/dbmd/diseaseinfo/foodborneinfections_g.htm#riskiestfoods. Accessed 1 June 2009.

57

Hall
RL
.
Foodborne illness: implications for the future
.
Emerg Infect Dis
.
1997
;
3
:
555
559
. Available at: http://www.cdc.gov/ncidod/EID/vol3no4/adobe/hall.pdf. Accessed 1 June 2009.

58

Motarjemi
Y
Adams
M
.
Emerging Foodborne Pathogens
. Cambridge:
Woodhead Publishing Limited
;
2006
.

59

U.S. Census Bureau
.
An Older and More Diverse Nation by Midcentury. U.S. Census Bureau News
.
2008
: Available at: http://www.census.gov/Press-Release/www/releases/archives/population/012496.html. Accessed 1 June 2009.

60

Mead
PS
Slutsker
L
Dietz
V
McCaig
LF
Bresee
JS
Shapiro
C
Griffin
PM
Tauxe
RV
.
Food-related illness and death in the United States
.
Emerg Infect Dis
.
1999
;
5
:
607
625
.

61

Food and Drug Administration–Center for Food Safety and Applied Nutrition (FDA–CFSAN)
.
Produce Safety From Production to Consumption: 2004 Action Plan to Minimize Foodborne Illness Associated with Fresh Produce Consumption
.
2004
: Available at: http://www.cfsan.fda.gov/~dms/prodpla2.html. Accessed 1 June 2009.

62

Buzby
JC
Roberts
T
Jordan Lin
CT
, et al.
Bacterial Foodborne Disease: Medical Costs and Productivity Losses
. United States Department of Agriculture–Economic Research Service (USDA–ERS). Agricultural Economics Report No. (AER741) 100 pp, August
1996
: Available at: http://www.ers.usda.gov/publications/aer741/. Accessed 1 June 2009.

63

Centers for Disease Control and Prevention
.
Surveillance for foodborne-disease outbreaks – United States, 1988–1992
. In: Surveillance Summaries, MMWR
1996
: 45(No. SS-5).

64

Centers for Disease Control and Prevention
.
Surveillance for foodborne-disease outbreaks – United States, 1993–1997
. In: Surveillance Summaries, MMWR
2000
: 49(No. SS-1).

65

Centers for Disease Control and Prevention
.
Annual Listing of Foodborne Disease Outbreaks, United States
.
2009
: Available at: http://www.cdc.gov/foodborneoutbreaks/outbreak_data.htm. Accessed 1 June 2009.

66

Voetsch
AC
Van Gilder
TJ
Angulo
FJ
, et al.
FoodNet Estimate of the Burden of Illness Caused by Nontyphoidal Salmonella Infections in the United States
.
Clin Infect Dis
.
2004
;
38
:
S3
.

67

Centers for Disease Control and Prevention
.
PulseNet Program Home. Atlanta, USA
.
2009
: Available at: http://www.cdc.gov/PULSENET/. Accessed 1 June 2009.

68

Gerner-Smidt
P
Hise
K
Kincaid
J
, et al.
PulseNet USA: a five-year update
.
Foodborne Pathog Dis
.
2006
;
3
:
9
19
.

69

Swaminathan
B
Barrett
TJ
Hunter
SB
Tauxe
RV
.
PulseNet: the molecular subtyping network for foodborne disease surveillance – United States
.
Emerg Infect Dis
.
2001
;
7
:
382
389
.

70

Office of Disease Prevention and Health Promotion
.
About Health People 2010
.
2010
: Department of Health and Human Services. Rockville, MD, USA. Available at: http://www.healthypeople.gov/ Accessed 1 June 2009.

71

Healthy People
.
Progress Review – Food Safety. U.S
.
2010
: Department of Health and Human Services, Public Health Service, 2007. Washington, DC, USA. Available at: http://www.healthypeople.gov/data/2010prog/focus10/default.htm. Accessed 1 June 2009.