Skip to main content
Top
Published in: BMC Infectious Diseases 1/2016

Open Access 01-12-2016 | Research article

Human Puumala hantavirus infection in northern Sweden; increased seroprevalence and association to risk and health factors

Authors: Kristina Bergstedt Oscarsson, Alette Brorstad, Maria Baudin, Anne Lindberg, Annika Forssén, Magnus Evander, Marie Eriksson, Clas Ahlm

Published in: BMC Infectious Diseases | Issue 1/2016

Login to get access

Abstract

Background

The rodent borne Puumala hantavirus (PUUV) causes haemorrhagic fever with renal syndrome in central and northern Europe. The number of cases has increased and northern Sweden has experienced large outbreaks in 1998 and 2006–2007 which raised questions regarding the level of immunity in the human population.

Methods

A randomly selected population aged between 25 and 74 years from northern Sweden were invited during 2009 to participate in a WHO project for monitoring of trends and determinants in cardiovascular disease. Health and risk factors were evaluated and sera from 1,600 participants were available for analysis for specific PUUV IgG antibodies using a recombinant PUUV nucleocapsid protein ELISA.

Results

The overall seroprevalence in the investigated population was 13.4 %, which is a 50 % increase compared to a similar study only two decades previously. The prevalence of PUUV IgG increased with age, and among 65–75 years it was 22 %. More men (15.3 %) than women (11.4 %) were seropositive (p < 0.05). The identified risk factors were smoking (OR = 1.67), living in rural areas (OR = 1.92), and owning farmland or forest (OR = 2.44). No associations were found between previous PUUV exposure and chronic lung disease, diabetes, hypertension, renal dysfunction, stroke or myocardial infarction.

Conclusions

PUUV is a common infection in northern Sweden and there is a high life time risk to acquire PUUV infection in endemic areas. Certain risk factors as living in rural areas and smoking were identified. Groups with increased risk should be targeted for future vaccination when available, and should also be informed about appropriate protection from rodent secreta.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jonsson CB, Figueiredo LT, Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010;23(2):412–41.CrossRefPubMedPubMedCentral Jonsson CB, Figueiredo LT, Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010;23(2):412–41.CrossRefPubMedPubMedCentral
2.
go back to reference Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A. Hantavirus infections in Europe. Lancet Infect Dis. 2003;3(10):653–61.CrossRefPubMed Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A. Hantavirus infections in Europe. Lancet Infect Dis. 2003;3(10):653–61.CrossRefPubMed
3.
go back to reference Brorstad A, Bergstedt-Oscarsson K, Ahlm C. Early diagnosis of hantavirus infection by family doctors can reduce inappropriate antibiotic use and hospitalization. Scand J Prim Health Care. 2010;28(3):179–84.CrossRefPubMedPubMedCentral Brorstad A, Bergstedt-Oscarsson K, Ahlm C. Early diagnosis of hantavirus infection by family doctors can reduce inappropriate antibiotic use and hospitalization. Scand J Prim Health Care. 2010;28(3):179–84.CrossRefPubMedPubMedCentral
4.
go back to reference Ahlm C, Juto P, Stegmayr B, Settergren B, Wadell G, Tarnvik A, Elgh F. Prevalence of serum antibodies to hantaviruses in northern Sweden as measured by recombinant nucleocapsid proteins. Scand J Infect Dis. 1997;29(4):349–54.CrossRefPubMed Ahlm C, Juto P, Stegmayr B, Settergren B, Wadell G, Tarnvik A, Elgh F. Prevalence of serum antibodies to hantaviruses in northern Sweden as measured by recombinant nucleocapsid proteins. Scand J Infect Dis. 1997;29(4):349–54.CrossRefPubMed
5.
go back to reference Ahlm C, Linderholm M, Juto P, Stegmayr B, Settergren B. Prevalence of serum IgG antibodies to Puumala virus (haemorrhagic fever with renal syndrome) in northern Sweden. Epidemiol Infect. 1994;113(1):129–36.CrossRefPubMedPubMedCentral Ahlm C, Linderholm M, Juto P, Stegmayr B, Settergren B. Prevalence of serum IgG antibodies to Puumala virus (haemorrhagic fever with renal syndrome) in northern Sweden. Epidemiol Infect. 1994;113(1):129–36.CrossRefPubMedPubMedCentral
6.
go back to reference Pettersson L, Boman J, Juto P, Evander M, Ahlm C. Outbreak of Puumala virus infection. Sweden Emerg Infect Dis. 2008;14(5):808–10.CrossRefPubMed Pettersson L, Boman J, Juto P, Evander M, Ahlm C. Outbreak of Puumala virus infection. Sweden Emerg Infect Dis. 2008;14(5):808–10.CrossRefPubMed
7.
go back to reference Makary P, Kanerva M, Ollgren J, Virtanen MJ, Vapalahti O, Lyytikainen O. Disease burden of Puumala virus infections, 1995–2008. Epidemiol Infect. 2010;138(10):1484–92.CrossRefPubMed Makary P, Kanerva M, Ollgren J, Virtanen MJ, Vapalahti O, Lyytikainen O. Disease burden of Puumala virus infections, 1995–2008. Epidemiol Infect. 2010;138(10):1484–92.CrossRefPubMed
8.
go back to reference Ferrés M, Vial P, Marco C, Yanez L, Godoy P, Castillo C, Hjelle B, Delgado I, Lee SJ, Mertz GJ, et al. Prospective evaluation of household contacts of persons with hantavirus cardiopulmonary syndrome in chile. J Infect Dis. 2007;195(11):1563–71.CrossRefPubMed Ferrés M, Vial P, Marco C, Yanez L, Godoy P, Castillo C, Hjelle B, Delgado I, Lee SJ, Mertz GJ, et al. Prospective evaluation of household contacts of persons with hantavirus cardiopulmonary syndrome in chile. J Infect Dis. 2007;195(11):1563–71.CrossRefPubMed
9.
go back to reference Pettersson L, Klingstrom J, Hardestam J, Lundkvist A, Ahlm C, Evander M. Hantavirus RNA in saliva from patients with hemorrhagic fever with renal syndrome. Emerg Infect Dis. 2008;14(3):406–11.CrossRefPubMedPubMedCentral Pettersson L, Klingstrom J, Hardestam J, Lundkvist A, Ahlm C, Evander M. Hantavirus RNA in saliva from patients with hemorrhagic fever with renal syndrome. Emerg Infect Dis. 2008;14(3):406–11.CrossRefPubMedPubMedCentral
10.
go back to reference Ahlm C, Thelin A, Elgh F, Juto P, Stiernstrom EL, Holmberg S, Tarnvik A. Prevalence of antibodies specific to Puumala virus among farmers in Sweden. Scand J Work Environ Health. 1998;24(2):104–8.CrossRefPubMed Ahlm C, Thelin A, Elgh F, Juto P, Stiernstrom EL, Holmberg S, Tarnvik A. Prevalence of antibodies specific to Puumala virus among farmers in Sweden. Scand J Work Environ Health. 1998;24(2):104–8.CrossRefPubMed
11.
12.
go back to reference Gherasim A, Hjertqvist M, Lundkvist A, Kuhlmann-Berenzon S, Carlson JV, Stenmark S, Widerstrom M, Osterlund A, Boman H, Ahlm C, et al. Risk factors and potential preventive measures for nephropatia epidemica in Sweden 2011–2012: a case-control study. Infection Ecol Epidemiol. 2015;5:27698. Gherasim A, Hjertqvist M, Lundkvist A, Kuhlmann-Berenzon S, Carlson JV, Stenmark S, Widerstrom M, Osterlund A, Boman H, Ahlm C, et al. Risk factors and potential preventive measures for nephropatia epidemica in Sweden 2011–2012: a case-control study. Infection Ecol Epidemiol. 2015;5:27698.
13.
go back to reference Vapalahti K, Virtala AM, Vaheri A, Vapalahti O. Case-control study on Puumala virus infection: smoking is a risk factor. Epidemiol Infect. 2010;138(4):576–84.CrossRefPubMed Vapalahti K, Virtala AM, Vaheri A, Vapalahti O. Case-control study on Puumala virus infection: smoking is a risk factor. Epidemiol Infect. 2010;138(4):576–84.CrossRefPubMed
14.
go back to reference Rasmuson J, Lindqvist P, Sorensen K, Hedstrom M, Blomberg A, Ahlm C. Cardiopulmonary involvement in Puumala hantavirus infection. BMC Infect Dis. 2013;13:501.CrossRefPubMedPubMedCentral Rasmuson J, Lindqvist P, Sorensen K, Hedstrom M, Blomberg A, Ahlm C. Cardiopulmonary involvement in Puumala hantavirus infection. BMC Infect Dis. 2013;13:501.CrossRefPubMedPubMedCentral
15.
go back to reference Connolly-Andersen AM, Hammargren E, Whitaker H, Eliasson M, Holmgren L, Klingstrom J, Ahlm C. Increased risk of acute myocardial infarction and stroke during hemorrhagic fever with renal syndrome: a self-controlled case series study. Circulation. 2014;129(12):1295–302.CrossRefPubMed Connolly-Andersen AM, Hammargren E, Whitaker H, Eliasson M, Holmgren L, Klingstrom J, Ahlm C. Increased risk of acute myocardial infarction and stroke during hemorrhagic fever with renal syndrome: a self-controlled case series study. Circulation. 2014;129(12):1295–302.CrossRefPubMed
16.
go back to reference Mäkelä S, Jaatinen P, Miettinen M, Salmi J, Ala-Houhala I, Huhtala H, Hurme M, Porsti I, Vaheri A, Mustonen J. Hormonal deficiencies during and after Puumala hantavirus infection. Eur J Clin Microbiol Infect Dis. 2010;29(6):705–13.CrossRefPubMed Mäkelä S, Jaatinen P, Miettinen M, Salmi J, Ala-Houhala I, Huhtala H, Hurme M, Porsti I, Vaheri A, Mustonen J. Hormonal deficiencies during and after Puumala hantavirus infection. Eur J Clin Microbiol Infect Dis. 2010;29(6):705–13.CrossRefPubMed
17.
go back to reference Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Koobi T, Vaheri AI, Pasternack AI, Porsti IH, Mustonen JT. Ten-year prognosis of Puumala hantavirus-induced acute interstitial nephritis. Kidney Int. 2006;69(11):2043–8.CrossRefPubMed Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Koobi T, Vaheri AI, Pasternack AI, Porsti IH, Mustonen JT. Ten-year prognosis of Puumala hantavirus-induced acute interstitial nephritis. Kidney Int. 2006;69(11):2043–8.CrossRefPubMed
18.
go back to reference Mäkelä S, Ala-Houhala I, Mustonen J, Koivisto AM, Kouri T, Turjanmaa V, Vapalahti O, Vaheri A, Pasternack A. Renal function and blood pressure five years after puumala virus-induced nephropathy. Kidney Int. 2000;58(4):1711–8.CrossRefPubMed Mäkelä S, Ala-Houhala I, Mustonen J, Koivisto AM, Kouri T, Turjanmaa V, Vapalahti O, Vaheri A, Pasternack A. Renal function and blood pressure five years after puumala virus-induced nephropathy. Kidney Int. 2000;58(4):1711–8.CrossRefPubMed
19.
go back to reference Niklasson B, Hellsten G, LeDuc J. Hemorrhagic fever with renal syndrome: a study of sequelae following nephropathia epidemica. Arch Virol. 1994;137(3–4):241–7.CrossRefPubMed Niklasson B, Hellsten G, LeDuc J. Hemorrhagic fever with renal syndrome: a study of sequelae following nephropathia epidemica. Arch Virol. 1994;137(3–4):241–7.CrossRefPubMed
20.
go back to reference Bothig S. WHO MONICA Project: objectives and design. Int J Epidemiol. 1989;18(3 Suppl 1):S29–37.PubMed Bothig S. WHO MONICA Project: objectives and design. Int J Epidemiol. 1989;18(3 Suppl 1):S29–37.PubMed
21.
go back to reference Stegmayr B, Lundberg V, Asplund K. The events registration and survey procedures in the Northern Sweden MONICA Project. Scand J Public Health Suppl. 2003;61:9–17.CrossRefPubMed Stegmayr B, Lundberg V, Asplund K. The events registration and survey procedures in the Northern Sweden MONICA Project. Scand J Public Health Suppl. 2003;61:9–17.CrossRefPubMed
22.
go back to reference SCB. Folk- och bostadsräkningen 1985; Yrke och socioekonomisk indelning (SEI). Stockholm: Statistiska Centralbyrån; 1989. SCB. Folk- och bostadsräkningen 1985; Yrke och socioekonomisk indelning (SEI). Stockholm: Statistiska Centralbyrån; 1989.
23.
go back to reference Stegmayr B, Eliasson M, Rodu B. The decline of smoking in northern Sweden. Scand J Public Health. 2005;33(4):321–4. discussion 243.CrossRefPubMed Stegmayr B, Eliasson M, Rodu B. The decline of smoking in northern Sweden. Scand J Public Health. 2005;33(4):321–4. discussion 243.CrossRefPubMed
24.
go back to reference Lindkvist M, Naslund J, Ahlm C, Bucht G. Cross-reactive and serospecific epitopes of nucleocapsid proteins of three hantaviruses: prospects for new diagnostic tools. Virus Res. 2008;137(1):97–105.CrossRefPubMed Lindkvist M, Naslund J, Ahlm C, Bucht G. Cross-reactive and serospecific epitopes of nucleocapsid proteins of three hantaviruses: prospects for new diagnostic tools. Virus Res. 2008;137(1):97–105.CrossRefPubMed
25.
26.
go back to reference LRF. The invisible entrepreneur. Gender and management in the green industry. Stockholm: Lantbrukarnas Riksförbunds Jämställdhetsakademi; 2009. LRF. The invisible entrepreneur. Gender and management in the green industry. Stockholm: Lantbrukarnas Riksförbunds Jämställdhetsakademi; 2009.
27.
go back to reference Jordbruksverket. Statistikrapport 2011:5; The development of male and female participation in the managing of agricultural holdings in Sweden 1999–2010. Jönköping: Statens Jordbruksverk; 2011. Jordbruksverket. Statistikrapport 2011:5; The development of male and female participation in the managing of agricultural holdings in Sweden 1999–2010. Jönköping: Statens Jordbruksverk; 2011.
28.
go back to reference Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Koobi T, Vaheri AI, Pasternack AI, Porsti IH, Mustonen JT. Tubular proteinuria and glomerular filtration 6 years after puumala hantavirus-induced acute interstitial nephritis. Nephron Clin Pract. 2009;112(2):c115–20.CrossRefPubMed Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Koobi T, Vaheri AI, Pasternack AI, Porsti IH, Mustonen JT. Tubular proteinuria and glomerular filtration 6 years after puumala hantavirus-induced acute interstitial nephritis. Nephron Clin Pract. 2009;112(2):c115–20.CrossRefPubMed
29.
go back to reference Sjolander KB, Elgh F, Kallio-Kokko H, Vapalahti O, Hagglund M, Palmcrantz V, Juto P, Vaheri A, Niklasson B, Lundkvist A. Evaluation of serological methods for diagnosis of Puumala hantavirus infection (nephropathia epidemica). J Clin Microbiol. 1997;35(12):3264–8.PubMedPubMedCentral Sjolander KB, Elgh F, Kallio-Kokko H, Vapalahti O, Hagglund M, Palmcrantz V, Juto P, Vaheri A, Niklasson B, Lundkvist A. Evaluation of serological methods for diagnosis of Puumala hantavirus infection (nephropathia epidemica). J Clin Microbiol. 1997;35(12):3264–8.PubMedPubMedCentral
30.
go back to reference Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Hurme MA, Koobi T, Partanen JA, Pasternack AI, Vaheri A, Porsti IH, et al. The severity of acute Puumala hantavirus infection does not predict the long-term outcome of patients. Nephron Clin Pract. 2010;116(2):c89–94.CrossRefPubMed Miettinen MH, Mäkelä SM, Ala-Houhala IO, Huhtala HS, Hurme MA, Koobi T, Partanen JA, Pasternack AI, Vaheri A, Porsti IH, et al. The severity of acute Puumala hantavirus infection does not predict the long-term outcome of patients. Nephron Clin Pract. 2010;116(2):c89–94.CrossRefPubMed
Metadata
Title
Human Puumala hantavirus infection in northern Sweden; increased seroprevalence and association to risk and health factors
Authors
Kristina Bergstedt Oscarsson
Alette Brorstad
Maria Baudin
Anne Lindberg
Annika Forssén
Magnus Evander
Marie Eriksson
Clas Ahlm
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2016
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-016-1879-2

Other articles of this Issue 1/2016

BMC Infectious Diseases 1/2016 Go to the issue