ARTICLE
Viruses in Mass Gatherings: Viral Waterborne and Foodborne Diseases
Silvana Augusta Rodrigues Portes1,2, Natália Maria Lanzarini1,2, Carmen Baur Vieira1, Jorlan Fernandes2,3, Alexandre dos Santos Silva2,4, Renata Carvalho de Oliveira3, Eliane Veiga da Costa4, Elba Regina
Sampaio de Lemos2*, Tulio Machado Fumian1
Laboratório de Virologia Comparada e Ambiental, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro/
RJ, Brazil 2Curso de Pós-Graduação em Medicina Tropical, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil 3Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil 4Laboratório Desenvolvimento Tecnológico em Virologia, Instituto Oswaldo Cruz, Fiocruz,
Rio de Janeiro, Brazil 5Laboratório de Enterovírus, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
1
Mass gatherings (MGs) events are attended by a number of people from different regions for several
purposes, such as sporting, religious or recreational activities. From August to September, 2016, Rio de Janeiro
hosted the Olympic and Paralympic Games. Based on this perspective, this article aims to review the updates
related to viral water and foodborne diseases and MGs. First, it describes poliovirus, a very important pathogen
in major events, especially on the aspect of vaccination coverage. Later, to make a brief overview on the situation
of viral gastroenteritis caused by rotavirus, norovirus, astrovirus and adenovirus, the work describes the importance of epidemiological and environmental surveillance and prevention of viral gastroenteritis outbreaks
Key words: viral waterborne diseases, viral foodborne diseases, mass gatherings
Mass gatherings (MGs) are defined as collective events which, for different reasons, as sporting,
religious or recreational activities, are attended by a
number of people from different regions of the world
(WHO 2010). The definition has been accepted when
over 1000 people attend such events; however, most
of the published literature reflects larger events, generally >25,000 spectators (Enock & Jacobs 2008).
These crowding events can lead to the emergence of infectious diseases, and rapid population movement can spread them across the world, posing a
challenge to public health policies (Abubakar et al.
2012). Several MGs are cited in the literature, including Hajj (religious), G20 (political), music festivals
(cultural), world cups and Olympics (sporting), being
the last ones cited in 68% of these papers (WHO 2008).
The significant increase in the international traffic and the rapid population movement at mass sporting
*Corresponding author: Elba Regina Sampaio de Lemos
E-mail: [email protected]
events provide health risks, including transmission of
emerging and reemerging diseases, epidemics and pandemics, facilitated by transportation and also through
people, animals, food, baggage and goods (Buss 2007).
A large portion of the studies reports the risk of
transmission of infectious diseases during MGs (Zieliński
2009). The main ones associated with outbreaks of illnesses caused by bacteria, while viral outbreaks have rarely
been evaluated in detail. In a review article, Abubakar et
al. (2012) cited 27 papers on detection of bacteria and 15
for virus detection in large events. Most of these 15 items
describes detection of airborne viruses such as influenza
virus, respiratory adenovirus and measles, and only one
food and waterborne outbreak of hepatitis A. In addition,
dengue, yellow fever, poliomyelitis, severe acute respiratory syndrome, viral hemorrhagic fevers, HIV, hepatitis B
and C, middle east respiratory syndrome, rabies, among
others, have also been considered in public health risks
policies in mass sporting events (Zieliński 2009, Blumberg et al. 2010, Gaines et al. 2014, Wilson et al. 2014).
Gallego et al. (2014) related the major communicable diseases in Brazil with risks for travelers, and
warned for water and foodborne illnesses caused by norovirus, rotavirus and astrovirus infections, but without
Virus Reviews & Research Vol 21 (2), July-December 2016
reference to adenovirus, poliovirus and hepatitis A virus.
Waterborne and Foodborne Viruses: Poliovirus, Rotavirus, Norovirus, Astrovirus and Adenovirus
Food and waterborne diseases remain a major
public health problem worldwide (European Food Safety
Authority 2012, Ritter & Tondo 2014). In Brazil, from 2000
to 2013, 8,857 food and waterborne outbreaks were reported, with 163,425 people infected and 112 deaths (Brazilian Ministry of Health 2015). Bacteria were detected in
53.69% of the outbreaks. However, it was not possible to
identify the etiological agent in 46.31% of them, probably
due to the lack of samples or because viruses are not included in the current Brazilian water and food regulations.
Gastroenteritis and hepatitis are among the major outbreaks reported in Brazil. The high incidence of
these illnesses in the country suggests that new food and
waterborne outbreaks could occur during the Olympic and Paralympic Games in 2016. Wilson et al. (2014)
corroborated these data, showing that 25% of diagnosed
diseases among travelers returning from Brazil between
1997 and 2013 were gastroenteritis. In addition, this author confirmed that in more than 50% of cases it was not
possible to identify the causative agent. It is noteworthy
that the lack of identification of the pathogen may be related to a failure in the surveillance system, leading consequently to the introduction or reintroduction of viral
agents. The major viral pathogens of gastroenteritis are
rotavirus, norovirus, astrovirus and enteric adenovirus.
For poliovirus, the risk of reintroduction of
wild poliovirus in Brazil, where the disease has been eliminated, needs to be considered and surveillance activities need to be intensified, especially during mass
events, when a large movement of people from all
over the world, especially tourists or residents in countries that still offer the risk to export the wild virus.
Poliovirus
Polioviruses are the etiologic agents of poliomyelitis, an acute viral infectious disease that affects humans. Among the different manifestations of the disease and aseptic meningitis in about 1% of cases, and the
classical picture of acute flaccid paralysis in 1 to 1.6% of
the cases, paralysis may occur affecting the breathing
and swallowing muscles, raising the risk of death for
the patient. The unapparent or asymptomatic infections
may occur in 90 to 95 % of cases (Stupka et al. 2012).
Poliomyelitis is caused by three serotypes of poliovirus (poliovirus type 1, 2 and 3), belonging to the
species Enterovirus C, genus Enterovirus, family Picornaviridae, order Picornavirales (Knowles et al. 2012).
Viruses are of 25 to 30 nm in diameter without lipid envelope and capsid of icosahedral symmetry. The poliovirus genome consists of a linear molecule of single stranded RNA (RNAss) of positive polarity (Rossignol et al.
2015). This virus spreads from person to person and the
33
most important route of transmission is fecal-oral, contaminated food and water, although the oral-oral route
may be responsible for some cases (Hird & Grassly 2012).
The incubation period ranges from 2 to 35 days
and the period of virus excretion in feces ranges from
2 to 3 days after the appearance of clinical manifestations(Mehndiratta et al. 2014). There is no treatment for
polio, but the disease is preventable through two vaccines administered in chilhood: a parenteral inactivated poliovirus 1, 2 and 3 vaccine (IPV) and a trivalent
attenuated polio vaccine (tOPV) (Sutter et al. 2010).
The initiative for global polio eradication poses
a major challenge to public health. Since 1988, when it
was launched at the 41st World Health Assembly in Geneva (GPEI 1988), the Global Eradication of Poliomyelitis Plan for 2000 was the scene of 125 endemic countries
and 350,000 cases per year. However, despite the efforts
to eradicate wild poliovirus, two countries, Afghanistan
and Pakistan remain endemic to this viral infection. In
2015, 54 and 20 cases were detected in Pakistan and Afghanistan, respectively and in 2016 (January to May) eight and four cases were detected in Pakistan and Afghanistan, respectively (GPEI, 2016, Morales et al 2016).
However, over the years several extra difficulties arose,
such as countries that had eliminated wild polioviruses
were surprised by the import and/or reintroduction by
countries that are still endemic. This fact was identified
mainly after 2005 and in recent years imported cases of
polio reported in 2014 in Equatorial Guinea, Cameroon,
Iraq, Syria and Ethiopia were observed (GPEI 2014 a, b).
Another factor of great importance in the process
of global eradication is associated with vaccine-derived
polioviruses (VDPVs). The VDPVs are identified from the
degree of genetic divergence from the Sabin vaccine strain.
Strains that have a level of divergence ≥1% for serotypes 1
and 3 or ≥0,6% for serotype 2 when compared to their corresponding vaccine strains are called VDPVs. VDPVs are
classified into 3 categories: 1. immunodeficiency-associated VDPV (iVDPV) are special cases that occur in people
with primary immunodeficiency. Unlike immunocompetent persons who excrete vaccine virus for a limited period
of time, some immunocompromised people are not able to
interrupt the replication of the vaccine virus after receiving
the oral polio vaccine (OPV). In this way, they may be excreting the vaccine virus with genetic mutations for prolonged
periods and serve as a source of reintroduction of poliovirus
after its eradication. iVDPVs pose a threat to the eradication. 2. Circulating vaccine-derived polioviruses (cVDPV)
occur when evidence of person to person transmission in
the community is carried out. 3. Ambiguous vaccine-derived polioviruses (aVDPV) is an exclusion classification,
where the investigation offers parameters not to be classified as cVDPV or iVDPV. Isolates may be of persons without known immunodeficiency or from an environmental
sample, with no evidence of movement (Guo et al. 2015).
The wild poliovirus has been eradicated in the
Americas, the Western Pacific region, Europe and Southeast Asia (Falleiros-Arlant et al. 2014). In Brazil, since
34
Viral gastroenteritis and mass gateherings • Portes et al.
1990 there are no cases and in 1994 the country received
the International Certificate for the eradication of indigenous transmission of wild poliovirus. By the circulation of wild poliovirus in these countries, Brazil faced
a major challenge during the Olympics and Pa­ralympic
Games. With major international traffic, the pos­sibility
of poliovirus reintroduction with consequent invol­
vement of people likely was considered, as that vaccine
coverage in Brazilian municipalities is still heterogeneous
Group A Rotavirus
Group A rotaviruses (RVA) are the main etiological agent of acute viral gastroenteritis in infants and young children worldwide (Tate et al. 2012). In 2011, a global
survey revealed that RVA was responsible for 197.000 of
700.000 acute gastroenteritis deaths, most of it recorded in
low-income countries of Asia and Africa (Tate et al. 2012,
Walker et al. 2013).
Anti-RVA vaccines have been developed over
the past 2 decades. The attenuated G1P[8] Rotarix vaccine (GlaxoSmithKline, Rixensart, Belgium) was introduced into the brazilian immunization program in
March, 2006. In Brazil, before routine universal mass
RVA vaccination, an estimated 3,525,053 diarrhea episodes, 655,853 outpatient healthcare facilities visits, 92,453
hospitalizations and 850 deaths in children younger
than 5 years were attributed to RVA infection annually
(Ministry of Health of Brazil 2015, Sartori et al. 2008).
Rotavirus genus belongs to the Reoviridae family,
is a 100-nm non-enveloped icosahedral particle with a
capsid made of three concentric protein layers, and its genome consist of 11 double-stranded RNA (dsRNA) gene
segments encoding six structural (VP) and six non-structural proteins (NSP). Based on two genes that codify the
outer capsid proteins, VP4 and VP7, a widely used binary
classification system was established for RVA, defined G
(from VP7, glycoprotein) and P (from VP4, protease-cleaved protein), genotypes (Bertol et al. 2015, Estes & Kapikian 2007). Based on antigenic properties of VP6, RVs
have been subdivided into eight serological species (A-H)
(Ciarlet & Estes 2002). Epidemiologically, RVA is the most
important for human infection and disease, responsible for
up to 90% of human infections (Armah et al. 2003). Thus
far, at least 27 G and 37 P genotypes have been identified
in RVA from humans and animals based on differences in
the nucleotide sequences of their VP7 and VP4 genes, respectively. Among these genotypes, more than three quarters of human RVAs are G1P[8], G2P[4], G3P[8], G4P[8]
and G9P[8], while approximately 12 % are G2P[4] (Banyai
et al. 2012, Matthijnssens et al. 2011, Trojnar et al. 2013).
RVA are the primary cause of acute dehydrating
diarrhea in infants and children under 5 years of age. These viruses are transmitted by the fecal-oral route, via contaminated water and food (Bernstein 2009). A significant
number of children can have asymptomatic infections,
yet shedding virus in their stools (up to 1011 particles per
gram of stool), thus serving as possible sources of virus wi-
thin the community (Desselberger 2014). The major symptoms associated with RVA disease in young children are
mild-to-severe watery diarrhea and vomiting (potentially
leading to dehydration), and low-grade fever, with symptoms lasting for up to 4–8 days (Estes & Kapikian 2007).
Despite their significance in causing severe acute
gastroenteritis (AGE), few studies have associated RVA
with foodborne AGE related outbreaks worldwide (Newell
et al. 2010). In the United States, RVA was associated
with less than 1% of all foodborne AGE related outbreaks
(Gastañaduy 2013). However, these viruses were a concern for the period of Rio 2016 Olympic and Paralympic
games, since new genotypes could be introduced or reintroduced in Brazil, reaching an unprotected population.
Norovirus
Noroviruses (NoVs), members of the Caliciviridae
family, are small, positive-polarity RNA viruses and were
recently recognized as the second most common cause
of severe childhood gastroenteritis (Rackoff et al. 2013).
Worldwide, NoVs are responsible for almost 50% of AGE
outbreaks and more than 90% of the non-bacterial AGE,
considered the major pathogens in outbreaks (Da Silva
Soares et al. 2014). Patients may present vomiting or diarrhea with or without nausea, and abdominal cramps are
common. The average incubation period is of 24–48 hours,
and symptoms typically resolve in 12–72 hours. Diarrheal stool is non-bloody, lacks mucus, and may be loose or
watery. Some individuals develop low-grade fever (Estes
2014). NoVs are now recognized to be a common cause of
gastroenteritis in closed settings, including nursing homes
and other healthcare settings, cruise ships and immunocompromised patients (Da Silva Soares et al. 2014; Clark &
Mckendrick 2004). NoVs transmission frequently occurs
by multiple routes, including by consumption of contaminated food or water, by person-to-person contact, and from
contaminated environments (fomites) (Sawyer et al. 1988,
Chadwick et al. 1994, Marks et al. 2000, Maunula et al. 2004).
Norovirus genus are small, positive-polarity RNA
viruses and were recently recognized as the second most
common cause of severe childhood gastroenteritis. Noroviruses are positive-sense, single-stranded, non-enveloped RNA viruses. The linear RNA genome is organized in
three open reading frames (ORFs). ORF1 encodes a large
polyprotein, which is cleaved by the virus-encoded protease into six non-structural proteins including the viral polymerase. ORF2 and ORF3 encode the major and minor capsid proteins VP1 and VP2, respectively (Glass et al. 2000).
NoV is classified into six genogroups (GI to GVI)
based on VP1 amino acid sequence. Each genogroup can
be further divided into genotypes, and at least 36 genotypes are recognized to date (Caddy et al. 2014). Despite
the wide genetic NoV diversity, GII.4 has been described as
the most prevalent NoV genotype associated with AGE outbreaks and sporadic cases worldwide, since the mid-1990s
(Fankhauser et al. 2002, Hasing et al. 2013, Vega et al. 2014),
including in Brazil (Victoria et al. 2007, Fioretti et al. 2011).
Virus Reviews & Research Vol 21 (2), July-December 2016
NoVs have been identified as the cause of 73%
to more than 95% outbreaks and approximately half of
all gastroenteritis outbreaks worldwide (Atmar & Estes
2006). NoV presents characteristics such as: highly contagious, rapidly and prolifically shed, constantly evolving,
evoking limited immunity, and only moderately virulent,
allowing most of those infected to fully recover, thereby
maintaining a large susceptible pool of hosts. These characteristics have enabled noroviruses to become the leading cause of endemic diarrheal disease across all age
groups, the leading cause of foodborne disease, and the
cause of half of all gastroenteritis outbreaks worldwide (Patel et al. 2009, Hall et al. 2011, Scallan et al. 2011).
Astrovirus
Human astrovirus (HAstVs) belongs to the Astroviridae family, Mamastrovirus genera, and contains
single-stranded, positive-sense, polyadenylated RNA 6.2–
7.8 kilobases (kb) in length without an envelope, encased
within an icosahedral capsid. The genome contains three
ORFs designated ORF1a, ORF1b and ORF2 (Mendez &
Arias 2007). The two first ORFs encode non-structural
proteins, including viral proteinase and RNA polymerase
and ORF2 encodes the capsid protein precursor. Mamastrovirus genera associated to human disease is subdivided
into four divergent species: MAstV 1 (the classical human astrovirus 1–8), MAstV 6 (AstV MLB1-3), MAstV 8
(AstV VA1 and VA3, also known as HMO-C and HMO-B, respectively) and MAstV 9 (AstV VA2, also known
as HMO-A, and VA4) (Finkbeiner et al.2008; Finkbeineret al.2009a,b, Jiang et al. 2013, Bosch et al. 2014).
HAstVs, especially classic HAstVs, are considered gastrointestinal pathogens affecting children worldwide, with very few reports of HAstV-mediated disease
in normal healthy adults (Grohmann 1993, Glass et al.
1996, Belliot et al. 1997). HAstVs are transmitted essentially through the fecal-oral route, and food and water may
act as vehicles for transmission of human enteric viruses.
Several large HAstV outbreaks have been associated with
consumption of contaminated food (Oishi et al. 1994,
Mitchell et al. 1995, Bosch 2007, Koopmans et al. 2008).
Infections are usually self-limiting but can also
spread systemically and cause severe infections in immunocompromised patients. The main symptom of infection
caused by HAstV is watery diarrhea, which is often associated with vomiting, fever, anorexia, and abdominal pain
(Matsui & Greenberg 2001, Bosch et al. 2014). HAstV-1 is
the most frequent genotype detected worldwide, followed
by HAstV-2, 3, 4, e 5 (Sakamoto et al. 2000, Méndez-Toss
et al. 2004). Several studies have reported the same pattern
in Brazil (Das Dores et al. 2002, Silva et al. 2006, Victoria
et al. 2014, Silva et al. 2009, Da Silva Soares et al. 2014).
Padron-Regalado et al. (2014) demonstrated detection of HAstVs in the years 2011 – 2013, during a molecular and epidemiological study performed to investigate
viral gastroenteritis in the annual Islamic pilgrimage to
Mecca (Hajj). These viruses were the most detected during
35
this three years study and most frequent genotypes were
HAstV-1, 2 e 5. These findings highlight the importance
of monitoring these viruses as well as new genotypes and
variants, during Rio 2016 Olympic and Paralympic Games.
Adenovirus
Human adenoviruses (HAdVs) belong to the family Adenoviridae, Mastadenovirus genus. Currently, there are 67 identifiable HAdVs serotypes. These are divided
into seven subgenera or species (A–G) (Ghebremedhin
2014). Adenoviruses have a non-enveloped, icosahedral virion that consists of a core containing linear double-stranded DNA (26–45 kb) enclosed by a capsid (Evans 2002).
The capsid is composed of 252 capsomers, 240 of which are
hexons and 12 are pentons. Each penton projects a single
fiber that varies in length for each serotype, an exception
being the enteric adenoviruse (EAd) pentons (serotypes 40
and 41) that project two fibers (De Jong et al. 1999; Horwitz 2001).
Adenoviruses are associated with several clinical
illnesses involving almost every organ of the human system.
Illnesses induced by adenoviruses include upper (pharyngitis and tonsillitis) and lower (bronchitis, bronchiolitis
and pneumonia) respiratory illnesses, conjunctivitis, cystitis and gastroenteritis. Several studies reported that HAdVs
are third only to rotaviruses and noroviruses as causative
agents of acute gastroenteritis in infants and young children (Rezig et al. 2006, Horwitz 2001). Species F HAdVs are
more frequently associated with acute gastroenteritis, more
specifically subtypes 40 and 41 (Ghebremedhin 2014).
Most illnesses caused by HAdVs are acute and self-limiting. Although the symptomatic phase may be short, all adenoviruses can remain in the
gastrointestinal tract and continue to be excreted
for an extended period of time (Wood et al. 1988).
Adenovirus transmission occurs by the fecal-oral route,
and by ingestion of contaminated food and water (Boone
& Gerba 2007). It is known that HAdVs show high stability in the environment (Lee & Kim 2002, Cheong et al.
2009, Hartmann et al. 2013) and in food matrices (Cheong et al. 2009). Brazilian studies have also demonstrated
that enteric HAdVs are high disseminated in the aquatic environment (Miagostovich et al. 2008, Barrella et al.
2009, Moresco et al. 2012, Fumian et al. 2013, Prado &
Miagostovich 2014). There is no report linking gastroenteritis outbreaks during big events and HAdVs, however
these viruses were considered a potential risk to human
health during Rio 2016 Olympic and Paralympic Games.
In addition, these viruses are considered viral markers
of human fecal contamination in aquatic environments.
DISCUSSION
The city of Rio de Janeiro, Brazil, was the host of
the Olympic and Paralympic Games, from 5-12th August
and 7-18th September, respectively. Football matches also
took place in other Brazilian cities such place in other Bra-
36
Viral gastroenteritis and mass gateherings • Portes et al.
zilian cities such as Belo Horizonte, Brasilia, São Paulo and
Salvador (Gaines et al. 2014). Major international events,
including sporting, are important challenges for recognition and management of infectious diseases in the host
country and travelers returning to their home countries,
demanding from the hosts a commitment to organize a safe
event for tourists, athletes as well as to the local population
(Blumberg et al, 2010, Jentes et al. 2010). Regulations and
multilateral agreements have been signed in order to monitor and control the international movement of these diseases. In the International Health Regulations (IHR), 2005,
the basic capabilities to optimize the response to public health events are planned. Brazilian Ministry of Health has
carried out assessments of installed capacities at the central, state and local levels to adapt them to IHR guidelines.
According to the Brazilian experience, the pressure on the unified health system (Sistema Único de Saúde
- SUS) is low during these large gathering events and does
not affect the provision of services to the local population.
This pattern is described in the international literature,
which showed that 1-2% of participants of these events required some kind of health care (WHO 2008). Even with
this experience, it is worth noting that gastroenteric viral
agents (RVA, NoV, HAstV and HAdV) may be responsible
for water and foodborne gastroenteritis outbreaks, endangering the health of tourists and local people during the
event. Prevalence of these pathogens in river waters, beaches, sewage, urban lakes and streams polluted in cities with
high population density, such as Rio de Janeiro, including
areas of Olympic competitions, is well known (Homma et
al. 1975, Prado & Miagostovich, 2014, Victoria et al. 2014).
Despite waterborne viral diseases, it should be noted that during sporting events, there is an increased supply
of food, with an estimation of more than 10 million extra
meals served and consumed, in which the risk of gastroenteritis outbreaks needs to always be considered (Cunha et al.
2014). In this context, in order to prevent food and waterborne diseases, Brazil has developed a risk assessment tool,
able to access and grade Brazilian food services in the cities
that will host mass sporting events (Ritter & Tondo 2014).
Regarding the overall picture of poliomyelitis, as
there were still countries with circulation of wild poliovirus
circulation and also with VDPV, Brazil faced some concerns on the scene offered to the Olympics and 2016 Paralympics, when there was a large influx of people from all over
the world. The Ministry of Health recommended indicators
to maintain the country free of the diseases, such as achieving and maintaining coverage of 95 % across the country,
surveillance of suspected clinical cases with sample collection, epidemiological investigation and mandatory reporting. It is worth mentioning that it is very difficult to identify the introduction and polio outbreak immediately, since
asymptomatic infections occur up to 72 % of cases, and
thus, there may be spread of infection to other individuals
before the first case of paralysis is detected (CDC 2015).
Given this context, the vaccine is the best form
of prevention. It was recommended that individuals, who
come to Brazil from endemic countries, complete the ba-
sic vaccination against poliomyelitis according to what
is recommended in the country of origin before the trip.
In the face of all challenges during mass gatherings, viral food and waterborne diseases are considered
important health risks. The literature is focused on studies reporting the aspects related to planning and management strategies for these events; however, there are few
reports on the occurrence of outbreaks caused by contaminated food (Morillo et al. 2010). Viral etiology of these cases may be improperly underestimated compared to
those of bacterial etiology. This may be due to difficulties
of identification and recognition of an outbreak of viral
origin, especially in less serious cases that most often are
not observed by health professionals. In terms of sporting events, where there is a greater probability of viral
gastroenteritis due to consumption of unsafe water and
food, monitoring and detection should be continuous, primarily to identify the source and detect the agent in order to prevent its spread. However, as most of the outbreaks are not identified, it is recommended that the public
(participants and spectators) obtain general health information, including risks and prevention of these diseases
in an attempt to minimize consequences of an outbreak.
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