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Human Puumala Hantavirus Infection in Northern Sweden

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Human Puumala Hantavirus Infection in Northern Sweden Bergstedt Oscarsson et al. BMC Infectious Diseases (2016) 16:566 DOI 10.1186/s12879-016-1879-2 RESEARCH ARTICLE Open Access Human Puumala hantavirus infection in northern Sweden; increased seroprevalence and association to risk and health factors Kristina Bergstedt Oscarsson1†, Alette Brorstad1†, Maria Baudin2, Anne Lindberg3, Annika Forssén4, Magnus Evander2, Marie Eriksson5 and Clas Ahlm1* 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. Keywords: Emerging infection, Hantavirus, Haemhorrhagic fever with renal syndrome, Puumala, seroepidemiology, Risk factors, Background (HPS) depending on the hantavirus species. HFRS in Hantaviruses of the Bunyaviridae family are globally Asia is caused by Hantaan and Seoul viruses, and in spread and each human pathogenic hantavirus is carried central and northern Europe Puumala virus (PUUV) is by different rodents [1]. The virus is mostly transmitted the endemic hantavirus whereas Dobrava virus is found to humans by inhalation of virus particles present in in the Balkans [1]. In the Americas, Andes, Sin Nombre rodent secreta and cause haemorrhagic fever with renal and related viruses cause HPS which is a more severe in- syndrome (HFRS) or hantavirus pulmonary syndrome fection. The prodrome in HPS is similar to HFRS, however the disease often proceeds into cardiopulmo- nary failure, with a case-fatality rate up to 40 % [1]. In * Correspondence: [email protected] † Scandinavia, the only human pathogenic hantavirus rec- Equal contributors 1Department of Clinical Microbiology, Infectious Diseases, Umeå University, ognized so far is PUUV which causes a less severe HFRS, SE-901 85 Umeå, Sweden also denoted nephropathia epidemica characterized by Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bergstedt Oscarsson et al. BMC Infectious Diseases (2016) 16:566 Page 2 of 7 abrupt onset of fever, resembling influenza with myalgia, 1994, the project continued as the Northern Sweden headache, fatigue and varying degrees of renal impairment MONICA study. [2]. In addition, abdominal pain, nausea, vomiting, and During spring 2009, 2,500 individuals from the backache may be present [3]. The seroprevalence has pre- counties of Norrbotten and Västerbotten were randomly viously been estimated at 9 % in northern Sweden [4]. In selected. 250 males and 250 females from each age Sweden, PUUV infection is a notifiable disease and the re- group 25–34, 25–44, 45–54, 55–64 and 65–74 were ported incidence rate varies from 20 to 313 per 100,000 invited to participate. After signing a written consent, persons each year, but the real figure is considered to be they received a free health check including measuring of seven to eight times higher [5, 6]. Hantavirus antibodies arterial blood pressure, waist − hip ratio and Body Mass have been found more than 50 years after a diagnosed Index (BMI). Levels of S − Creatinine were measured. PUUV infection, and life-long immunity is suggested [7]. A questionnaire regarding quality of life, previous and The primary reservoir is bank voles, Myodes glareolus, present illness, social support, health, work, physical and the incidence of PUUV infection is correlated to the activity, diet and use of tobacco was answered. size of the bank vole populations [1]. Person-to-person Subjects not responding to the study invitation (n = 771), transmission has been shown for the South American were contacted and asked to complete a basic questionnaire Andes hantavirus [8]. In Europe, transmission between of which 485 answered. They were on average younger humans has not been reported, although PUUV has been (46.7 vs. 50.8 years, p < 0.001), less likely to being married/ detected in human saliva [9]. Known risk factors for con- cohabitant (63.6 % vs. 73.9 %, p < 0.001), and less likely to tracting the infection are agricultural work and activities haveauniversityeducation(23.9%vs.29.9%,p =0.010) in peridomestic areas such as cleaning of sheds or summer than the participants. They more often reported themselves cottages, wood handling and smoking [2, 10–13]. The as diabetics (7.7 % vs. 4.8 %, p = 0.013), and as smokers case-fatality rate is less than 1 % [7, 11] and PUUV infec- (17.5 % vs. 11.0 %, p < 0.001). BMI, based on self − reported tion has generally a favourable prognosis. However, car- height and weight, was equivalent to the BMI measured in diopulmonary involvement, increased risk for myocardial participants (data not shown). Treatment with hypertensive infarction, stroke, and hormonal deficiencies may occur medication (22.7 % vs. 19.3 %, p = 0.106) and lipid − lower- during and after the infection [14–16]. ing drugs (9.1 % vs. 12.4 %, p = 0.052) did not differ signifi- Furthermore, several studies indicate possible associ- cantly between participants and non − participants. ation to hypertension and renal impairment [17, 18] although the findings have been contradictory [19]. During the winter 2006–2007 a very large outbreak of Definitions PUUV infection occurred in northern Sweden [6]. This Rural areas were defined as communities having less sudden outbreak raised questions regarding the level of than 1,000 inhabitants. The municipalities of the immunity against PUUV among the population, risk counties of Västerbotten and Norrbotten were divided factors for disease and health consequences. into inland or coastal. The participants stated their The aims of the present study were; to define the highest educational level as primary school (up to nine current seroprevalence of PUUV infection in northern years of school), secondary school (ten to twelve years of Sweden; to define risk factors for infection, and link school) or university studies (higher education). The these findings to demographic and health data in a large, participants were asked to describe their main occupa- randomly selected and stratified population sample. In tion, descriptions later classified according to the addition, we investigated potential associations between “Nordic standard of occupational classification” of 1985 previous PUUV infection and cardiovascular risk factors [22]. In order to identify possible occupational risks for and/or chronic diseases. hantavirus infection, occupations with similar assumed exposure were grouped together as; 1) office personnel; Methods 2) teaching, clergy, police and military; 3) healthcare Study site and population workers; 4) construction, wood industry and plumbers; The MONICA project, “Multinational Monitoring of 5) engineers; 6) transportation, trade and service; 7) Trends and Determinants in Cardiovascular Disease” was industry; 8) agricultural work. In addition, it was asked initiated by the World Health Organisation (WHO) in whether the participants were owners of farmland or 1982. The purpose was to study levels, trends and risk forests. factors of stroke and coronary disease globally [20]. In Smoking habits were classified as regular smoker, northern Sweden, the counties of Norrbotten and smoking a least one cigarette a day, or non-smokers Västerbotten, with a combined population of approximately [23]. Individuals were asked to rank their own present 500,000 inhabitants, joined the MONICA project in 1985 health in one of five categories; 1) Very well, 2) Quite [21]. When the official WHO assignment was concluded
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