Download A Novel Mode of Transmission for Human Enterovirus Infection Is

E D I T O R I A L C O M M E N TA R Y
A Novel Mode of Transmission for Human Enterovirus
Infection Is Swimming in Contaminated Seawater:
Implications in Public Health and in Epidemiological
Surveillance
Nicolas Leveque and Andreoletti Laurent
Medical and Molecular Virology Laboratory (EA/IFR53), University Hospital Center and Medical School of Reims, Reims, France
(See the article by Begier et al. on pages 616–23)
Enteroviruses (EVs; Picornaviridae) are
among the most common viruses infecting humans worldwide [1]. These positive-RNA viruses possess a high genetic
diversity (89 serotypes), and they can
evolve through genetic mutations or recombination events that are associated
with the potential emergence of new epidemic serotypes [2, 3]. Although the majority of human EV infections remain
asymptomatic, these viruses are associated
with a large diversity of clinical syndromes,
ranging from minor febrile illness to severe and potentially fatal pathologies, including aseptic meningitis, encephalitis,
myopericarditis, acute flaccid paralysis,
and severe neonatal sepsis-like disease [1,
4]. The primary mode of direct or indirect
transmission of EV remains the fecal-oral
route [4]. However, other efficient modes
of transmission, such as respiratory or eye
Received 2 June 2008; accepted 2 June 2008;
electronically published 18 July 2008.
Reprints or correspondence: Dr. Laurent Andréoletti,
Laboratoire de Virologie, Service de Microbiologie, Hôpital
Robert Debré, EA/IFR53 Faculté de médecine de Reims, Ave.
du Général Koenig, 51092 Reims Cedex, France (landreoletti
@chu-reims.fr).
Clinical Infectious Diseases 2008; 47:624–6
2008 by the Infectious Diseases Society of America. All
rights reserved.
1058-4838/2008/4705-0006$15.00
DOI: 10.1086/590563
mucosal routes, have been reported [5, 6].
Patterns such as direct person-to-person
contact seem to be important in many
outbreaks of EV infection. However, because human EVs are enteric viruses,
water-related transmission remains of primary importance for indirect viral transmission and represents a potentially significant human health risk [7, 8].
Consequently, the information regarding
the detection of EV in water, such as epidemiological data related to waterborne
diseases, is crucial to modern public health
survey systems [8].
In this issue of Clinical Infectious Diseases, Begier et al. [9] present an epidemiological and virological analysis of an
outbreak of concurrent echovirus 30 (E30)
and coxsackievirus A1 (CVA1) infections
associated with sea swimming among a
group of travelers to Mexico in 2004. This
study reports, for the first time to our
knowledge, an important public health
problem: swimming in contaminated seawater as a novel mode of transmission of
EVs. Previous studies reported potential
transmission of EVs through clams or oysters, drinking water, and recreational hot
spring waters but never through contaminated seawater [10–13]. In the study by
Begier et al. [9], the authors identified
624 • CID 2008:47 (1 September) • EDITORIAL COMMENTARY
cases of concurrent E30 and CVA1 infections associated with swimming in seawater. They used partial viral capsid protein 1 (VP1) gene analysis to perform
direct genotyping identification, which revealed the presence of E30 in CSF samples
and the presence of E30 and CVA1 in stool
samples [14]. For the 29 symptomatic travelers, the clinical and epidemiological parameters related to this epidemic event were
recovered and analyzed; some clinical syndromes were statistically significantly associated with EV contamination through swimming in seawater. The originality of this article
also resides in the description of the first potential outbreak of CVA1 infection reported
among immunocompetent patients since the
only published outbreak of CVA1 gastroenteritis among immunocompromised children
(bone marrow transplant recipients) was
previously reported [15, 16].
Because EVs are easily dispersed, display
serotypic and genetic diversity, and can
tolerate extreme conditions (naked viruses), they are ubiquitous and can easily
contaminate water [4, 17]. The presence
of these waterborne enteric pathogens in
recreational water presents a potentially
significant human health risk [12]. Although major outbreaks of waterborne
disease are comparatively rare, there is
substantial evidence that human EVs are
frequently present in recreational waters
and are responsible for a low incidence of
waterborne microbial disease [8, 10]. Usually, these diseases are associated with low
morbidity rates among healthy adults [8].
However, it is possible that new recombinant EV strains may escape the immune
system or demonstrate high fitness or infectivity levels and, therefore, may cause
severe clinical syndromes, even in immunocompetent persons, as observed in
the study by Begier et al. [9]. Moreover,
EVs can cause severe illness and even death
in young children, the elderly, or persons
with compromised immune systems [1,
4]. As the epidemiology of waterborne diseases is changing, there is growing global
public health concern about new and reemerging infectious diseases, which are occurring through a complex interaction of
social, economic, evolutionary, and ecological factors [17, 18].
A relatively small number of viruses
have been proven to be true etiologic
agents in outbreaks of waterborne disease
in humans; these viruses include rotavirus,
calicivirus, astrovirus, and some enteric
adenoviruses [19]. Etiologic agents in outbreaks of waterborne disease have infrequently been identified because of inadequate diagnostic technology, but many
outbreaks of infection of unknown etiology that have been recently reported were
likely attributable to viral agents [19]. In
the study by Begier et al. [9], the integration of new molecular techniques for identification of EVs provides an important
complement to the field investigation, as
shown by the identification of CVA1, an
EV rarely identified in outbreaks of EV
disease [1]. It is evident that new molecular tools are useful and of major interest
to detect and to quantify the levels of EV
genomes in recreational water [10]. Genetic identification of the EV serotype by
partial sequencing of VP1 and 3Dpol genes
can allow identification of recombinant or
mosaic EV strains [3]. Moreover, it is necessary to use new, integrated cell culture
and molecular systems to determine the
infectivity of the EV strains detected in
water samples [20]. The combination of
these systems is now necessary to detect
infectious EV strains, to observe the levels
of contamination in recreational water,
and to genetically identify and compare
serotypes or strains incriminated as causes
of cases or outbreaks of waterborne
disease.
Prevention of an epidemic of waterborne EV infection could be efficiently
performed by prospective virological surveillance to indicate the infectivity of the
strains and the levels of contamination [7,
8]. However, this approach should be associated with a public health surveillance
system, such as the US Outbreak Surveillance System, for data collection and reporting of outbreaks of waterborne disease
[21–24]. Moreover, sewage has to be
treated to achieve efficient inactivation of
the viral agents before it is poured in seawater, especially in tourist areas [10]. In
the context of an increasing tourist population, it is of major importance to establish specific epidemiological and virological measures aimed at reducing the risk
of viral waterborne infectious diseases.
Moreover, recent studies identified links
between climate variability and the occurrence of microbial agents in water.
These relationships need further evaluation in the present context of ecological
stresses.
In conclusion, the detection of EVs and
other enteric viruses in seawater and the
determination of the epidemiology of waterborne diseases are crucial to modern
public health and epidemiological survey
systems. These measures for the epidemiological and virological control of recreational seawater may become additional
prerequisites to obtain quality labels for
the housing of tourist populations.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
Acknowledgments
Potential conflicts of interest. N.L. and L.A.:
no conflicts.
14.
References
1. Khetsuriani N, Lamonte-Fowlkes A, Oberste
S, Pallansch MA; Centers for Disease Control
and Prevention. Enterovirus surveillance—
United States, 1970–2005. MMWR Surveill
Summ 2006; 55:1–20.
Stanway G, Brown F, Christian P, et al. Picornaviridae. In: Fauquet CM, Mayo MA,
Maniloff J, Desselberger U, Ball LA, eds. Virus
taxonomy-classification and nomenclature of
viruses. 8th Report of the International Committee on the Taxonomy of Viruses. Amsterdam: Elsevier Academic Press, 2005:757–78.
Lukashev AN, Ivanova OE, Eremeeva TP,
Gmyl LV. Analysis of echovirus 30 isolates
from Russia and new independent states revealing frequent recombination and reemergence of ancient lineages. J Clin Microbiol
2008; 46:665–70.
Khetsuriani N, Parashar UD. Enteric viral infections. In: Dale DC, Federman DD, eds.
Scientific American medicine. New York:
WebMD, 2003:1758–66.
Jacques J, Moret H, Minette D. Epidemiological, molecular and clinical features of enterovirus respiratory infections in French children between 1999 and 2005. J Clin Microbiol
2008; 46:206–13.
Nilsson EC, Jamshidi F, Johansson SM, Oberste MS, Arnberg N. Sialic acid is a cellular
receptor for coxsackievirus A24 variant, an
emerging virus with pandemic potential. J Virol 2008; 82:3061–8.
Hot D, Legeay O, Jacques J, et al. Detection
of somatic phages, infectious enteroviruses
and enterovirus genomes as indicators of human enteric viral pollution in surface water.
Water Res 2003; 37:4703–10.
Fong TT, Lipp EK. Enteric viruses of humans
and animals in aquatic environments: health
risks, detection, and potential water quality
assessment tools. Microbiol Mol Biol Rev
2005; 69:357–71.
Begier EM, Oberste MS, Landry ML, et al.
High morbidity associated with an outbreak
of concurrent echovirus 30 and coxsackievirus
A1 infections associated with sea swimming
among a group of travelers to mexico. Clin
Infect Dis 2008; 47:616–23 (in this issue).
Hsu BM, Chen CH, Wan MT. Prevalence of
enteroviruses in hot spring recreation areas of
Taiwan. FEMS Immunol Med Microbiol
2008; 52:253–9.
Choo YJ, Kim SJ. Detection of human adenoviruses and enteroviruses in Korean oysters
using cell culture, integrated cell culture-PCR,
and direct PCR. J Microbiol 2006; 44:162–70.
Nwachuku N, Gerba CP. Health risks of enteric viral infections in children. Rev Environ
Contam Toxicol 2006; 186:1–56.
Lodder-Verschoor F, de Roda Husman AM,
van den Berg HH, Stein A, van Pelt-Heerschap
HM, van der Poel WH. Year-round screening
of noncommercial and commercial oysters for
the presence of human pathogenic viruses. J
Food Prot 2005; 68:1853–9.
Oberste MS, Nix WA, Maher K, Pallansch MA.
Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing.
J Clin Virol 2003; 26:375–7.
EDITORIAL COMMENTARY • CID 2008:47 (1 September) • 625
15. Townsend TR, Bolyard EA, Yolken RH, et al.
Outbreak of Coxsackie A1 gastroenteritis: a
complication of bone-marrow transplantation. Lancet 1982; 1:820–3.
16. Madeley CR. Fatal diarrhoea and coxsackie A1
virus. Lancet 1982; 1:1013–4.
17. Theron J, Cloete TE. Emerging waterborne
infections: contributing factors, agents, and
detection tools. Crit Rev Microbiol 2002; 28:
1–26.
18. Lund E. Waterborne virus diseases. Ecol Dis
1982; 1:27–35.
19. Leclerc H, Schwartzbrod L, Dei-Cas E. Mi-
crobial agents associated with waterborne diseases. Crit Rev Microbiol 2002; 28:371–409.
20. Shieh YC, Wong CI, Krantz JA, Hsu FC. Detection of naturally occurring enteroviruses in
waters using direct RT-PCR and integrated cell
culture–RT-PCR. J Virol Methods 2008; 149:
184–9.
21. Dziuban EJ, Liang JL, Craun GF, et al.; Centers
for Disease Control and Prevention. Surveillance for waterborne disease and outbreaks
associated with recreational water—United
States, 2003–2004. MMWR Surveill Summ
2006; 55:1–30.
626 • CID 2008:47 (1 September) • EDITORIAL COMMENTARY
22. Naumova EN, O’Neil E, MacNeill I. INFERNO. A system for early outbreak detection
and signature forecasting. MMWR Morb
Mortal Wkly Rep 2005; 54(Suppl):77–83.
23. Berger M, Shiau R, Weintraub JM. Review of
syndromic surveillance: implications for waterborne disease detection. J Epidemiol Community Health 2006; 60:543–50.
24. Henning KJ. What is syndromic surveillance?
MMWR Morb Mortal Wkly Rep 2004;
53(Suppl):5–11.