Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus

BMC Microbiology

Volumn 11, Issue , 2011, Pages

  Salvador, Alexis Ribas ^a   Guivier, Emmanuel ^b   Xuéreb, Anne ^b   Chaval, Yannick ^b   Cadet, Patrice ^c,d   Poulle, Marie Lazarine ^c,d   Sironen, Tarja ^e   Voutilainen, Liina ^f   Henttonen, Heikki ^f   Cosson, Jean François ^b   Charbonnel, Nathalie ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c 2C2A CERFE ^*  (France)

^d UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^e UNIVERSITY OF HELSINKI   (Finland)

^f FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AONCHOTHECA MURIS SYLVATICI; ARTICLE; CRICETIDAE; ENVIRONMENTAL FACTOR; GEOGRAPHIC DISTRIBUTION; HELIGMOSOMUM MIXTUM; HELMINTH; HELMINTHIASIS; INFECTION RISK; LANDSCAPE; MIXED INFECTION; MYODES GLAREOLUS; NEMATODE; NONHUMAN; ORGANISMAL INTERACTION; PUUMALA VIRUS; RISK FACTOR; SEROLOGY; SEROPREVALENCE; VIRUS INFECTION; VIRUS LOAD; ANIMAL; ARVICOLINAE; GROWTH, DEVELOPMENT AND AGING; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMAN; PARASITOLOGY; PATHOGENICITY; VIROLOGY;

AONCHOTHECA; CLETHRIONOMYS GLAREOLUS; HANTAVIRUS; HELIGMOSOMUM MIXTUM; MURIDAE; PUUMALA VIRUS; VERMES;

ANIMALS; ARVICOLINAE; HELMINTHIASIS; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMANS; PUUMALA VIRUS;

EID: 79951959772     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-11-30     Document Type: Article

References (80)

1. Bank vole monoclonal antibodies against Puumala virus envelope glycoproteins: identification of epitopes involved in neutralization. A Lundkvist B Niklasson, Arch Virol 1992 126 93 105 10.1007/BF01309687 1381914
2. Hantavirus infections in Europe. O Vapalahti J Mustonen A Lundkvist H Henttonen A Plyusni (Pubitemid 37210229)
3. Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. IN Gavrilovskaya NS Apekina AD Bernshtein VT Demina NM Okulova YA Myasnikov MP Chumakov, Arch Virol 1990 Suppl 1 57 S62
4. Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. M Brummer-Korvenkontio A Vaheri T Hovi CH von Bonsdorff J Vuorimies T Manni K Penttinen N Oker-Blom J Lahdevirta, J Infect Dis 1980 141 131 134 6102587 (Pubitemid 10100286)
5. Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover. J Klingstrom P Heyman S Escutenaire KB Sjolander F De Jaegere H Henttonen A Lundkvist, J Med Virol 2002 68 4 581 588 10.1002/jmv.10232 12376967 (Pubitemid 35231786)
6. Haemorrhagic fever with renal syndrome: an analysis of the outbreaks in Belgium, France, Germany, the Netherlands and Luxembourg in 2005. P Heyman C Cochez G Ducoffre A Mailles H Zeller M Abu Sin,, et al. Euro Surveillance 2007 12 167 171
7. epidémiologie des infections hantavirus en France. C Penalba JM Galempoix P Lanoux, Med Mal Infect 2001 31 2 272 284 10.1016/S0399-077X(01) 80067-6 (Pubitemid 32530945)
8. Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. B Niklasson B Hörnfeldt Lundkvist S Björsten J Leduc, Am J Trop Med Hyg 1995 53 134 140 7677213
9. Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. K Tersago R Verhagen A Servais P Heyman G Ducoffre H Leirs, Epidemiol Infect 2009 137 2 250 256 10.1017/S0950268808000940 18606026
10. Relating increasing hantavirus incidences to the changing climate: the mast connection. J Clement J Vercauteren WW Verstraeten G Ducoffre JM Barrios AM Vandamme P Maes M Van Ranst, Int J Health Geogr 2009 8 1 10.1186/1476-072X-8-1 19149870
11. Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. K Tersago A Schreurs C Linard R Verhagen S Van Dongen H Leirs, Vector Borne Zoonotic Dis 2008 8 2 235 244 10.1089/vbz.2007.0160 18370592 (Pubitemid 351630136)
12. Increased host species diversity and decreased prevalence of Sin Nombre virus. LJ Dizney LA Ruedas, Emerg Infect Dis 2009 15 7 1012 1018 10.3201/eid1507.081083 19624913
13. Testing mechanisms of the dilution effect: deer mice encounter rates, Sin Nombre virus prevalence and species diversity. CA Clay EM Lehmer S St Jeor MD Dearing, Ecohealth 2009 6 2 250 259 10.1007/s10393-009-0240-2 19495881
14. Sin Nombre virus and rodent species diversity: a test of the dilution and amplification hypotheses. CA Clay EM Lehmer SS Jeor MD Dearing, PLoS One 2009 4 7 6467 10.1371/journal.pone.0006467 19649283
15. Environmental conditions and Puumala virus transmission in Belgium. C Linard K Tersago H Leirs EF Lambin, Int J Health Geogr 2007 6 55 10.1186/1476-072X-6-55 18078526
16. Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. C Linard P Lamarque P Heyman G Ducoffre V Luyasu K Tersago SO Vanwambeke EF Lambin, Int J Health Geogr 2007 6 15 10.1186/1476-072X-6-15 17474974
17. Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). S Escutenaire P Chalon F De Jaegere L Karelle-Bui G Mees B Brochier F Rozenfeld PP Pastoret, Emerg Infect Dis 2002 8 9 930 936 12194769 (Pubitemid 35000811)
18. Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. F Sauvage M Langlais NG Yoccoz D Pontier, J Anim Ecol 2003 72 1 1 13 10.1046/j.1365-2656.2003.00675.x (Pubitemid 36251169)
19. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. ER Kallio J Klingstrom E Gustafsson T Manni A Vaheri H Henttonen O Vapalahti A Lundkvist, J Gen Virol 2006 87 8 2127 2134 10.1099/vir.0.81643-0 16847107 (Pubitemid 44178089)
20. Transmission ecology and the structure of parasite communities in small mammals. IM Cattadori V Haukisalmi H Henttonen P Hudson, Micromammals and macroparasites: from evolutionary ecology to management Tokyo: Springer, Morand S, Krasnov B, Poulin R, 2006 349 369
21. Ecological rules governing helminth-microparasite coinfection. AL Graham, Proc Natl Acad Sci USA 2008 105 2 566 570 10.1073/pnas.0707221105 18182496 (Pubitemid 351171748)
22. Polyparasitism and its impact on the immune system. T Supali JJ Verweij AE Wiria Y Djuardi F Hamid MM Kaisar LJ Wammes L van Lieshout AJ Luty E Sartono,, et al. Int J Parasitol 2010 40 10 1171 1176 10.1016/j.ijpara.2010.05. 003 20580905
23. Concomitant infections, parasites and immune responses. FE Cox, Parasitology 2001 122 Suppl 23 38 10.1017/S003118200001698X 11442193
24. Immune regulation by helminth parasites: cellular and molecular mechanisms. RM Maizels M Yazdanbakhsh, Nat Rev Immunol 2003 3 9 733 744 10.1038/nri1183 12949497 (Pubitemid 41070814)
25. Immune modulation by helminthic infections: worms and viral infections. SM Kamal K El Sayed Khalifa, Parasite Immunol 2006 28 10 483 496 10.1111/j.1365-3024.2006.00909.x 16965284 (Pubitemid 44370854)
26. Can eradication of helminthic infections change the face of AIDS and tuberculosis? Z Bentwich A Kalinkovich Z Weisman G Borkow N Beyers AD Beyers, Immunol Today 1999 20 11 485 487 10.1016/S0167-5699(99)01499-1 10529774 (Pubitemid 29507090)
27. Reciprocal immunomodulation in a schistosome and hepatotropic virus coinfection model. MJ Edwards E Buchatska M Ashton M Montoya QD Bickle P Borrow, J Immunol 2005 175 10 6275 6285 16272278 (Pubitemid 41598866)
28. Helminth-HIV Coinfection: Should We Deworm? G Borkow C Teicher Z Bentwich, Plos Neglect Trop Dis 2007 1 3 10.1371/journal.pntd.0000160 (Pubitemid 352024632)
29. Population dynamics of common and rare helminths in cyclic vole populations. V Haukisalmi H Henttonen F Tenora, J Anim Ecol 1988 57 807 826 10.2307/5094
30. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrionomys glareolus). AD Bernshtein NS Apekina TV Mikhailova YA Myasnikov LA Khlyap YS Korotkov IN Gavrilovskaya, Arch Virol 1999 144 12 2415 2428 10.1007/s007050050654 10664394 (Pubitemid 30057179)
31. Dispersal in the bank vole. J Gliwicz RA Ims, Polish Journal of Ecology 2000 51 61 (Pubitemid 32103005)
32. Methods for trapping and sampling small mammals for virologic testing. JN Mills J Childs TG Ksiazek CJ Peters WM Velleca, Atlanta: Centers for Disease Control and Prevention 1995
33. Nutritional epidemiology. WC Willett, New York: Oxford University Press 1998
34. Antigenic variation of European haemorrhagic fever with renal syndrome virus strains characterized using bank vole monoclonal antibodies. AI Lundkvist A Fatouros B Niklasson, J Gen Virol 1991 72 2097 2103 10.1099/0022-1317-72-9- 2097 1716651
35. The hantaviral load in tissues of naturally infected rodents. M Korva D Duh A Saksida T Trilar T Avsic-Zupanc, Microbes Infect 2009 11 344 351 10.1016/j.micinf.2008.12.016 19397875
36. Model selection and inference. A practical information-theoretic approach. KP Burnham DR Anderson, New York: Heidelberg 1998
37. Model selection in ecology and evolution. JB Johnson KS Omland, Trends Ecol Evol 2004 19 101 108 10.1016/j.tree.2003.10.013 16701236 (Pubitemid 38105895)
38. Generalized linear models. P McCullagh JA Nelder, Chapman and Hall, London 1989
39. Glim for ecologists. MJ Crawley, Blackwell, Oxford, U.K 1993
40. ADE-4: a multivariate analysis and graphical display software. J Thioulouse D Chessel S Dolédec JM Olivier, Stat Comput 1997 7 75 83 10.1023/A:1018513530268
41. Genetic markers in the playground of multivariate analysis. T Jombart D Pontier AB Dufour, Heredity 2009 102 4 330 341 10.1038/hdy.2008.130 19156164
42. The estimation and significance of the logarithm of a ratio of frequencies. JBS Haldane, Ann Hum Genet 1956 20 309 311 10.1111/j.1469-1809. 1955.tb01285.x 13314400
43. Detecting interspecific macroparasite interactions from ecological data: patterns and process. A Fenton ME Viney J Lello, Ecol Lett 2010 13 5 606 615 10.1111/j.1461-0248.2010.01458.x 20529102
44. Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. RC Furze T Hussell ME Selkirk, Infect Immun 2006 74 3 1924 1932 10.1128/IAI.74.3.1924-1932.2006 16495568 (Pubitemid 43346830)
45. Infection with Toxoplasma gondii reduces established and developing Th2 responses induced by Nippostrongylus brasiliensis infection. O Liesenfeld IR Dunay KJ Erb, Infect Immun 2004 72 7 3812 3822 10.1128/IAI.72.7.3812-3822.2004 15213122 (Pubitemid 38821893)
46. Transmission consequences of coinfection: cytokines writ large? AL Graham IM Cattadori JO Lloyd-Smith MJ Ferrari ON Bjornstad, Trends Parasitol 2007 23 6 284 291 10.1016/j.pt.2007.04.005 17466597 (Pubitemid 46771350)
47. Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions. or pure randomness? JM Behnke, Parasitology 2008 135 7 751 766 10.1017/S0031182008000334 18371244 (Pubitemid 351913469)
48. Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 1. Regional fauna and component community levels. JM Behnke A Bajer PD Harris L Newington E Pidgeon G Rowlands C Sheriff K Kulis-Malkowska E Sinski FS Gilbert,, et al. Parasitology 2008 135 8 985 997 18598578 (Pubitemid 351950129)
49. Co-existence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. V Haukisalmi H Henttonen, J Anim Ecol 1993 62 221 229 10.2307/5353
50. Co-existence in helminths of the bank vole Clethrionomys glareolus. II. Intestinal distributions and interspecific interactions. V Haukisalmi H Henttonen, J Anim Ecol 1993 62 230 238 10.2307/5354
51. Helminth dynamics and community structure in the bank vole Clethrionomys glareolus. V Haukisalmi H Henttonen, Polish J Ecol 2000 48 219 S230
52. Association between the DQA MHC class II gene and Puumala virus infection in the specific reservoir Myodes glareolus. J Deter Y Chaval M Galan H Henttonen J Laakkonen L Voutilainen A Ribas Salvador J Bryja S Morand JF Cosson,, et al. Infect Genet Evol 2008 8 450 458 10.1016/j.meegid.2007.07.003 17693139 (Pubitemid 351695119)
53. Disease patterns in field and bank vole populations during a cyclic decline in central Finland. T Soveri H Henttonen E Rudback R Schildt R Tanskanen J Husu-Kallio V Haukisalmi A Sukura J Laakkonen, Comp Immunol Microbiol Infect Dis 2000 23 2 73 89 10.1016/S0147-9571(99)00057-0 10670697 (Pubitemid 30044277)
54. Habitat factors associated with bank voles (Clethrionomys glareolus) and concomitant hantavirus in northern Sweden. GE Olsson N White J Hjalten C Ahlm, Vector Borne Zoonotic Dis 2005 5 4 315 323 10.1089/vbz.2005.5.315 16417427 (Pubitemid 43192870)
55. Puumala hantavirus excretion kinetics in bank voles. J Hardestam M Karlsson KI Falk G Olsson J Klingstrom A Lundkvist, Emerg Infect Dis 2008 14 8 1209 1215 10.3201/eid1408.080221 18680643
56. Hantavirus infections in fluctuating host populations: the role of maternal antibodies. ER Kallio M Begon H Henttonen E Koskela T Mappes A Vaheri O Vapalahti, Proc Roy Soc Lond, B 2010 277 3783 3791 10.1098/rspb.2010.1022
57. Long-term dynamics of Sin Nombre viral RNA and antibody in deer mice in Montana. AJ Kuenzi RJ Douglass CW Bond CH Calisher JN Mills, J Wildl dis 2005 41 3 473 481 16244056 (Pubitemid 41622850)
58. Maternal antibodies postpone hantavirus infection and enhance individual breeding success. ER Kallio A Poikonen A Vaheri O Vapalahti H Henttonen E Koskela T Mappes, Proc Biol Sci 2006 273 1602 2771 2776 10.1098/rspb.2006.3645 17015326 (Pubitemid 44671922)
59. The immunology of human hookworm infections. HJ McSorley A Loukas, Parasite Immunol 2010 32 8 549 559 20626810
60. Hantavirus-induced immunity in rodent reservoirs and humans. G Schoenrich A Rang N Lütteke MJ Raftery N Charbonnel RG Ulrich, Immunol Rev 2008 225 163 189 10.1111/j.1600-065X.2008.00694.x 18837782
61. IL-13 Receptor alpha 2 Regulates the Immune and Functional Response to Nippostrongylus brasiliensis Infection. M Morimoto AP Zhao R Sun J Stiltz KB Madden M Mentink-Kane T Ramalingam TA Wynn JF Urban T Shea-Donohue, J Immunol 2009 183 3 1934 1939 10.4049/jimmunol.0804299 19587021
62. Hookworm-induced persistent changes to the immunological environment of the lung. JJ Reece MC Siracusa TL Southard CF Brayton JF Urban AL Scott, Infect Immun 2008 76 8 3511 3524 10.1128/IAI.00192-08 18505812
63. Infection with the helminth Nippostrongylus brasiliensis does not interfere with efficient elimination of Mycobacterium bovis BCG from the lungs of mice. KJ Erb C Trujillo M Fugate H Moll, Clinic Diagn Lab Immunol 2002 9 3 727 730 (Pubitemid 34538242)
64. Associations between Major Histocompatibility Complex genes and PUUV infection in Myodes glareolus are detected in wild populations but not from experimental infection data. E Guivier M Galan PJ Male ER Kallio L Voutilainen H Henttonen G Olsson A Lundkvist K Tersago D Augot,, et al. J Gen Virol 2010 91 2507 2512 10.1099/vir.0.021600-0 20573856
65. Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. A Kloch W Babik A Bajer E Sinski J Radwan, Mol Ecol 2010 19 255 265 10.1111/j.1365-294X.2009.04476.x 20331784
66. Tnf- expression and promoter sequences reflect the balance of tolerance/resistance to Puumala virus infection in European bank vole populations. E Guivier M Galan A Ribas Salvador A Xuéreb Y Chaval G Olsson S Essbauer H Henttonen L Voutilainen JF Cosson,, et al. Infect Genet Evol 2010 10 8 1208 1217 10.1016/j.meegid.2010.07.022 20691810
67. Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). GE Olsson N White C Ahlm F Elgh AC Verlemyr P Juto RT Palo, Emerg Infect Dis 2002 8 9 924 929 12194768 (Pubitemid 35000810)
68. Dynamics of Puumala virus infection in bank voles in Ardennes department (France). D Augot D Muller JM Demerson F Boue C Caillot F Cliquet, Pathol Biol 2006 54 10 572 577 10.1016/j.patbio.2006.07.039 17027178 (Pubitemid 44792384)
69. Changes of cytokine mRNA expression and IgG responses in rats infected with Capillaria hepatica. D-K Kim K-H Joo M-S Chung, Korean J Parasitol 2007 45 2 95 102 10.3347/kjp.2007.45.2.95 17570971
70. Type I interferons in host defense. DB Stetson R Medzhitov, Immunity 2006 25 373 381 10.1016/j.immuni.2006.08.007 16979569 (Pubitemid 44354218)
71. Viral danger signals control CD1d de novo synthesis and NKT cell activation. MJ Raftery F Winau T Giese SH Kaufmann UE Schaible G Schonrich, Eur J Immunol 2008 38 668 679 10.1002/eji.200737233 18253929
72. The impact of climatic factors and host density on the long-term population-dynamics of vole helminths. V Haukisalmi H Henttonen, Oecologia 1990 83 3 309 315
73. Ecology drives the worldwide distribution of human diseases. V Guernier ME Hochberg JF Guegan, PLoS Biol 2004 2 6 141 10.1371/journal.pbio.0020141 15208708
74. Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. PJ Hudson IM Cattadori B Boag AP Dobson, J Helminthol 2006 80 2 175 182 10.1079/JOH2006357 16768860 (Pubitemid 44065908)
75. Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component community levels. JM Behnke A Bajer PD Harris L Newington E Pidgeon G Rowlands C Sheriff K Kulis-Malkowska E Sinski FS Gilbert,, et al. Parasitology 2008 135 8 985 997 18598578 (Pubitemid 351950129)
76. Variabilité de la résistance.tolérance des campagnols rousstres l'hantavirus Puumala et conséquences épidemiologiques. E Guivier, PhD thesis Université Montpellier 2, Montpellier, France 161
77. Effects of habitat fragmentation on the bank vole, Clethrionomys glareolus, in an agricultural landscape. RC van Apeldoorn WT Oostenbrink A van Winden FF van der Zee, Oikos 1992 65 265 274 10.2307/3545018 (Pubitemid 23396897)
78. The evolution of life-histories. SC Stearns, Oxford: Oxford University press 1992
79. A role for immunology in invasion biology. KA Lee KC Klasing, Trends Ecol Evol 2004 19 10 523 529 10.1016/j.tree.2004.07.012 16701317 (Pubitemid 39234758)
80. Trade-offs within the immune systems of female white-footed mice, Peromyscus leucopus. LB Martin ZM Weil JR Kuhlman RJ Nelson, Funct Ecol 2006 20 630 636 10.1111/j.1365-2435.2006.01138.x (Pubitemid 44035842)