Food- and Waterborne Microorganisms



Food- and Waterborne Microorganisms


Gerald McDonnell



Food- and waterborne infective microorganisms constitute a diverse group that includes viruses, bacteria, algae, protozoa, fungi, and helminths. These agents can cause acute, chronic, or latent infections with incubation periods of a few hours, days, or even weeks; severity ranges from mild, transient, to fatal episodes. The illness may be manifested by preformed toxins or by the invading pathogens or both. The organism may be free living and saprophytic in nature or fastidious, multiplying only in the host. The agent may show single host specificity, or it may infect hosts of different species. The organism may be highly susceptible to physical-chemical agents, or it may form highly resistant spores. The pathogens may be highly aerobic, or they may show extreme oxygen sensitivity and be anaerobic. Some of these agents may cause local intestinal infections, whereas others cause septicemia. Some pathogens have the potential to cause explosive epidemics, and others only localized outbreaks; however, all these pathogens use food and water as a common vehicle and the gastrointestinal tract as a common route of infection.


CHANGING PATTERN OF INFECTIONS

Food and water have been the most common sources of infectious diseases because the gastrointestinal tract offers pathogens a more direct access to the interior of the host. The pathogenic microorganisms often use food and water both as a vehicle and as a growth medium. Ingestion of contaminated food and water has been the cause of serious outbreaks, large epidemics, or waves of pandemics of diseases. One of the pathogens that have caused ravaging epidemics with high fatality rates is the etiologic agent of cholera, Vibrio cholerae. A brief historical perspective of this typical food- and water-infective pathogen is interesting. Cholera, as the term was used in Hippocratic writings 2400 years ago, represented sporadic gastrointestinal derangements of diverse origin.1 Since the late 19th century, cholera has designated the illness caused by V cholerae. The illness represents most significantly an altered disease pattern resulting from industrialization without sanitation practices.2 In seven pandemics, each starting from 1817, 1829, 1852, 1863, 1881, 1889, and 1961, respectively, it has claimed millions of lives in several countries. Transmission of cholera through water was discovered during the study known as “the cause of Broad street pump.”3 The victims used well water that had been contaminated by drainage. The epidemic was arrested by removal of the handle of the pump located on Broad Street, and sand filtration of water was effective in containing the cholera epidemic in Altona, Germany, at the end of the 19th century. The original biotype of V cholerae has been replaced by the El Tor strain in most parts of the world.4

During the first half of the 20th century, pathogens such as Salmonella ser Typhimurium, V cholerae, Shigella species, Brucella species, Streptococcus pyogenes, Clostridium botulinum, Entamoeba histolytica, and viruses such as polio viruses were known as primary foodborne and waterborne pathogens. Most recent and notable examples include outbreaks with Escherichia coli (including the shiga-toxin producing strains, such as the serogroup O157),5 Listeria,6 Campylobacter,7 and norovirus.8 Indeed, recent reports from the United States suggested that the top 5 pathogens associated with foodborne outbreaks were norovirus, Salmonella, Clostridium perfringens, E coli, and Campylobacter species.9 Many of these are equally associated with waterborne sources, particularly Cryptosporidium, norovirus, Giardia, Campylobacter, and rotavirus.10 These and many other pathogens still cause widespread illnesses in developing countries. For foodborne illness, the World Health Organization has estimated that the global burden of such diseases is significant and particularly in developing countries, with the main pathogens being norovirus and Campylobacter
species leading to diarrheal diseases.11 Others included Salmonella species, Taenia solium, hepatitis A virus, and from fungal sources of aflatoxins. Examples of some of the more notable causes of food- and waterborne microbiological risks associated with outbreaks are summarized in Table 56.1.








TABLE 56.1 The most common causes worldwide of food- and waterborne outbreaks





















Microorganism Type


Examples


Viruses


Hepatitis A virus


Norovirus


Bacteria


Bacillus cereus


Brucella species


Campylobacter species


Clostridium species


Escherichia coli


Listeria species


Mycobacterium bovis


Salmonella species


Shigella species


Staphylococcus aureus


Vibrio cholerae


Protozoa


Cryptosporidium species


Giardia species


Helminths


Ascaris species


Echinococcus species


Fasciola species


Taenia solium


Toxoplasma gondii


Trichinella species


Toxins


Aflatoxin


Salmonella ser Typhi (leading to typhoid fever) and Salmonella ser Paratyphi (paratyphoid fever) continue to be leading causes of morbidity and mortality worldwide, despite the availability of a vaccine for at least typhoid fever and available antibiotic therapies.12 These rates are further exasperated by increased reports of antibiotic resistance.13 Incident rates vary from region to region, being particularly high in African, Latin American, and other developing countries. S Typhi was encountered in probably one of the largest recorded epidemics of typhoid fever in recent history, resulting from contaminated well water in Sangli, India, during 1975 through 1976.14 Another similarly large typhoid epidemic (10 766 cases) was reported in Dushanbe, Tajikistan, as a result of contaminated municipal water supply.15 Recent estimates worldwide suggest at least 27 million cases of typhoid and some 200 000 deaths annually, particularly in African and Asian countries,16 although outbreaks are also frequently reported in other countries that are considered to have better controls on food and water sources.17 V cholerae infections are estimated to occur in 3 to 5 million cases, and responsible for 100 000 to 120 000 deaths annually.18 Reports and outbreaks continue to be endemic in certain regions of the world seasonally, including in parts of the Americans, Africa, and Asia. Large outbreaks are also frequently reported.19 Other examples include larger outbreak with Shigella species in bacillary dysentery in Nigeria,20 in India,21 and more recent concerns with antibiotic-resistant strains such as in China.22 High incidence of brucellosis, one of the most common causes of zoonotic disease reported worldwide, was once consider high in countries such as Argentina, Peru, Iran, Laos, Spain, Malta, and Italy,23 but the implementation of control measures in developing countries have led to some success but remains of concern.24 Of the viruses, in the last 10 years, the rates of reported norovirus and rotavirus outbreaks have become very common, particularly seasonally (autumn/winter) with common sources being food, water, and associated outbreak due to dissemination by infected patients (eg, due to vomitus and diarrhea).8,25,26 Tables 56.2, 56.3, and 56.4 present lists of specific food- and waterborne microorganisms
pertaining to bacteria, viruses, and parasites, respectively. Each of these classes of microbes includes several genera and species of infective agents. Mention should be made that there are more than 45 types of parasites, and a number of toxin-producing fungi and algae that should also be considered as concerning food- and water-infective microorganisms. Harmful algal blooms in water bodies (and associated drinking water contamination with cyanobacterial toxins) have been associated with human, fish, and animal toxicity, such as in the Great Lakes in the United States.29 Parasitic infections are endemic and widespread in developing countries, with pathogens such as Cryptosporidium and Giardia frequently associated with outbreaks.30,31,32








TABLE 56.2 Food- and water-infective bacteriaa



















































Produce Toxins in Food


Bacillus cereus


Clostridium botulinum


Escherichia coli


Staphylococcus aureus


Produce Infection


Aeromonas hydrophila


Brucella abortus, Brucella suis, Brucella melitensis


Campylobacter jejuni, Campylobacter coli,


Campylobacter fetus


Clostridium botulinum


Clostridium perfringens


Escherichia coli


Klebsiella pneumoniae


Legionella pneumophila


Listeria monocytogenes


Mycobacterium bovis


Plesiomonas shigelloides


Salmonella species


Shigella sonnei, Shigella dysenteriae, Shigella flexneri


Streptococcus pyogenes (Group A)


Vibrio cholerae, Vibrio mimicus, Vibrio vulnificus, Vibrio parahaemolyticus


Yersinia enterocolitica, Yersinia pseudotuberculosis


a From Madden et al.27









TABLE 56.3 Food- and water-infective virusesa



























Adenoviruses


Astroviruses


Caliciviruses, noroviruses (or Norwalk viruses)


Coronaviruses


Cytomegaloviruses


Enteroviruses: coxsackie, ECHO, polio, and hepatitis A


Hepatitis E virus


Norwalk-like viruses


Papovaviruses


Parvoviruses


Rotaviruses


Abbreviation: ECHO, enteric cytopathogenic human orphan.


a From European Food Safety Authority.28


In many countries, different patterns of food- and waterborne infections are often considered as “emerging” because of previously little-noticed or newly discovered pathogens.33 The increasing incidence of many of these pathogens becomes more evident in developed countries because our mechanisms of diagnosis and detection have improved and in the era of modern infection prevention strategies or controls leading to the declining incidence of previously recognized pathogens and emergence of new pathogens. Examples may include the following:



  • Antibiotic-resistant bacteria including various strains of carbapenem-resistant Enterobacteriaceae, including Klebsiella, E coli, and Pseudomonas species that are associated with a high mortality rate34


  • Bacterial pathogens with newly identified virulence factors, such as Shiga toxin-producing E coli O157: H735


  • Viral pathogens, such as rotaviruses and noroviruses.8,25,26 Further examples include other nonenveloped viruses such as sapovirus, adenoviruses, coxsackievirus, mamastrovirus, and torovirus.36


  • Transmissible spongiform encephalopathies (TSEs), particularly scrapie, bovine spongiform encephalopathy (BSE), and chronic wasting disease (CWD) (see chapter 68)37,38


  • Sources of even low levels of fungal and algal toxins that have been linked to acute and chronic health effects39,40

Many previously recognized pathogens, such as Staphylococcus aureus, E histolytica, Shigella, and Cryptosporidium species are also often included as the emerging pathogens because they either maintain a significant incidence or are sporadically encountered even in developed countries. Therefore, at present, the term emerging should be assigned to the incidence of the pathogens under apparently improved sanitary conditions or have been newly identified. These are further considered in the next section.


RECOGNITION OF EMERGING PATHOGENS

Numerous related or unrelated factors have been responsible for the recognition of emerging pathogens. An emerging pathogen may be a new agent, a pathogen jumping the species barrier, a reemerging or reappearing known pathogenic agent of the past, or a pathogen showing a sudden and noteworthy increase in otherwise uneventful or low incidence of infection. Some of the pathogens, such as Legionella pneumophila, rotavirus, or noroviruses (often referred to as Norwalk or Norwalk-like agents), are relatively newer examples, whereas others, such as Giardia lamblia, have been known for centuries. The increased detection of psychrotrophic Listeria monocytogenes or Yersinia enterocolitica could be linked to certain practices in the modern food industry, such as longer storage of products at refrigeration temperature. Emergence of L pneumophila and atypical Mycobacterium species (eg, Mycobacterium chelonae, Mycobacterium avium, and Mycobacterium chimaera) have been associated with piped cold- and hot-water systems. Higher incidences of latent and otherwise uneventful infections, such as with the parasites Isospora belli, Cryptosporidium species, or Sarcocystis species have been associated with the increased population of immunocompromised persons in health care systems worldwide (eg, during cancer chemotherapy or associated with viral infections such as AIDS). Regardless of the factors associated with recognition of the emerging pathogens, their emergence has been marked by outbreaks that are often cited in the popular media. Outbreaks associated with food contamination or cross-contamination are frequent examples. Although improvement have been made to reduce the risks of waterborne outbreaks due to better standards and guidance to control chemical and microbiological quality worldwide,41 outbreaks are still commonly reported.











TABLE 56.4 Common food- and water-infective protozoa and helminths











































































































































































































Source


Agent


Comments


Amoeba



Fecal contamination of food and water


Entamoeba histolytica


Human pathogen; incubation period is variable, from a few days to several weeks. Invasion of colonic tissue results in acute diarrhea, abdominal pain, and bloody mucoid stools. Complication of lung, brain, or liver in severe cases



Recreational water (swimming)


Naegleria fowleri


Free living; found in soil, fresh water, sewage, and sludge; more common in lakes used for cooling water; causes amebic meningoencephalitis



Recreational water (swimming)


Acanthamoeba culbertsoni, Acanthamoeba castellanii, Acanthamoeba polyphaga, Acanthamoeba astronyx


Free living; found in soil, fresh water, brackish water, and sea water; causes chronic granulomatous amebic encephalitis that may be fatal. May cause eye infections, immunocompromised individuals may get infection by inhalation of cysts from soil


Flagellates



Community water and raw vegetables


Giardia lamblia


Both warm- and cold-blooded animals serve as carriers; does not multiply outside the body


Causes diarrhea, flatulence, cramps, nausea, anorexia, and fatigue and acute and chronic infection in asymptomatic persons



Oral-fecal contamination of food and water


Dientamoeba fragilis


Flagellate without flagella and cyst form. Infection is associated with Enterobius (pinworm infection). Probably uses Enterobius eggs to bypass stomach acidity. Illness results in diarrhea, nausea, and vomiting.


Ciliates



Food and water contaminated with pig feces


Balantidium coli


More common in tropics; largest protozoan parasite. Both cyst and trophozoite. Symptoms include nausea, vomiting, and watery diarrhea. Both acute and chronic infections and colonic ulcers are observed.


Coccidia



Fecal contamination of food and water by carnivorous host


Isospora belli


Inhabits mucosa of small intestine. Intracellular parasite; can produce severe intestinal disease with diarrhea, nausea, and fever. Disease may persist for months or years. Fatal in immunocompromised persons



Fecal contamination of food and water


Cryptosporidium parvum


Infects brush border of intestinal epithelium, infects other organs in immunocompromised individuals; causes profuse and watery diarrhea, epigastric pain, and nausea that is prolonged in immunocompromised persons



Fecal contamination of food and water


Cyclospora cayetanensis


Watery diarrhea, mild-to-severe nausea, anorexia, abdominal cramping, fatigue, and weight loss; diarrhea can be intermittent and protracted. Persons with no previous immunity and very young children are likely to exhibit symptoms.



Fecal contamination of food water


Sarcocystis hominis, Sarcocystis suihominis


Intestinal mucosa as the primary site of infection



Fecal contamination of cats and undercooked meat of intermediate hosts


Toxoplasma gondii


Causes acute and chronic infections; disease may resemble mononucleosis. Congenital infection may involve CNS and ocular abnormalities and may be fatal. Reactivated in immunocompromised individuals, resulting in encephalitis, pneumonitis, and myocarditis.


Cats serve as primary host. Frequency of infection can be as high as 80% in regions of France to as low as 1% in the United States.


Helminths


Nematodes (tissue)




Undercooked raw pork, bear meat


Trichinella spiralis


Develop in mucosa of small intestine. Nonspecific gastroenteritis, fever eosinophilia, and myositis



Ingestion of animal livers or food contaminated with eggs from soil


Capillaria hepatica


Develops in liver parenchyma



Food contaminated with dog feces


Toxocara canis


Hyper-eosinophilia, hepatomegaly, fever, and pneumonitis



Consumption of raw fish dishes: sushi, sashimi, and ceviche


Anisakis species


Anisakiasis, abdominal pain, vomiting, eosinophilic granuloma


Phocanema species



Terranova species




Raw or undercooked shrimp, crabs, large edible snails; improperly washed lettuce, fruits, and strawberries


Angiostrongylus cantonensis


Lungworms inhabiting pulmonary artery of rats and passed on to slugs and snails. Causes human eosinophilic meningitis or meningoencephalitis. Observed in Hawaii, Thailand, Indonesia, and other southeast Asian countries and Cuba. Worms migrate to brain, spinal cord, and eye, giving prolonged severe headache and other CNS complications.


Nematodes (intestinal)



Fecal contamination of food and water


Enterobius vermicularis


Infections associated with gastrointestinal tract. Human pinworm. Primarily infects children; eggs survive for prolonged periods in feces.


Ascaris lumbricoides


Human large roundworm found in cecum


Trichuris trichiura


Human whipworm common in moist, warm regions



Raw and poorly cooked fish


Capillaria philippinensis


Parasite of fish-eating birds and fish. Common in Philippines, Thailand, and areas around South China Sea


Cestodes (tissue)



Poorly cooked fish or the use of frog and snake poultices


Spirometra mansoni


Parasites of cats, dogs, wild canids, and wild felids; common in China, Japan, Korea, and Vietnam


Spirometra mansonoides


Common in United States



Food contaminated by dog feces


Taenia multiceps


Parasite of dogs, cats, and fishes. Human infection through dog feces



Consumption of undercooked meat


Echinococcus granulosis


Domestic and wild canids as primary host. Common in sheep and cattle raising areas.



Forms hydatid cysts and CNS complications


Echinococcus multilocularis


Develops invasive cysts in liver. Common in Europe, Japan, North and South America, Australia, and New Zealand


Echinococcus vogeli


Primarily found in Latin America. Bush dogs and large rodents are primary hosts. Develops invasive cysts in liver


Cestodes (intestinal)



Undercooked fish


Diphyllobothrium latum


Fish tapeworm found in cold, clear lakes of United States, Canada, Russia, Japan, and Europe



Beef


Taenia saginata


Cattle tapeworm



Pork


Taenia solium


Pig tapeworm. Most prevalent in Latin America, India, China, Africa, and Europe. Can cause severe CNS and eye infections



Grains and cereals


Hymenolepis nana


Mice are primary host; grains- and cereal-infecting beetles are secondary host.



Food contaminated with dog and cat feces


Dipylidium caninum


Dogs and cats are primary hosts; children are most susceptible.


Trematodes



Consumption of undercooked water vegetables like water chestnut and water caltrop and watercress


Fasciolopsis buski


Largest and most pathogenic intestinal fluke. Common in China, India, Indonesia, Thailand, Taiwan, and Vietnam



Water vegetables such as watercress


Fasciola hepatica


Worldwide occurrence



Undercooked and pickled fish


Clonorchis sinensis


Parasite found in bile duct of humans, cats, and dogs



Poorly cooked crustaceans


Paragonimus westermani


Parasite of dogs, cats, and wild animals


Abbreviation: CNS, central nervous system.



Noteworthy Outbreaks and Events

G lamblia is probably one of the earliest recognized pathogens, discovered or observed by Antonie van Leeuwenhoek in 1681.42 It was recognized as an important pathogen during one of the largest laboratory-confirmed outbreaks in Rome, New York, during 1974 through 1975, with an estimated 4000 to 5000 cases.43 In the United States alone, giardiasis continues to be one of the leading causes of human enteric disease. G intestinalis is now estimated to cause approximately 1.2 million reported cases of infection, with an estimated number of 242 reported outbreaks associated with at least 41 000 people affected and about 3581 hospitalizations yearly.44 The infectious dose is considered low, at an estimated level of 10 cysts, noting than an infected individual can release billions of cysts per day and over many months of active and latent infection. The dormant, or cyst forms have known higher resistance levels to inactivation by chemical disinfectants (see chapter 3, including chlorine concentrations traditionally used for water disinfection; see chapter 37) and are therefore more robust under environmental conditions. Reports in outbreaks, which may be due to improvement in diagnosis and reporting in the United States, had actively increased from 1996 to 2001 but since that time have been stable or even decreased. The majority (approximately 75%) of these outbreaks were sources to contaminated drinking water, with the remaining sources being from recreational water (approximately 16%) and zoonotic or human-to-human transmission particularly through food. A greater emphasis on preventative measures, such as filtration or different chemical disinfection applications to control drinking water and as emphasis on good hygiene practices on handling of animals and food clearly have an impact of reducing the potential for outbreaks. But it may be suggested that the emphasis in recent years has turned to another protozoal source of outbreaks, Cryptosporidium species. From 2009 to 2017, again in the United States, active surveillance and reporting had identified over 444 outbreaks of infection, with an estimated impact on at least 7465; overall, it was estimated during this time to have been a 135 increase per year of outbreaks.30 The source of the outbreaks in most of these cases was due to recreational water, but cases associated with human-to-human and zoonotic transmission have also been reported and similar to Giardia outbreak cases. Large outbreaks have also been reported in drinking water,45 highlighting limitations in chemical and filtration disinfection practices due to the lack of controls and tolerance of Cryptosporidium oocysts that are even more resistant to chemical inactivation compared to investigations with Giardia cysts.46,47 The rates of such protozoal infections are likely to be higher in other parts of the world but are often not reported or investigated. There is also a risk in many of these cases that protozoa may be the source of other bacterial and viral infection associated with water and food contamination due to the ability of many protozoa to maintain or even allow the active growth of other pathogens within their vegetative and dormant forms of their respective life cycles (see chapter 3).48

There continues to be attention on various gramnegative bacteria associated with water- and foodborne outbreaks, such as those associated with Salmonella species such as Salmonella enteritidis and S Typhi that were probably some of the earliest bacteria identified to be associated with foodborne infections.49,50 The importance of these and other nontyphoidal salmonellae even in the countries with well-established controls was realized after the largest milk-borne outbreak of S Typhi in Illinois, United States, in 1985 resulted in 16 000 cases.51 Other larger outbreaks include a toasted oatmeal cereal product was an unlikely
source of multistate outbreaks of Salmonella agona infections, with 209 cases in 11 states in the United States,52 and with Salmonella species infections linked to backyard poultry in 768 people (approximately 30% hospitalized and two deaths) across 48 states.53

The most prominent causes of bacterial gastrointestinal infections in the United States is still considered to be Campylobacter jejuni, with an estimated 1.3 million illnesses each year in the United States.54 These are often associated with contamination poultry, water, or other products such as unpasteurized milk. The magnitude of these infections was realized only after improved isolation procedures were developed during the early 1980s55 and now including part or whole genome sequencing.56 Y enterocolitica was recognized as an emerging pathogen after an epidemic in New York state, which was marked by several unnecessary appendectomies57 and a multistate outbreak in Arkansas, Tennessee, and Mississippi that involved several thousand cases.58 Y enterocolitica and other species are frequently linked to pigs and other environmental sources.59,60 The pathogenic potential of the gram-positive bacteria L monocytogenes was initially observed after the epidemics in Germany,61 Canada,62 and the United States.63 In 1998, several cases of illnesses caused by a strain of L monocytogenes, serotype 4b, were reported in 11 states, associated with the consumption of hot dogs and deli meat.64 Some of these epidemics involved several hundred cases and were marked by high mortality rates linked to contaminated foods, with recent examples including from salads65 and apples.6 The widespread nature of Vibrio parahaemolyticus infection became evident after its first isolation in Japan in 1950.66 The pathogen accounted for 40% to 50% of bacterial gastroenteritis cases in Japan67 and is commonly associated with the consumption of seafood.68,69 C perfringens, long known to be the causative agent of gas gangrene, was associated with food poisoning during the early 1960s.70 The ability of this bacterium to survive in food due to spore formation and subsequently sporulate in the intestines results in poisoning from the production of various toxins.71 C perfringens infections are in the top three causes of bacterial foodborne illness, along with Salmonella and Campylobacter species in the United States.72 Similar spore-forming bacteria such as C botulinum (types A, B, and E) have been known as the classic toxin-producing bacterium in canned foods.73 They can produce various neurotoxins (8 types, designated A-H) that can enter the body following digestion, but it is known that the toxins can be neutralized by heat treatment (eg, at 85°C for 5 min). During the 1960s, the ability of different C botulinum strains to grow and produce toxin under refrigeration conditions was recognized.74 In addition to direct ingestion of the toxin, the bacterium also can multiply in the gastrointestinal tract and activity product toxin overtime. Outbreaks are most often associated with canned foods,75 but others have included contaminated honey in infants.76,77 This pathogen has also been incriminated in botulism attributed to contaminated rainwater in rural Australia.78 Aeromonas hydrophila was first described as an enteropathogen in 1955,79 and since then, it has been associated with gastrointestinal infections.80,81 Its ubiquitous nature and enhanced virulence for immunocompromised persons make it an important member of the emerging pathogens both in food and water sources.81

E coli was previously considered as a nonpathogenic inhabitant of the human and animal intestine; however, pathogenic strains were found to account for the largest number of diarrheal infections in developing countries and in the young associated with contaminated food or water.82,83 In many cases, E coli strains can be harmless or may cause mild disease associated with short-lived diarrhea, but some strains can lead to more severe cases of disease associated with toxin production including vomiting, abdominal pain, and severe diarrhea. Virulent strains can also lead to other complications such as urinary tract and bloodstream infections.83,84 A particularly virulent strain, referred to as coli-hemorrhagic or Shiga toxin-producing E coli O157:H7 (STEC), was isolated during rapidly spreading outbreaks of hemorrhagic colitis in Canada85 and in the United States.86,87 Since that time, a variety of pathogenic E coli and their virulence determinants have been described.83 These have been classified into different pathotypes such as enteropathogenic, STEC (including enterohemorrhagic strains), enteroinvasive, enteroaggregative, diffusely adherent, enterotoxigenic, adherent invasive E coli. The presence of various virulent factors includes toxins, adhesins, and invasins in these and other E coli strains are further exasperated by the increasing development of multiantibiotic-resistant strains; antibiotic resistance has been well described with antibiotics that have been traditionally used for many years in humans and animals (eg, penicillin and ampicillin), but in more recent years, there has been an alarming increase in reports of multidrug resistance to include newer antibiotics such as cephalosporins and fluoroquinolones.83,84 Environmental detection of and outbreaks with these strains are frequently reported and often due to their difficulty in treating patients and persistence of the infection leading to greater rates of morbidity and mortality.88,89,90 Most of these virulent factors, including antibiotic-resistant genes, are associated with mobile genetic elements such as transposons and plasmids. These are of further concern because they can be transferred from one strain to another and even between different gram-negative bacteria species. The impact of this can be highlighted by the growing incident rates of the detection of carbapenem-resistant strains of Enterobacteriaceae, such as in Klebsiella, Pseudomonas, and E coli.91 The rates of infection with these pathogens in patients that are immunocompromised (eg, health care-acquired infections) is a major threat given that treatment options in these patients are limited. Many of these outbreaks are associated with water sources, such
as from sinks and drains,92,93 as well as associated with food contamination.90,94

L pneumophila is an example of fairly recent member of the emerging pathogens from water sources. Numerous outbreaks of infections of L pneumophila since 1977 give testimony to its virulence potential and the link to various water sources.95,96 The initial discovery of L pneumophila in an outbreak of respiratory illness associated with the American Legion convention in Philadelphia was unusual and widely publicized.97 The etiologic agent turned out to be a gram-negative bacterium, not a rickettsia-like agent as indicated by isolation procedures and the nature of illness. Since then, L pneumophila was found to have been associated with past outbreaks of unknown cause98 and often found to be persistent in water systems despite remediation (including waterline disinfection) attempts.96

Increasing reports of outbreaks due to atypical mycobacteria have been linked to the persistence of many of these strains in water sources and, in some cases, unusual tolerance profiles to disinfectants. These infections are often difficult to treat due to the intrinsic (or acquired) resistance to antibiotics in these isolates. Examples include outbreaks (or pseudo-outbreaks) associated with ice machines (Mycobacterium fortuitum99), M chimaera infections following cardiac surgery and sources to heatercooler units,100 Mycobacterium massiliense outbreaks associated with resistance to aldehyde-based disinfectants, antibiotic resistance and increased virulence,101,102 M avium outbreak from contaminated pork meat.103 Atypical (or nontuberculous) mycobacteria are found to be ubiquitous in the environment and widely detected in water sources, although they do require specific attention to culturing methods (media, growth temperatures, and extended incubation times) to allow for their detection. Interestingly, the ability of bacteria such as Legionella and mycobacteria to enter and survive within protozoa is used a method to detect fastidious strains (using protozoa essentially as a cell culture method) and as a mechanism of resistance (or persistence) to water disinfection due to their survival in the dormant (cyst/oocyst) forms of these microorganisms (see chapter 3).104

Overall, many outbreaks associated with food and water will be further exasperated by our ability to travel more widely and rapidly than in previous times. Examples include the speed at which strains of bacteria or viruses can transfer from one, isolated area of the world to other. Probably the most noteworthy example of this in recent years is the Spanish flu that peaked in 1918-1919.105 Although it is unsure where exactly the source of the outbreak was, in recent years, the H1N1 virus was found to have genes of avian origin. Estimates of infection rates was approximately 500 million people, which at the time was about one-third of the world’s population, and about one-tenth of those infected died (although it is generally believed that many died due to complications of virus infection, such as secondary bacterial infections). Recent cases or concerns on pandemics include severe acute respiratory syndrome, Middle East respiratory syndrome, viral hemorrhagic fevers (eg, Ebola or Marburg viruses), and antibiotic-resistant bacteria. Food and water sources, as well as being mechanisms of transmission, will continue to be of concern.106

It is clear that a wider range of infection or outbreaks can occur in individuals or groups that are immune or otherwise compromised, as highlighted earlier in hospitalized patients. This will include populations that are younger, older, or with underlying infections that affect the immune system (such as acquired immunodeficiency syndrome [AIDS]) or open the body to a greater risk of infection (eg, during surgery or in damaged skin; see chapters 43 and 44) or following cancer therapy. In may be that as we see increases in populations (especially those concentrated in urban areas), longevity, obesity or poor eating habits, use of more common or invasive medical treatment, and different types of pharmaceutical treatment (eg, depression of the immune system in case of psoriasis or inflammatory bowel disease), that we will continue to identify unique or emerging pathogens. Earlier examples include M avium serovars that had caused enteritis, bacteremia, or granulomata in the liver and bone marrow in patients with AIDS.106 A large percentage of these population (20%-80%) were found to be infected by Toxoplasma gondii through fecal contamination or by consumption of undercooked meat.107 This normally uneventful infection is reactivated in AIDS or transplantation patients to give rise to encephalitis, pneumonitis, and myocarditis. Similarly, I belli, Sarcocystis species, and Cryptosporidium species are known to cause severe and often fatal infections in immunocompromised persons.108 Large outbreaks of protozoan infections in healthy population resulted from the survival of Cryptosporidium cysts in chlorinated water. One massive outbreak of Cryptosporidium infection originated from contaminated municipal water supply in Wisconsin and another from recreational water fountain in Minnesota.45,109 Cyclosporiasis outbreaks are frequently reported due to contaminated foods such with the consumption of raspberries and snap peas imported to the United States and Canada.110,111,112 Approximately 370 clinically defined cases of cyclosporiasis were reported from eight states (California, Florida, Maryland, Nebraska, Nevada, New York, Rhode Island, and Texas) and one province in Canada (Ontario). In addition, approximately 220 clinically defined cases were reported among persons on a cruise ship that departed from Florida. Microsporidia and Blastocystis are further intestinal protozoa associated with infections in the immunocompromised.113 Other bacterial and protozoal pathogens associated with food and waterborne outbreaks emerge from time to time as summarized in Tables 56.1, 56.2, and 56.4, but as diagnostic methods have and continue to improve, it is likely that further emerging pathogens will continue to be identified in outbreaks.


As highlighted earlier, many types of viruses are associated such as hepatitis A and emerging pathogens including hepatitis E, sapovirus, adenoviruses, coxsackievirus, mamastrovirus, and torovirus (see Table 56.3).36 But special consideration is given to rotavirus and norovirus as recent leading causes of viral outbreaks.8,25,26 Rotaviruses are one of the leading causes of diarrheal diseases in the United States. The most common species associated with infection is rotavirus A, but there are at least 8 other species that can infect humans, animals, and birds (norovirus B to I). Infection is usually associated with severe diarrhea, vomiting, and abdominal pain. In the past, infection was often associated with severe illness and high rates of death, but overall, these rates have been reduced with prevention methods (vaccination) and management of disease (eg, oral rehydration therapy). These viruses have been recognized as a major cause of viral diarrhea in infants and young children, acquired by the fecal-oral route. Outbreaks associated with food114,115 and water10,116 are now frequently reported in both children and adults. Noroviruses (Norwalk or Norwalk-like viruses), which are also small, nonenveloped viruses, are now the more prevalent causes of gastroenteritis associated with food and water contamination in the United States and other countries.10,117 In the United States alone, out of 31 major pathogens, norovirus was the top cause of illness at 58%, followed by major bacterial sources such as Salmonella (11%), Clostridium (10%), and Campylobacter (9%); however, Salmonella remained the leading cause of death (at 28%) and norovirus was at 11%.72 In 1989 a major outbreak of 900 cases of gastroenteritis was reported in north central Arizona traced to contaminated well water.118 Outbreaks are now frequently reported with food,119,120 often associated with nonsymptomatic food handlers, and with water (including ice).121,122 It is interesting to note, in a review of drinking water-associated outbreaks during 2000 and 2014 affecting large numbers of consumers, that norovirus and rotavirus, as well as the protozoal pathogens Cryptosporidium and Giardia species, were prevalent and that these pathogens are associated with higher levels of resistance to disinfection and water preservation methods (see chapter 3).123

Finally, one of the most notable causes of foodborne disease has to be the transmission of BSE (commonly known as mad cow disease) in cattle and the association to a variant form of Creutzfeldt-Jakob disease (vCJD) in humans. These diseases are examples of TSEs or generally known as prion diseases. These are progressive, neurodegenerative diseases that are associated with the deterioration of mental and physical effects in humans and animals and culminate in death. Although the incubation times can be long, once these effects are diagnosed the progression of the disease can be rapid, with patients dying within a year. Prions are unique as both infectious and transmissible agents because they are proposed to be composed exclusively of proteins (see chapter 3 and 68).124 The protein associated with these diseases is known as PrP (in its normal form, PrPc), a glycoprotein associated with the cell membrane of human/animal cells including the neurons as various neural tissues such as the brain and spinal cord. The exact function of the protein in normal cells is not known but is known to be associated with functions such as copper trafficking and/or oxidative stress.125 But during the disease progression, the secondary/tertiary structure of PrPc is converted to an abnormal, protease-resistant form of the protein (PrPres). This form cannot be fully degraded by normal cellular processes and therefore accumulates to eventually lead to cell death and transmission to other neighboring cells. As the disease progresses, further neurons are destroyed, and this eventually leads to the interruption of normal neural tissue structure and function that eventually culminates in death. Prion diseases are generally rare diseases in humans (eg, the classic form of CJD being the most prevalent at rates approximately 1.4 cases in a million population worldwide),124 although some animal forms of these diseases are considered more prevalent (eg, the rates of scrapie in sheep is difficult to estimate but has been reported to be as low as 0.3% and as high at 35%).126 But the sudden outbreak of BSE in the United Kingdom (and to a less extent in some other countries such as Ireland, France, and Switzerland) was associated with the disease in approximately 200 000 confirmed cases, that was first identified in the United Kingdom in 1986, peaked in 1991-1993, and has subsequently declined but are still reported yearly.127 It is considered that the outbreak was sourced from the contamination (that was speculated to have been sourced from sheep with scrapie) of meat and bone meal that had been rendered (by grinding and heat treatment) of waste meat and bone from animals.128 This outbreak was further exasperated by the emergence of a new form of CJD (variant or vCJD) that occurred in humans at the same time, which has been linked to the consumption of contaminated meat.129,130 By 2019, 178 deaths (peaking at 28 in 2000) from vCJD have been confirmed as being likely caused during the outbreak in the United Kingdom alone, with cases being reported in other countries such as in France, Ireland, United States, and Spain.131 No new cases had been identified in the United Kingdom since 2016 (when one case was reported), but there remains much speculation about the potential for a further wave of cases in the future.132 In addition to BSE and vCJD, there remains much speculation about the potential of transmission of other TSEs, particularly scrapie and CWD. In the United States, for example, CWD is a concern in deer and elk populations, but there is a continued debate on the transmissibility of this disease to humans by contaminated meat.133

A whole new spectrum of emerging pathogens ranging from viruses to protozoa and prions has been observed during foodborne and waterborne outbreaks of infections. The emergence of new infectious diseases has been associated with changes taking place during human evolution. Multiple, sometimes similar, factors were responsible for
these outbreaks, but greater diagnostic methods and attention to investigating and reporting such outbreaks will continue to highlight the risks of food- and waterborne infections.


Causative and Recognition Factors of Outbreaks Caused by Emerging Pathogens


Awareness of Inadequacy of Legislative Guidelines on Sanitation in the Food Industry

Automation of large-scale food-processing facilities has resulted in the reduction of contamination of food as a result of manual handling. The practices of pasteurization and refrigeration and the use of disinfectant (sanitizers) during processing, transportation, and storage have increased shelf life and improved organoleptic properties of food products. Early legislative guidelines on sanitation were directed toward control of infections caused by previously recognized pathogens. These measures also resulted indirectly in the production of desired organoleptic quality of food through the control of mesophilic spoilage and pathogenic microorganisms. Thus, desired organoleptic properties and microbiological safety became synonymous in the food industry; the microbiological aspect apparently became secondary as long as the organoleptic quality of food product was maintained. This brought about certain degree of consumer complacency with regard to safe handling of food and other food safety precautions. The practice of using outdated but organoleptically acceptable pasteurized milk that had been returned from supermarket shelves for the preparation of ice cream and other frozen dairy products presented an underlying danger of contamination by psychrotrophic pathogens such as L monocytogenes. The ability of L monocytogenes to multiply at refrigeration temperatures in stored dairy products, hot dogs, and delicatessen meats resulted in large outbreaks of infection.63,64 Listeria is also found to be ubiquitous in the environment and persist in food processing environments.134 Factors such as the operation of the processing facilities for extended periods, poor sanitation of hard-to-reach dead spaces (eg, in water or product pipelines), and difficult-to-clean intricate mechanical parts (eg, fillers) may result in an ill-defined loss of microbiologic quality. Mechanical parts also result in cross-contamination with pathogens. Defeathering rubber fingers were found to spread C jejuni in poultry processing plants.135 Similarly, Salmonella species were spread by cross-contamination in a cattle-slaughtering plant.136 Overall attention to process design, sanitization practices, and environmental monitoring are all important to control Listeria as well as other bacterial pathogens.137

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May 9, 2021 | Posted by in MICROBIOLOGY | Comments Off on Food- and Waterborne Microorganisms
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