Reemergence of West Nile Virus Infections in Southern Greece, 2017

Maria Mavrouli Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Maria Mavrouli in
Current site
Google Scholar
PubMed
Close
,
Georgia Vrioni Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Georgia Vrioni in
Current site
Google Scholar
PubMed
Close
,
Violetta Kapsimali Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Violetta Kapsimali in
Current site
Google Scholar
PubMed
Close
,
Constantinos Tsiamis Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Constantinos Tsiamis in
Current site
Google Scholar
PubMed
Close
,
Spyridon Mavroulis Department of Dynamic Tectonic Applied Geology, Faculty of Geology and Geoenvironment, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Spyridon Mavroulis in
Current site
Google Scholar
PubMed
Close
,
Danai Pervanidou Hellenic Center for Disease Control and Prevention, Department of Epidemiological Surveillance and Intervention, Vector-borne Diseases Office, Athens, Greece;

Search for other papers by Danai Pervanidou in
Current site
Google Scholar
PubMed
Close
,
Charalambos Billinis Laboratory of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Thessaly, Karditsa, Greece;

Search for other papers by Charalambos Billinis in
Current site
Google Scholar
PubMed
Close
,
Christos Hadjichristodoulou Department of Hygiene and Epidemiology, Faculty of Medicine, University of Thessaly, Larissa, Greece

Search for other papers by Christos Hadjichristodoulou in
Current site
Google Scholar
PubMed
Close
, and
Athanassios Tsakris Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece;

Search for other papers by Athanassios Tsakris in
Current site
Google Scholar
PubMed
Close
Restricted access

Greece experienced the largest European West Nile virus (WNV) outbreak in 2010 since the 1996 Romania epidemic. West Nile virus reemerged in southern Greece during 2017, after a 2-year hiatus of recorded human cases, and herein laboratory findings, clinical features, and geographic distribution of WNV cases are presented. Clinical specimens from patients with clinically suspected WNV infection were sent from local hospitals to the Microbiology Department of Medical School, National and Kapodistrian University of Athens, and were tested for the presence of specific anti-WNV antibodies and WNV RNA. From July to September 2017, 45 confirmed or probable WNV infection cases were identified; 43 of them with an acute/recent infection, of which 24 (55.8%) experienced WNV neuroinvasive disease (WNND). Risk factors for developing WNND included advanced age, hypertension, and diabetes mellitus. A total of four deaths (16.7%) occurred, all in elderly patients aged > 70 years. Thirty-nine cases were identified in regional units that had not been affected before (36 in Argolis and two in Corinth, northeastern Peloponnese, and one in Rethymno, Crete). The remaining four cases were reported from previously affected regional units of northwestern Peloponnese. The reemergence of WNV after a 2-year hiatus of recorded human cases and the spread of the virus in newly affected regions of the country suggests that WNV has been established in Greece and disease transmission will continue in the future. Epidemiological surveillance, intensive mosquito management programs, and public awareness campaigns about personal protective measures are crucial to the prevention of WNV transmission.

Author Notes

Address correspondence to Athanassios Tsakris, Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Mikras Asias 75, Athens 11527, Greece. E-mail: atsakris@gmail.com

Authors’ addresses: Maria Mavrouli, Georgia Vrioni, Violetta Kapsimali, Constantinos Tsiamis, and Athanassios Tsakris, Department of Microbiology, Medical School, National and Kapodistrian University of Athens, Athens, Greece, E-mails: mmavrouli@med.uoa.gr, gvrioni@med.uoa.gr, vkapsimali@med.uoa.gr, ctsiamis@med.uoa.gr, and atsakris@gmail.com. Spyridon Mavroulis, Department of Dynamic Tectonic Applied Geology, Faculty of Geology and Geoenvironment, National and Kapodistrian University of Athens, Athens, Greece, E-mail: smavroulis@geol.uoa.gr. Danai Pervanidou, Hellenic Center for Disease Control and Prevention, Department of Epidemiological Surveillance and Intervention, Vector-borne Diseases Office, Athens, Greece, E-mail: pervanidou.keelpno@gmail.com. Charalambos Billinis, Laboratory of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Thessaly, Karditsa, Greece, E-mail: billinis@vet.uth.gr. Christos Hadjichristodoulou, Department of Hygiene and Epidemiology, Faculty of Medicine, University of Thessaly, Larissa, Greece, E-mail: xhatzi@med.uth.gr.

  • 1.

    Mavrouli M, Vrioni G, Vlahakis A, Kapsimali V, Mavroulis S, Antypas A, Tsakris A, 2015. West Nile virus: biology, transmission, clinical manifestations, diagnosis, therapeutic approaches, climatic correlates and prevention. Acta Microbiol Hellenica 60: 7–34.

    • Search Google Scholar
    • Export Citation
  • 2.

    Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M, 2003. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9: 311–322.

    • Search Google Scholar
    • Export Citation
  • 3.

    Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR, 2006. Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis 12: 468–474.

    • Search Google Scholar
    • Export Citation
  • 4.

    Marka A et al. 2013. West Nile virus state of the art report of MALWEST project. Int J Environ Res Public Health 10: 6534–6610.

  • 5.

    Colpitts TM, Conway MJ, Montgomery RR, Fikrig E, 2012. West Nile virus: biology, transmission, and human infection. Clin Microbiol Rev 25: 635–648.

    • Search Google Scholar
    • Export Citation
  • 6.

    Petersen LR, Marfin AA, 2002. West Nile virus: a primer for the clinician. Ann Intern Med 137: 173–179.

  • 7.

    Smithburn KC, Hughes TP, Burke AW, Paul JH, 1940. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 20: 471–473.

    • Search Google Scholar
    • Export Citation
  • 8.

    Gubler DJ, 2007. The continuing spread of West Nile virus in the western hemisphere. Clin Infect Dis 45: 1039–1046.

  • 9.

    Tsai TF, Popovici F, Cernescu C, Campbell GL, Nedelcu NI, 1998. West Nile encephalitis epidemic in southeastern Romania. Lancet 352: 767–771.

  • 10.

    Platonov AE et al. 2001. Outbreak of West Nile virus infection, Volgograd region, Russia, 1999. Emerg Infect Dis 7: 128–132.

  • 11.

    Nash D et al. 2001. The outbreak of West Nile virus infection in the New York City area in 1999. N Engl J Med 344: 1807–1814.

  • 12.

    Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, Savini G, Lelli R, 2010. Epidemiology of West Nile in Europe and in the Mediterranean basin. Open Virol J 4: 29–37.

    • Search Google Scholar
    • Export Citation
  • 13.

    Papa A et al. 2010. Ongoing outbreak of West Nile virus infections in humans in Greece, July–August 2010. Euro Surveill 15: 1–5, pii: 19644.

    • Search Google Scholar
    • Export Citation
  • 14.

    Danis K et al. 2011. Outbreak of West Nile virus infection in Greece, 2010. Emerg Infect Dis 17: 1868–1872.

  • 15.

    Vrioni G, Mavrouli M, Kapsimali V, Stavropoulou A, Detsis M, Danis K, Tsakris A, 2014. Laboratory and clinical characteristics of human West Nile virus infections during 2011 outbreak in southern Greece. Vector Borne Zoonotic Dis 14: 52–58.

    • Search Google Scholar
    • Export Citation
  • 16.

    Hogrefe WR, Moore R, Lape-Nixon M, Wagner M, Prince HE, 2004. Performance of immunoglobulin G (IgG) and IgM enzyme-linked immunosorbent assays using a West Nile virus recombinant antigen (preM/E) for detection of West Nile virus- and other flavivirus-specific antibodies. J Clin Microbiol 42: 4641–4648.

    • Search Google Scholar
    • Export Citation
  • 17.

    Prince HE, Lape’-Nixon M, Moore RJ, Hogrefe WR, 2004. Utility of the focus technologies West Nile virus immunoglobulin M capture enzyme-linked immunosorbent assay for testing cerebrospinal fluid. J Clin Microbiol 42: 12–15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Hadjichristodoulou C et al. 2015. West Nile Virus seroprevalence in the Greek population in 2013: a nationwide cross-sectional survey. PLoS One 10: e0143803.

    • Search Google Scholar
    • Export Citation
  • 19.

    Paz S, Semenza JC, 2013. Environmental drivers of West Nile fever epidemiology in Europe and western Asia—a review. Int J Environ Res Public Health 10: 3543–3562.

    • Search Google Scholar
    • Export Citation
  • 20.

    Lanciotti RS et al. 1999. Origin of West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 2333–2337.

    • Search Google Scholar
    • Export Citation
  • 21.

    Papa A, Bakonyi T, Xanthopoulou K, Vazquez A, Tenorio A, Nowotny N, 2011. Genetic characterization of West Nile virus lineage 2, Greece 2010. Emerg Infect Dis 17: 920–922.

    • Search Google Scholar
    • Export Citation
  • 22.

    Barzon L et al. 2013. Genome sequencing of West Nile virus from human cases in Greece, 2012. Viruses 5: 2311–2319.

  • 23.

    Danis K et al. 2011. Ongoing outbreak of West Nile virus infection in humans, Greece, July to August 2011. Euro Surveill 16: 1–5, pii: 19951.

    • Search Google Scholar
    • Export Citation
  • 24.

    Chaintoutis SC, Gewehr S, Mourelatos S, Dovas CI, 2016. Serological monitoring of backyard chickens in central Macedonia-Greece can detect low transmission of West Nile virus in the absence of human neuroinvasive disease cases. Acta Trop 163: 26–31.

    • Search Google Scholar
    • Export Citation
  • 25.

    ECDC, 2017. West Nile Fever—Annual Epidemiological Report for 2015. Available at: https://ecdc.europa.eu/sites/portal/files/documents/AER_for_2015-West-Nile-fever.pdf. Accessed April 10, 2018.

  • 26.

    Nur YA, Groen J, Heuvelmans H, Tuynman W, Copra C, Osterhaus AD, 1999. An outbreak of West Nile fever among migrants in Kisangani, Democratic Republic of Congo. Am J Trop Med Hyg 61: 885–888.

    • Search Google Scholar
    • Export Citation
  • 27.

    ECDC, 2018. Epidemiological Update: West Nile Virus Transmission Season in Europe, 2017. Available at: https://ecdc.europa.eu/en/news-events/epidemiological-update-west-nile-virus-transmission-season-europe-2017. Accessed April 10, 2018.

  • 28.

    Anis E, Grotto I, Mendelson E, Bin H, Orshan L, Gandacu D, Warshavsky B, Shinar E, Slater PE, Lev B, 2014. West Nile fever in Israel: the reemergence of an endemic disease. J Infect 68: 170–175.

    • Search Google Scholar
    • Export Citation
  • 29.

    Bernabeu-Wittel M, Ruiz-Perez M, del Toro MD, Aznar J, Muniain A, de Ory F, Domingo C, Pachon J, 2007. West Nile virus past infections in the general population of southern Spain. Enferm Infecc Microbiol Clin 25: 561–565.

    • Search Google Scholar
    • Export Citation
  • 30.

    Pervanidou D et al. 2014. West Nile virus outbreak in humans, Greece, 2012: third consecutive year of local transmission. Euro Surveill 19: 1–11, pii: 20758.

    • Search Google Scholar
    • Export Citation
  • 31.

    Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ, 2002. West Nile virus. Lancet Infect Dis 2: 519–529.

  • 32.

    Murray K et al. 2006. Risk factors for encephalitis and death from West Nile virus infection. Epidemiol Infect 134: 1325–1332.

  • 33.

    Pezzotti P et al. 2011. Prevalence of IgM and IgG antibodies to West Nile virus among blood donors in an affected area of north-eastern Italy, summer 2009. Euro Surveill 16: 1–5, pii: 19814.

    • Search Google Scholar
    • Export Citation
  • 34.

    Mansfield KL, Horton DL, Johnson N, Li L, Barrett AD, Smith DJ, Galbraith SE, Solomon T, Fooks AR, 2011. Flavivirus-induced antibody cross-reactivity. J Gen Virol 92: 2821–2829.

    • Search Google Scholar
    • Export Citation
  • 35.

    Gaibani P, Rossini G, 2017. An overview of Usutu virus. Microbes Infect 19: 382–387.

  • 36.

    Chaintoutis SC et al. 2014. Evaluation of a West Nile virus surveillance and early warning system in Greece, based on domestic pigeons. Comp Immunol Microbiol Infect Dis 37: 131–141.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 51 51 10
Full Text Views 532 126 1
PDF Downloads 218 49 1
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save