The new American diet and the changing face of foodborne illness

CLEVELAND CL IN IC JOURNAL OF MEDICINE VOLUME 69 • NUMBER 5 MAY 2002 419

The new American dietand the changing face of foodborne illness

ALAN J. TAEGE, MDDepartment of Infectious Diseases, Cleveland Clinic

■ ABSTRACTPathogens responsible for foodborneillness are changing, owing tochanges in the American diet as wellas in food production and distribution.Microbial adaptations to heat, acid,cold, and antibiotics have madefood safety a challenging task.This article reviews the commonpathogens, their sources, andtreatment.

OODBORNE ILLNESS isn’t just about badpotato salad any more. As the

American diet and methods of food produc-tion and distribution have been transformedin recent decades, so have the patterns offoodborne illness and the pathogens thatcause it.

Now we have to contend with Cyclosporacontamination in imported raspberries andmultistate distribution of deli meat contami-nated with Listeria. Other pathogens areemerging or reemerging as well.

Fortunately, the US food supply is one ofthe safest in the world. However, muchremains to be improved concerning methodsof production, importation, processing, andstorage.

Because consumers are the ultimate bioas-say for food contamination, physicians oftensee the results of food safety problems in theiroffices. Certain pathogens may cause chronicsequelae (TABLE 1).1 It is crucial to understandthe scope and best treatment of the most com-mon foodborne illnesses and to be alert to thepotential sequelae.

■ CHANGING CAUSES,PROMINENT PATHOGENS

An estimated 76 million cases of foodborneillness occur each year in the United States1;as many as 500,000 people are hospitalizedand 9,000 may die. The economic impact isestimated to be as high as $25 billion per year.

These statistics may be gross underesti-mates because many cases of foodborne illnessare never reported. Despite tracking by the USPublic Health Service and investigations bylocal, state, and national agencies, the sourceof foodborne illness is determined in only 40%to 45% of cases. Sporadic outbreaks, which faroutnumber large outbreaks, receive relativelylittle attention or investigation.

F

MEDICAL GRAND ROUNDS TAKE-HOME

POINTS FROM

LECTURES BY

CLEVELAND CLINIC

AND VISITING

FACULTY

Chronic sequelae of somefoodborne illnessesCampylobacter

Guillain-Barré syndromeReactive arthritis

Escherichia coli O157:H7Hemolytic uremic syndrome

(especially in children)Listeria monocytogenes

EncephalitisNeurologic effects

SalmonellaReactive arthritis

ShigellaReactive arthritis

Yersinia enterocoliticaReactive arthritis

ADAPTED FROM CENTERS FOR DISEASE CONTROL AND PREVEN-TION. DIAGNOSIS AND MANAGEMENT OF FOODBORNE ILLNESS.

MMWR 2001; 50(RR02):1–69.

T A B L E 1

Consumers arethe ultimatebioassay forfoodcontamination

420 CLEVELAND CL IN IC JOURNAL OF MEDICINE VOLUME 69 • NUMBER 5 MAY 2002

Several important shifts in the epidemio-logic factors of foodborne illness have beennoted in the last century.1• Eighty percent of foodborne illnesses orig-inate from sources outside the home, asopposed to early in the last century whenhome-preservation of foods with its inherentproblems was much more common.• Food poisoning is more likely to occur andbe more severe at the extremes of age and inimmunocompromised people. This becomesparticularly important with our aging popula-tion and with increasing numbers of patientson immunosuppressive drugs.• Two thirds of foodborne illnesses arethought to have a viral source and thereforeare difficult to track. The remaining third areattributed to bacteria, with a small numberderived from parasites, toxins, or chemicals.• Foodborne illnesses caused by Salmonella,Campylobacter, and Escherichia coli O157:H7have eclipsed those attributed to Clostridiumand Staphylococcus.• Heat-tolerant, acid-tolerant, and antibiot-ic-resistant pathogens are increasing. Listeriahas the ability to multiply in a refrigerator; Ecoli O157:H7 has become significantly acid-tolerant. Strains of Salmonella have acquiredmultidrug resistance, likely as a result of theuse of antibiotics in animal production.

■ WHY?

Health consciousness, demographic shifts, andconsumption of ethnic foods have led tochanges in the dietary habits of Americansduring the last 20 to 30 years. Some of thesechanges had a positive impact on health, butothers have resulted in greater consumption offoods likely to contain pathogens.

Preferences have changedThe demands of American consumers haveresulted in new food demographics.1• Consumption of red meat has decreased,while consumption of poultry has increased90%.• Cheese consumption has risen 120%.• Fifteen percent to 20% more fruit and25% to 30% more vegetables are being con-sumed.• “Health foods,” which typically have few

preservatives and a short shelf life, havebecome very popular.• The demand for exotic imported foods hasincreased. The US government has little con-trol over the production and handling ofimported foods. In addition, supermarket own-ers tend to leave these generally more expen-sive foods on the shelves for longer periods oftime in order to recoup their costs.

Lack of educationWhen home economics classes were morepopular in high schools, students were educat-ed about food preparation and safety issues.These classes are currently less often selected.In addition, dining out has become muchmore common. As a result, children havefewer opportunities to learn proper foodpreparation, care, and storage in their homes.

Handwashing is a frequently neglectedaspect of disease prevention. This may becomea significant issue at buffets and salad barswhere many people share the same servingutensils.

The threat of bioterrorismThe September 11 terrorist attacks were acall to reflect on other avenues for vulnera-bility. Our food supply is one such potentialavenue. Small attempts at contaminatingfood have already been made. Several hun-dred people became ill in 1984 when theBhagwan Shree Rajneesh cult contaminatedsalad bars in The Dalles, Oregon, withSalmonella typhimurium, to decrease voterturnout on election day.

Authorities recognize the serious threatthat could be posed by some foodbornepathogens. For example, 1 gram of botulinumtoxin, derived from the bacterium Clostridiumbotulinum, would be enough to kill 1 millionpeople.2 This toxin can be easily procured anddispersed. The resulting illness may be difficultto quickly recognize and treat.

In response to recent threats, the US Foodand Drug Administration (FDA) in January2002 issued guidelines to food establishmentsto prevent food tampering and terroristactions.3 The guidelines highlight securitymeasures in every facet of food preparation,from control of physical facilities to the hiringand monitoring of employees.

FOODBORNE ILLNESS TAEGE

80% offoodborneillnesses arefrom sourcesoutside thehome

Increased international travelIncreasing international travel affords theopportunity to bring potentially contaminat-ed foods home. Despite some degree of cus-toms inspection, many travelers return withcontaminated goods. Examples have includedcholera-carrying crabs from Latin Americaand Bahamian barracudas with ciguatoxin.

Large-scale food productionIn the last 100 years, mass production of foodhas been centralized to the point that one food-handling mistake can affect huge amounts offood. For example, a plant in Minnesota wastemporarily closed in 1994 after 80 peoplebecame ill from eating ice cream contaminatedwith Salmonella enteritidis.4 The ice cream hadbeen distributed in three states.

Corporate farming operations havereplaced the family farm as the source of mostof the nation’s meat and poultry. It is possiblethat a single pathogen may affect thousands oflaying hens, cattle, or pigs simultaneouslybecause of the proximity of the animals.

Widescale food distributionImported international foods are widely distrib-uted throughout the United Sates and othercountries. Mass-produced foods likewise reachdiverse geographic regions. Contaminatedalfalfa sprouts from the Netherlands were usedto prepare sandwiches for an airline; thesesandwiches were served on 219 flights, result-ing in illness to people arriving in 24 states,Washington DC, and four countries. The diffi-culty tracking such an outbreak is obvious.5

More demand for nonseasonal foodsNonseasonal demands by consumers haveincreased import pressures. Often these items areimported from areas that may have lax produc-tion standards, resulting in the potential for con-tamination by pathogens. Imported Mexicanwatermelons were found to have been washed incontaminated water prior to shipping, causingillness in American consumers.

The North American Free Trade Agree-ment has allowed the importation of lessexpensive products. To remain competitive,the US producers need to seek cost-cuttingmeasures, some of which have the potential tocompromise quality and safety of the products.

■ THE USUAL SUSPECTS

To determine the source of food poisoning, itis important to be familiar with foods associat-ed with common foodborne organisms (TABLE

2), incubation periods, duration of the result-ing illness, clinical symptoms, and the typicalpopulation involved in the outbreak.

Physicians who suspect foodborne illnessshould question patients carefully about theirrecent activities (TABLE 3).1 If foodborne illnessseems possible, specimens should be submittedfor laboratory analysis, and the local or statehealth department should be alerted.

It is economically and logistically impos-sible to investigate every suspected food-relat-


Common pathogensand associated foodsMost common

CampylobacterChickenUnpasteurized milkWater

SalmonellaAnimal foods, eggs, fruits, vegetables

ShigellaFruits and vegetables

Escherichia coli O157:H7Alfalfa sproutsHamburger, salamiUnpasteurized milk and juice

Less commonClostridium botulinum

Home-canned foodsCryptosporidia

WaterCyclospora

RaspberriesListeria monocytogenes

Deli meatsSoft cheeses, unpasteurized milkVegetables

Vibrio vulnificusShellfish

Yersinia enterocoliticaRaw porkUnpasteurized milkWater

T A B L E 2

On corporatefarms, a singlepathogen canaffectthousands ofanimals


ed illness. Most are not reported, the majorityare viral in origin, and those affected usuallyexperience a short illness with no conse-quences. Health care providers need to be vig-ilant for foodborne illness in the very youngand old, the immunocompromised, and inpregnant patients, as they often experiencethe most severe disease and serious outcomes.

Clinicians need to be alert for unusual ill-ness as a clue to food contamination; hemolyt-ic uremic syndrome as a sequela to E coliO157:H7, bullous cellulitis and sepsis fromVibrio vulnificus, or a flaccid descending paral-ysis suggestive of botulism (TABLE 4).

C botulinumTwelve to 72 hours after ingestion, botulismmanifests as symmetric descending flaccidparalysis with bulbar palsies (ie, diplopia,dysarthria, dysphonia, dysphagia). It can causenausea, vomiting, diarrhea, and cramps.

Differential diagnostic considerationsinclude tick-borne paralysis, myastheniagravis, the Miller Fisher variant of Guillain-Barré syndrome, and the Lambert-Eaton syn-drome. If botulism is suspected, physiciansshould perform blood assays for the toxin andsend stool, vomitus, gastric aspirate, or suspect-ed foods for analysis to state or federal facilities.

Laboratory confirmation is low; therefore,botulism requires a rapid clinical diagnosis.An antitoxin is available. However, it must beadministered quickly to be effective, and itonly prevents further paralysis rather than

reversing already existent paralysis. In addi-tion, serum sickness develops in 9% ofpatients who receive the antitoxin, and 2%experience anaphylaxis. Treatment is other-wise supportive.

CampylobacterChicken, unpasteurized milk, and untreatedwater are the most common sources ofCampylobacter. One to 7 days after ingestion,approximately two thirds of affected peoplehave fever, and about half have bloody diar-rhea. The duration of illness is usually only 1week in healthy people. Immunocompromisedor otherwise unhealthy people may benefitfrom erythromycin or a quinolone.

CryptosporidiaIn 1993, more than 400,000 people inMilwaukee became ill after drinking watercontaining cryptosporidia. Chlorine does notkill this organism; a special filter is required toprotect water supplies. After an incubation of2 to 10 days, symptoms including diarrhea,headache, cramping, nausea, vomiting, andlow-grade fever may last 1 or 2 weeks.Treatment is supportive. Spread by fecal con-tamination, this parasite can be transmittedfrom person to person in a fecal-oral manner.

CyclosporaCyclospora emerged as a food-related illnessafter its association with imported raspberries.It has also been found on lettuce, basil, andother foods after fecal contamination. Two to10 days after ingestion, it manifests as cramp-ing, bloating, flatulence, and nonbloody diar-rhea lasting for a few days to a month. Anacid-fast stain of a stool sample is required fordiagnosis. Treatment with trimethoprim-sulfa-methoxazole may assist in recovery, particular-ly in prolonged cases.

E coli O157:H7Hamburger, unpasteurized apple cider, milk,lettuce, and water have been associated withoutbreaks of E coli O157:H7.6 In 1993, fourchildren died and hundreds of people becameill after eating E coli-tainted hamburger fromJack-in-the-Box restaurants in the PacificNorthwest, which occurred because of inade-quate cooking. An estimated 20,000 cases

Questions to ask patients presentingwith potential foodborne illness

Have you recently eaten raw or undercooked eggs, meats,shellfish, or fish; unpasteurized milk or juice; home-canned foods;fresh produce; or soft cheeses?

Are family members or close contacts experiencingsimilar symptoms?

Have you recently visited a foreign country, farm, day care center,coastal area, or campground with untreated water?

Have you recently attended a picnic?

Have you had recent contact with pets or other animals?ADAPTED FROM CENTERS FOR DISEASE CONTROL AND PREVENTION. DIAGNOSIS

AND MANAGEMENT OF FOODBORNE ILLNESS. MMWR 2001; 50(RR02):1–69.

T A B L E 3


The USgovernmenthas limitedcontrol over thegrowing orhandling ofimported foods

occur annually, resulting in approximately250 deaths.

E coli O157:H7 has an incubation periodof 4 to 8 days and causes abdominal pain andbloody diarrhea, but not usually fever. The ill-ness is caused by a toxin produced from aShigella-derived gene.

Antibiotics appear to have no role in thetreatment, leaving supportive care as themainstay.

The hemolytic uremic syndrome that canfollow this illness usually occurs 5 to 10 daysafter the diarrhea has abated. Children aremost commonly afflicted.

ListeriaThis organism has been associated with delimeats, soft cheeses, and coleslaw. In 1999,Bosell Foods in Cleveland, Ohio, recalled 350pounds of sliced ham contaminated withListeria. That same month, the Oscar Mayercompany recalled 28,313 pounds of deli meatfor the same reason. Not only is Listeria cold-tolerant, it has also developed some degree ofheat tolerance.

After an incubation of 1 or 2 days, fever,gastrointestinal upset, and nonbloody diar-rhea develop. Pregnant women, newborns,and people with weakened immune systemsare most susceptible. Listeria, along with Vibriovulnificus, has the highest hospitalization andmortality rate of all food-related pathogens.Ampicillin appears to be the most effectiveantibiotic for listerial illness.

SalmonellaSalmonella species are commonly found incontaminated fruits, vegetables, eggs, and ani-mal foods. S enteritidis can be transmittedtransovarially from one generation to the nextthrough a poultry population. Despite a reduc-tion in recent years, there may be an evolvingtrend of resurgence of Salmonella cases associ-ated with animal foods.

Salmonellosis has an incubation period of1 to 2 days, usually lasts less than 10 days, andpresents as a gastroenteritis with vomiting anddiarrhea. No treatment is required in mostcases, but newborns, immunocompromisedpeople, people with inflammatory bowel dis-ease or hemoglobinopathy, and those withendovascular prosthetic devices may benefit

from antibiotic treatment with ampicillin,gentamicin, trimethoprim-sulfamethoxazole,or ciprofloxacin.

ShigellaMuch less common than Campylobacter andSalmonella, Shigella is associated with fecalcontamination of fruits, vegetables, and shell-fish. It has an incubation period of 2 to 4 daysand manifests as fever, abdominal cramping,and bloody diarrhea for 5 to 7 days.

Shigella is usually treated with third-genera-tion cephalosporins and quinolones. Multidrug-resistant species occur.

VibrioThis organism is often associated with rawseafood from the southern US seacoast. Thehighest risk is in late summer or early autumn,when warm waters encourage bacterial growth.V parahaemolyticus has the ability to tolerateand proliferate in a cold environment.

One to 4 days after ingestion, Vibrio maycause vomiting, diarrhea, and abdominal pain.In immunocompromised people—particularlyin those with underlying liver disease—V vul-nificus may manifest as a sepsis-like syndromeor bullous cellulitis.

Treatment consists of tetracycline or cef-triaxone.


Signs of serious foodborneillness that should lead tosubmission of laboratoryspecimensBloody diarrheaDiarrhea leading to dehydrationFeverNeurologic involvement (eg, paresthesias,motor weakness, cranial nerve palsies)Prolonged diarrhea (ie, three or moreunformed stools daily for several days)Severe abdominal painSudden onset of nausea, vomiting, diarrheaWeight loss

ADAPTED FROM CENTERS FOR DISEASE CONTROL ANDPREVENTION. DIAGNOSIS AND MANAGEMENT OF FOODBORNE

ILLNESS. MMWR 2001; 50(RR02):1–69.

T A B L E 4

E coli O157:H7causesabdominal painand bloodydiarrhea, butnot usuallyfever

■ REFERENCES1. Centers for Disease Control and Prevention. Diagnosis

and management of foodborne illness. MMWR 2001;50(RR02):1–69

2. Arnon SS, Schecter R, Inglesby TV, et al. Botulinumtoxin as a biological weapon: medical and publichealth management. Working Group on CivilianBiodefense. JAMA 2001; 285:1059–1070.

3. US Food and Drug Administration. Center for FoodSafety and Applied Nutrition. Guidance for industry:food producers, processors, transporters, and retailers.Food security preventive measures guidance. Jan 9,2002. http://www.cfsan.fda.gov/~dms/secguid.html.Accessed 1/22/02.

4. Centers for Disease Control and Prevention. Outbreakof Salmonella enteritidis associated with nationally dis-tributed ice cream products: Minnesota, South Dakota,and Wisconsin. MMWR 1994; 43(40):740–741.

5. Gruber AM. Meals in the skies: a safe benefit or amicrobiological risk? University of Helsinki.http://www.helsinki.fi/lehdet/uh/101b.htm. Accessed1/22/02.

6. US Food and Drug Administration. HACCP: a state-of-

the-art approach to food safety.http://www.cfsan.fda.gov/opacom/backgrounders/haccp.html. Accessed 1/22/02.

7. Centers for Disease Control and Prevention. What isFoodnet? http://www.cdc.gov/foodnet/what_is.htm.Accessed 1/22/02.

■ SUGGESTED READINGAmerican Medical Association. Diagnosis and management of

foodborne illnesses: a primer for physicians.http://www.ama-assn.org/foodborne. Accessed 1/22/02

Centers for Disease Control and Prevention.http://www.cdc.gov. Accessed 1/22/02.

Center for Food Safety and Applied Nutrition (US Food andDrug Administration). http://www.fda.gov/cfsan.Accessed 1/22/02.

Food Safety and Inspection Service, US Department ofAgriculture. http://www.usda.gov/fsis. Accessed 1/22/02.

ADDRESS: Alan J. Taege, MD, Department of InfectiousDiseases, The Cleveland Clinic Foundation, 9500 Euclid Avenue,Cleveland, OH 44195; e-mail [email protected].


Yersinia enterocoliticaIllness caused by this organism is rare in theUnited States and affects mostly young chil-dren. It is typically acquired by eating rawpork or drinking unpasteurized milk or water.An ethnic food, chitterlings, has been associ-ate with cases of yersiniosis.

Yersinia has an incubation period of 4 to 7days. Symptoms include fever, abdominalpain, and diarrhea that is often bloody. Right-sided abdominal pain and fever may be con-fused with appendicitis. Carditis, joint pain, orsepsis may occur. The illness usually resolveswithout antibiotic therapy, but severe illnessor complications may require the use of anti-biotics such as aminoglycosides, doxycycline,trimethoprim/sulfamethoxazole, or fluoro-quinolones.

■ EFFORTS TO ENSURE SAFETY

In addition to technical advances in foodpreparation, handling, and storage, strideshave been made to improve surveillance.

In 1995, the Centers for Disease Controland Prevention (CDC), the FDA, the USDepartment of Agriculture (USDA), and fivestates unveiled the Foodborne Diseases ActiveSurveillance Network (FoodNet at www.cdc.gov/foodnet/).7 FoodNet now includes moni-toring sites in eight states. The goal of this net-work is to survey, characterize, and respond tofoodborne illness in a timely fashion.

PulseNet is a nationwide computer net-work designed to track and link foodborne out-breaks by DNA fingerprinting with pulse-fieldgel electrophoresis, thereby rapidly identifyingclusters of similar cases. See www.cdc.gov/ncidod/dbmd/pulsenet/pulsenet.htm.

HACCPEstablished in 1996, the Hazard AnalysisCritical Control Point (HACCP) system6 isan effort to increase the safety of meat andpoultry processing. It is a preventive effort tar-geting the production industry in a preemp-tive fashion by establishing sanitation stan-dards and monitoring critical points in theproduction process.

IrradiationBy slowing cell division, irradiation of foodcan delay ripening and sprouting, eliminateinsect infestations, maintain food freshness,and attempt to sterilize the foods. In 1992, theFDA approved the use of irradiation in thepoultry industry. In 2000, it was put into effectthrough federal enactment to be used in grainsand fresh produce.

However, irradiation systems are expen-sive to install, and the public remains skepti-cal about irradiation. It is important to under-stand that ionizing irradiation is used and thatit is not radioactive. More public educationabout the safety of this method is necessarybefore it will be widely accepted.


Listeria andVibrio cantolerate andproliferate incoldenvironments

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The new American diet and the changing face of foodborne illness