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food poisoning
 Food poisoning in children
. Clinical manifestations range from mild gastroenteritis to life-threatening neurologic, hepatic, and renal syndromes.
Although foodborne illnesses attack patients in all age groups, young children, the elderly, and immunocompromised hosts are at highest risk for serious consequences from these diseases.
Factors leading to the emergence of foodborne diseases and a brief discussion of common and emerging causes of foodborne illness in children are reviewed here. The specific agents producing these illnesses are discussed in more detail separately.
 DEFINITIONS — The CDC defines a foodborne-disease outbreak as any cluster of two or more individuals who develop similar symptoms following the ingestion of a common food. Of 2,751 outbreaks affecting more than 86,000 people investigated between 1993 and 1997, 68 percent had an undetermined etiology Of the remaining 32 percent of outbreaks, 75 percent were caused by bacteria and 17, 6, and 2 percent by chemical agents, viruses, and parasites, respectively.
When the agent of a foodborne outbreak cannot be determined, incubation times are used as clues (ie, <1 hour = probable chemical ingestion; 1 to 7 hours = probable Staphylococcus aureus or Bacillus cereus toxin mediated; 8 to 14 hours = other agents, especially bacteria; 15 hours = other agents, especially viruses). The CDC maintains a collaborative surveillance program for foodborne diseases but recognizes that this system results in an underestimate of the incidence of these illnesses, especially those caused by viruses. Criteria for confirming the etiology of an outbreak have been published
 CONTRIBUTING FACTORS — Many factors contribute to the emergence of foodborne disease in the United States and around the world. They include changes in human behavior and demographics, advances in industry and technology, lack of adequate public heath infrastructure, and changing antimicrobial susceptibility patterns of the organisms
Commercially or institutionally prepared food causes 79 percent of cases of food poisoning. The increasing number of meals eaten either away from home or brought to the home for immediate consumption after being purchased elsewhere has created greater demand for food from catering services, restaurants, and institutional kitchens. The burgeoning market for quick, convenient, and inexpensive food renders careful handling and storage of foods mandatory
 Improper food storage — Holding and food storage at improper temperatures was the most common contributor to foodborne disease from 1983 through 1992, with CDC estimates reaching 97 percent It includes leaving prepared food at temperatures that allow bacteria to grow, improperly heating or reheating food, and allowing cross contamination of food. Cross contamination of food can occur either through direct contact or following contact with contaminated food preparation surfaces
 Food handlers — The personal hygiene practices of food handlers was the second most common cause of foodborne illness
Fecal-oral transmission can result from poor hygiene, particularly failure to wash hands after using bathroom facilities.
 Widespread distribution of foods — Small farms, factories, and dairies are being replaced with large factories supplying millions of individuals in far reaching parts of the world, magnifying the impact of a single contamination ]. Small outbreaks may be seemingly unrelated, and tracing the source of contamination becomes a greater challenge. All of these factors add to the opportunity for outbreaks of foodborne illness that may affect hundreds to thousands of people.
 COMMON AND EMERGING MICROBIAL AGENTS — A wide variety of microorganisms can cause food poisoning. Salmonella sp. produce the majority of outbreaks of foodborne disease when an etiology can be established. However, Escherichia coli have become frequent foodborne pathogens.
 Salmonella — Salmonella is the number one cause of foodborne illness in the United States and is responsible for more deaths than any other foodborne pathogen The spectrum of clinical illness ranges from occult bacteremia to typhoid fever and acute gastroenteritis to pseudomembranous colitis
Antimicrobial resistance among Salmonella isolates has become a major problem, partially because of the extensive use of antimicrobial drugs in livestock
Multidrug-resistant salmonella typhimurium DT104 has emerged as a cause of salmonellosis in Europe and the United States. In one outbreak, Mexican-style soft cheese made with unpasteurized milk was an important vehicle for transmission in children [
While occult nontyphoidal salmonella bacteremia in children accounts for <0.2 percent of fevers (39.0ºC) in outpatients 3 to 36 months of age, severe complications can result if this condition is unrecognized and untreated. Persistent bacteremia, osteomyelitis, meningitis, sepsis, and death have been reported. Sequelae are much more common in infants younger than three months or immunocompromised older children [
 Campylobacter — C. jejuni and C. coli most commonly cause diarrhea in humans, although 15 species of Campylobacter have been identified Campylobacter sp. account for less than 1 percent of foodborne outbreaks in the United Statesbut have been estimated to be responsible for more than 2,000,000 cases of diarrhea
. The rate of isolation in the FoodNet surveillance sites in the United States in 1999 was 17.3 per 100,000 population compared to 14.8 and 5.0 per 100,000 for Salmonella and Shigella, respectively
The organism is transmitted primarily through contaminated food. Risk factors for disease include handling raw chicken, eating raw or undercooked chicken, having contact with cats, and consuming untreated water, raw milk, or eggs
Campylobacter is isolated most commonly in the first year of life, reaching rates of 15 per 100,000
The male to female ratio is 1.3 to 1. Campylobacter causes disease ranging from asymptomatic secretion to frank dysentery. It is unique in that constitutional symptoms such as coryza, headache, and general malaise may accompany the diarrhea, which can persist for two weeks
 Escherichia coli — Enterotoxigenic and enterohemorrhagic are the most common E. coli strains to produce foodborne illness worldwide. E. coli is a prominent constituent of normal stool flora, and E. coli O157:H7 is the only pathogenic stool strain for which testing is performed in clinical laboratories.
 Enterohemorrhagic E. coli — Enterohemorrhagic E. coli (EHEC) was first recognized as a human pathogen in 1982, after an outbreak of severe bloody diarrhea in individuals who had consumed hamburgers from a fast food chain
. EHEC are Shiga toxin-producing strains
; E. coli O157:H7 is the most prevalent strain in the United States. However, this prevalence may be secondary to the fact that only this strain can be identified in most clinical laboratories. Infection is characterized by bloody stool with little or no fever.
Eighty-four outbreaks with a total of 2,772 cases were reported in the United States between 1993 and 1997 . Because of difficulties in the detection of the organism since E. coli is a prominent constituent of normal stool flora, the number of cases probably is an underestimation. In many cases, subclinical disease and lack of appropriate testing in sorbitol-MacConkey agar leads to gross underreporting
Improperly cooked beef and unpasteurized milk traditionally have been the source of EHEC ingestion. Healthy cattle, dogs, deer, sheep, horses, and goats serve as reservoirs. However, E. coli O157:H7 can be transmitted by food or water or from person to person. The organism has been isolated from manure as well as water troughs. Recent outbreaks have been traced back to tainted fruits and vegetables. Radish sprouts, lettuce, unpasteurized apple juice and cider, and alfalfa sprouts also have been implicated.
In the pediatric population, young children carry the organism longer than do older children or adults. EHEC strains have been linked with the development of hemolytic uremic syndrome (HUS), the leading cause of acute renal failure in children.
Non-0157:H7 strains also have been linked. HUS complicates 6 to 9 percent of EHEC infections and usually begins five to 10 days after the onset of diarrhea . HUS characterized by microangiopathic hemolytic anemia, thrombocytopenia, and renal failure is almost exclusive to pediatrics
A retrospective study identified in multivariate analyses use of antimotility agents within the first three days of the development of diarrhea and vomiting for patients under the age of five years as risk factors for HUS [. Risk factors identified in other reports (eg, bloody diarrhea, degree of fever, elevated leukocyte count, and female sex) were not significant in this study. A prospective study of 71 children younger than 10 years of age with E. coli O157:H7 isolated from stool found that those receiving antibiotics were more likely to develop HUS (5 of 9 [56 percent] versus 5 of 62 [8 percent], p = 0.002) Early administration of antibiotics to these children may promote the development of HUS by enhancing release of Shiga toxin as the bacteria are killed.
 Enterotoxigenic E. coli — Enterotoxigenic E. coli (ETEC) is one of the most common causes of dehydrating diarrhea in children younger than two years of age in the developing world
. These strains also frequently produce diarrhea in travelers to tropical regions as a result of being exposed to contaminated food and water. ETEC, in contrast to EHEC, usually induces watery diarrhea caused by the production of secretory toxins
. The duration of illness generally is 24 to 72 hours, and the appropriate treatment is oral rehydration therapy unless the diarrhea is severe.
 Shigella — Shigella causes classic bacillary dysentery. Shigella dysenteriae 1 produces Shiga toxin, but it is rarely found in the United States. Shigella, which can survive in the acidic pH of the stomach, can cause disease after ingestion of as few as 100 organisms. Shigellosis can be acquired through fecal-oral contact or through ingestion of contaminated food or water Consumption of cold salads such as potato or macaroni salads has been implicated in several common source outbreaks. Whereas Shigella account for fewer than two percent of outbreaks or hospitalizations for foodborne illness in the United States, shigellosis is a major cause of diarrhea in the developing world .
Shigellosis frequently is implicated in outbreaks in daycare centers and nursing homes. Infections occur most frequently in children between the ages of one and four years old Seizures can occur in Shigella infection in children. In a prospective study from Bangladesh, 41 of 792 patients (5 percent) younger than 15 years of age hospitalized with shigellosis had a documented seizure and 73 patients were unconscious; no patient older than 5 years of age developed seizures
Risk factors for seizures, including fever, dehydration, hypoglycemia, hyponatremia or meningitis, were present in 92 percent of those with definite seizures.
 Staphylococcus aureus — Staphylococcal food poisoning is another common foodborne illness, accounting for 43 outbreaks and 1,555 cases between 1993 and 1997 in the United States . The illness is caused by toxins elaborated by the organism. Symptoms may begin as early as 30 minutes or as late as eight hours after eating contaminated food; the illness is characterized by the sudden onset of nausea, vomiting, and diarrhea. The incubation period and the severity of disease depend upon individual host factors and the amount of the inoculum.
The disease usually is self limited, but deaths have been reported. Foods containing staphylococcal enterotoxin usually look and taste normal. Cooking does not destroy either the organism or the toxin. In fact, both the organism and its toxin proliferate in temperatures between 68 ºF and 99 ºF. Precooked, prepackaged meats with high salt contents are ideal vehicles for Staphylococci. Staphylococcal disease is reported most often as a result of ham ingestion
 Cyclospora — Cyclospora cayetanensis is one of the emerging pathogens inducing diarrhea that was not even named until 1993 . It gained increased attention as a foodborne pathogen after large outbreaks of illness in the United States in 1996 and 1997 linked to raspberry farms in Guatemala
. The exact source for contamination of the raspberries is not known, and rinsing does not prevent disease. As a consequence, importation of raspberries into the United States was banned
In a study from Guatemala, cyclospora infection was found to be relatively uncommon among children younger than 18 months of age
. Infection was most common in children between the ages of 1.5 and 9 years; 19 percent of children with gastroenteritis in this age group had cyclospora identified in stool. Disease was more severe in children younger than five years of age, who were more likely to have fever and tended to have diarrhea for up to 15 days, a higher median number of stools per day, and a higher probability of mucoid stools. Soil contact was a strong risk factor for disease in those under the age of two
 Cryptosporidiosis — The parasite Cryptosporidium parvum is a prominent cause of waterborne diarrheal illness
. The largest outbreak of waterborne disease occurred in 1993 when 403,000 residents of Milwaukee developed gastrointestinal symptoms after their drinking water became contaminated
Outbreaks associated with apple cider contaminated by Cryptosporidia oocysts also have been reported
Foodborne outbreaks are uncommon. However, 88 students and four university employees became ill in one outbreak associated with consumption of food in a university cafeteria
. Genotyping linked a C. parvum genotype 1 isolate to an infected food handler who prepared raw produce.
Watery diarrhea, nausea, vomiting, and fever are common symptoms with cryptosporidiosis. The illness usually is self-limited in immunocompetent hosts, but it can cause severe, protracted diarrhea in immunocompromised hosts.
 Other pathogens — Numerous other pathogens are associated with foodborne illness.
 Clostridium perfringens — Acute self-limiting gastroenteritis caused by contaminated food products often is associated with Clostridium perfringens. Primary contamination of meat with spores is common when the food is allowed to stand at a temperature between 80ºF and 120ºF; temperatures of cooked meat must exceed 210ºF to ensure that spores are killed. Symptoms are caused by the production of enterotoxins by the organism once it resides in the gut. Clinical manifestations typically include crampy abdominal pain and watery diarrhea without fever.
Clostridium perfringens type C produces a beta toxin that can cause enteritis necroticans (pigbel), a hemorrhagic necrosis of the jejunum. It is a health problem in developing countries, but is rarely seen in developed countries. Factors associated with enteritis necroticans include decreased GI acidity and motility, as well as chronic disease or malnutrition. A case of pigbel in a 12-year-old diabetic associated with the consumption of pig intestines (chitterlings) was reported
The simultaneous ingestion of sweet potatoes, which contain trypsin inhibitors preventing the intestinal degradation of the toxin, can be a potentiating factor.
 Botulism — Botulism is a rare but potentially life-threatening neuroparalytic syndrome resulting from the action of a neurotoxin elaborated by the spore-forming microorganism Clostridium botulinum. The spores are heat resistant and survive food preservation and preparation. Botulism in children occurs in two ways:
• Foodborne botulism — Ingestion of food contaminated by preformed botulinum toxin.
• Infant botulism — Ingestion of clostridial spores that then colonize the gastrointestinal tract of the host and release toxin produced in vivo.
Infantile botulism is the most frequent form of the disease, with a mean of 71 cases annually in the United States and a mortality rate up to five percent ]. Unlike other foodborne diseases, infantile botulism does not occur in outbreaks ; in 85 percent of cases, the source of ingestion is unknown. Honey has been directly linked to infant botulism. Corn syrup, although implicated, has never been directly linked with botulism. Currently, the recommendation is that honey not be given to infants under one year of age. Breastfed infants older than two months of age have an increased risk for being hospitalized with botulism. However, because breastfed infants typically present at a later age than do formula-fed infants, these children may have a slower progression of disease Although initially thought to be involved in some cases of sudden infant death syndrome (SIDS), a ten-year prospective study failed to show an association
 Listeria monocytogenes — Listeria monocytogenes infection is an uncommon cause of foodborne illness, but the outcome of infection can be serious, especially in the very young and elderly. It accounts for less than 0.1 percent of foodborne illness but 28 percent of the estimated number of deaths [ 1]. Infection with L. monocytogenes typically produces a febrile illness, sepsis, or central nervous system infection, principally in immunocompromised patients. Pregnant women also can be affected and should avoid unpasteurized dairy products. It is now recognized that L. monocytogenes can cause febrile gastroenteritis in immunocompetent individuals.
In one outbreak at primary schools, 1566 of 2189 people (72 percent) had symptoms of gastroenteritis traced to the consumption of a corn salad in the cafeterias The median time from meal consumption to onset of symptoms was 24 hours.
 Yersinia enterocolitica — Yersinia enterocolitica can cause both outbreaks and sporadic cases of foodborne gastroenteritis. The most common vehicle is undercooked pork products. One outbreak involved children in Vermont and was linked to consumption of milk from one dairy . A dairy pig from the farm had the organism isolated from feces, and pigs were the presumed source of contamination. Y. enterocolitica classically can induce a clinical picture that mimics appendicitis; other diarrheal pathogens such as Campylobacter also can cause this condition.
 Brucella — Brucellosis is uncommon in the United States and most industrialized countries, but worldwide it is a significant cause of disease in domesticated animals; humans serve an incidental hosts. Most reported cases in the United States are from California or Texas
Brucellosis is acquired from ingestion of contaminated food such as raw milk, cheeses made from unpasteurized milk (often imported), or raw meat. This foodborne illness does not typically produce diarrhea; brucellosis is characterized by fever and a protean variety of other manifestations.
 SEAFOOD INGESTIONS — Seafood is a frequent source of foodborne illness. Such illness can arise from consumption of fish, especially shellfish, contaminated by viruses such as Norwalk or Hepatitis A; ingestion of a toxin such as scombroid found in certain finfish; or poisoning from fish or shellfish contaminated with toxins from algae and other marine lifeforms such as dinoflagellates that produce toxins causing ciguatera fish poisoning and paralytic shellfish poisoning or G. breve which causes red tide
 Human calicivirus and other viruses — Viruses such as the caliciviruses, formerly known as Norwalk viruses, probably account for a sizeable proportion of foodborne illness, perhaps as high as 67 percent by some estimates
. The application of new molecular diagnostic methods suggests that the calicivirus family of viruses is the most common cause of acute gastroenteritis outbreaks in the United States
. Approximately 20 to 40 percent of illnesses associated with these viruses are assumed to be foodborne
Calicivirus virus was responsible for 42 percent of outbreaks of shellfish-associated illness in which a pathogen was identified
Viruses can be transmitted from contaminated food or water, and food handlers often are suspected as the source of foodborne outbreaks. Genomic characterization of viruses has allowed the development of reverse transcriptase polymerase chain reaction assays that can be used in the testing of clinical stool samples. The assays were used in an outbreak of gastroenteritis to trace the source to a foodhandler whose infant was sick with the infection
The incubation period generally is 24 to 48 hours, with a range from 18 to 72 hours. Clinical manifestations include nausea, vomiting, abdominal pain and diarrhea. Disease manifestations generally last 48 to 72 hours with a full and rapid recovery.
 Vibrio species — The vibrio species, which include V. vulnificus, V. parahemolyticus, and V. cholerae, are major causes of seafood- and fish-acquired food poisoning.
• V. cholera 01 and 0139 cause pandemic and epidemic cholera, a disease characterized by voluminous watery diarrhea
. An isolate indistinguishable from the epidemic Latin American strain was identified in oysters from Mobile Bay, Alabama in 1991 and 1992, but no clinical cases of cholera resulted .
• V. vulnificus most frequently is implicated in outbreaks from the United States. V. vulnificus infection can be acquired by eating raw or undercooked shellfish, as well as directly by contaminating open wounds while swimming or cleaning shellfish [
. V. vulnificus infection usually results in cellulitis, wound infection, or septicemia.
• V. parahaemolyticus infection typically produces a diarrheal illness. Outbreaks of V. parahaemolyticus infection have been associated with raw oysters and clams from the northeastern, as well as Pacific northwestern, coasts of the United States
 Scombroid — Scombroid fish poisoning occurs after the ingestion of finfish, notably tuna, mahi-mahi, and bluefish
. The illness is caused by histamine and other products from bacteria that propagate on the fish in warm water or when they are inadequately refrigerated. The CDC reported 69 outbreaks of scombroid from 1993 to 1997 resulting in 297 cases One Pennsylvania outbreak was associated with consumption of a tuna and spinach salad in a restaurant
. Flushing, nausea, sweating, diarrhea, and headache occurred from five minutes to two hours after ingestion and resolved within hours.
Histamine levels were found to be elevated in the fish, which had been caught in the Gulf of Mexico by a long-line method that kept the fish suspended for 12 to 24 hours on the line in the relatively warm water prior to harvesting
Prompt harvesting and refrigeration until the fish is cooked are the best means of preventing this poisoning.
 Ciguatera fish poisoning — Ciguatera poisoning is the most common form of seafood poisoning and occurs after ingestion of certain species of local reef fish, which vary from location to location. Between 1993 and 1997, 60 outbreaks resulting in 205 cases were reported to the CDC ; several recent outbreaks have been described in Australia
The fish appear and taste normal; cooking does not destroy the toxin and, thus, avoidance of these fish is the only means of prevention. Most resort areas in the Caribbean and Hawaii do not serve implicated species of local reef fish.
Patients develop gastrointestinal symptoms generally within three to six hours of eating the fish. Neurologic symptoms, including circumoral paresthesias and weakness in the lower extremities, can occur later; occasionally a reversal of hot-cold taste sensation is reported
. Neurologic symptoms often persist for several weeks, but in some cases can last for years.
 MUSHROOM INGESTIONS — Collecting and eating wild mushrooms has increased in popularity. Many people forage for mushrooms with great enthusiasm, but few appreciate the difficulty in differentiating poisonous from edible mushrooms. Although mushroom poisoning is rare, it can cause significant morbidity and mortality
 Amanita phalloides — Virtually all of the deaths attributed to mushroom poisoning in the United States are caused by the ingestion of Amanita phalloides. The principal toxin, alpha amanitina, is a low-molecular-weight compound that acts by selective inhibition of RNA polymerase II
. It binds to serum albumin and may undergo enterohepatic recirculation.
Poisoning typically is manifested as acute gastroenteritis, with colicky abdominal pain, nausea, vomiting, and diarrhea occurring 10 to 14 hours after ingestion. Although apparent recovery usually occurs after 12 to 34 hours, it can be followed by the onset of acute renal failure and/or fulminant hepatic necrosis, with a mortality rate of 20 to 30 percent. Risk factors for mortality included age less than seven years, short latency between ingestion and onset of symptoms, and severe coagulopathy
Patients who are suspected to have ingested poisonous mushrooms should undergo gastric lavage and be given activated charcoal, whether or not they are symptomatic
Because Amanita may indergo enterohepatic recirculation, activated charcoal should be given every four hours for 72 hours when Amatoxin-containing mushroom is suspected
. Fluid replacement and electrolyte disturbances or coagulopathy should be corrected. Hemodialysis and hemoperfusion may be effective in removing the toxin if initiated within 24 hours of ingestion
The only definitive treatment may be liver transplantation once fulminant liver failure occurs
Mushroom poisoning should be reported to the local poison control center. The poison control center may offer clues to identification and have the name and number of a mycologist who can aid in treatment. Amatoxins are found in blood and urine
. Radioimmunoassay of amatoxins is available through a few reference laboratories
 Gyromitra — Gyromitra esculenta is one of the false morel mushrooms. It contains a thermolabile toxin, Gyromitin, which typically produces symptoms at five to 12 hours after ingestion of Gyromitra mushrooms. These patients may have nausea, vomiting, watery diarrhea, and abdominal pain. Gyromitra mushroom poisoning also affects the nervous system. Patients may experience fatigue, severe headache, vertigo, muscle cramps, faintness, dizziness, loss of coordination, and seizures
In addition to the charcoal, gastric lavage, and other supportive measures listed above, pyridoxine (5 g IV for adults and 25 mg/kg for children) should be administered in patients who have seizures. Gyromitin is metabolized into monomethylhydrazine, which inhibits the formation of GABA centrally and induces a state of pyridoxine deficiency. However, repeated doses have been known to cause peripheral neuropathy and should be repeated only in patients with prolonged or recurrent seizures or patients in coma
 PREVENTION THROUGH FOOD IRRADIATION — Irradiation is extremely effective in reducing pathogens associated with food products. Irradiation of flour, fruits, vegetables, meats, and spices has been approved by the United States Food and Drug Administration (FDA). Meat, pork, and poultry also have been approved by the USDA for irradiation up to 3.0 Grays. This dose of irradiation destroys S. aureus, Salmonella, Shigella, Campylobacter, and Cyclospora. However, E. coli O157:H7 requires much higher doses. Food irradiation at approved levels causes no significant change in the amino acid or fatty acid content of food. Reduction in thiamine is minimal
Irradiating food prolongs shelf life, delays ripening time for fruit, and destroys the bacteria that cause foodborne illnesses. Many countries already use irradiation widely. In the United States, many foods are irradiated, and astronauts go into space with food that has been irradiated to the point of sterilization
 PREVENTION THROUGH SAFE FOOD HANDLING — Proper food storage and preparation also can reduce the risk of food poisoning. The USDA has identified several "critical control points" in food safety:
• Purchase
• Home storage
• Preparation
• Cooking
• Serving
• Storage of leftovers.
• Avoid contact between cooked and uncooked foods
• Refrigerate foods promptly after purchase, preparation, or eating
• Wash hands and preparation surfaces after handling raw meats, poultry, fish, and eggs before contact with other items
• Cook meats, poultry, fish, and eggs thoroughly
• Maintain proper refigerator and freezer temperatures and never leave cooked foods at room temperature for more than two hours (shorter if ambient temperatures are higher).
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