Emerging Rodent-Borne Viral Zoonoses in Trento, Italy

EcoHealth - Tập 15 - Trang 695-704 - 2018
Valentina Tagliapietra1, Roberto Rosà1, Chiara Rossi1, Fausta Rosso1, Heidi Christine Hauffe1, Michele Tommasini2, Walter Versini2, Attilio Fabio Cristallo3, Annapaola Rizzoli1
1Department of Biodiversity and Molecular Ecology, Research and Innovation Center, Fondazione Edmund Mach, San Michele all’Adige, Italy
2Azienda Provinciale per i Servizi Sanitari di Trento, Trento, Italy
3Servizio di Immunoematologia e Trasfusione, Ospedale S. Chiara, Trento, Italy

Tóm tắt

Rodent-borne hanta- and arenaviruses are an emerging public health threat in Europe; however, their circulation in human populations is usually underestimated since most infections are asymptomatic. Compared to other European countries, Italy is considered ‘low risk’ for these viruses, yet in the Province of Trento, two pathogenic hantaviruses (Puumala and Dobrava-Belgrade virus) and one arenavirus (Lymphocytic Choriomeningitis Virus) are known to circulate in rodent reservoirs. In this paper, we performed a follow-up serological screening in humans to detect variation in the prevalence of these three viruses compared to previous analyses carried out in 2002. We also used a statistical model to link seropositivity to risk factors such as occupational exposure, cutting firewood, hunting, collecting mushrooms, having a garden and owning a woodshed, a dog or a companion rodent. We demonstrate a significant increase in the seroprevalence of all three target viruses between 2002 and 2015, but no risk factors that we considered were significantly correlated with this increase. We conclude that the general exposure of residents in the Alps to these viruses has probably increased during the last decade. These results provide an early warning to public health authorities, and we suggest more detailed diagnostic and clinical investigations on suspected cases.

Tài liệu tham khảo

Aberle S (2013) Hantavirus Infektionen in Österreich. [Hantavirus infections in Austria]. Virusepidemiologische Information. 2013:6/13. Vienna: University of Austria. Available from: http://www.virologie.meduniwien.ac.at/home/upload/vei/v2013/0613.pdf Abu Sin M, Stark K, van Treeck U, Dieckmann H, Uphoff H, Hautmann W, Bornhofen B, Jensen E, Pfaff G, Koch J (2007) Risk factors for hantavirus infection in Germany, 2005. Emerging Infectious Diseases 13:1364–1366 Armstrong LR, Zaki SR, Goldoft MJ, Todd RL, Khan AS, Khabbaz RF, Ksiazek TG, Peters CJ (1995) Hantavirus pulmonary syndrome associated with entering or cleaning rarely used, rodent-infested structures. Journal of Infectious Diseases 172(4):1166 Avšič Županc T, Korva M, Markotić A (2014) HFRS and hantaviruses in the Balkans/South-East Europe. Virus Res earch 187:27-33. https://doi.org/10.1016/j.virusres.2013.12.042 Bonthius DJ (2012) Lymphocytic choriomeningitis virus: an underrecognized cause of neurologic disease in the fetus, child, and adult. Seminars in Pediatric Neurology 19(3):89-95. https://doi.org/10.1016/j.spen.2012.02.002 Bordes F, Blasdell K, Morand S (2015) Transmission ecology of rodent-borne diseases: New frontiers. Integrative Zool ogy 10(5):424-35. https://doi.org/10.1111/1749-4877.12149 Bundesamt für Gesundheit (BAG) (2013) Meldepflichtige Infektionskrankheiten Schweiz und Fürstentum Liechtenstein. Datendetails Hantavirus-Infektionen, VHF. [Notifiable Infectious diseases Switzerland and Principality of Liechtenstein. Data details Hantavirus-Infections, VHF]. Berne: BAG; Accessed 10 Dec 2013. German. Available from: https://www.bag.admin.ch/bag/it/home.html Childs JE, Glass GE, Korch GW, Ksiazek TG, LeDuc JW (1992) Lymphocytic choriomeningitis virus infection and house mouse (Mus musculus) distribution in urban Baltimore. The American Journal of Tropical Medicine and Hygiene 47:27–34 Clement J, Vercauteren J, Verstraeten W, Ducoffre G, Barrios J, Vandamme AM, Maes P, Van Ranst M (2009) Relating increasing hantavirus incidences to the changing climate: the mast connection. International Journal of Health Geographics 8:1. https://doi.org/10.1186/1476-072x-8-1 Crowcroft NS, Infuso A, Ilef D, Le Guenno B, Desenclos JC, Van Loock F, et al (1999) Risk factors for human hantavirus infection: Franco-Belgian collaborative case-control study during 1995-6 epidemic. British Medical Journal 318(7200):1737-1738 de Lamballier X, Fulhorst CH, Charrel RN (2007) Prevalence of antibodies to lymphocytic choriomeningitis virus in blood donors in southeastern France. Transfusion 47: 172-173 De Ory F, Gegúndez MI, Fedele CG, Sánchez-Seco MP. Los virus Toscana, West Nile y de la coriomeningitis linfocitaria como causantes de meningitis en España. Med Clin (Barc). 2009;132:587–90 https://doi.org/10.1016/j.medcli.2008.10.057 Dobec M, Dzelalija B, Punda-Polic V, Zoric I (2006) High prevalence of antibodies to lymphocytic choriomeningitis virus in a murine typhus endemic region in Croatia. Journal of Medical Virology 78(12):1643-1647 Engler O, Klingstrom J, Aliyev E, Niederhauser C, Fontana S, Strasser M, Portmann J, Signer J, Bankoul S, Frey F, Hatz C, Stutz A, Tschaggelar A, Mutsch M (2013) Seroprevalence of hantavirus infections in Switzerland in 2009: difficulties in determining prevalence in a country with low endemicity. Eurosurveillance 18(50):pii=20660. doi: http://dx.doi.org/10.2807/1560-7917.ES2013.18.50.20660 European Network for Diagnostics of “Imported” Viral Diseases (ENIVD): Case Definition of Hantavirus. Hantavirus Hemorrhagic Fever with Renal Syndrome (HFRS). (Created by M. Niedrig, A. Vaheri, R.Schädler). http://www.enivd.de/index.htm. Faber M, Wollny T, Schlegel M, Wanka KM, Thiel J, Frank C, Rimek D, Ulrich RG, Stark K (2013) Puumala virus outbreak in Western Thuringia, Germany, 2010: epidemiology and strain identification. Zoonoses and Public Health 60(8):549-554. https://doi.org/10.1111/zph.12037 Faulde M, Sobe D, Kimmig P, Scharninghausen J (2000) Renal failure and hantavirus infection in Europe. Nephrology Dialysis Transplantation 15(6):751-753 Fritz CL, Fulhorst CF, Enge B, Winthrop KL, Glaser CA, Vugia DJ (2002) Exposure to rodents and rodent-borne viruses among persons with elevated occupational risk. Journal of Occupational and Environmental Medicine 44(10):962-967 Gherasim A, Hjertqvist M, Lundkvist Å, Kühlmann-Berenzon S, Carlson JV, Stenmark S, Widerström M, Österlund A, Boman H, Ahlm C, Wallensten A (2015) Risk factors and potential preventive measures for nephropatia epidemica in Sweden 2011-2012: a case-control study. Infect Ecol Epidemiol 5:27698. https://doi.org/10.3402/iee.v5.27698 Guzzetta G, Tagliapietra V, Perkins SE, Hauffe HCH, Poletti P, Merler S, Rizzoli A (2017) Population dynamics of wild rodents induce stochastic fadeouts of a zoonotic pathogen. Journal of Animal Ecology https://doi.org/10.1111/1365-2656.12653 Haredasht SA, Taylor CJ, Maes P, Verstraeten WW, Clement J, Barrios M, Lagrou K, Van Ranst M, Coppin P, Berckmans D, Aerts JM (2013) Model-based prediction of nephropathia epidemica outbreaks based on climatological and vegetation data and bank vole population dynamics. Zoonoses and Public Health 60(7):461-477. https://doi.org/10.1111/zph.12021 Heyman P, Ceianu CS, Christova I, Tordo N, Beersma M, Joao Alves M, Lundkvist A, Hukic M, Papa A, Tenorio A, Zelena H, Esbauer S, Visontai I, Golovljova I, Connell J, Nicoletti L, Van Esbroeck M, Gjeruldsen Dudman S, Aberle SW, Avšić-Županc T, Korukluoglu G, Nowakowska A, Klempa B, Ulrich RG, Bino S, Engler O, Opp M, Vaheri A (2011) A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005–2010. Eurosurveillance 16(36):pii=19961 Heyman P, Vervoort T, Colson P, Chu YK, Avšić-Županc T, Lundkvist Å (1999) A major outbreak of hantavirus infection in Belgium in 1995 and 1996. Epidemiology and Infection 122(3):447-453 Jonsson CB, Figueiredo LT, Vapalahti O (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical Microbiology Reviews 23(2):412-441. https://doi.org/10.1128/cmr.00062-09 Kallio ER, Poikonen A, Vaheri A, Vapalahti O, Henttonen H, Koskela E, Mappes T (2006) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of the Royal Society of London B: Biological Sciences 273(1602):2771-2776. https://doi.org/10.1098/rspb.2006.3645 Kallio-Kokko H, Laakkonen J, Rizzoli A, Tagliapietra V, Cattadori I, Perkins SE, Hudson PJ, Cristofolini A, Versini W, Vapalahti O, Vaheri A, Henttonen H (2006) Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiology and Infection 134(4):830-836. https://doi.org/10.1017/s0950268805005431 Karesh WB, Dobson A, Lloyd-Smith JO, Lubroth J, Dixon MA, Bennett M, Aldrich S, Harrington T, Formenty P, Loh EH, Machalaba CC, Thomas MJ, Heymann DL (2012) Ecology of zoonoses: natural and unnatural histories. The Lancet 380(9857):1936-1945. https://doi.org/10.1016/s0140-6736(12)61678-x Kirsanovs S,Klempa B,Franke R,Lee MH,Schönrich G,Rang A,Kruger DH. Genetic reassortment between high-virulent and low-virulent Dobrava-Belgrade virus strains. Virus Genes.2010;41(3):319-28. https://doi.org/10.1007/s11262-010-0523-2 Klempa, B, Avšić-Županc T., Clement J, Dzagurova TK, Henttonen H, Heyman P, Jakab F, Kruger DH, Maes P, Papa A, Tkachenko EA, Ulrich RG, Vapalahti O, Vaheri A (2013) Complex evolution and epidemiology of Dobrava-Belgrade hantavirus: definition of genotypes and their characteristics. Archives of Virology 158: 521–529 Klingström J, Hardestam J, Lundkvist Å (2006) Dobrava, but not Saaremaa, hantavirus is lethal and induces nitric oxide production in suckling mice. Microbes and Infection 8(3):728-737 Lapošová K, Lukáčiková Ľ, Ovečková I, Pastoreková S, Rosocha J, Kuba D, Beňa Ľ, Tomášková J (2016) Development and application of ELISA for the detection of IgG antibodies to lymphocytic choriomeningitis virus. Acta Virologica 60(2):143-150 Linard C, Lamarque P, Heyman P, Ducoffre G, Luyasu V, Tersago K, Vanwambeke SO, Lambin EF (2007) Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6;15. https://doi.org/10.1186/1476-072x-6-15 Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35(3):221-270. https://doi.org/10.1080/10408410902989837 Moll van Charante AW, Groen J, Osterhaus AD (1994) Risk of infections transmitted by arthropods and rodents in forestry workers. European Journal of Epidemiology 10(3):349-351 Monson R (1990) Occupational Epidemiology. Boca Raton, Florida: CRC Press Inc Mustonen J, Vapalahti O, Henttonen H, Pasternack A, Vaheri A (1998) Epidemiology of hantavirus infections in Europe. Nephrology Dialysis and Transplantation 13(11):2729–2731. https://doi.org/10.1093/ndt/13.11.2729 Nuti M, leradi LA, Cristaldi M, Gibbs CJ Jr (1990) Prevalence of antibody to hantaviruses in humans and rodents in Italy: provisional evidence of Hantaan-like virus infections in humans and Seoul like virus infections in rodents. Archives of Virology 1:81-86 Nuti M., Amado ED, Autorino GL, Crovatto M, Crucil C, Ghionni A, Giommi M, Salvati F, Santini GF (1992) Seroprevalence of antibodies to hantaviruses and leptospires in selected italian population groups. European Journal of Epidemiology 8(1):98-102 Oldstone MB, Dixon FY (1967) Lymphocytic choriomeningitis: production of antibody by “tolerant” infected mice. Science 158:1193–1195 Olsson GE, Leirs H, Henttonen H (2010) Hantaviruses and their hosts in Europe: reservoirs here and there, but not everywhere? Vector borne and zoonotic diseases 10(6):549-561. https://doi.org/10.1089/vbz.2009.0138 Papa A. (2012) Dobrava-Belgrade virus: phylogeny, epidemiology, disease. Antiviral Research 95(2):104-117. https://doi.org/10.1016/j.antiviral.2012.05.011 Pérez-Ruiz M, Navarro-Marí J-M, Sánchez-Seco M-P, Gegúndez M-I, Palacios G, Savji N et al. Lympphocytic chroriomeningitis virus–associated meningitis, southern Spain. Emerg Infect Dis. 2012 http://dx.doi.org/10.3201/eid1805.111646 R Core Team. (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna, Austria Reiserová L, Kaluzová M, Kaluz S, Willis AC, Závada J, Závodská E, Závadová Z, Ciampor F, Pastorek J, Pastoreková S (1999) Identification of MaTu-MX agent as a new strain of lymphocytic choriomeningitis virus (LCMV) and serological indication of horizontal spread of LCMV in human population. Virology 257(1):73-83 Reusken C, Heyman P (2013) Factors driving hantavirus emergence in Europe. Curr Opin Virol. 3(1):92-99. https://doi.org/10.1016/j.coviro.2013.01.002 Rizzoli A, Tagliapietra V, Rosà R, Hauffe HC, Marini G, Voutilainen L, Sironen T, Rossi C, Arnoldi D, Henttonen H (2015) Recent increase in prevalence of antibodies to Dobrava-Belgrade virus (DOBV) in yellow-necked mice in northern Italy. Epidemiology and Infection 134(10):2241-2244. https://doi.org/10.1017/s0950268814003525 Rousseau MC, Saron MF, Brouqui P, Bourgeade A (1997) Lymphocytic choriomeningitis virus in southern France: four case reports and a review of the literature. European Journal of Epidemiology 13(7):817-823 Tagliapietra V, Rosà R, Hauffe HC, Laakkonen J, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Rizzoli A (2009) Spatial and temporal dynamics of lymphocytic choriomeningitis virus in wild rodents, northern Italy. Emerging Infectious Diseases 15(7):1019-1025. https://doi.org/10.3201/eid1507.081524 Tersago K, Crespin L, Verhagen R, Leirs H (2012) Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. Journal of Wildlife Diseases 48(1):148-156 Tersago K, Verhagen R, Servais A, Heiman P, Ducoffre G, Leirs H (2009) Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. Epidemiology and Infection 137(2):250–256. https://doi.org/10.1017/s0950268808000940 Tersago K,Verhagen R,Vapalahti O,Heyman P,Ducoffre G, LeirsH (2011) Hantavirus out-break in Western Europe: reservoir host infection dynamics related to human disease patterns. Epidemiology and Infection 139:381–390 Vaheri A, Henttonen H, Voutilainen L, Mustonen J, Sironen T, Vapalahti O (2012) Hantavirus infections in Europe and their impact on public health. Reviews in Medical Virology 23(1):35-49. https://doi.org/10.1002/rmv.1722 Van Loock F, Thomas I, Clement J, Ghoos S, Colson P (1999) A case-control study after a hantavirus infection outbreak in the south of Belgium: who is at risk? Clinical Infectious Diseases 28(4):834-839 Vapalahti K, Virtala AM, Vaheri A, Vapalahti O (2010) Case-control study on Puumala virus infection: smoking is a risk factor. Epidemiology and Infection 138(4):576-584. https://doi.org/10.1017/s095026880999077x Vapalahti O, Plyusnin A, Vaheri A, Henttonen H (1995) Hantavirus antibodies in European mammalogists. The Lancet 345(8964):1569 Voutilainen L, Sironen T, Tonteri E, Bäck AT, Razzauti M, Karlsson M, Wahlström M, Niemimaa J, Henttonen H, Lundkvist Å (2015) Life-long shedding of Puumala hantavirus in wild bank voles (Myodes glareolus). Journal of General Virology 96(6):1238-1247. https://doi.org/10.1099/vir.0.000076 Watson DC, Sargianou M, Papa A, Chra P, Starakis I, Panos G (2014) Epidemiology of Hantavirus infections in humans: a comprehensive, global overview. Crit Rev Microbiol 40(3):261-272. https://doi.org/10.3109/1040841x.2013.783555 Winter CH, Brockmann SO, Piechotowski I, Alpers K, van der Heiden M, Koch J, Stark K, Pfaff G (2009) Survey and case-control study during epidemics of Puumala virus infection. Epidemiol Infect 137(10):1479-1485. https://doi.org/10.1017/s0950268809002271 Zinkernagel RM, LaMarre A, Ciurea A, Hunziker L, Ochsenbein AF, McCoy KD, Fehr T, Bachmann MF, Kalinke U, Hengartner H (2001) Neutralizing antiviral antibody responses. Advances in Immunology 79:1-53 Zöller L, Faulde M, Meisel H, Ruh B, Kimmig P, Schelling U, Zeier M, Kulzer P, Becker C, Roggendorf M, Bautz EKF, Krüger DH, Darai G (1995) Seroprevalence of hantavirus antibodies in Germany as determined by a new recombinant enzyme immunoassay. European Journal of Clinical Microbiology and Infectious Diseases 14(4):305-313