Microbiological Safety of Foods

Authored by: Kumar Venkitanarayanan , Anup Kollanoor-Johny , Michael P. Doyle

Handbook of Nutrition and Food

Print publication date:  July  2013
Online publication date:  April  2016

Print ISBN: 9781466505711
eBook ISBN: 9781466505728
Adobe ISBN:

10.1201/b15294-5

 

Abstract

The microbiological safety of foods is a major concern to consumers and to the food industry. Despite considerable progress made in technology, consumer education, and regulations, food safety continues to be a major challenge to our public health and economy. During the last decade, food safety received considerable attention due to the emergence of several new foodborne pathogens and the involvement of foods that traditionally have been considered safe, in many foodborne disease outbreaks. Further, industrialization of the food supply through mass production, distribution, increased globalization, and consumer demands for preservative-free, convenience foods and ready-to-eat meals highlights the significance of the microbial safety of foods. Recently, the U.S. Centers for Disease Control and Prevention (CDC) reported an estimated 48 million cases of foodborne illnesses, with 130,000 hospitalizations and 3000 deaths in the United States annually. 1 Besides the public health impact, outbreaks of food-borne illness impose major economic losses to both the food industry and society. The annual estimated cost of foodborne illnesses accounts for approximately $152 billion with nearly $32 billion attributed to contaminated produce. 2 , 3 Moreover, isolation of antibiotic-resistant foodborne bacteria as etiologic agents implicated in outbreaks has been increasingly reported. According to the Center for Science in the Public Interest (CSPI), 35 foodborne outbreaks during the last three decades were caused by bacteria resistant to at least one antibiotic. 4 The various microbiological hazards associated with foods can be classified broadly as bacterial, viral, fungal, and parasitic.

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Microbiological Safety of Foods

Introduction

The microbiological safety of foods is a major concern to consumers and to the food industry. Despite considerable progress made in technology, consumer education, and regulations, food safety continues to be a major challenge to our public health and economy. During the last decade, food safety received considerable attention due to the emergence of several new foodborne pathogens and the involvement of foods that traditionally have been considered safe, in many foodborne disease outbreaks. Further, industrialization of the food supply through mass production, distribution, increased globalization, and consumer demands for preservative-free, convenience foods and ready-to-eat meals highlights the significance of the microbial safety of foods. Recently, the U.S. Centers for Disease Control and Prevention (CDC) reported an estimated 48 million cases of foodborne illnesses, with 130,000 hospitalizations and 3000 deaths in the United States annually. 1 Besides the public health impact, outbreaks of food-borne illness impose major economic losses to both the food industry and society. The annual estimated cost of foodborne illnesses accounts for approximately $152 billion with nearly $32 billion attributed to contaminated produce. 2 , 3 Moreover, isolation of antibiotic-resistant foodborne bacteria as etiologic agents implicated in outbreaks has been increasingly reported. According to the Center for Science in the Public Interest (CSPI), 35 foodborne outbreaks during the last three decades were caused by bacteria resistant to at least one antibiotic. 4 The various microbiological hazards associated with foods can be classified broadly as bacterial, viral, fungal, and parasitic.

Bacterial Foodborne Pathogens

Bacteria are major agents causing microbial foodborne illnesses and account for an estimated 4.8 million foodborne illnesses annually in the United States (Table 3.1). 5 Bacterial foodborne diseases can be classified into foodborne infections and foodborne intoxications. Foodborne infection is a condition caused by the ingestion of viable cells of a pathogen. Foodborne intoxication is a condition in which pre-formed toxins in the food produced by a toxigenic pathogen act as the underlying cause of disease. 6 The various bacterial pathogens associated with foodborne diseases are discussed in the following.

Shiga Toxin Escherichia coli (STEC)

There are six different pathotypes of E. coli, including enteropathogenic E. coli (EPEC), enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), diffusely adhering E. coli (DAEC), enteroaggregative E. coli (EAEC), and enterohemorrhagic E. coli (EHEC), 7 that have been associated with gastrointestinal illness. Among these, EHEC, which produce Shiga toxins (verotoxins), are most frequently implicated in foodborne disease outbreaks and generally classified into O157 and non-O157 serogroups. EHEC O157:H7 emerged in 1982 as a foodborne pathogen and is now recognized as a major public health concern in the United States. 8 A recent report indicated that E. coli O157:H7 causes an estimated 63,000 cases annually in the United States with 2,138 hospitalizations and 20 deaths, accounting for a loss of $607 million. 3 Although approximately 50% of the reported outbreaks in the United States have been associated with consumption of undercooked beef burgers, a wide variety of other foods, including raw milk, roast beef, venison jerky, salami, yogurt, lettuce, unpasteurized apple juice, cantaloupe, alfalfa sprouts, and coleslaw, have been implicated as vehicles of E. coli O157:H7 infection. 9 , 10 Fresh fruits and vegetables are increasingly being identified as vehicles of EHEC infections around the world. 7 , 11 In the United States, iceberg lettuce and spinach have been implicated in several outbreaks. 7 In addition, outbreaks involving person-to-person and waterborne transmission have been reported. 9 Cattle have been implicated as one of the principal reservoirs of E. coli O157:H7. 12 15 In adult cattle, E. coli O157:H7 primarily colonizes the terminal rectum, particularly an anatomical area within the terminal rectum referred to as the rectoanal junction. 16 E. coli O157:H7 can survive in bovine feces for many months, 17 hence potentially contaminating cattle, food, water, and the environment. Although surveys conducted in the late eighties and nineties estimated a low fecal prevalence of E. coli O157:H7 in cattle, 15 , 18 , 19 later studies using improved enrichment and isolation procedures have showed that the overall prevalence of E. coli O157:H7 in cattle may be significantly higher than originally estimated. 20 23 A survey conducted by Elder et al. 20 indicated that of the 29 feedlots of cattle presented for slaughter in the Midwestern United States, 72% had at least one E. coli O157-positive fecal sample and 38% had positive hide samples. The study revealed an overall E. coli O157 prevalence of 28% (91 out of 327) in feces and 11% (38 out of 355) in hide. Subsequent research by others estimated that up to 30% of cattle are asymptomatic carriers of EHEC. 24 , 25 Recently, Woerner et al. 26 observed a relationship between fecal incidence rate (FIR) in cattle and hide contamination by EHEC. When FIR is more than 20%, hides positive for EHEC were about 26%, whereas when FIR was lower than 20%, only 5% of the cattle hides were contaminated. Studies by other researchers revealed that the prevalence of E. coli O157 in feedlots in the United States can reach 63%, particularly during the summer, under muddy conditions, or with feeding of barley. 27 , 28 However, other investigations revealed that EHEC shedding could be as high as 80% during the summer to as low as 5%–10% during winter, 29 , 30 a factor that could be attributed to the greater occurrence of foodborne outbreaks caused by EHEC during the summer. 31 These results are of particular concern because high fecal shedding and the presence of E. coli O157:H7 on hides would lead to contamination of foods of bovine origin with the pathogen during slaughtering and processing operations. 32 In addition, many E. coli O157:H7 outbreaks involving nonbovine foods, such as fruits and vegetables, are linked to cross contamination of the implicated food with contaminated bovine manure. 33 36 Direct zoonotic and environmental transmission is a newly recognized mode of E. coli O157:H7 spread to humans. Contact with farming environment, including recreational or occupational visits, has been associated with E. coli O157:H7 infections in humans. 37 , 38 Since reduced fecal shedding of E. coli O157:H7 by cattle would potentially decrease foodborne outbreaks of E. coli O157:H7, a variety of approaches for decreasing the gastrointestinal carriage of E. coli O157:H7 in cattle have been investigated. These approaches have been focused on three important factors, namely, reduction of exposure of cattle to the pathogen, applying the pathogen exclusion principle, and implementing a direct pathogen reduction strategy. 39 E. coli O157:H7 can be largely controlled if sufficient hygienic measures are undertaken on farms, including providing good-quality water, feed, and housing for cattle; isolating preweaned calves from the adult herd, because calves can shed the pathogen in large numbers; and excluding non-bovine pathogen sources such as dogs, raccoons, opossums, and wild birds from farms, because they may potentially introduce E. coli O157:H7 to farms. 37 , 39 42 Avoidance of feed ingredients known to increase E. coli O157:H7 shedding such as barley, corn silage, and beet pulp and use of probiotics (e.g., Bovamine® that contains a mix of Lactobacillus acidophilus and Propionibacterium freudenreichii) and prebiotics are other potential strategies to exclude or reduce pathogen colonization in cattle. 39 , 43 Direct E. coli O157:H7 reduction strategies such as feeding of antimicrobial compounds, for example, sodium chlorate, 44 ionophores, neomycin, and bacteriophages, have been investigated. A recent intervention approach has emphasized vaccination of cattle against E. coli O157:H7 colonization, targeting intimin 45 of the type III secretion system (Bioniche®), lipopolysaccha-ride (LPS), and siderophore receptors 46 48 (Epitopix®) in the bacterium. In addition, a variety of postharvest interventions against E. coli O157:H7 have been examined, including thermal processing, high-pressure treatment, ultrasound, ionizing radiation, ozone treatment, ultraviolet light, radio waves, chemical antimicrobials, naturally occurring antimicrobial chemicals in plants, electrochemically activated water, and bacteriophages. 7

Table 3.1   Bacterial Foodborne Pathogens

Microorganism

Biochemical and Growth Characteristics

Sources/Reservoirs

Examples of Vehicles

Estimated No. of Foodborne Cases Annually in the United States 2 , 3

Incubation Period, Symptoms, and Duration

Detection Methods

Control/Prevention

E. coli O157:H7

Gram negative, facultative anaerobe, nonspore-forming, optimum growth at 37°C-40°C, inability to grow at ≥44.5°C in the presence of selective agents, inability to ferment sorbitol within 24 h, does not produce glucuronidase, acid tolerance

Cattle, humans

Raw or undercooked beef, unpasteurized milk and apple juice, lettuce, alfalfa sprouts, water

63,153

3–9 days

Severe abdominal cramps, watery diarrhea that can become bloody, absence of fever, kidney failure, seizures, coma

Duration is days to weeks

Cultural methods followed by confirmatory biochemical tests 374 , 375

Latex agglutination assay 376 , 377

ELISA 378 - 380

PCR381-384

Immunomagnetic separation 384 biosensors 385 , 386

Fourier transform infrared (FT-IR)

Spectroscopy and chemometrics 387

Bacteriophage-based assay 388

DNA microarray 389

Adequate cooking of beef, pasteurization of milk and apple juice, use of potable water for drinking, avoid eating raw alfalfa and vegetable sprouts, good personal hygiene

Salmonella spp. (nontyphoid)

Gram negative, facultative anaerobe, oxidase negative, catalase positive, nonspore-forming, growth at 5°C-47°C, optimum growth at 37°C, metabolize nutrients by respiratory and fermentative pathways

Cattle, swine, poultry, humans

Raw or undercooked meat, poultry, eggs, and milk, untreated water

1,027,561

6-72 h up to 4 days Abdominal cramps, diarrhea, fever, chills, headache, and vomiting Duration is few days to 1 week, occasionally up to 3 weeks

Cultural methods followed by confirmatory biochemical tests 390 - 392

Latex agglutination assay 393

ELISA 394

Immunoassay 395

PCR 396 - 399

Adequate cooking of food, avoid cross contamination of raw foods of animal origin with cooked or ready-to-eat foods, avoid eating raw or undercooked foods of animal origin, use of potable water, good personal hygiene

Salmonella typhi

Gram negative, facultative anaerobe, ferment D-xylose

Humans

Raw milk, shellfish, raw salads, undercooked foods

1,821

7-28 days

Remittent fever with stepwise increments over a period of days, high temperature of 103°F-104°F, abdominal pain, diarrhea, and headache

Duration is up to 3 weeks

Biochemical tests 400

Latex test 401

ELISA 402

PCR 403 - 405

Quantum dot assay 406

ELISA 407

Good personal hygiene and food handling practices, proper sewage systems, effective surveillance of known carriers

Campylobacter jejuni and C. coli

Gram negative, microaerophilic, nonspore-forming, optimal growth at 42°C, CO2 is required for good growth, growth optimal in 3%-6% O2, sensitive to dehydration, survives best at refrigeration temperature

Poultry

Swine

Cattle

Sheep

Wild birds

Raw or undercooked chicken, pork, and beef and unpasteurized milk

845,024

1-11 days, usually 2-5 days

Abdominal pain, diarrhea, malaise, headache, fever

Duration is up to 10 days

Cultural methods followed by confirmatory biochemical tests 408 , 409

Immunoassay 410 , 411

PCR 412 - 418

Quantum dot sandwich assay 419

Loop-mediated isothermal amplification (LAMP) assay 420

Biosensor 421

DNA microarray 422

Adequate cooking of meat; avoid cross contamination of raw foods of animal origin with cooked or ready-to-eat foods; pasteurization of milk

Shigella spp.

Gram negative, facultative anaerobe, nonspore-forming, does not ferment lactose, growth at 10°C-45°C, optimal growth at 37°C

Humans

Raw foods and water contaminated with human feces, prepared salads

131,254

1-7 days Severe abdominal and rectal pain, bloody diarrhea with mucus, fever, dehydration

Duration is few days to few weeks

Cultural methods followed by confirmatory biochemical tests 423

ELISA 424 , 425

PCR 426 - 430

Apyrase-based colorimetric test 431

DNA microarray 432

Good personal hygiene, adequate cooking of food, drinking potable water

Y. enterocolitica

Gram negative, facultative anaerobe, nonspore-forming, growth at 0°C-44°C, optimal growth at ca. 29°C, growth at pH 4.6-9.0, growth in presence of 5% NaCl but not 7% NaCl

Swine is principal reservoir of pathogenic strains.

Humans can also act as a source through contaminated blood transfusion.

Undercooked or raw pork, especially tongue

97,656

1-11 days, usually 24-36 h

Severe abdominal pain, nausea, diarrhea, fever, sometimes vomiting

Duration is usually 2-3 days but may continue for up to 3 weeks

Cultural methods followed by confirmatory biochemical tests 433

PCR 434 - 436

Monoclonal antibody-based dot blot assay 437

LAMP assay 438

Mass spectrometry 439

DNA microarray 432

Adequate cooking of pork, disinfection of drinking water, control of Y. enterocolitica in pigs, prevent cross contamination of pig viscera, feces, and hair with food and water

V. cholerae

Gram negative, facultative anaerobe, nonspore-forming, growth at 18°C-42°C with optimal growth at 37°C, growth is stimulated in the presence of 3% NaCl, pH range for growth is 6-11

Humans, marine waters, especially brackish water and estuaries

Undercooked or raw seafoods, vegetables fertilized with contaminated human feces or irrigated with contaminated water, water

84

1-3 days

Profuse watery diarrhea, which can lead to severe dehydration, abdominal pain, vomiting

Duration is up to 7 days

Cultural methods followed by confirmatory biochemical tests 440 - 442

ELISA 443 , 444

Immunoassay 445

PCR 446 - 451

Biosensor 450

LAMP assay 420 , 452

DNA microarray 432 , 453

Safe disposal of human sewage, disinfection of drinking water, avoid eating raw seafood, adequate cooking of food

Vibrio parahaemolyticus

Gram negative, facultative anaerobe, nonspore-forming, growth in presence of 8% NaCl, optimal growth at 37°C with rapid generation time (ca. 10 min), growth at 10°C, sensitive to storage at refrigeration temperature

Coastal seawater, estuarine brackish waters above 15°C, marine fish, shellfish

Raw or undercooked fish and seafoods

34,664

9-25 h, up to 3 days,

Profuse watery diarrhea, abdominal pain, vomiting, fever

Duration is up to 8 days

Cultural methods followed by confirmatory biochemical tests 440 , 441

ELISA 454

PCR 455 - 460

LAMP assay 461

DNA microarray 432 , 462

Adequate cooking of seafood, rapid chilling of seafoods, prevent cross contamination from raw seafoods to other foods and preparation surfaces

Vibrio vulnificus

Gram negative, nonspore-forming, optimal growth at 37°C

Coastal and estuarine waters

Raw seafood, especially raw oysters

96

12 h to 3 days

Profuse diarrhea with blood in feces, fulminating septicemia, hypotension

Duration is days to weeks

Cultural methods followed by confirmatory biochemical tests 440 , 441 , 463

ELISA 464 , 465

PCR 466 - 470

LAMP assay 469 , 471

DNA microarray 432 , 472

Avoid eating raw seafood, especially raw oysters when have a history of liver disease or alcoholism

C. sakazakii

Gram negative, facultative anaerobe, nonspore-forming, α-glucosidase positive, phosphoamidase negative, growth at 5.5°C-37°C, tolerant to high osmotic pressure and desiccation

Not known

Dry, powdered infant formula

Not available

Sepsis, meningitis, meningoencephalitis, brain abscess, ventriculitis, hydrocephalus, necrotizing enterocolitis in infants

Bacteremia, osteomyelitis, and pneumonia in elderly adults

Cultural and biochemical methods 473 , 474

PCR 475 - 478

DNA-microarray 477 , 479

Proper refrigerated storage of reconstituted infant formula

Avoid feeding nonrefrigerated formula and formula refrigerated for more than 24 h

Prepared infant formula should not be kept warm in bottle heaters or thermoses

A. hydrophila

Gram negative, facultative anaerobe, nonspore-forming, oxidase positive, some strains are psychrotrophic (4°C) optimum growth at ca. 28°C

Aquatic environment, freshwater fish (especially salmonids)

Untreated water

Undercooked seafoods, especially fish

Very few

24-48 h

Abdominal pain, vomiting, watery stools, mild fever

Duration is days to weeks

Cultural methods followed by confirmatory biochemical tests 480 - 483

ELISA 484

PCR 485 - 488

Biosensors 489

Indirect fluorescent antibody assay 490

Monoclonal antibody-based dot blot assay 491

LAMP assay 492

DNA microarray 493

Avoid consumption of raw seafoods, avoid long-term storage of refrigerated foods, adequate cooking of foods, disinfection of drinking water

P. shigelloides

Gram negative, facultative anaerobe, nonspore-forming, oxidase positive, some strains are psychrotrophic

Fresh and estuarine waters, fish, and shellfish

Fish, shellfish, oysters, shrimp, and untreated water

Very few

1-2 days

Abdominal pain, nausea, vomiting, diarrhea, chills, headache

Duration is days to weeks

Cultural methods followed by confirmatory biochemical tests 480 , 481

PCR 494

Avoid consumption of raw seafoods, disinfection of drinking water

L. monocytogenes

Gram positive, facultative anaerobe, nonspore-forming, growth at 2°C-45°C, optimal growth at 30°C-35°C, growth in presence of 10% NaCl

Soil, sewage, vegetation, water, and feces of humans and animals

Raw milk, soft cheese, pâte, ready-to-eat cooked meat products (poultry, hot dogs) and cooked seafoods (smoked fish), and raw vegetables

1,591

Few days to several weeks

Flu-like symptoms such as fever, chills, headache

Abdominal pain and diarrhea are present in some cases

In pregnant women, spontaneous abortion and stillbirth

Duration is days to weeks

Cultural methods followed by confirmatory biochemical tests 495 - 498

Immunoassay 499 - 501

PCR 502 - 507

Biosensors 508

LAMP assay 509

Fluorescent in situ hybridization (FISH) 510

Proper sanitation of food processing equipment and environments; adequate cooking of meat and meat products; prevent recontamination of cooked products; proper reheating of cooked food; avoid drinking raw milk, avoid certain high-risk foods (e.g., soft cheeses and pâtes) by pregnant women and immunocompromised individuals

S. aureus (staphylococcal enterotoxin)

Gram positive, facultative anaerobe, nonspore-forming, coagulase positive, growth at 7°C-48°C, optimal growth at ca. 37°C, toxin production at aw of 0.86; toxin is heat stable (can withstand boiling for 1 h)

Humans (nose, throat, and skin) and animals

Ham, chicken and egg salads, cream-filled pastries

241,148

2-6 h

Abdominal cramps, nausea, vomiting, diarrhea, headache, chills, and dizziness

Duration is up to 2 days

Cultural methods followed by confirmatory biochemical tests 511 , 512

PCR 513 - 517

Immunoassay 518 - 520

Detection of toxin by microslide gel double diffusion 521

FISH 522

ssDNA aptamer detection 523

Good personal hygiene in food preparation and handling, adequate cooking of foods, proper refrigeration of cooked foods

C. botulinum (botulinum neurotoxin)

Gram positive, obligate anaerobe, spore-forming, produce seven potent neurotoxins A-G (only A, B, E, and rarely F associated with human illness); proteolytic strains grow at 10°C-50°C, and nonproteolytic strains can grow at 3.3°C; spores are resistant to normal cooking temperatures and survive freezing and drying

Soil, dust, vegetation, animals, birds, insects, and marine and fresh water sediments and the intestinal tracts of fish (type E)

Beef, pork, fish, vegetables, and honey (infant botulism)

55

12-36 h, can range from few hours to 8 days

Very severe life-threatening intoxication, headache, fixed and dilated pupils, vertigo, blurred or double vision, lack of muscle coordination, dry mouth, difficulty in breathing

Gastrointestinal symptoms include abdominal pain, nausea, vomiting, and constipation

Duration is days to months (8 months)

Cultural methods followed by confirmatory biochemical tests 524

PCR 525 - 531

Detection of toxin by mouse bioassay 532 immunoaffinity chromatograpgy 533 mass spectrophotometry 534 immunodetection kit 535

LAMP assay 536

DNA microarray 537

Boiling of foods will destroy toxin; adequate heat processing of home-canned foods; proper refrigeration of vacuum-packaged fresh or lightly cooked/smoked foods; acid-preserved foods should be below pH 4.6; discard swollen cans; avoid feeding honey to infants

C. perfringens

Gram positive, anaerobe, spore-forming, optimum growth at 37°C-47°C, grows slowly below 20°C

Soil, sewage, dust, vegetation, feces of humans and animals

Cooked meat and poultry, especially roast beef, turkey, and gravies

965,958

8-24 h

Abdominal pain and diarrhea

Duration is 1-2 days

Cultural methods followed by confirmatory biochemical tests 243

Latex agglutination test 538

Colony hybridization assay 539

ELISA 540 , 541

PCR 538 , 542 - 545

FISH 546

DNA microarray 547

Adequate cooking of foods; cooked food should be rapidly cooled (<5°C) or held hot (>60°C); proper refrigeration and adequate reheating of stored cooked foods

C. difficile

Gram positive, spore-forming, anaerobic, showing optimal growth at human body temperature

Water, air, human and animal feces, soil

Ground beef, ground veal, veal chops, ground pork, chicken, vegetables

Not available

Abdominal pain, fever, fulminant colitis, toxic megacolon, sepsis, shock, mild diarrhea in asymptomatic carriers, relapse or reinfection within 2 months

Cultural methods followed by confirmatory biochemical tests 249

ELISA 548

PCR 549 - 551

LAMP assay 552

PCR ribotyping 553

DNA microarray 554

Hospital setting:

Limit use of antimicrobial drugs, wash hands between contact, use precautions for infected people with diarrhea, clean the environment meticulously

Community setting:

Proper cooking of meat 555

B. cereus

Gram positive, facultative anaerobe, spore-forming; some strains can grow at 4°C-6°C, optimum growth at 28°C-37°C

Widely distributed in nature, soil, dust, vegetation

Cereals, fried rice, potatoes, cooked meat products, milk and dairy products, spices, dried foods

63,400

Diarrheal syndrome (toxic infection): 8-16 h

Abdominal pain, watery diarrhea

Duration is 24-36 h

Emetic syndrome (preformed, heat-stable toxin): 1-5 h

Nausea, vomiting, malaise, sometimes diarrhea

Duration is 24-36 h.

Cultural methods followed by confirmatory biochemical tests 556

ELISA 557 , 558

Colony blot immunoassay 559 , 560

PCR 561 - 565

Tecra VIA kit 566

Oxoid BCET-RPLA kit 566

CHO cell culture assay 566

DNA microarray 567

Adequate cooking of foods; cooked foods should be rapidly cooled (<5°C) or held hot (60°C); avoid leaving cooked foods at room temperature for long time

A. butzleri

Fastidious, gram negative, nonspore-forming, motile, spiral organisms, grows microaerobically and aerobically, ability to grow at 15°C differentiating it from Campylobacter

Preferred temperature for growth is 30°C

Domestic and pet animals, birds including chickens and turkeys, humans

Increased isolation from raw meat products, surface and groundwater, foodborne transmission is not definitive

Unknown

Human enteritis characterized by persistent and watery diarrhea, vomiting, nausea, and fever

Cultural detection by enrichment under aerobic conditions at 25°C 568

Charcoal cefoperazone deoxycholate agar and broth for selective identification

Johnson and Murano broth 569

PCR 570

SDS-PAGE 571 , 572

Random amplification of polymorphic DNA coupled with enterobacterial repetitive intergenic consensus PCR 573

Pulsed-field gel electrophoresis 574

Brucella spp.

Gram negative, aerobe, nonspore-forming, optimal growth at 37°C

Cattle, sheep, pig, goat

Raw milk and products made from unpasteurized milk

839

Acute form: 3-21 days, infrequently months

Pyrexia, profuse sweats, chills, constipation, weakness, malaise, body aches, joint pains, weight loss, anorexia

Chronic form: several months

Long history of fever, inertia, recurrent depression, sexual impotence, insomnia

Duration is weeks

Cultural methods 575

ELISA 576 - 578

PCR 579 - 582

LAMP assay 583

Lateral-flow assay 584

Vaccination of livestock against Brucella spp.; avoid contact with infected animals; eradication of diseased animals; pasteurization of milk; avoid eating unpasteurized dairy products

H. pylori

Gram negative, microaerophile to anaerobe

Humans, cats

Untreated water; foodborne transmission of disease has not been proven

Unknown

Gastritis, dyspepsia, peptic ulcer, gastric carcinoma

Cultural methods 292 , 585 ELISA 290

Immunoassay 586 , 587

PCR 588 , 589

Rapid paper urease test 590

Oligonucleotide-based multiplex PCR 591

Avoid contact with infected animals; use of chlorinated water for cooking and drinking

Acidification is commonly used in food processing to control survival and growth of spoilage-causing and pathogenic microorganisms in foods. The U.S. Food and Drug Administration does not consider foods with pH ≤ 4.6 (high-acid foods) to be microbiologically hazardous for many foodborne pathogens. However, E. coli O157:H7 has been associated with outbreaks attributed to high-acid foods, including apple juice, mayonnaise, fermented sausage, and yogurt, 49 raising concerns about the safety of these foods. Several studies have revealed that many strains of E. coli O157:H7 are highly tolerant to acidic conditions, being able to survive for extended periods of time in synthetic gastric juice and in highly acidic foods. 49 , 50 Further, exposure of E. coli O157:H7 to mild or moderate acidic environments can induce an acid tolerance response, which enables the pathogen to survive extreme acidic conditions. For example, acid-adapted cells of E. coli O157:H7 survived longer in apple cider, fermented sausage, and hydrochloric acid than nonacid-adapted cells. 51 , 52 However, E. coli O157:H7 is not unusually heat resistant 53 or salt tolerant 54 unless cells are preexposed to acid to become acid adapted. Acid-adapted E. coli O157:H7 cells also have increased heat tolerance.

In humans, two principal manifestations of illness have been reported in E. coli O157:H7 infection. These include hemorrhagic colitis (HC) and hemolytic uremic syndrome (HUS). 55 HC is characterized by a watery diarrhea that progresses into grossly bloody diarrhea, indicative of significant amounts of gastrointestinal bleeding. Severe abdominal pain is common, but fever is usually not present. The illness typically lasts from 2 to 9 days. HUS is a severe condition, particularly among the very young and the elderly. Both these manifestations involve damage to kidneys, leading to renal failure and death. Treatment of E. coli O157:H7 infections with antibiotics may result in severe outcomes. 56 , 57 Administration of antibiotics, particularly β-lactams, is risk factor for development of HUS. 58

The pathogenicity of EHEC is determined by virulence factors encoded by pathogenicity islands, phage chromosomes, and plasmids. The important factors attributed to the pathogenesis of E. coli O157:H7 include the ability of the pathogen to adhere to the intestinal mucosa of the host by the locus for enterocyte effacement (LEE) and production of Shiga toxin I (Stx1) and/or Shiga toxin II (Stx2) 35 and the large plasmid pO157. 7 The LEE encodes for an adhesion factor called intimin. Together, these factors are able to produce attaching and effacing lesions on host intestine in EHEC infections. 59 The toxins, both chromosomally and phage encoded, are produced in the colon and have the ability to reach kidneys via blood to cause HUS. 60 STEC isolates capable of producing Stx2, in particular Stx2a, are most often associated with serious disease in affected individuals than isolates that produce only Stx1. 61 The plasmid pO157, which is commonly found in most EHEC isolates, encodes for a hemolysin that is toxic to both human and bovine cells. 62 Retrospective analysis of foods implicated in outbreaks of E. coli O157:H7 infection suggests a low oral infectious dose of the pathogen, probably less than a hundred cells. 55

Although infections caused by non-O157 serogroups were reported as early as 1982, a lack of reliable detection methods hindered the identification of their epidemiologic role in causing disease compared to E. coli O157:H7. 63 It is estimated that Shiga toxin-producing non-O157 isolates cause annually 112,750 cases with 271 hospitalizations, which account for an economic loss of $100 million. 3 Among the STEC non-O157 serogroups, serogroups O26, O45, O103, O111, O121, and O145 are leading causes of STEC inflections in the United States. 64 Recent reports suggest that the infections caused by O157 serotypes are more severe, albeit non-O157 serotypes caused significant morbidity. 65 Recently, an Stx2a-producing isolate of enteroaggregative E. coli O104:H4 caused a major outbreak of severe HUS and bloody diarrhea in the European Union, particularly Germany. 66 There were more than 4000 cases that included more than 900 cases of HUS and approximately 50 deaths.

Salmonella Species

Salmonella spp. are facultatively anaerobic, gram-negative, rod-shaped bacteria belonging to the family Enterobacteriaceae. Members of the genus Salmonella have an optimum growth temperature of 37°C and utilize glucose with the production of acid and gas. 67 Salmonella spp. are widely distributed in nature. They colonize the intestinal tract of humans, animals, birds, and reptiles and are excreted in feces, which contaminate the environment, water, and foods. 68 Many food products, especially foods having contact with animal feces, including beef, pork, poultry, eggs, milk, fruits, and vegetables, have been associated with outbreaks of salmonellosis. 69 Salmonella spp. can be divided into host-adapted serovars and those without any host preferences. Most of the foodborne serovars are in the latter group.

The ability of many strains of Salmonella to adapt to extreme environmental conditions emphasizes the potential risk of these microorganisms as foodborne pathogens. Although salmonellae optimally grow at 37°C, the genus Salmonella consists of strains, which are capable of growth from 5°C to 47°C. 70 Salmonella spp. can grow at pH values ranging from 4.5 to 7.0, with optimum growth observed near neutral pH. 68 Preexposure of Salmonella to mild acidic environments (pH 5.5–6.0) can induce in some strains an acid tolerance response, which enables the bacteria to survive for extended periods of exposure to acidic and other adverse environmental conditions such as heat and low water activity. 71 , 72 However, most Salmonella spp. possess no unusual tolerance to salt and heat. A concentration of 3%–4% NaCl can inhibit the growth of Salmonella. 73 Most salmonellae are sensitive to heat; hence, ordinary pasteurization and cooking temperatures are capable of killing the pathogen. 74

Salmonellosis is one of the most frequently reported food-borne diseases worldwide. 75 The overall incidence of salmonellosis in the United States declined by approximately 8% during the period from 1996 to 2004. 76 However, a recent CDC study revealed that foodborne salmonellosis in the United States during the past decade has not decreased significantly. 1 Food-associated Salmonella infections in the United States are estimated by the U.S. Department of Agriculture to cost $3 billion annually. 77 CDC epidemiologists recently estimated 1 million cases of nontyphoidal salmonellosis annually in the United States, resulting in 19,226 hospitalizations and 378 deaths, accounting for an economic loss of $4.4 billion. 3 Among the 7564 foodborne Salmonella isolates serotyped in 2010 in the United States, S. Enteritidis was most common, followed by S. Newport and S. Typhimurium. 1 Although the overall incidence of human salmonellosis in 2005 was lower than that in the mid-1990s, the incidence of S. Enteritidis infections increased by approximately 25%. 78

S. Enteritidis outbreaks are most frequently associated with the consumption of poultry products, especially under-cooked eggs and chicken. Moreover, international travel especially to developing countries has been associated with human infections of S. Enteritidis in the United States. 79 A report from the CDC revealed 677 outbreaks of eggborne S. Enteritidis with 23,366 illnesses, 1,988 hospitalizations, and 33 deaths in the United States during the period 1990–2001. 80 Another study reported an estimate of 700,000 cases of eggborne salmonellosis in the United States, which accounted for approximately 47% of total foodborne salmonellosis, costing more than $1 billion annually. 81 In 2010, a nationwide outbreak of S. Enteritidis infection consisting of 3578 cases associated with the consumption of shell eggs was reported in the United States during the months from May to November. 82 Given that approximately 65 billion shell eggs are sold annually in the United States, 83 with a per capita consumption of approximately 254 eggs/year, Salmonella-contaminated eggs potentially constitute a major health hazard to humans. In light of the mounting evidence linking human salmonellosis with shell eggs, the Food and Drug Administration in 2009 announced that eggs constitute an important source of S. Enteritidis infections and issued a final rule that requires shell egg producers to implement measures to prevent S. Enteritidis from contaminating eggs on the farm and further growth during storage and transportation.

Apart from eggs, salmonellae are isolated from poultry carcasses and meat. From 1998 through 2003, the U.S. Department of Agriculture-Food Safety Inspection Service (USDA-FSIS) reported isolation of Salmonella from 11.2% to 22.5% of broiler and ground chicken samples, respectively. 77 In another study, White et al. 84 reported isolation of Salmonella from 26.4% of ground turkey, 22.5% of ground chicken, and 11.2% of broiler samples (N = 12,699/293,938 samples positive for Salmonella), with the largest number of S. Enteritidis isolates recovered from broiler carcasses.

S. Typhimurium is another significant Salmonella sero-type causing foodborne infections worldwide. 1 A wide variety of foods, including chicken, turkey, beef, pork, peanut butter, and milk, have been associated with outbreaks caused by S. Typhimurium. Although the incidence of S. Typhimurium infections in the United States has decreased by approximately 40% during 1996–2004, 76 the emergence of S. Typhimurium DT 104, a new multidrug-resistant phage type in the 1990s in the United States and Europe, became a major public health concern. This is because S. Typhimurium DT 104 is resistant to multiple antibiotics, including ampicillin, chloramphenicol, penicillin, streptomycin, tetracycline, and sulfonamides. 85 , 86 A major risk factor identified in the development of S. Typhimurium DT 104 infection in humans was prior treatment with antimicrobial agents to which the infecting strain was resistant, during four preceding weeks of infection. 87 The CDC reported that 11% of the total Salmonella spp. isolated from humans in 2000 were resistant to at least five different antibiotics and a few of the multidrug-resistant strains were also resistant to gentamicin and cephalosporins. 88 These aforementioned reports underscore the prudent use of antibiotics in humans and animal husbandry.

In addition to S. Enteritidis and S. Typhimurium, several other serotypes of Salmonella are linked with food-borne outbreaks. These include S. Hadar, S. Newport, S. Virchow, and S. Heidelberg for which poultry meat has been a major vehicle. 89 S. Baildon, S. Braenderup, S. Javiana, S. Montevideo, S. Newport, and S. Saintpaul have been associated with fresh produce-associated outbreaks. 90 A variety of pre- and postharvest strategies including competitive exclusion bacteria, bacteriophages, organic acids, prebiotic oligosaccharides, and vaccines 91 97 have been determined to help mitigate Salmonella contamination of chickens but with varied degrees of success rates. Recently, medium-chain fatty acids and plant-derived antimicrobials reportedly can reduce S. Enteritidis colonization of broiler chickens. 98 , 99

In the host, Salmonella establishes a successful infection utilizing a variety of virulence factors, including motility, adherence to and invasion of host cells, macrophage survival, evasion of the host immune system, systemic dissemination, and finally dissemination to new hosts. Several Salmonella pathogenicity islands (SPI), including SPI1 and SPI2, play critical roles in the process. The pathogenicity island SPI1 controls bacterial motility, adherence, and invasion of Salmonella in the host’s intestinal tract, whereas SPI2 regulates systemic dissemination to reach internal organs, including, for some strains such as S. Enteritidis, reproductive organs in chickens. 100 Salmonella infection in humans is characterized by fever, headache, abdominal pain, vomiting, and diarrhea and is mostly self-limiting. 101 The incubation period of the disease typically ranges from 12 to 72 h, with the illness lasting for 2–7 days. Patients usually recover within a week without any antibiotic treatment except in cases of severe diarrhea, where intravenous fluid therapy is warranted. However, severe illness caused by antibiotic-resistant strains of S. Enteritidis may result in an extended treatment period. 102 Vulnerable populations such as infants, children, the elderly, and immunocompromised are prone to more severe outcomes leading to an invasive disease, characterized by bacteremia and rarely death. 103 In addition, in a small percentage of affected individuals, the lingering effects of disease include chronic reactive arthritis, osteoarthritis, appendicitis, meningitis, and peritonitis. 103

S. Typhi is the causative agent of typhoid (enteric fever), a serious human disease. Typhoid fever has a long incubation period of 7–28 days and is characterized by prolonged and spiking fever, abdominal pain, diarrhea, and headache. 67 The disease can be diagnosed by isolation of the pathogen from urine, blood, or stool specimens of affected individuals. In 2003, a total of 356 cases of typhoid fever were reported in the United States. 104 S. Typhi is an uncommon cause of food-borne illness in the United States, and approximately 74% of these cases reported in the United States occurred among persons who traveled internationally, especially South Asia during the preceding 6 weeks of infection. 104

Campylobacter Species

The genus Campylobacter consists of 14 species; however, C. jejuni subsp. jejuni and C. coli are the dominant food-borne pathogens. C. jejuni is a slender, rod-shaped, micro-aerophilic bacterium that requires approximately 3%–6% oxygen for growth. It can be differentiated from C. coli by its ability to hydrolyze hippurate. 105 The bacterium does not survive well in the environment, being sensitive to drying, highly acidic conditions, and freezing. It is also readily killed in foods by adequate cooking. 106

C. jejuni is one of the most commonly reported bacterial causes of foodborne infection in the United States 78 , 106 , 107 and the European Union. 108 The estimated incidence of campylobacteriosis in the United States is 13.02 per 100,000 population, 109 with an estimated 845,000 cases, 8,463 hospitalizations, and 76 deaths occurring annually. 2 Many animals, including poultry, swine, cattle, sheep, horses, and domestic pets, harbor C. jejuni in their intestinal tracts serving as sources of human infection. However, chickens serve as the most common reservoir of C. jejuni, where the bacterium primarily colonizes the mucus over-lying the epithelial cells in the ceca and small intestine. l-Fucose, the major carbohydrate component present in the mucin of chicken cecal mucus, is used by C. jejuni as a sole substrate for growth, which gives the pathogen a competitive advantage over other competing flora for survival in the intestine. 110 , 111 Hence, the cecal environment in chickens is favorable for the survival and proliferation of C. jejuni 110 and selects for colonization of C. jejuni in the birds. Although a number of vehicles such as beef, pork, eggs, and untreated water have been implicated as vehicles of outbreaks of campylobacter enteritis, with chicken and unpasteurized milk being the most commonly involved foods, 112 , 113 epidemiologic investigations have revealed a significant link between human campylobacter infection and handling or consumption of raw or undercooked poultry meat. 113 117 Since colonization of broiler chickens by C. jejuni results in horizontal transmission of the pathogen and carcass contamination during slaughter, a variety of approaches for reducing its cecal carriage by chickens have been undertaken. These approaches include competitive exclusion, 94 feeding birds with bacteriophages 118 , 119 and acidified feed, 120 medium-chain fatty acids, 121 , 122 and vaccination. 123 , 124 In the United States, an increasing number of fluoroquinolone-resistant (e.g., ciprofloxacin) human campylobacter infections had been reported, 125 and this was attributed to the use of this antibiotic in food animal production, especially poultry. 126 Besides resistance to fluoroquinolones, strains resistant to tetracyclines and erythromycins have been recently reported. 108

Usually campylobacter enteritis in humans is a self-limiting illness characterized by abdominal cramps, diarrhea, headache, and fever lasting up to 4 days. However, severe cases, involving bloody diarrhea and abdominal pain mimicking appendicitis, also occur. 105 Guillain–Barré syndrome (GBS) is an infrequent sequel to Campylobacter infection in humans. 127 GBS is characterized by acute neuromuscular paralysis 106 and is estimated to occur in approximately one of every 1000 cases of campylobacter enteritis. 128 A few strains of C. jejuni reportedly produce a heat-labile enterotoxin similar to that produced by Vibrio cholerae and ETEC. 105 Some strains of C. jejuni and C. coli can also produce a cytolethal distending toxin, which causes a rapid and specific cell cycle arrest in HeLa and Caco-2 cells. 129

Shigella Species

Shigella is a common cause of human diarrhea in the United States. The genus Shigella is divided into four major groups: S. dysenteriae (group A), S. flexneri (group B), S. boydii (group C), and S. sonnei (group D) based on the organism’s somatic (O) antigen. Although all the four groups have been involved in human infections, S. sonnei accounts for more than 75% of shigellosis cases in humans 130 and has been linked to persistent infections in community and day-care centers. 131 133 Humans are the natural reservoirs of Shigella spp. The fecal–oral route is the primary mode of transmission of Shigellae and proper personal hygiene and sanitary practices of cooks and food handlers can greatly reduce the occurrence of outbreaks of shigellosis. Most foodborne outbreaks of shigellosis are associated with ingestion of foods such as salads and water contaminated with human feces containing the pathogen. Shigellosis is characterized by diarrhea containing bloody mucus, which lasts 1–2 weeks. The infectious dose for Shigella infection is low. The ID50 of S. flexneri and S. sonnei in humans is approximately 5000 microorganisms and that of S. dysenteriae is a few hundred cells; hence, secondary transmission of Shigella by person-to-person contact frequently occurs in outbreaks of foodborne illness. The incidence of shigellosis has decreased significantly during the 1996–2010 surveillance period, 1 although it is estimated to cause an economic loss of $257 million annually. 3 An emerging serotype of S. boydii, namely, serotype 20, has been reported in the United States. 134

Yersinia enterocolitica

Yersinia enterocolitica is a gram-negative, rod-shaped, facultative anaerobic bacterium, which was first isolated and described during the 1930s. 135 Swine have been identified as an important reservoir of Y. enterocolitica, in which the pathogen colonizes primarily the buccal cavity. 136 Although pork and pork products are considered to be the primary vehicles of Y. enterocolitica, a variety of other foods, including milk, ice cream, beef, lamb, seafood, and vegetables, have been identified as vehicles of Y. enterocolitica infection. 137 One of the largest outbreaks of yersiniosis in the United States was associated with milk. 138 Water has also been a vehicle of several outbreaks of Y. enterocolitica infection. 138 Surveys have revealed that Y. enterocolitica is frequently present in foods, having been isolated from 11% of sandwiches, 15% of chilled foods, and 22% of raw milk in Europe. 139 Several serovars of pathogenic Y. enterocolitica have been reported, which include O:3, O:5, O:8, and O:9, 140 142 with serovar O:3 (bioserotype 4) being the most common causing human disease in the United States. 105 107 Although the incidence of Yersinia infection from 1996 to 2010 has decreased by 52% compared to the 1996–1998 surveillance period, 1 the pathogen causes annually an estimated 97,700 cases, 533 hospitalizations, and 29 deaths, accounting for $400 million loss. 3

In addition to foodborne outbreaks, reports of blood trans-fusion-associated Y. enterocolitica sepsis indicate another potential mode of transmission of this pathogen. 143 , 144 Among bacteria, Y. enterocolitica has emerged as a significant cause of transfusion-associated bacteremia and mortality (53%), with 49 cases reported since this condition was first documented in 1975. 145 A review of these cases revealed that bacteremia may occur in a subpopulation of individuals with Y. enterocolitica gastrointestinal infection. 140 The strains of Y. enterocolitica responsible for transfusion-acquired yersiniosis are the same serobiotypes as those associated with enteric infections.

An unusual characteristic of Y. enterocolitica that influences food safety is its ability to grow at low temperatures, even as low as −1°C. 146 Y. enterocolitica readily withstands freezing and can survive in frozen foods for extended periods, even after repeated freezing and thawing. 147 Refrigeration (4°C) is one of the common methods used in food processing to control growth of spoilage and pathogenic microorganisms in foods. However, several studies have revealed growth of Y. enterocolitica in foods stored at refrigeration temperature. Y. enterocolitica grew on pork, chicken, and beef at 0°C–1°C. 148 , 149 The psychrotrophic nature of Y. enterocolitica also poses problems for the blood transfusion industry, mainly because of its ability to proliferate and release endotoxin in blood products stored at 4°C without manifesting any alterations in their physical appearance. The ability of Y. enterocolitica to grow well at refrigeration temperature has been exploited for isolating the pathogen from foods, water, and stool specimens. Such samples are incubated at 4°C–8°C in an enrichment broth for several days to selectively culture Y. enterocolitica based on its psychrotrophic nature.

Y. enterocolitica is primarily an intestinal pathogen with a predilection for extraintestinal spread under appropriate host conditions such as immunosuppression. In the gastrointestinal tract, Y. enterocolitica can cause acute enteritis, enterocolitis, mesenteric lymphadenitis, and terminal ileitis often mimicking appendicitis. 140 In the intestinal tract, the pathogen employs major virulence determinants such as invasins (Inv)—the proteins that mediate binding to host cell integrins, attachment invasion locus (Ail)—an outer-membrane protein associated with adhesion and invasion of the pathogen, a high-pathogenicity island (HPI) that sequesters iron, and a virulence plasmid (pVY) that encodes for YadA and Yop proteins for increased pathogenicity. 142 Infection with Y. enterocolitica often leads to secondary, immunologically induced sequelae such as arthritis (most common), erythema nodosum, Reiter’s syndrome, glomerulonephritis, and myocarditis.

Vibrio Species

Seafoods form a vital part of the American diet, and their consumption in the United States has risen steadily over the past few decades from an average of 4.5 kg/person in 1960 to about 7 kg in 2002. 150 , 151 However, according to a recent report published by the CSPI, contaminated seafoods have been recognized as a leading known cause of most foodborne illness outbreaks in the United States. 152 Vibrios, especially V. parahaemolyticus, V. vulnificus, and V. cholerae, which are commonly associated with estuarine and marine waters, represent the major pathogens resulting in disease outbreaks through consumption of seafoods and cause severe infections in cirrhotic patients. 153 The CDC reported a 115% increase in Vibrio infections during 1996–2010. 1 In addition, a recent epidemiologic investigation revealed that Vibrio spp. cause an estimated 34,800 cases with 195 hospitalizations and 40 deaths annually, accounting for $336 million in losses. However, among the vibrios, V. vulnificus caused the greatest economic impact, accounting for a loss of $268 million. V. parahaemolyticus and V. vulnificus are halophilic in nature, requiring the presence of 1%–3% sodium chloride for optimum growth. V. cholerae can grow in media without added salt, although their growth is stimulated by the presence of sodium ions.

Among the three species of Vibrio, V. parahaemolyticus accounts for the largest number of foodborne disease outbreaks (it was responsible for 34,664 of the total 34,844 cases reported for Vibrio spp.). 3 V. parahaemolyticus is present in coastal waters of the United States and the world. V. parahaemolyticus being an obligate halophile can multiply in substrates with sodium chloride concentrations ranging from 0.5% to 10%, with 3% being the optimal concentration for growth. The ability of V. parahaemolyticus to grow in a wide range of salt concentrations reflects on its existence in aquatic environments with various salinities. V. parahaemolyticus has a remarkable ability for rapid growth, and generation times as short as 12–18 min in seafoods have been reported at 30°C. Growth rates at lower temperatures are slower, but counts were found to increase from 10 2 to 10 8 colony-forming units (CFU)/g after 24 h storage at 25°C in homogenized shrimp and from 10 3 to 10 8 CFU/g after 7 days of storage at 12°C in homogenized oysters. 154 Because of its rapid growth, proper refrigeration of cooked seafoods to prevent regrowth of the bacterium is critical to product safety. A survey by the U.S. Food and Drug Administration revealed that 86% of 635 seafood samples contained V. parahaemolyticus, being isolated from codfish, sardine, mackerel, flounder, clam, octopus, shrimp, crab, lobster, crawfish, scallop, and oyster. 155 The pathogen has been a major seafood-associated Vibrio in Asian countries, including Japan, Taiwan, and China. 156 A new serotype of V. parahaemolyticus, O3:K6, that emerged in the Southeast Asia in the 1990s has been implicated in oyster-related outbreaks in the United States in 1997 and 1998. 157 An important virulence characteristic of pathogenic strains of V. parahaemolyticus is their ability to produce a thermostable hemolysin (Kanagawa hemolysin). 158 Studies in humans on the infectious dose of pathogenic V. parahaemolyticus strains revealed that ingestion of approximately 105–107 bacteria can cause gastroenteritis. 155

Among the 206 serogroups of V. cholerae identified thus far, serogroups O1 and O139, the causative agents of cholera in humans, are a part of the normal estuarine microflora, and foods such as raw fish, mussels, oysters, and clams have been associated with outbreaks of cholera. 159 The clinical course of cholera, which is a toxin-mediated acute illness, results in severe diarrhea. The bacterium secretes an enterotoxin that binds to receptors on the epithelial cell membrane of the small intestine causing increased levels of cAMP. Subsequently, elevated secretion of fluid and electrolytes results in a characteristic “rice water” diarrhea with large amounts of mucus in the stools. 153 The presence of a type VI secretion system (T6SS) in V. cholerae involved in its pathogenesis was recently identified. 160 Infected humans can serve as short-term carriers, shedding the pathogen in feces. Cholera is characterized by profuse diarrhea, potentially fatal in severe cases, and often described as “rice water” diarrhea due to the presence of prolific amounts of mucus in the stools. Gastroenteritis caused by non-O1 and non-O139 serovars of V. cholerae is usually mild in nature. During the period from 1996 to 2005, a total of 64 cases of toxigenic V. cholerae O1 were reported in the United States, of which 35 (55%) cases were acquired during foreign travel and 29 (45%) cases were domestically acquired. 161 Seven (24%) of the 29 domestic cases were attributed to consumption of Gulf Coast seafood (crabs, shrimp, or oysters). Moreover, seven of the eleven domestic cholera cases in 2005 were reported during October–December, after Hurricanes Katrina and Rita, although no evidence suggests increased risk for cholera among Gulf Coast residents or consumers of Gulf Coast seafood after the hurricanes. In 2003, a total of 111,575 cases of cholera worldwide were reported to the World Health Organization from 45 countries. 162

V. vulnificus is the most serious of the vibrios and is responsible for most of the seafood-associated deaths in the United States, especially in Florida. 155 V. vulnificus results in life-threatening bacteremia, septicemia, and necrotizing fasciitis in persons with liver disorders and high iron level in blood, diabetes mellitus, end-stage renal disorders, and immunodeficiency conditions. 163 Although a number of seafoods have been associated with V. vulnificus infection, raw oysters are the most common vehicle associated with cases of illness. 164 The major virulence factors responsible for causing sepsis and bacteremia in V. vulnificus include its ability to escape acidic conditions in the stomach and its expression of capsular polysaccharide and surface LPSs, cytotoxins, pili, and flagella. 165

Cronobacter sakazakii

Cronobacter sakazakii, formerly Enterobacter sakazakii, is a foodborne pathogen that causes severe meningitis, meningoencephalitis, sepsis, and necrotizing enterocolitis in neonates and infants, with a case fatality rate of 40%–80%. 159 163 C. sakazakii infections may also result in severe neurological sequelae such as hydrocephalus, quadriplegia, and retarded neural development in survivors. 166 The epidemiology and reservoir of this pathogen are still unknown and most strains have been isolated from clinical specimens such as cerebrospinal fluid, blood, skin, wounds, urine, and respiratory and digestive tract samples. 167 The bacterium has also been isolated from foods such as cheese, eggs, fish, pork, shellfish, sausage, barley, biscuits, cowpea paste, nuts, seeds, rice, soy, sweets, tea, minced beef, sausage, and vegetables, namely, salads and tomato. 168 , 169 Recently, Kandhai et al. 170 , 171 isolated C. sakazakii from household and food production facility environmental samples, such as scrapings from dust, vacuum cleaner bags, and spilled product near equipment, and proposed that the organism could be more widespread in the environment than previously thought. Although the environmental source of C. sakazakii has not been identified, epidemiologic studies implicate dried infant formula as the primary route of transmission to infants. 172 175 The bacterium has been isolated from powdered infant formula by numerous investigators. 174 , 176 178 Muytjens et al. 178 isolated the pathogen from powdered infant formula from 35 different countries.

C. sakazakii possesses several characteristics that enable it to grow and survive in infant formula. For example, the pathogen can grow at temperatures as low as 5.5°C, 179 which is within the temperature range of many home refrigerators. 180 A study on the thermal resistance of C. sakazakii in reconstituted infant formula indicated that it is one of most thermotolerant bacteria under Enterobacteriaceae. 181 A recent study by Breeuwer et al. 182 reported that C. sakazakii also has a high tolerance to osmotic stress and desiccation. In addition, C. sakazakii possesses a short lag time and generation time in reconstituted infant formula, 179 raising concerns that improper storage of reconstituted formula may permit its substantial growth. Recently, Iversen and Forsythe 183 reported the isolation of C. sakazakii from a variety of foods, including powdered infant formula, dried infant food and milk powder, as well as certain herbs and spices. The first case of neonatal meningitis caused by C. sakazakii was reported in 1958, 184 and since then a number of C. sakazakii infections have been reported worldwide, including the United States. In the United States, an outbreak of C. sakazakii involving four infants occurred in the neonatal intensive care unit of a hospital in Memphis, resulting in sepsis, bloody diarrhea, and intestinal colonization. The source of infection was traced to contaminated infant formula. 174 In 2002, Himelright et al. 185 reported a case of fatal neonatal meningitis caused by C. sakazakii in Tennessee, associated with feeding of contaminated infant formula. The infection occurred in the neonatal intensive care unit of a hospital and surveillance studies identified two more cases of suspected infection with positive stool or urine in seven more infants. There were many recalls of C. sakazakii-contaminated infant formula in the United States. In November 2002, a nationwide recall of more than 1.5 million cans of dry infant formula contaminated with C. sakazakii was reported. 186 Besides survival and growth in several foods including reconstituted infant formula, C. sakazakii is a good biofilm former on abiotic surfaces such as latex, silicon and stainless steel, and neonatal nasogastric feeding tubes. 187 The International Commission on Microbiological Specification for Foods classified C. sakazakii as “severe hazard for restricted populations, life-threatening or substantial chronic sequelae of long duration.” This places C. sakazakii in the same category as other serious food- and waterborne pathogens such as Listeria monocytogenes, Clostridium botulinum types A and B, and Cryptosporidium parvum. 188

The most common clinical manifestations of infections due to C. sakazakii are sepsis and meningitis in neonates. In more than 90% of the cases reported, patients developed meningitis with a very high prevalence for developing brain abscesses and less frequently ventriculitis and hydrocephalus. 189 , 190 While the reported mortality rates of C. sakazakii infections in neonates have declined over time from 50% or more to less than 20% due to advances in antimicrobial chemotherapy, an increasing incidence of resistance to commonly used antibiotic necessitates a reevaluation of existing treatment strategies. 167 Biering et al. 176 indicated that besides the high rate of mortality, the CNS infections due to C. sakazakii often lead to permanent impairment in mental and physical capabilities in surviving patients. In addition to meningitis, C. sakazakii is also reported to cause necrotizing enterocolitis in neonates and bacteremia, osteomyelitis, and pneumonia in elderly adults. 172 , 191 193

Aeromonas hydrophila

Although Aeromonas species have been recognized as pathogens of cold-blooded animals, their potential to cause human infections, especially foodborne illness, received attention only recently. A. hydrophila has been isolated from drinking water, fresh and saline waters, and sewage. 194 It also has been isolated from a variety of foods such as fish, oyster, shellfish, raw milk, ground beef, chicken, and pork. 194 A. hydrophila was isolated from cultured channel catfish, Ictalurus punctatus, during a disease outbreak in West Alabama in 2009. 195 Although A. hydrophila is sensitive to highly acidic conditions and does not possess any unusual thermal resistance, some strains are psychrotrophic and grow at refrigeration temperature. 196 A. hydrophila can grow on a variety of refrigerated foods, including pork, asparagus, cauliflower, and broccoli. 197 , 198 However, considering the widespread occurrence of A. hydrophila in water and food and its relatively infrequent association with human illness, it is likely that most strains of this bacterium are not pathogenic for humans. A. hydrophila infection in humans is characterized by watery diarrhea and mild fever. Virulent strains of A. hydrophila produce a 52 kDa polypeptide, which possesses enterotoxic, cytotoxic, and hemolytic activities. 199 A. hydrophila strains with resistance to multiple antibiotics have been reported. 200

Plesiomonas shigelloides

Plesiomonas shigelloides has been implicated in several cases of sporadic and epidemic gastroenteritis 201 and is regarded as an emerging enteric pathogen in humans. 202 The pathogen is present in fresh and estuarine waters and has been isolated from various aquatic animals. 196 Seafoods such as fish, crabs, and oysters have been associated with cases of P. shigelloides infection. The isolation of P. shigelloides from vertebrate animals, including swine, cats, dogs, and monkeys, suggests its potential for being a zoonotic pathogen. 202 The most common symptoms of P. shigelloides infection include abdominal pain, nausea, chills, fever, and diarrhea. Potential virulence factors of P. shigelloides include cytotoxic enterotoxin, inva-sins, and β-hemolysin. 196 An outbreak of P. shigelloides infection associated with drinking well water and involving 30 persons was reported in New York in 1996. 203

Listeria monocytogenes

L. monocytogenes has emerged into a highly significant and fatal foodborne pathogen throughout the world, especially in the United States. There is an estimated 2500 cases of listeriosis annually in the United States, with a mortality rate of ca. 25%. 204 Further, L. monocytogenes is of tremendous economic significance, causing an estimated monetary loss of $2.3 billion annually in the United States. 205 A large outbreak of listeriosis involving more than 100 cases and associated with eating contaminated turkey frankfurters occurred during 1998–1999. 206 During this period of time, there were more than 35 recalls of a number of different food products contaminated with listeriae. 206 In 2002, a large outbreak of listeriosis in the United States involving 46 people, 7 deaths, and 3 miscarriages resulted in a recall of 27.4 million pounds of fresh and frozen ready-to-eat chicken and turkey frankfurters. 88 In 2003, 696 cases of listeriosis were reported in the United States, with more than 50% of the cases occurring in persons above 60 years of age. 104 Contaminated ready-to-eat meat was implicated as the vehicle of two large multiprovince Listeria outbreaks that occurred in Canada in 2008. 207 In the same year in Austria, contaminated jellied pork was the vehicle of invasive listeriosis characterized by febrile gastroenteritis. 208 In 2011, a nationwide outbreak of listeriosis in the United States, involving more than 130 people with 30 deaths and one abortion, was associated with consumption of contaminated cantaloupe. 1

L. monocytogenes is widespread in nature, occurring in soil, vegetation, and untreated water. Humans and a wide variety of farm animals, including cattle, sheep, goat, pig, and poultry, are known sources of L. monocytogenes. 209 L. monocytogenes also occurs frequently in food processing facilities, especially in moist areas such as floor drains, floors, and processing equipment. 210 L. monocytogenes can also grow in biofilms attached to a variety of processing plant surfaces such as stainless steel, glass, and rubber. 211 A wide spectrum of foods, including milk, cheese, beef, pork, chicken, seafoods, fruits, and vegetables, has been identified as vehicles of L. monocytogenes. 209 However, ready-toeat cooked foods such as low-acid soft cheese, pâtes, and cooked poultry meat, which can support the growth of listeriae to large populations (>106 cells/g) when held at refrigeration temperature for several weeks, have been regarded as high-risk foods. 212 , 213 L. monocytogenes possesses several characteristics, which enable the pathogen to successfully contaminate, survive, and grow in foods, thereby resulting in outbreaks. These traits include an ability to grow at refrigeration temperature and in a medium with minimal nutrients; ability to survive in acidic conditions, e.g., pH 4.2; ability to tolerate up to 10% sodium chloride; ability to survive incomplete cooking or subminimal pasteurization treatments; and ability to survive in biofilms on equipment in food processing plants and resist superficial cleaning and disinfection treatments. 206

Approximately 3%–10% of humans carry listeriae in their gastrointestinal tract with no symptoms of illness. 214 Human listeriosis is an uncommon illness with a high mortality rate. The infection most frequently occurs in people who are older, pregnant, or possess a compromised immune system. Clinical manifestations range from mild influenza-like symptoms to meningitis and meningoencephalitis. Pregnant females infected with the pathogen may not present symptoms of illness or may exhibit only mild influenza-like symptoms. However, spontaneous abortion, premature birth, and stillbirth are frequent sequelae to listeriosis in pregnant females. 213 Although the infective dose of L. monocytogenes is not known, published reports indicate that it is likely to be more than 100 CFU per gram of food. 213 However, the infective dose largely depends on the age, condition of health, and immunological status of the host.

L. monocytogenes crosses the intestinal barrier in hosts infected by the oral route. However, before reaching the intestine, the bacterium must withstand the adverse environment of the stomach. Gastric acidity may destroy a significant number of L. monocytogenes ingested with contaminated food. The site at which intestinal translocation of L. monocytogenes occurs is not clearly elucidated. However, both epithelial cells and M cells in the Peyer’s patches are believed to be the potential sites of entry. 215 The bacteria are then internalized by macrophages where they survive and replicate. This is followed by the transport of the pathogen via blood to the mesenteric lymph nodes, spleen, and the liver. The primary site of L. monocytogenes replication in the liver is the hepatocyte. In the initial phase of infection, the infected hepatocytes are the target for neutrophils and subsequently for mononuclear phagocytes, which aid the control and resolution of the infection. 213 If the immune system fails to contain L. monocytogenes, subsequent propagation of pathogen via blood to the brain or uterus takes place. 216 The major virulence factors in L. monocytogenes include hemolysin, phospholipases, metalloprotease, Clp proteases and ATPases, internalins, surface protein p104, protein p60, listeriolysin O, and the surface protein ActA. 213

Staphylococcus aureus

Recent epidemiologic estimates indicate 241,000 cases of S. aureus-related illnesses, resulting in 1,064 hospitalizations and 6 deaths annually in the United States, which account for a loss of $130 million. 3 Preformed, heat-stable enterotoxin that can resist boiling for several minutes is the agent responsible for staphylococcal food poisoning. Among these, enterotoxin A is the most common cause of food poisoning episodes. 217 Humans are the principal reservoir of S. aureus strains involved in outbreaks of foodborne illness. In addition, a recent study revealed that S. aureus can be transmitted between healthy, lactating mothers without mastitis and their infants by breastfeeding. 218 Colonized humans can be long-term carriers of S. aureus and thereby contaminate foods and other humans. 219 The organism commonly resides in the throat and nasal cavity and on the skin, especially in boils and carbuncles. 219 Staphylococcal protein A (Spa) typing and DNA microarray have revealed striking similarities between the nasal isolates of food handlers and isolates involved in outbreaks. 220 Protein-rich foods such as ham, poultry, fish, dairy products, custards, cream-filled bakery products, and salads containing cooked meat, chicken, and potatoes are the vehicles most frequently associated with S. aureus food poisoning. 221 Additionally, other food vehicles, including hamburgers, milk, pasta salad, and raw milk cheese, have been implicated in S. aureus food poisoning. 222 S. aureus is usually overgrown by competing bacterial flora in raw foods; hence, raw foods are not typical vehicles of staphylococcal food poisoning. Cooking eliminates most of the normal bacterial flora of raw foods, thereby enabling the growth of S. aureus, which can be introduced by infected cooks and food handlers into foods after cooking. The incubation period of staphylococcal food poisoning is very short, with symptoms being observed within 2–6 h after eating toxin-contaminated food. Symptoms include nausea, vomiting, diarrhea, and abdominal pain.

S. aureus can grow within a wide range of pH values from 4 to 9.3, with optimum growth occurring at pH 6–7. S. aureus has an exceptional tolerance to sodium chloride, being able to grow in foods in the presence of 7%–10% NaCl, with some strains tolerating up to 20% NaCl. 221 S. aureus has the unique ability to grow at a water activity as low as 0.83–0.86. 223 S. aureus produces nine different enterotoxins, which are quite heat resistant, losing their serological activity at 121°C but not at 100°C for several minutes. 223

Besides being a foodborne pathogen, S. aureus has emerged as an important pathogen in nosocomial infections and community-acquired diseases, because of its toxin-mediated virulence, invasiveness, and antibiotic resistance. 224 This is especially significant due to the emergence of methicillin-resistant strains of S. aureus (MRSA), and 50% of health-care-acquired S. aureus isolates in the United States in 1997 were methicillin resistant. 225 Although MRSA are commonly linked to nosocomial infections, the first report of MRSA-associated foodborne disease in a community was reported in 2002. 225 The community-acquired MRSA are particularly virulent, resulting in tissue destructing infections, necrotizing fasciitis, and fulminant pneumonia, and this is attributed to a factor called Panton–Valentine leukocidin (PVL). 226 In addition, the gene responsible for methicillin resistance, mecA, encodes a low-affinity penicillin-binding protein called PBP2a that confers resistance to not only methicillin but also to the entire class of β-lactam antibiotics such as cephalosporins, penicillins, and carbapenems. 226 Some clones of MRSA are colonizers of the pig intestinal tract, and recent reports reveal that pig-to-human transmission is possible, highlighting its zoonotic potential. 227 , 228 Researchers have observed an expanding spectrum of antibiotic resistance in MRSA, with emerging linezolid resistance in MRSA strains. 229

Clostridium botulinum

Foodborne botulism is an intoxication caused by ingestion of foods containing preformed botulinal toxin, a 150 kDa metalloprotease produced by C. botulinum under anaerobic conditions. Botulinal toxin is a neurotoxin, which causes the neuroparalytic disease called botulism. The genes encoding botulinum toxins and other related proteins are located together in a cluster found on the C. botulinum chromosome or plasmid. There are two conserved cluster types in C. botulinum: the “ha cluster” and the “orf-X cluster.” 230 The toxin binds irreversibly to the presynaptic nerve endings of the nervous system, where it inhibits the release of acetylcholine. Unlike botulism in adults, infant botulism results from the colonization and germination of C. botulinum spores in the infant’s gastrointestinal tract. The disease usually happens in infants during the second month of age and is characterized by constipation, poor feeding or sucking, and decreased muscle tone with a “floppy” head. 231 Although the source of infection is unknown in majority of the cases, most commonly suspected food in infant botulism is honey. 232

There are seven types of C. botulinum (A, B, C, D, E, F, and G) classified on the basis of the antigenic specificity of the neurotoxin they produce. 233 The organism is present in soil, vegetation, and sedimentation under water. Type A strains are proteolytic, whereas type E strains are nonproteolytic. 234 Another classification divides C. botulinum into four groups: group 1 (type A strains and proteolytic strains of types B and F), group II (type E strains and nonproteolytic strains of B and F), group III (type C and D strains), and group IV (type G strains). The association of C. botulinum types I–III in disease outbreaks in cattle has raised concerns regarding the potential transmission of the toxin to humans via dairy products. 235

Type A C. botulinum occurs frequently in soils of the western United States, whereas type B strains are more often present in the eastern states and in Europe. 234 Type E strains are largely associated with aquatic environments and fish. Type A cases of botulism in the United States are frequently associated with temperature-abused, home-prepared foods. Proteolytic type A, B, and F strains produce heat-resistant spores, which pose a safety concern in low-acid canned foods. In contrast, nonproteolytic type B, E, and F strains produce heat-labile spores, which are of concern in pasteurized or unheated foods. 234 The minimum pH for growth of group I and group II strains is 4.6 and 5, respectively. 233 Group I strains can grow at a minimum water activity of 0.94, whereas group II strains do not grow below a water activity of 0.97. 236 The proteolytic strains of C. botulinum are generally more resistant to heat than nonproteolytic strains.

Types of foods associated with cases of botulism include fish, meat, honey, soup, chilli sauce, baked potato, sausage, tofu, and home-canned vegetables. 230 , 233 , 237 Several other vehicles such as poultry litter, water, water fowls, silage, brewer’s grain, bakery waste, and cat and cattle carcasses have also been implicated in botulism outbreaks during the past three decades. 235 In September 2011, two cases of botulism were associated with ground green olive paste in France. 238

Clostridium perfringens

C. perfringens is a major bacterial cause of foodborne disease, with 1062 cases reported in the United States in 2004. 8 C. perfringens strains are grouped into five types: A, B, C, D, and E, based on the type(s) of toxin(s) produced. C. perfringens foodborne illness is almost exclusively associated with type A isolates of C. perfringens that carry the plasmid-borne C. perfringens enterotoxin (cpe) gene. 239 This toxin type causes gangrene in humans and severe enteric disease in humans and animals. 240 C. perfringens is commonly present in soil, dust, water, and in the intestinal tract of humans, animals, and birds. 241 It is frequently present in foods; about 50% of raw or frozen meat and poultry contain C. perfringens. 242 Spores produced by C. perfringens are quite heat resistant and can survive boiling for up to 1 h. 242 C. perfringens spores can survive in cooked foods, and if not properly cooled before refrigerated storage, the spores will germinate and vegetative cells can grow to large populations during holding at growth temperatures. Large populations of C. perfringens cells (>106/g) ingested with contaminated food will enter the small intestine, multiply, and sporulate. During sporulation in the small intestine, C. perfringens enterotoxin is produced, which induces a diarrheal response. The enterotoxin is a 35 kDa heat-labile polypeptide that damages the epithelial cells of the gastrointestinal tract to cause fluid and electrolyte loss. 243 , 244 Although vegetative cells of C. perfringens are sensitive to cold temperature and freezing, spores tolerate cold temperature well and can survive in refrigerated foods.

Clostridium difficile

Clostridium difficile is a major cause of enteric disease in humans, and recent evidence indicates that it has emerged into a community-associated pathogen. C. difficile has been isolated from the intestinal tract of many food animals, 245 , 246 and several small-scale studies conducted in different parts of the world have revealed the presence of C. difficile in retail meat and meat products. 247 , 248 This has raised concerns that foods could potentially be involved in the transmission of C. difficile to humans.

C. difficile is a gram-positive, spore-forming, anaerobic bacterium, which causes a toxin-mediated enteric disease in humans. 249 The total annual number of cases of C. difficile infection in the United States is estimated to exceed 250,000, 250 resulting in approximately U.S. $1 billion annually in health-care costs. Among patients diagnosed with C. difficile infection, relapse or reinfection occurs in 12%–24% within 2 months. 251 Moreover, the mortality rates of disease associated with C. difficile in the United States have increased from 5.7 per million to 23.7 per million from 1999 to 2004, respectively. 252 The symptoms in C. difficile disease include abdominal pain, fever, fulminant colitis, toxic megacolon (bowel perforation), sepsis, and shock. 245 In addition, asymptomatic colonization of C. difficile causing mild diarrhea has been reported in some patients. C. difficile infection has been associated with the use of gastric acid-suppressing agents and antibiotics, which result in the germination of spores in the stomach and selection for C. difficile in the intestine. 253

Historically, C. difficile was considered a nosocomial pathogen that mainly affected the elderly, the severely ill, and the long-term hospital inpatients. 254 However, recently some changes in the epidemiology of C. difficile have been reported. For example, an increase in community-acquired C. difficile-associated disease (CDAD) has been reported, especially in populations that were not previously considered at risk of infection. 254 Another change in the epidemiology of C. difficile is that an increase in morbidity, mortality, and relapse rate in infections has been reported in the United States and elsewhere, which is attributed to the emergence and dissemination of a new hypervirulent strain, classified as North American Pulse type 1(NAP 1) using pulsed-field gel electrophoresis. 245 , 249 The strain belongs to the toxin type III and ribotype 027. 255 Emerging antimicrobial resistance in C. difficile has been reported by many investigators, especially resistance to fluoroquinolones, clindamycin and erythromycin, metronidazole, vancomycin, gatifloxacin, and moxifloxacin. 256

The major virulence factors of C. difficile include two large toxins, namely, toxin A (TcdA, enterotoxin) and toxin B (TcdB, cytotoxin). 257 In addition, a third toxin called C. difficile binary toxin (CDT) has been detected in some strains of the pathogen. 258 TcdA and TcdB are encoded by two genes present in a single operon and are highly expressed during late log and stationary phases of growth upon exposure to environmental stimuli. 259 The binary toxin was detected in approximately 6% of clinical C. difficile isolates obtained from the United States and Europe, 260 and an increase in the prevalence of binary toxin-producing C. difficile strains has been reported during the last decade. 255 , 261

The common means of contracting C. difficile infection in humans is via the fecal–oral route. The bacterium is ingested in the vegetative form or as spores, which can persist for long periods in the environment and overcome the acidity in the stomach. In the intestine, C. difficile spores germinate into the vegetative form, especially if the normal flora has been disrupted by antibiotic therapy. C. difficile multiplies in the intestinal crypts, releasing the A and B toxins, causing severe inflammation and disruption of intestinal epithelial cells, thereby leading to colitis, pseudomembrane formation, and watery diarrhea. 251

Recent studies conducted worldwide have revealed the occurrence of C. difficile in a variety of food animals. 246 , 262 Pigs and calves are among the most common reservoirs of C. difficile. Apart from animals serving as reservoirs, foods such as ground beef, ground veal, veal chops, retail chicken (thighs, wings, and legs), raw milk, summer sausage, ground pork, ground turkey, braunschweiger, water, and raw vegetable samples have been identified as potential vehicles of C. difficile. 247 , 248 , 263

Bacillus cereus

B. cereus is a spore-forming pathogen present in soil and on vegetation. It is responsible for an increasing number of foodborne diseases in industrial countries, 264 with 103 outbreak-associated confirmed cases reported in the United States in 2004. 8 It is reported as the fourth largest cause of foodborne disease in the European Union. 265 It is frequently isolated from foods such as meat, spices, vegetables, dairy products, and cereal grains, especially fried rice. 266 There are two types of foodborne illness caused by B. cereus, i.e., a diarrheagenic illness and an emetic syndrome. 264 , 267 The diarrheal syndrome caused by heat-labile enterotoxins is usually mild and is characterized by abdominal cramps, nausea, and watery stools similar to that observed in C. perfringens infection. 268 Types of foods implicated in outbreaks of diarrheal syndrome include cereal food products containing corn and corn starch, mashed potatoes, vegetables, milk, and cooked meat products. The emetic syndrome is caused by a heat-stable dodecadepsipeptide toxin called cereulide that is produced in food 264 and is characterized by severe vomiting. The clinical symptoms are similar to those observed in S. aureus poisoning. 269 Refried or rewarmed boiled rice, pasta, noodles, ice cream, and pastry are frequently implicated in outbreaks of emetic syndrome. 270 , 271 The dose of B. cereus required to produce diarrheal illness is estimated at more than 105 cells/g. 272 The toxin-induced pathogenicity of B. cereus is regulated by a pleiotropic transcriptional activator, PlcR, that controls the production of enterotoxins—hemolytic Hbl and nonhemolytic Nhe—and the cytotoxin CytK. 273 , 274

Arcobacter butzleri

Arcobacter species belong to the family of Campylobacteraceae and occur primarily as commensals in the gut of animals and humans. 275 Arcobacters are Gram-negative, aerotolerant Campylobacter-like organisms that can grow under microaerobic conditions. 276 There are 13 species of Arcobacter, of which A. butzleri, A. cryaerophilus, and A. skirrowii are of public health importance. 277 They can grow at 25°C, a differentiating feature from Campylobacter, and can hydrolyze indoxyl acetate and reduce nitrate. 278 Although Arcobacter can grow at a range of 15°C–37°C, the optimum temperature for growth is 30°C. 279 Among the arcobacters, A. butzleri is most commonly associated with human enteritis, characterized by persistent and watery diarrhea, vomiting, nausea, and fever. 280 A. butzleri strains resistant to antibiotics such as clindamycin, ciprofloxacin, metronidazole, carbenicillin, cefoperazone, nalidixic acid, and azithromycin have been reported. 277

A. butzleri is the most common Arcobacter isolated from livestock species. There is mounting evidence that arcobacters in general, and A. butzleri in particular, are efficient colonizers in healthy swine, sheep, horses, and cattle, 281 with poultry being the most significant reservoir. However, there are conflicting reports on the pathogen’s role as a commensal in the chicken intestinal tract. 282 Humans may contract Arcobacter infection via consumption of contaminated food of animal origin and water, 277 although this is not fully understood. 280 Recent reports have revealed that the pathogen has been isolated from raw beef, pork, and chicken, of which the rate of isolation from chicken was greater compared to others. The prevalence of A. butzleri on broiler carcasses suggests its presence in poultry abattoirs, and that contamination could be processing associated. 283 In addition, A. butzleri has been isolated from several water sources, including ground-water, seawater, bays, surface water, and raw sewage. 275 More importantly, the pathogen has been isolated from well water, water treatment plants, and other sources of water storage. 276 It has also been observed that A. butzleri can attach to stainless steel, copper, and plastic pipelines 276 that carry water indicating its adherence potential on abiotic surfaces.

Little information is known regarding the virulence mechanisms by which A. butzleri infects humans and animals. However, it has been determined that A. butzleri is highly adherent, invasive, and cytotoxic to cell cultures. A. butzleri is the most invasive species among the arcobacters 284 based on its ability to colonize piglet intestines, although variable results on colonization of chicken and turkeys were observed.

Brucella Species

Brucella spp. are pathogens in many animals, causing sterility and abortion. In humans, Brucella is the etiologic agent of undulant fever. The genus Brucella consists of six species, of which those of principal concern are B. abortus, B. suis, and B. melitensis. 285 B. abortus causes disease in cattle and B. suis in swine, and B. melitensis is the primary pathogen of sheep. B. melitensis is the most pathogenic species for humans. Human brucellosis is primarily an occupational disease of veterinarians and meat industry workers. Brucellosis can be transmitted by aerosols and dust. Foodborne brucellosis can be transmitted to humans by consumption of meat and milk products from infected farm animals. The most common food vehicle of brucellosis for humans is unpasteurized milk. 285 Meat is a less common source of foodborne brucellosis because the organisms are destroyed by cooking. Since the National Brucellosis Education program has almost eradicated B. abortus infection from U.S. cattle herds, the risk of foodborne infection of brucellosis through consumption of domestically produced milk and dairy products is minimal. 103

Helicobacter pylori

H. pylori is a human pathogen causing chronic gastritis, gastric ulcer, and gastric carcinoma. 286 , 287 Once colonized in humans, the pathogen could be the predominant species present in the stomach. The infection is mostly acquired early in life (<10 years of age). 288 Although humans are the primary host of H. pylori, the bacterium has been isolated from cats. 212 H. pylori does not survive well outside its host, but it has been detected in water and vegetables. 289 , 290 A study on the effect of environmental and substrate factors on the growth of H. pylori indicated that the pathogen likely lacks the ability to grow in most foods. 291 However, H. pylori may survive for long periods in low-acid environments under refrigerated conditions. H. pylori infections spread primarily by person-to-person transmission, especially among children, and contaminated water and food are considered potential vehicles of the pathogen. In the United States, a significant association between H. pylori infection and iron-deficiency anemia, regardless of the presence or absence of peptic ulcer, has been reported. 292 , 293

Viral Foodborne Pathogens

Estimates by the CDC of the incidence of foodborne illness in the United States indicate that viruses are responsible for approximately 67% of the total foodborne illnesses of known etiology annually (Table 3.2). 204 Viruses are obligate intra-cellular microorganisms and most foodborne viruses contain RNA rather than DNA. Since viruses are intracellular organisms requiring a host for multiplication, they cannot grow in foods. Therefore, the number of virus particles on foods will not increase during processing, transport, or storage, causing no deterioration in food quality. 294 Foodborne viruses are generally enteric in nature, causing illness through ingestion of foods and water contaminated with human feces (fecal– oral route). Viruses disseminated through foods also can be spread by person-to-person contact. For example, research with hepatitis A virus has revealed that a few hundred virus particles can readily be transferred from fecally contaminated fingers to foods and surfaces. 295 Fresh produce and shellfish are generally common sources of viral contamination and thus considered as high-risk foods. 296 Hepatitis A virus, norovirus (previously known as Norwalk-like viruses), and possibly rotavirus are among the most significant of the viruses that are foodborne.

Hepatitis A Virus

Hepatitis A virus is a member of the family Picornaviridae and is transmitted by the fecal–oral route. Raw shellfish harvested from waters contaminated by human sewage is among the foods most frequently associated with outbreaks of hepatitis A virus. 297 Besides shellfish, other foods including sandwiches, dairy products, baked products, salads, fruits, and vegetables have also been implicated in various outbreaks of hepatitis A virus. 298 , 299 A large outbreak in Pennsylvania in 2003 involving more than 500 cases was linked to ingestion of contaminated green onions. 300 Hepatitis A virus is more resistant to heat and drying than other picornaviruses. 297 The incubation period for onset of symptoms of hepatitis A infection ranges from 15 to 45 days, and symptoms include nausea, abdominal pain, jaundice, and fever. The virus is shed in feces by infected humans many days before the onset of symptoms, indicating the importance of good personal hygienic practices of cooks and food handlers who could otherwise contaminate food during the period of asymptomatic fecal shedding. The overall incidence of hepatitis A virus in the United States has decreased since the implementation of routine childhood vaccination against the virus in 1996. 104 In 2007, the CDC reported that the incidence of hepatitis A infections was at their lowest level. 301

Norovirus

Norovirus belongs to the family Caliciviridae and is often referred to as small, round-structured viruses. Norovirus is recognized as the most common viral cause of foodborne and waterborne acute gastroenteritis in the United States. 1 The virus possesses a low infectious doze of less than 100 virus particles. 302 Raw or undercooked shellfish and other seafoods are common vehicles of norovirus. The incubation period of infection ranges from 24 to 48 h, and symptoms include nausea, vomiting, and diarrhea. The young, immunocompromised, and elderly are considered to be at greatest risk of developing severe illness caused by the pathogen. 303 Infected humans shed the virus in feces for up to a week after symptoms have subsided. The virus survives freezing, heating to 60°C, and chlorine levels up to 10 ppm. 302 Qualitative studies in human volunteers indicate that the viruses are infective for up to 3 h when exposed to a medium at pH 2.2 at room temperature or for 60 min at pH 7 at 60°C. 304

The impact of norovirus on the U.S. economy is large. A recent study revealed that the virus causes an estimated 5 million cases, resulting in 14,663 hospitalizations and 149 deaths, which accounts for a loss of $2.8 billion. 3 In 2009, the United States launched CaliciNet, an outbreak surveillance network for noroviruses. Of 558 norovirus outbreaks submitted to the CaliciNet since 2009, 14% were associated with foodborne transmission. Of the five genogroups (GI–GV), GI and GII were the most common affecting humans. The genogroup GII has 19 genotypes, of which GII.4 caused more than 85% of the norovirus outbreaks. A GII.4 variant called GII.4 New Orleans emerged as the major disease-causing genotype in October 2009, replacing another variant, GII.4 Minerva, that was the common outbreak strain since 2005. 305

Rotavirus

Rotavirus is a nonenveloped, double-shelled virus, with a genome comprised of 11 segments of double-stranded RNA. It is characterized by two surface-expressed neutralizing antigens, a glycosylated outer surface protein (G protein) encoded by the VP7 gene and a protease-cleaved protein (P protein) encoded by the VP4 gene. Rotavirus is the most common cause of diarrhea in children worldwide, especially in developing countries. In the United States and other countries with a temperate climate, infection with rotavirus has been reported to peak during the winter season (November to April). In the United States, there are an estimated 3.9 million cases of rotavirus diarrhea each year; however, only 39,000 cases are estimated to be acquired through contaminated foods. 204 Rotavirus infection has an incubation period of 1–3 days and is characterized by fever, vomiting, and diarrhea. The virus is shed in the feces of infected humans and can survive on vegetables at 4°C or 20°C for many days. 306 It has also been shown to survive the process of making soft cheese. 306 The primary mode of transmission of rotavirus is by fecal-to-oral route. In early 2006, the U.S. Food and Drug Administration approved a new live, oral vaccine (RotaTeq™) for the prevention of rotavirus gastroenteritis in infants. This pentavalent vaccine expresses five different genotypes of the virus, namely, G1, G2, G3, G4, and, the most common P-type, P1A. During the surveillance periods 2005–2006 and 2006–2007, G1 was predominant, and during 2007–2008, G3 replaced G1. Currently monitoring of strains for any possible vaccine-pressure-induced changes is underway. Another live attenuated rotavirus vaccine based on genotype G1P, Rotarix, is currently approved for use in the United States. 307

Table 3.2   Viral Foodborne Pathogens

Microorganism

Significant Characteristics

Sources/Reservoirs

Examples of Vehicles

Estimated No. of Foodborne Cases Annually in the United States 2 , 3

Incubation Period, Symptoms, and Duration

Detection Methods

Control/Prevention

Hepatitis A virus

Single-stranded RNA virus, spherical in shape, remains viable for long periods of time in foods stored at refrigeration temperature; virus multiplies in the gut epithelium before being carried by blood to the liver. Virus is shed in feces before symptoms of liver damage become apparent.

Humans, sewage-polluted waters

Raw or undercooked shellfish and seafoods harvested from sewage-polluted water, ready-to-eat foods such as salads prepared by infected food handler

1,566

15-45 days, usually ca. 25 days.

Loss of appetite, nausea, abdominal pain, fever, jaundice, dark urine, pale stools.

Duration is a few weeks to months.

Cultural methods 592 , 593

Enzyme immunoassay 594

PCR 595 - 598

LAMP assay 599

Immunochromatography assay 600

Avoid consumption of raw seafoods; disinfection of drinking water, good personal hygiene and food handling practices, vaccination of professional food handlers, safe sewage disposal

Norovirus

Single-stranded RNA virus, spherical in shape, does not multiply in any known laboratory host.

Humans, sewage-polluted waters

Raw or undercooked shellfish and seafoods harvested from sewage-polluted water, drinking water

5,461,731

1-2 days.

Loss of appetite, nausea, abdominal pain, diarrhea, vomiting, headache.

Duration is 2 days.

Enzyme immunoassay 601 , 602

PCR 603 - 607

Latex agglutination test 608

Third-generation ELISA coupled with immunochromatography 609

DNA microarray 610

Avoid consumption of raw seafoods, disinfection of drinking water, good personal hygiene and food handling practices, hygienic sewage disposal, treatment of wastewater used for irrigation

Rotavirus

Double-stranded RNA virus, icosahedral in shape.

Humans

To be determined

15,433

1-3 days.

Vomiting, abdominal pain followed by watery diarrhea.

Duration is 6-8 days.

Cultural methods 592 , 593

ELISA 611 , 612

PCR 612 - 615

Flow cytometry 310 , 616

Immunobiosensor 617

Avoid consumption of raw seafoods

Avoid drinking of untreated water

Good personal hygiene

Avian influenza virus

Single-stranded RNA virus, medium sized, pleomorphic, enveloped.

Chicken, turkey, guinea fowl, and migratory waterfowl

Raw or undercooked contaminated egg and poultry meat

Emerging disease

Not reported in the United States

132 cases worldwide (1997-2005)

Typical flu symptoms such as fever, cough, sore throat, and muscle aches. Also eye infections (conjunctivitis), pneumonia, and acute respiratory distress can be present.

Cultural method 310

Rapid antigen detection test 618

PCR 310 , 619 , 620

Serological test 310

Resequencing microarray 621

Avoid consumption of raw or undercooked poultry meat and egg

Avoid using raw eggs for preparing foods that are not cooked

Avoid handling and slaughtering of infected birds or birds suspected of infection

Use hygienic practices during slaughter and postslaughter operations

Avian Influenza Virus

Avian influenza (bird flu) is a highly contagious viral infection affecting a wide species of birds, including chicken, turkey, guinea fowl, and migratory waterfowl. The disease is of tremendous economic significance to the poultry industry. Recent outbreaks of avian influenza infections in poultry and humans highlight the zoonotic potential of the disease and its impact on public health. 308 During the period from 1997 to 2005, 132 human cases of avian influenza with 64 deaths have been reported worldwide. 309 Based on virulence, avian influenza virus can be classified into the highly pathogenic avian influenza (HPAI) strains that cause a systemic lethal infection, resulting in death of birds as early as 24 h to 1 week postinfection, and the low pathogenic avian influenza (LPAI) viruses that rarely result in fatal disease in birds. 284 The HPAI viruses that cause “fowl plague” are restricted to the subtypes H5 and H7; however, all the viruses of these subtypes do not cause HPAI. H5N1 is the influenza A virus subtype that occurs mainly in birds, causing fatal disease in birds.

Avian influenza viruses, belonging to the family Orthomyxoviridae, are medium-sized, pleomorphic, enveloped viruses with glycoprotein projections from the envelope having hemagglutinating (HA) and neuraminidase (NA) activities. 310 The genome of the virus consists of eight segments of single-stranded RNA of a negative sense, which code for ten viral proteins. Antigenically, three distinct types of influenza viruses are reported, namely, type A, type B, and type C, with the former type causing natural infections in birds. Based on the antigenic properties of hemagglutinin and neuraminidase surface glyco-proteins, type A influenza viruses are divided into various subtypes. 311 Currently, 15 HA and 9 NA subtypes have been reported. 284 The ability of these viruses to transform by recombination and assortment enables them to adapt to new hosts, including humans.

The hemagglutinin glycoproteins play a vital role in the pathogenicity by mediating attachment of the virus to host cell receptors followed by release of viral RNA. 308 The HA glycoprotein precursor (HA0) is posttranslationally cleaved into HA1 and HA2 subunits by host proteases, with the HA2 amino terminus mediating fusion between the viral envelope and the endosomal membrane. 312 Klenk et al. 313 reported that proteolytic activation of HA glycoprotein is essential for viral infectivity and dissemination, thus highlighting its role in the pathogenesis of avian influenza virus. The HA precursor proteins of LPAI viruses have a single arginine at the cleavage site; hence, these viruses are limited to cleavage by host proteases such as trypsin-like enzymes. Therefore, replication of LPAI viruses is limited to sites (organs) where such enzymes are found (respiratory and intestinal tracts), thereby resulting in mild infections. However, the HAs of HPAI viruses contain multiple basic amino acids at the cleavage site, which are cleaved by ubiquitous proteases present in a variety of host cells. These viruses therefore are able to replicate throughout the bird, causing lethal systemic infection and death. 314 , 315

The source of infection to poultry in most outbreaks is direct or indirect contact with waterbirds. Once the infection is established in birds, the disease is highly contagious. Fecal-to-oral transmission is the most common mode of spread between birds. Contact with infected material is the most important mode of transmission from bird to bird. In infected birds, the virus is excreted in the droppings and nasal and ocular discharges. Fecal shedding of the virus by infected birds has been documented up to 4 weeks postinfection. Contaminated feed, water, rodents, and insects can also play a role in the spread of virus. Movement of infected birds, contaminated equipment, egg flats, feed truck, and service crew can also spread the virus from flock to flock. Airborne transmission of the virus can potentially occur if birds are kept in close proximity and with air movement. Since lesions have been reported in the ovaries and oviducts of infected egg-laying chickens, avian influenza virus could potentially be transmitted via the egg either through virus in the internal egg contents or on the surface from virus-infected feces. 316 This could potentially lead to hatching of infected chicks and contamination of the hatchery. Implementation of strict biosecurity measures can greatly reduce the risk of secondary spread after an initial outbreak.

Although humans can contract avian influenza virus by handling and slaughtering of infected birds, there is no epidemiologic evidence to suggest transmission of the virus by consumption of properly cooked eggs or other cooked poultry products derived from infected birds. Cooking poultry meat to 160°F (71°C) inactivates the virus. 309 Consumption of raw or partially cooked eggs (runny yolk) or foods containing raw eggs should be avoided. Avian influenza viruses remain viable in contaminated poultry meat and potentially spread through the marketing and distribution of contaminated fresh or frozen poultry meat.

In addition to birds, swine can serve as a critical animal reservoir for the emergence of new influenza A viruses because swine can be infected by both human and avian influenza viruses. For example, the classical H1N1 swine influenza viruses were very similar to the human pandemic influenza isolates of 1918. Moreover, human-associated H3N2 viruses were isolated from pigs shortly after they were identified as disease-causing agents in humans. 317

Fungal Foodborne Pathogens

Molds are widely distributed in nature and are an integral part of the microflora of foods. Although molds are major spoilage agents of many foods, many molds also produce mycotoxins of which some are carcinogenic and mutagenic (Table 3.3). Mycotoxins are secondary metabolites produced by molds usually at the end of their exponential phase of growth. Some of the principal species of molds, which produce mycotoxins in foods, include the following.

Table 3.3   Fungal Foodborne Pathogens

Microorganism/Toxin

Significant Characteristics

Sources/Reservoirs of Fungi

Examples of Vehicles of Toxins

Toxic Effects

Detection Methods

Control/Prevention

A. parasiticus and A. flavus/aflatoxin

Growth at 10°C-43°C, optimal growth at 32°C, produces aflatoxins at 12°C-40°C, growth at pH 3-11

Environment, soil, vegetation

Corn, peanuts, cottonseed

Effects of aflatoxin in animals:

Acute: hemorrhage in the gastrointestinal tract, liver damage, death

Chronic: cirrhosis of liver, liver tumors, immunosuppression

Cultural methods 330 , 622 - 624

ELISA 625

Immunoassay 626 , 627

PCR 628 - 632

Functionalized-gold nanoparticles 633

Enzyme-linked-immunomagnetic-electrochemical array 634

Near-infrared spectroscopy 635

Monoclonal antibody-based ELISA 636

Electrochemical immunosensor 637

Antibody-based microarray 638

Proper storage of cereal products, detoxification of mycotoxins in cereal products by treatment with hydrogen peroxide, ammonia

P. expansum/patulin, P. citrinum/citrinin

P. expansum is psychrotrophic, capable of growth at −2°C - -3°C and optimal growth at 25°C,

Environment, soil, vegetation

P. expansum: Fruits, especially apples and pears

P. citrinum: Cereals, especially rice, wheat, corn

Effects of patulin:

Gastrointestinal, neurological immunological effects in animals

Citrinin:

Fatty degeneration and renal necrosis in pigs and dogs; significance in human health is unresolved

Cultural methods 330 , 623 , 639

PCR 640 - 642

Detection of mycotoxin by HPLC 643 , 644

mass spectrometry 645

Competitive fluorescence assay 646

ELISA 647

Avoid consumption of rotten apples and pears, proper storage of cereal products

F. graminearuml deoxynivalenol, nivalenol, zearalenone

Growth at 5°C but not at 37°C, optimal growth at 25°C

Environment, soil, vegetation

Cereals, especially wheat, barley, corn

Effects of deoxynivalenol: nausea, vomiting, abdominal pain, diarrhea, headache, fever, chills, throat irritation

Cultural methods followed by morphology 648 , 649

PCR 642 , 650 - 654

Immunoassay 655

ELISA 656

LAMP assay 657

Proper storage of cereal products

Aspergillus Species

A. flavus and A. parasiticus are the most important toxigenic foodborne aspergilli. A wide variety of foods such as nuts, corn, oil seeds, and sorghum are potential vehicles of these aspergilli. Aspergillus species can cause disease in animals and humans by infection (aspergillosis) or by toxin production (aflatoxicosis). A. flavus and A. parasiticus produce aflatoxins, which are difuranocoumarin derivatives. 318 The common types of aflatoxins that are produced are B1, B2, G1, and G2. 319 In addition, two other types of aflatoxins, namely, M1 and M2, have also been reported as contaminants in food and feeds. Aflatoxicosis in animals can be acute or chronic. Acute cases are characterized by severe liver damage, whereas liver cirrhosis, liver cancer, and teratogenesis occur in chronic toxicity. Chronic intake of aflatoxins in animals can lead to poor feed conversion and low weight gain. Although fungal toxins cause an estimated economic loss of $1 billion in the United States, most of this is from aflatoxin contamination. The FDA has regulated the concentration of aflatoxin in the milk at not more than 0.5 and 20 ppb in crops. 320 Several outbreaks associated with aflatoxin consumption by humans have been recorded in developing countries. 320 322

In humans, aflatoxins have been reported to cause hepatic cancer. A significant correlation between aflatoxin exposure and stunted growth has been reported in children exposed to aflatoxin during neonatal stages. 323 Additionally, since aflatoxins can cross the placental barrier, they can potentially lead to genetic defects in the fetus. 324 Following intake, aflatoxins are metabolized into a variety of products such as aflatoxicol, aflatoxin Q1, aflatoxin P1, and aflatoxin M1 in the liver by cytochrome p450 group of enzymes. In addition, another metabolite called aflatoxin 8,9 epoxide can also be formed, which can induce mutations by forming DNA adducts, ultimately leading to hepatic carcinoma. 325 327 Susceptibility of a given species to aflatoxins depends on its liver detoxification systems, genetic makeup, age, and other nutritional factors. 328

Penicillium Species

The genus Penicillium consists of more than 150 species, of which nearly 100 produce known toxins. Three important foodborne toxigenic Penicillium species include P. verrucosum, P. expansum, and P. citrinum. P. verrucosum is present on grains grown in temperate zones and is commonly associated with Scandinavian barley and wheat. 329 P. verrucosum produces ochratoxin A, which has immunosuppressive and potential carcinogenic properties. 329 Ochratoxin A also has been associated with nephritis in pigs in Scandanavia. 330 Penicillium expansum, a psychrotrophic mold and one of the most common fruit pathogens, causes a condition known as “blue mold rot” on a variety of fruits, including apples, cherries, nectarines, and peaches. 331 334 Besides its economic impact, P. expansum is also of potential public health significance since it produces patulin, a mycotoxin known to cause immunological, neurological, and gastrointestinal toxic effects in animal models. 329 Exposure to high levels of patulin also results in vomiting, salivation, anorexia, polypnea, weight loss, leukocytosis, erythropenia, and necropsy lesions of hemorrhagic enteritis in piglets. 335 Although the toxic effects of patulin in humans have not been proven conclusively, the presence of patulin has been demonstrated in apple juice 336 and grape juice. 337 This is a major concern since fruit juices, especially apple juice, are commonly consumed by infants and children. P. expansum is commonly present in rotten apples and pears and to a lesser extent in cereals. Use of moldy fruits contaminated with P. expansum greatly increases the risk of patulin contamination in fruit juices. An unusual characteristic of P. expansum is its ability to grow at low temperature, i.e., −2°C to −3°C. 329

P. citrinin is a widely occurring mold commonly present on rice, wheat, and corn. P. citrinin produces the metabolite citrinin. Although the toxicological effect of citrinin in humans is not known, it has been reported to cause renal toxicity in pigs and cats. 338

Fusarium graminearum

F. graminearum is a toxigenic mold commonly present in soil and on cereals such as wheat and corn. It causes “head blight” of wheat and barley and “stalk and cob rot” of maize. The head blight condition resulted in an estimated $1 billion loss in 1993 alone and affected cereal farming in the United States significantly. 339 It produces a number of mycotoxins, including deoxynivalenol and zearalenone. 340 Cereals containing high levels of deoxynivalenol are unacceptable for human or animal consumption. Ingestion of foods containing deoxynivalenol produces illness termed scabby grain intoxication, which is characterized by anorexia, nausea, vomiting, diarrhea, dizziness, and convulsions. Foods most frequently implicated as vehicles of deoxynivalenol include cereal grains, wheat, barley, and noodles. Zearalenone, the other Fusarium toxin, is an estrogenic compound that causes sterility in animals. 341

Parasitic Foodborne Pathogens

Parasitic diseases account for 3% of foodborne illnesses and 21% of foodborne illness-related deaths in the United States (Table 3.4). 204 However, the actual number of parasitic diseases could be higher since they are often underdiagnosed and underreported in the United States. 341 Parasites constitute more of a food safety concern now than in the past because of the globalization of our food supply with growing imports of fruits, vegetables, and ethnic foods from countries, where the hygienic and quality control standards in food production may be suboptimal. Foods can be vehicles of several types of parasites, including protozoa, roundworms, and flatworms. Although foodborne transmission of parasites such as Trichinella spiralis and Taenia solium has been known for many years, the foodborne disease potential of many protozoan parasites such as Cryptosporidium and Cyclospora has only recently been recognized. Unlike bacteria, parasites do not multiply in foods. Moreover, parasites need at least one specific host to complete their life cycle. Many of the well-recognized parasites that can be transmitted to humans through foods include the following.

Table 3.4   Parasitic Foodborne Pathogens

Parasite

Significant Characteristics

Sources/Reservoirs

Vehicles

Estimated No. of Foodborne Cases Annually in the United States 2 , 3

Incubation Period, Symptoms, and Duration

Detection Methods

Control/Prevention

G. lamblia

Flagellate protozoa, produces oval-shaped cysts ranging from 8 to 20 μm in length and 5-12 μm in width; cysts contain four nuclei and are resistant to chlorination used to disinfect water

Humans, animals, especially beavers and muskrats, water

Drinking water, raw fruits and vegetables contaminated with cysts, ready-to-eat foods such as salads contaminated by infected food handlers

76,840

4-25 days, usually 7-10 days

Abdominal cramps, nausea, abdominal distension, diarrhea that can be chronic and relapsing, fatigue, weight loss, anorexia

Duration is weeks to years

Immuno-fluorescence 658

Immunochromatography 659 , 660

PCR 661 - 665

ELISA 666

Surface-enhanced resonance spectroscopy 667

Biosensors 668

Flow cytometry 669

Adequate cooking of foods, filtration of drinking water, good personal hygiene and food handling practices

E. histolytica

Amoeboid protozoa, anaerobe survives in environment in crypted form, cysts remain viable in feces for several days and in soil for at least 8 days at 30°C and for more than 1 month at 10°C, relatively resistant to chlorine

Humans, dogs, rats

Foods and water contaminated with feces or irrigation water

Unknown

2-4 weeks

Abdominal pain, fever, vomiting, diarrhea containing blood and mucus, weight loss

Duration is weeks to months

Microscopic examination

Line dot

hybridization assay 670

ELISA 671 , 672

PCR 663 , 673 , 674

LAMP assay 675

Good personal hygiene and food handling practices, adequate cooking of foods, filtration of water, hygienic disposal of sewage water, treatment of irrigation water

C. parvum

Obligate intracellular coccidian parasite; oocysts are spherical to oval in shape with an average size of 4.5-5.0 μm; oocysts are resistant to chlorination used to disinfect water

Humans, wild and domestic animals, especially calves

Contaminated drinking and recreational water, raw milk from infected cattle, fresh vegetables and other foods contaminated with feces from infected humans and animals

57,616

2-14 days

Profuse, watery diarrhea, abdominal pain, nausea, vomiting

Duration is few days to 3 weeks

Immunofluorescence assay 676

PCR 673 , 677 - 680

Rapid assay 681

Monoclonal antibody-based dot blot assay 682

Electrochemical-based enzyme-linked biosensor 683

Surface-enhanced resonance spectroscopy 667

Piezoelectric-excited millimeter-sized cantilever sensor 684

Thorough cooking of food, avoid contact with infected animals, filtration of drinking water, good personal hygiene and food handling practices

C. cayetanensis

Obligate intracellular coccidian parasite; oocysts are spherical in shape with an average size of 8-10 μm

Humans

Water, fruits, and vegetables contaminated with oocysts

11,407

1 week

Watery diarrhea, abdominal pain, nausea, vomiting, anorexia, myalgia, weight loss

Duration is a few days to 1 month

Staining and microscopic examination 671

Flow cytometry 685

PCR 686 - 689

Good personal hygiene, filtration of drinking water

T. gondii

Obligate intracellular coccidian protozoa

Cats, farm animals, transplacental transmission from infected mother to fetus

Raw or undercooked meat, raw goat milk, raw vegetables

86,686

5-23 days

Fever, rash, headache, muscle pain, swelling of lymph nodes; transplacental infection may cause abortion

Duration is variable

Cell culture and mouse inoculation 690

Immunoassay 691

Serological assay 692

Immunofluorescence 693

PCR 694 - 698

LAMP assay 699

Oligonucleotide microarray 700

Prevent environmental contamination with cat feces, avoid consumption of raw meat and milk, safe disposal of cat feces, wash hands after contact with cats

T. spiralis

Nematode with no free-living stage in the life cycle; adult female worms are 3-4 mm in length; transmissible form is larval cyst, which can occur in pork muscle

Wild and domestic animals, especially swine and horses

Raw or undercooked meat of animals containing encysted larvae such as swine or horses

156

Initial symptoms: 24-72 h

Systemic symptoms: 8-21 days

Initial phase:

Abdominal pain, fever, nausea, vomiting, diarrhea

Systemic phase:

Periorbital edema, eosinophilia, myalgia, difficulty in breathing, thirst, profuse sweating, chills, weakness, prostration

Duration is 2 weeks to 3 months

Microscopic examination

ELISA 701 , 702

Immunoassay 703

PCR 704 - 707

Adequate cooking of meat, freezing of meat at −15°C for 30 days or at −35°C, preventing trichinosis in pigs by not feeding swine garbage containing infected meat

Anisakis spp.

Nematode, slender threadlike parasite measuring 1.5-1.6 cm in length and 0.1 cm in diameter

Sea mammals

Some undercooked salt water fish, sushi, herring, sashimi, ceviche

Unknown

4-12 h

Epigastric pain, nausea, vomiting, sometimes hematemesis

Duration is variable

ELISA 708 , 709

Immunoblot 710

PCR 711 - 714

Fluorescence PCR 715

Adequate cooking of saltwater fish, freezing fish at −23°C for 7 days

T. solium T. saginata

Tapeworm, dependent on the digestive system of the host for nutrition

Humans, cattle, swine

Raw or undercooked beef or pork

Unknown

Few days to >10 years

Nausea, epigastric pain, nervousness, insomnia, anorexia, weight loss, digestive disturbances, weakness, dizziness

Duration is weeks to months

Detection of eggs or proglottids in feces

ELISA 716 , 717

PCR 718 - 720

Adequate cooking of beef and pork, proper disposal of sewage and human wastes, freezing of meat at −10°C for 2 weeks

D. latum

Largest human tapeworm

Saltwater fish, humans

Raw or undercooked saltwater fish

Unknown

Epigastric pain, nausea, abdominal pain, diarrhea, weakness, pernicious anemia

Duration is months to years

Detection of eggs in feces

Adequate cooking of fish, proper disposal of sewage and human waste

Giardia lamblia

Giardiasis is the most common parasitic infection reported in the United States, with 21,300 confirmed cases in 1997. 342 However, the numbers have significantly increased over 15 years. A recent study revealed 76,840 cases of Giardia lamblia infections causing 225 hospitalizations. 3 G. lamblia is a flagellated protozoan parasite that colonizes the intestinal tract of humans and animals. It is commonly present in lakes, rivers, and stagnated waters. The parasite has a very low infective dose, with about 25–100 cysts for causing infection. 343 The life cycle of G. lamblia includes flagellated trophozoites, which become pear-shaped cysts. 344 The cysts contaminate water or food through feces of infected animals or humans. Following ingestion of cyst-contaminated water or food, the trophozoites reach the small intestine where they undergo excystation and multiply by binary fission. New trophozoites subsequently become cysts in the distal small intestine, and the encysted trophozoites are shed in the feces. The symptoms of giardiasis include abdominal pain, abdominal distension, nausea, vomiting, and diarrhea. Although water and foods contaminated with cysts are primary vehicles of giardiasis, little is known about the survival characteristics of the cysts in foods. In most cases of foodborne transmission, infected food handlers transfer the cysts to foods they prepare. Humans can also contract giardiasis through the use of contaminated water for irrigating or washing fruits and vegetables. 345 Contaminated water was identified as the source of Giardia oocysts in several outbreaks of giardiasis from 1954–2001. 346

Entamoeba histolytica

E. histolytica is a protozoan parasite that causes amoebiasis or amoebic dysentery in humans. Although the parasite survives in the environment and water, humans are the principal source of amoebiasis. In humans, cysts containing the trophozoites are released, which in turn multiply, and are subsequently excreted in the feces as cysts. 278 Foods and water contaminated with the cysts transmit the disease. Since the fecal–oral route is the principal route of transmission of amoebiasis, personal hygiene of infected food handlers plays a critical role in preventing foodborne amoebiasis. Human amoebiasis can occur in two forms: intestinal amoebiasis and amoebic liver abscess, which is usually a sequel to the intestinal form. Intestinal amoebiasis is characterized by abdominal pain, vomiting, and watery diarrhea containing mucus and blood. Symptoms of the hepatic form of amoebiasis include wasting, painful and enlarged liver, weight loss, and anemia. Amoebiasis is a common cause of diarrhea in tropical and subtropical countries, and most cases in the United States are reported in immigrants and persons returning from endemic areas. 345

Cryptosporidium parvum

C. parvum is a protozoan parasite that infects a wide range of animals and humans. C. parvum is monoxenous in its life cycle, requiring only one host for its development. 344 Infected hosts shed in their feces oocysts of the parasite, subsequently contaminating the environment, food, and water. The life cycle of C. parvum can be summarized as follows. 344 Upon ingestion of contaminated water or food, or by inhalation of oocysts, sporozoites are released by excystation of oocysts into the gastrointestinal or respiratory tract. The sporozoites enter the epithelial cells and develop into trophozoites, which in turn differentiate into type I and type II meronts. The merozoites from type I meronts invade new tissues and develop into trophozoites to continue the life cycle. The merozoites from type II meronts invade infected cells and undergo sexual multiplication to give rise to male and female gametes. The zygotes resulting from fertilized gametes become infectious by sporulation, and the sporulated oocysts are excreted in feces. C. parvum has an infectious dose of about 9–1042 oocysts. 343

Cryptosporidiosis is a self-limiting disease with an incubation period of 1–2 weeks and is characterized by profuse, watery diarrhea, abdominal pain, vomiting, and low-grade fever. During the period from 1993 to 1998, seven major outbreaks of cryptosporidiosis have been reported in the United States. 345 Since then, Cryptosporidium spp. caused an estimated 57,600 illnesses, 210 hospitalizations, and 4 deaths. 3 Water is the most common source of C. parvum for human infections. 212 The largest outbreak of cryptosporidiosis (waterborne) in the United States occurred in Milwaukee, Wisconsin, in 1993 involving more than 400,000 people with 69 deaths. 347 , 348 In addition to drinking water, water can also potentially contaminate produce when it is used for irrigating plants or washing fruits and vegetables. Oocysts of the pathogen have been detected in fresh vegetables, raw milk, sausage, mussels, oysters, and apple cider. 212 Infected food handlers can also transfer the oocysts to foods. 349 , 350 C. parvum oocysts are sensitive to freezing and freeze-drying. The oocysts lose infectivity in distilled water stored at 4°C. 351 However, the oocysts are quite resistant to chlorine; no loss in infectivity was observed in water containing 1%–3% chlorine for up to 18 h. 352 However, the oocysts are sensitive to ozone, losing more than 90% infectivity in the presence of 1 ppm ozone for 5 min. 353

Besides affecting humans, C. parvum can infect cattle, preweaned calves, sheep and goats, pigs, and horses. 354 C. parvum oocysts were responsible for an outbreak of cryptosporidiosis in veterinary students involved in research with cattle, 355 underscoring the pathogen’s zoonotic potential.

Cyclospora cayetanensis

C. cayetanensis is a waterborne protozoan pathogen that is also transmitted by contaminated food. The parasite was implicated in several foodborne outbreaks in the United States during 1996 and 1997. 356 The pathogen causes an estimated 11,400 cases, with 11 hospitalizations annually, costing approximately $11 million. 3 Water and foods, especially fruits and vegetables containing oocysts, are common vehicles of human infection. 345 , 357 During the period from 1996 to 2000, eight major outbreaks of cyclosporidiosis were reported, with imported raspberries as the vehicle of infection in half of the outbreaks. 345 Other types of produce implicated in C. cayetanensis outbreaks include lettuce 358 and fresh basil. 359 Humans are the only identified reservoir of C. cayetanensis. 357 The symptoms of C. cayetanensis infection in humans include watery diarrhea, nausea, abdominal pain, vomiting, and weight loss. Presently, there is very little information on the effects of heat, freezing, and disinfection agents on Cyclospora oocysts. Exposure of oocysts to −20°C for 24 h or 60°C for 1 h prevented oocysts from sporulating. Exposing oocysts to 4°C or 37°C for 14 days delayed sporulation. 360

Toxoplasma gondii

T. gondii is an obligate intracellular protozoan parasite for which cats are the definitive host. A survey on the prevalence of T. gondii in cats at spay or neuter clinics in Ohio revealed that 48% of the cats were infected with the parasite. 361 In the intestine of cats, the parasite undergoes sexual reproduction to form oocysts, which are excreted in feces. 362 The oocysts undergo maturation and survive in the environment for months and spread by wind, insects, and tapeworms. Toxoplasmosis in humans results following ingestion of food or water contaminated with oocysts. Raw or undercooked meats contaminated with cysts are potential sources of T. gondii. The parasite has been isolated from meat of game, sheep, goats, horses, chickens, and swine. 344 , 363 Transmission also occurs from an infected pregnant mother to child by transplacental transmission. 364 In the United States, T. gondii has been reported to cause about 4000 congenital infections annually, potentially resulting in blindness, learning disabilities, and mental retardation in children. 341 T. gondii is also attributed as the leading cause of CNS infection in persons with AIDS. 365 Symptoms in healthy adults are usually mild and include rash, headache, muscle pain, and swelling of lymph nodes. Although the oocysts can survive in refrigerated meat for weeks, they are inactivated by freezing at <12°C. 366 The oocysts are sensitive to irradiation and heat (>67°C). Properly cooked foods are not a vehicle of T. gondii. 367 T. gondii causes an estimated 86,700 cases, 4,428 hospitalizations, and 327 deaths annually, costing an estimated $3 billion, second only to nontyphoidal salmonellosis. 3

Trichinella spiralis

T. spiralis is a roundworm that primarily infects wild and domestic animals, especially pigs. Humans contract trichinosis by consumption of raw or undercooked meat containing larvae of the parasite. Pigs are infected by consuming uncooked scraps of infected pork. The encysted larvae upon ingestion are liberated from the cyst in the intestine, where they sexually mature. 368 The mature male and female worms copulate in the lumen of the small intestine, giving rise to a new generation of larvae. The newly born larvae migrate to various tissues in the body. Those larvae that reach the striated muscles penetrate into the sarcolemma of the muscle fibers and develop to maturity as encapsulated cysts. 368 The larvae continue their life cycle when raw or undercooked meat, especially pork containing the larvae, is consumed by humans. Major clinical systems include myalgia, diarrhea, fever, facial edema, conjunctival hemorrhages, and headache. 369

Trichinosis is a notifiable disease in the United States, with the number of cases progressively decreasing since the 1940s. 345 The decline in trichinosis in the United States has been attributed to changes in swine feeding practices and routine inspections at slaughterhouses. The average number of trichinosis cases reported in the United States in 1997–2001 was 14 per year, down from 400 cases/year in the 1940s. 370 On the other hand, game meat was identified as the most common source of the parasite to humans during 1997–2001. 345 Globally, Trichinella spp. cause an estimated 65,818 cases and 42 deaths reported from 41 countries during 1986–2009. 369

Anisakis Species

Anisakiasis in humans is caused by two foodborne roundworms. These include A. simplex, whose definitive host is whales, and Pseudoterranova decipiens, which primarily inhabits seals. The eggs of these roundworms are excreted in feces by their respective hosts. The eggs then undergo molting in suitable intermediate hosts and subsequently develop into larvae, which are ingested by fish. 371 Humans contract anisakiasis by consumption of raw or undercooked fish and seafoods containing the larvae. In noninvasive anisakiasis, the worms released from ingested foods migrate to the pharynx, resulting in “tingling throat syndrome.” 371 The worms are ultimately expelled by coughing. In the invasive form of anisakiasis, the worms penetrate the intestinal mucosa, thereby causing symptoms that include epigastric pain, nausea, vomiting, and diarrhea.

Taenia Species

The genus Taenia includes two meatborne pathogenic flatworms, T. saginata (beef tapeworm) and T. solium (pork tapeworm). The eggs of T. saginata survive in the environment, including on pastures, and are ingested by cattle in which they hatch into embryos. 368 The embryos migrate to skeletal muscles or the heart and develop into larvae known as Cysticercus bovis. They become infective to humans in approximately 10 weeks. 343 Humans become infected by consuming raw or undercooked beef containing the larvae. Larvae that are released into the small intestine develop into mature, adult worms. Cattle get infected with contaminated human hands or by drinking contaminated feed or water. 372 The symptoms of T. saginata infection in humans include decreased appetite, headache, dizziness, diarrhea, and weight loss.

In the normal life cycle of T. solium, pigs serve as the intermediate host. Eggs ingested by pigs develop into embryos in the duodenum, penetrate the intestinal wall, migrate through the blood and the lymphatic system, and finally reach the skeletal muscles and myocardium, where they develop into larvae known as Cysticercus cellulosae. Humans, the definitive host, consuming raw or undercooked pork are infected with the larvae, which develop into adult worms in the small intestine. The symptoms of T. solium infection in humans include discomfort, hunger pains, anorexia, and nervous disorders. Worms are passed in the feces. In the abnormal life cycle of T. solium, humans serve as intermediate hosts in which the larvae develop in striated muscles and in sub-cutaneous tissue. T. solium infections are most common in the developing world. However, due to immigration of people from endemic areas, infections have been increasingly diagnosed and reported in developed countries. 373

Diphyllobothrium latum

D. latum is commonly referred to as the broad tapeworm because it is the largest human tapeworm. 371 Humans contract diphyllobothriasis by consuming raw or undercooked fish containing the larval forms called plerocercoids. Upon ingestion, the larvae develop into mature worms in the intestines. Eggs produced by mature worms are excreted in feces. If feces containing the eggs contaminate water, the eggs develop into free-swimming larvae called coricidia. Coricidia are ingested by crustaceans, where they develop into a juvenile stage known as procercoid. Following ingestion of infected crustaceans by fish, procercoids develop into plerocercoids to continue the life cycle. Diphyllobothriasis in humans is characterized by nausea, abdominal pain, diarrhea, weakness, and pernicious anemia. 371 Cases of diphyllobothriasis have been associated with eating foods containing raw salmon such as sushi.

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