Spatial and temporal dynamics of Puumala hantavirus infection in red bank vole (Clethrionomys glareolus) populations in Belgium

Virus Research

Volumn 67, Issue 1, 2000, Pages 91-107

  Escutenaire, S ^a   Chalon, P ^a   Verhagen, R ^b   Heyman, P ^c   Thomas, I ^d   Karelle Bui, L ^a   Avsic Zupanc, T ^e   Lundkvist, Å ^f   Plyusnin, A ^g   Pastoret, P P ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c QUEEN ASTRID MILITARY HOSPITAL   (Belgium)

^d PASTEUR INSTITUTE OF BRUSSELS   (Belgium)

^e UNIVERSITY OF LJUBLJANA   (Slovenia)

^f KAROLINSKA INSTITUTE   (Sweden)

^g UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Belgium; Clethrionomys glareolus; Hantavirus; Puumala virus

Indexed keywords

AGE; ARTICLE; BELGIUM; INFECTION RATE; NONHUMAN; POPULATION DENSITY; POPULATION DYNAMICS; PRIORITY JOURNAL; PUUMALA VIRUS; RISK FACTOR; RODENT; SEROPREVALENCE; VIRUS INFECTION; VOLE;

ANIMALS; ANTIGENS, VIRAL; ARVICOLINAE; BELGIUM; CERCOPITHECUS AETHIOPS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HANTAVIRUS; HANTAVIRUS INFECTIONS; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEROEPIDEMIOLOGIC STUDIES; TIME FACTORS; VARIATION (GENETICS); VERO CELLS;

ANIMALIA; APODEMUS SYLVATICUS; CLETHRIONOMYS GLAREOLUS; HANTAVIRUS; MURIDAE; PUUMALA VIRUS; RODENTIA;

EID: 0034118124     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-1702(00)00136-2     Document Type: Article

References (75)

1. Abbott K.D., Ksiazek T.G., Mills J.N. Long-term hantavirus persistence in rodent populations in Central Arizona. Emerg. Infect. Dis. 5:1999;102-112.
2. Ahlm C., Alexeyev O.A., Elgh F., Aava B., Wadell G., Tärnvik A., Juto P., Palo T. High prevalence of hantavirus antibodies in bank voles (Clethrionomys glareolus) captured in the vicinity of households afflicted with nephropathia epidemica. Am. J. Trop. Med. Hyg. 56:1997;674-678.
3. Antic D., Kang C.Y., Spik K., Schmaljohn C., Vapalahti O., Vaheri A. Comparison of the deduced gene products of the L, M and S genome segments of hantaviruses. Virus Res. 24:1992;35-46.
4. Avsic-Zupanc T., Xiao S.Y., Stojanovic R., Gligic A., van der Groen G., LeDuc J.W. Characterization of Dobrava virus: a Hantavirus from Slovenia, Yugoslavia. J. Med. Virol. 38:1992;132-137.
5. Avsic-Zupanc T., Petrovec M., Furlan P., Kaps R., Elgh F., Lundkvist Å. Hemorrhagic fever with renal syndrome in the Dolenjska region of Slovenia - a 10-year survey. Clin. Infect. Dis. 28:1999;860-865.
6. Boone J.D., Otteson E.W., Mc Gwire K.C., Villard P., Rowe J.E., St Jeor S.C. Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. Am. J. Trop. Med. Hyg. 59:1998;445-451.
7. Brummer-Korvenkontio M., Vaheri A., Hovi T., von Bonsdorff C.H., Vuorimies J., Manni T., Penttinen K., Oker-Blom N., Lahdevirta J. Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. J. Infect. Dis. 141:1980;131-134.
8. Calisher C.H., Sweeney W., Mills J.N., Beaty B.J. Natural history of Sin Nombre virus in western Colorado. Emerg. Infect. Dis. 5:1999;126-134.
9. Hantavirus infection - southwestern United States: interim recommendations for risk reduction. Morbid. Mortal. Weekly Rep. (MMWR). 42:1993;1-13.
10. Laboratory management of agents associated with hantavirus pulmonary syndrome: interim biosafety guidelines. Morbid. Mortal. Weekly Rep. (MMWR). 43:1994;1-7.
11. Childs J.E., Korch G.W., Smith G.A., Terry A.D., LeDuc J.W. Geographical distribution and age related prevalence of antibody to Hantaan-like virus in rat populations of Baltimore, Maryland, USA. Am. J. Trop. Med. Hyg. 34:1985;385-387.
12. Childs J.E., Glass G.E., Korch G.W., LeDuc J.W. Prospective seroepidemiology of hantaviruses and population dynamics of small mammal communities of Baltimore, Maryland. Am. J. Trop. Med. Hyg. 37:1987;648-662.
13. Childs J.E., Korch G.W., Glass G.E., LeDuc J.W., Shah K.V. Epizootiology of Hantavirus infections in Baltimore: isolation of a virus from Norway rats, and characteristics of infected rat populations. Am. J. Epidemiol. 126:1987;55-68.
14. Childs J.E., Ksiazek T.G., Spiropoulou C.F., Krebs J.W., Morzunov S., Maupin G.O., Gage K.L., Rollin P.E., Sarisky J., Enscore R.E., Frey J.K., Peters C.J., Nichol S.T. Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. J. Infect. Dis. 169:1994;1271-1280.
15. Clement J., Mc Kenna P., Colson P., Damoiseaux P., Penalba C., Halin P., Lombart D. Hantavirus epidemic in Europe, 1993. Lancet. 343:1994;114.
16. Clement J., Mc Kenna P., Leirs H., Verhagen R., Lefevre A., Song G., Tkachenko E.A., van der Groen G. Hantavirus infections in rodents. Osterhaus A.D.M.E. Virus Infections of Rodents and Lagomorphs. 44:1994;293-316 Elsevier Science, Amsterdam.
17. Duchin J.S., Koster F.T., Peters C.J., Simpson G.L., Tempest B., Zaki S.R., Ksiazek T.G., Rollin P.E., Nichol S., Umland E.T., Moolenaar R., Reef S., Nolte K., Gallagher M., Butler J., Breiman R. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. New Engl. J. Med. 330:1994;949-955.
18. Elliott R.M. Molecular biology of the Bunyaviridae. J. Gen. Virol. 71:1990;501-522.
19. Flowerdew J.R., Gardner G. Small rodent populations and food supply in a Derbyshire ashwood. J. Anim. Ecol. 47:1978;725-740.
20. Gajdusek D.C. Virus hemorrhagic fevers. J. Pediatr. 60:1962;841-857.
21. Gavrilovskaya, I.N., Apekina, N.S., Bernshtein, A.D., Demina, V.T., Okulova, N.M., Myasnikov, Y.A., Chumakov, M.P., 1990. Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. Arch. Virol., Suppl. 1, S57-S62.
22. Glass G.E., Childs J.E., Korch G.W., LeDuc J.W. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol. Infect. 101:1988;459-472.
23. Glass G.E., Livingstone W., Mills J.N., Hlady W.G., Fine J.B., Biggler W., Coke T., Frazier D., Atherley S., Rollin P.E., Ksiazek T.G., Peters C.J., Childs J.E. Black Creek Canal virus infection in Sigmodon hispidus in southern Florida. Am. J. Trop. Med. Hyg. 59:1998;699-703.
24. Graham T.B., Chomel B.B. Population dynamics of the deer mouse (Peromyscus maniculatus) and Sin Nombre virus, California Channel Islands. Emerg. Infect. Dis. 3:1997;367-370.
25. Hansson L., Henttonen H. Gradients in density variations of small rodents: the importance of latitude and snow cover. Oecologia. 67:1985;394-402.
26. Heyman P., Vervoort T., Colson P., Chu Y.-K., Avsic-Zupanc T., Lundkvist A. A major outbreak of hantavirus infection in Belgium in 1995 and 1996. Epidemiol. Infect. 122:1999;447-453.
27. Hilborn R., Redfield J.A., Krebs C.J. On the reliability of enumeration for mark and recapture census of voles. Can. J. Zool. 54:1976;1019-1024.
28. Hörling J., Lundkvist Å., Jaarola M., Plyusnin A., Tegelström H., Persson K., Lehvaslaiho H., Hörnfeldt B., Vaheri A., Niklasson B. Distribution and genetic heterogeneity of Puumala virus in Sweden. J. Gen. Virol. 77:1996;2555-2562.
29. Hörnfeldt B. Delayed density dependence as a determinant of vole cycles. Ecology. 75:1994;791-806.
30. Jay M., Ascher M.S., Chomel B.B., Madon M., Sesline D., Enge B.A., Hjelle B., Ksiazek T.G., Rollin P.E., Kass P.H., Reilly K. Seroepidemiologic studies of hantavirus infection among wild rodents in California. Emerg. Infect. Dis. 3:1997;183-190.
31. Krebs C.J. Demographic changes in fluctuating populations of Microtus californicus. Ecol. Monogr. 36:1966;239-273.
32. Krebs C.J., Myers J.H. Population cycles in small mammals. Adv. Ecol. Res. 8:1974;267-399.
33. Kuenzi A.J., Morrison M.L., Swann D.E., Hardy P.C., Downard G.T. A longitudinal study of Sin Nombre virus prevalence in rodents, Southeastern Arizona. Emerg. Infect. Dis. 5:1999;113-117.
34. LeDuc J.W. Epidemiology of Hantaan and related viruses. Lab. Anim. Sci. 37:1987;413-418.
35. LeDuc J.W., Smith G.A., Bagley L.R., Hasty S.E., Johnson K.M. Preliminary evidence that Hantaan or a closely related virus is enzootic in domestic rodents. New Engl. J. Med. 307:1982;624.
36. Le Guenno B., Camprasse M.A., Guilbaut J.C., Lanoux P., Hoen B. Hantavirus epidemic in Europe, 1993. Lancet. 343:1994;114-115.
37. Lee H.W., Lee P.W., Johnson K.M. Isolation of the etiologic agent of Korean hemorrhagic fever. J. Infect. Dis. 137:1978;289-308.
38. Lee H.W., Baek L.J., Johnson K.M. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J. Infect. Dis. 146:1982;638-644.
39. Lundkvist Å., Apekina N., Myasnikov Y., Vapalahti O., Vaheri A., Plyusnin A. Dobrava hantavirus outbreak in Russia. Lancet. 350:1997;781-782.
40. Lundkvist Å., Hukic M., Hörling J., Gilljam M., Nichol S., Niklasson B. Puumala and Dobrava viruses cause hemorrhagic fever with renal syndrome in Bosnia-Herzegovina: evidence of highly cross-neutralizing antibody responses in early patient sera. J. Med. Virol. 53:1997;51-59.
41. Lundkvist Å., Vasilenko V., Golovljova I., Plyusnin A., Vaheri A. Human Dobrava hantavirus infections in Estonia. Lancet. 352:1998;369.
42. Lyubsky S., Gavrilovskaya I., Luft B., Mackow E. Histopathology of Peromyscus leucopus naturally infected with pathogenic NY-1 hantaviruses: pathologic markers of HPS viral infection in mice. Lab. Invest. 74:1996;627-633.
43. Mertz G.J., Hjelle B.L., Bryan R.T. Hantavirus infection. Dis. Mon. 44:1998;85-138.
44. Mills J.N., Ksiazek T.G., Ellis B.A., Rollin P.E., Nichol S.T., Yates T.L., Gannon W.L., Levy C.E., Engelthaler D.M., Davis T., Tanda D.T., Frampton J.W., Nichols C.R., Peters C.J., Childs J.E. Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am. J. Trop. Med. Hyg. 56:1997;273-284.
45. Mills J.N., Johnson J.M., Ksiazek T.G., Ellis B.A., Rollin P.E., Yates T.L., Mann M.O., Johnson M.R., Campbell M.L., Miyashiro J., Patrick M., Zyzak M., Lavender D., Novak M.G., Schmidt K., Peters C.J., Childs J.E. A survey of hantavirus antibody in small-mammal populations in selected United States National Parks. Am. J. Trop. Med. Hyg. 58:1998;525-532.
46. Mills J.N., Ksiazek T.G., Peters C.J., Childs J.E. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg. Infect. Dis. 5:1999;135-142.
47. Netski D., Thran B.H., St Jeor S.C. Sin Nombre virus pathogenesis in Peromyscus maniculatus. J. Virol. 73:1999;585-591.
48. Nichol S.T., Spiropoulou C.F., Morzunov S., Rollin P.E., Ksiazek T.G., Feldmann H., Sanchez A., Childs J., Zaki S., Peters C.J. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science. 262:1993;914-917.
49. Niklasson B., LeDuc J.W. Epidemiology of nephropathia epidemica in Sweden. J. Infect. Dis. 155:1987;269-276.
50. Niklasson B., Hörnfeldt B., Lundkvist Å., Björsten S., Leduc J. Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. Am. J. Trop. Med. Hyg. 53:1995;134-140.
51. Nyström K. Incidence and prevalence of endemic benign (epidemic) nephropathy in AC County, Sweden, in relation to population density and prevalence of small rodents. Acta Med. Scand. Suppl. 609:1977;1-92.
52. Otteson E.W., Riolo J., Rowe J.E., Nichol S.T., Ksiazek T.G., Rollin P.E., St.Jeor S.C. Occurrence of hantavirus within the rodent population of northeastern California and Nevada. Am. J. Trop. Med. Hyg. 54:1996;127-133.
53. Parker R.A., Erdman D.D., Anderson L.J. Use of mixture models in determining laboratory criterion for identification of seropositive individuals: application to parvovirus B19 serology. J. Virol. Methods. 27:1990;135-144.
54. Parmenter R., Vigil R. The Hantavirus Epidemic in the Southwest: An Assessment of Autumn Rodent Densities and Population Demographics in Central and Northern New Mexico. Report to the Federal Centers for Disease Control and Prevention. 1993;Federal Centers for Disease Control and Prevention, Atlanta, GA.
55. Pilaski J., Feldmann H., Morzunov S., Rollin P.E., Ruo S.L., Lauer B., Peters C.J., Nichol S.T. Genetic identification of a new Puumala virus strain causing severe hemorrhagic fever with renal syndrome in Germany. J. Infect. Dis. 170:1994;1456-1462.
56. Plyusnin A., Vapalahti O., Lehvaslaiho H., Apekina N., Mikhailova T., Gavrilovskaya I., Laakkonen J., Niemimaa J., Henttonen H., Brummer-Korvenkontio M., Vaheri A. Genetic variation of wild Puumala viruses within the serotype, local rodent populations and individual animal. Virus Res. 38:1995;25-41.
57. Plyusnin A., Vapalahti O., Vaheri A. Hantaviruses: genome structure, expression and evolution. J. Gen. Virol. 77:1996;2677-2687.
58. Plyusnin A., Vapalahti O., Vasilenko V., Henttonen H., Vaheri A. Dobrava hantavirus in Estonia: does the virus exist throughout Europe? Lancet. 349:1997;1369-1370.
59. Root J.J., Calisher C.H., Beaty B.J. Relationships of deer mouse movement, vegetative structure, and prevalence of infection with Sin Nombre virus. J. Wildlife Dis. 35:1999;311-318.
60. Schmaljohn C.S., Dalrymple J.M. Analysis of Hantaan virus RNA: evidence for a new genus of Bunyaviridae. Virology. 131:1983;482-491.
61. Schmaljohn C.S., Hjelle B. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:1997;95-104.
62. Schmaljohn C.S., Hasty S.E., Dalrymple J.M., LeDuc J.W., Lee H.W., von Bonsdorff C.H., Brummer-Korvenkontio M., Vaheri A., Tsai T.F., Regnery H.L., Goldgaber D., Lee P.W. Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science. 227:1985;1041-1044.
63. Stone R. The mouse-piñon nut connection. Science. 262:1993;833.
64. Tkachenko E.A., Ivanov A.P., Dzagurova T.K., Donets M.A., Rezapkin G.V., Leshchinskaya E.V., Zagidulin U.M., Ivanova A.A., Stradukhin O.V., Mustafin N.M., Savinova T.I. Immunosorbent assays for diagnosis of haemorrhagic fever with renal syndrome. Lancet. 2:1981;257-258.
65. Traavik T., Sommer A.I., Mehl R., Berdal B.P., Stavem K., Hunderi O.H., Dalrymple J.M. Nephropathia epidemica in Norway: antigen and antibodies in rodent reservoirs and antibodies in selected human populations. J. Hyg. (Lond.). 93:1984;139-146.
66. Tsai T.F. Hemorrhagic fever with renal syndrome: mode of transmission to humans. Lab. Anim. Sci. 37:1987;428-430.
67. Verhagen R., Leirs H., Tkachenko E., van der Groen G. Ecological and epidemiological data on Hantavirus in bank vole populations in Belgium. Arch. Virol. 91:1986;193-205.
68. Verhagen R., van der Groen G., Ivanov A., Van Rompaey J., Leirs H., Verheyen W. Occurrence and distribution of Hantavirus in wild living mammals in Belgium. Acta Virol. 31:1987;43-52.
69. Vizard A.L., Anderson G.A., Gasser R.B. Determination of the optimum cut-off value of a diagnostic test. Prev. Vet. Med. 10:1990;137-143.
70. Weigler B.J., Ksiazek T.G., Vandenbergh J.G., Levin M., Sullivan W.T. Serological evidence for zoonotic hantaviruses in North Carolina rodents. J. Wildlife Dis. 32:1996;354-357.
71. Haemorrhagic fever with renal syndrome: memorandum from a WHO meeting. Bull. Who. 61:1983;269-275.
72. Xu Z.Y., Guo C.S., Wu Y.L., Zhang X.W., Liu K. Epidemiological studies of hemorrhagic fever with renal syndrome: analysis of risk factors and mode of transmission. J. Infect. Dis. 152:1985;137-144.
73. Yanagihara R., Gajdusek D.C. Hemorrhagic fever with renal syndrome: a historical perspective and review of recent advances. Gears J.H.S. CRC Handbook of Viral and Rickettsial Hemorrhagic Fevers. 1988;151-188 CRC, Boca Raton, FL.
74. Yanagihara R., Amyx H.L., Gajdusek D.C. Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica in bank voles (Clethrionomys glareolus). J. Virol. 55:1985;34-38.
75. Young J.C., Mills J.N., Enria D.A., Dolan N.E., Khan A.S., Ksiazek T.G. New world hantaviruses. Br. Med. Bull. 54:1998;659-673.