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 1980s
55 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 appendectomies
57 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 salads
65 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 Japan
67 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 Canada
85 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 cause
98 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 food
114,
115 and water
10,
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, PrP
c), 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 PrP
c is converted to an abnormal, protease-resistant form of the protein (PrP
res). 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.