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Q Fever, Austria 2009 Allerberger F*, Apfalter P, Aspöck C, Bellmann-Weiler R, Daghofer E, Grund E, Hartmann G, Maass M, Silberbauer K, Thalhammer F, Walder G, Stanek G “Austrian Voluntary Q Fever Surveillance Group” Address for correspondence: Univ. Prof. Dr. Franz Allerberger Österreichische Agentur für Gesundheit und Ernährungssicherheit (AGES) Spargelfeldstraße 191 A-1220 Wien Tel. +43 (0) 50555--35500 Fax +43 (0) 50555--95-35500 E-mail: [email protected] ABSTRACT In Austria, C. burnetii infections in humans and in animals are not notifiable diseases. We performed a survey to assess the prevalence of human Q fever in Austria in 2009. In January 2010, a questionnaire was sent to nine laboratories in nine Austrian provinces, requesting anonymized data on Q fever tests performed in 2009. In parallel, all Austrian Departments of Infectious Disease were asked to report clinical cases of Q fever diagnosed in 2009. In total, 5361 initial sera were tested, 166 yielding antibody titers’ specific for C. burnetii (3.1 %). Three patients showed signs and symptoms compatible with Q fever, two of them with connections to highly likely animal reservoirs. No outbreak was documented in 2009. Our survey confirms that infection by C. burnetii is endemic in Austria. Occurrence of Q fever always should prompt investigations for a source of infection (contact with cattle, sheep, goats or parturient cats; consumption of raw milk). Although cases of miscarriage among cattle had reportedly occurred at the farm of one patient in the weeks before her hospitalization for Q-fever in Vorarlberg in 2009, to our knowledge no attempt was made to verify the presence of C. burnetii in this herd. Also in the case of the female patient from Tirol, to the best of our knowledge no attempt was made to identify C. burnetii in her sheep herd. An estimated 2,300 people contracted Q fever in the Netherlands in 2009, highly likely due to an increasingly large number of animals per farm (especially on large dairy goat farms). In all there are around 1.2 million sheep and 400,000 goats on 350 farms in the Netherlands, a country of 16 million people. In Austria (total population 8.3 Mio. inhabitants) there were (per 1.4.2008) 389,379 sheep on 15,276 farms and 77,655 goats on 10,278 farms. This significant difference - seven goats per Austrian farm versus 1142 goats per Dutch farm – may explain the absence of the “new Q-fever problem” in Austria. Whether global warming plays a role in the increasing prevalence of this desiccation-resistant organisms as recently hypothesized by various experts still has to be answered. A travel-warning against 1 Europe, issued by the USA in December 2009, underlines the need for valid data on the occurrence of human Q fever in Austria. INTRODUCTION Query fever is an acute (on occasion chronic) febrile illness caused by Coxiella burnetii, an intracellular, gram-negative pleomorphic bacterium. Goats, cattle, and sheep are the most common animal reservoirs, which – when infected – shed the desiccation-resistant organisms in urine, faeces, milk, and especially in birth products. A spore-like stage explains the ability of C. burnetii to withstand harsh environmental conditions. Humans are primarily infected by inhalation of contaminated aerosols and are the only animals known to develop illness regularly as a result of C. burnetii infection. Ingestion of contaminated food such as unpasteurised milk or cheese, and close contact with infected animals, particularly when these give birth, are other frequent causes of infection. Self-limited febrile illness is probably the most common form of acute Q fever; after an incubation period of 2-3 weeks patients suffer fever, headache, malaise and chills. The case fatality ratio in untreated cases is usually less than 1 %; it is negligible in treated cases, except for individuals who develop endocarditis [1]. Some infections may be totally asymptomatic. Pneumonia, endocarditis, hepatitis, osteomyelitis and neurological manifestations are other possible syndromes. A post Q fever fatigue syndrome has been described [1]. Endocarditis is the prime manifestation of chronic Q fever, especially in people with antecedent valvular disease. Occurrence of C. burnetii is considered worldwide (except New Zealand). In Austria, Q fever in humans and C. burnetii infections in animals are not notifiable diseases. We performed a survey to assess the prevalence of Q fever in Austria in 2009. MATERIAL AND METHODS In January 2010, a questionnaire was sent to nine laboratories in nine Austrian provinces, requesting anonymized data on Q fever tests performed in 2009. In parallel, all Austrian Departments of Infectious Diseases were asked to report clinical cases of Q fever diagnosed in 2009. Laboratory diagnosis is made by demonstration of a rise in specific antibodies between acute and convalescent stages by IF or CF, or by IgM detection through IF or ELISA. Diagnosis is facilitated by use of two antigen preparations: phase I, which represents the virulent agent, and avirulent phase II (generated by repeated passage of phage I organisms in embryonated chicken eggs). In the acute period, antibodies to phase II antigens are found at higher levels than antibodies to phase I. The reverse is true in chronic disease: high antibody titers to phase I may indicate chronic infection, such as endocarditis. To date, the serological criteria used for diagnosis of Q fever, the Tissot-Dupont cut-off for acute Q fever (anti–phase II IgG titre 1/200 and anti–phase II IgM titre 1/50) [2], are controversial, since many patients without acute Q fever meet these criteria [3]. In countries with mandatory reporting, a positive laboratory result without clinical disease [signs and symptoms that are consistent with Q fever infection] is not sufficient for notification [4]. Bacteria may be identified in tissues (liver biopsy or heart valve) by immunhistochemistry, EM and PCR. Culture requires BSL-3 facilities. 2 RESULTS Table 1 summarizes the results according to province. In total 5361 initial sera were tested, 166 yielding antibody titers specific for C. burnetii. Three patients showed signs and symptoms compatible with Q fever. No outbreak was documented in 2009. For comparison, the tests performed at the “Institut für Hygiene und angewandte Immunologie” (Ao.Univ.-Prof. Dr. med. Gerold Stanek) are listed in Table 2; no clinical information is available on these later data. Table 1: Summarized data on serological testing for human Q fever in 2009 as reported by nine laboratories in nine Austrian provinces Austrian province: Number of sera tested: Vorarlberg 10 Number of sera yielding antibody titers specific for C. burnetii 1 Tyrol 950 38 Salzburg Upper Austria Lower Austria Carinthia Styria Vienna Burgenland Total: 25 67 361 1 2855 1092 0 5361 0 2 25 0 32 68 166 3 Clinical cases: Lethal outcome #female 29 a: “acute febrile illness”, 1 week hospitalization #male 38 a: “fatigue” #female 25 a: „persistent subfebrile illness, fatigue” 3 0 0 0 Table 2: Summarized data on serological testing for human Q-fever performed at the “Institut für Hygiene und angewandte Immunologie” (Medical University Vienna) in 2009. Number of sera tested: Vorarlberg Tyrol Salzburg Upper Austria Lower Austria Carinthia Styria Vienna Burgenland Total: 15 4 136 67 361 41 18 1092 17 1751 Number of sera yielding antibody titers specific for C. burnetii 3 0 9 2 25 2 2 68 0 111 % 20.00 0.00 6.62 2.99 6.93 4.88 11.11 6.23 0.00 6.34 DISCUSSION In Austria, the first case of Q fever was documented in 1948 in Carinthia; in his publication, Hintermann described five sporadic cases [5]. The disease was also reported from the province Tyrol by Lass, who in 1952 described 360 self-observed cases [6]. While the validity of his diagnoses can be questioned, a WHO survey conducted in 1951 revealed 4 out of 9 positive sera from Tyrol to be correct positive [7]. Our survey confirms that infection by C. burnetii is endemic in Austria. For Austria, to our knowledge only two C. burnetii isolates have been cultured so far, both in Slovakia from Ixodes ricinus ticks collected in the Alpine region of Tyrol [8,9], although no tick-borne Q fever has been described in Austria. In a study conducted between 2005 and 2007, dealing with the prevalence of tick-borne pathogens in Austria, approximately 900 questing ticks (mainly Ixodes ricinus) were investigated using molecular biological methods [10]. Coxiella sp. was detected in two I. ricinus ticks in the province of Salzburg by nestedPCR, however sample sequencing has not been applied to confirm the results [10]. Approximately 0.6 to 6 % of the Austrian population are considered seropositive for antibodies against C. burnetii [11,12,13,14]. This complies well with the results of our finding, yielding seroprevalences of 3.1 % and 6.4 % among the serum samples tested in 2009. Also in 2009, Brockmann et al. performed a population-based cross sectional survey in rural and urban areas of Southern Germany to assess the seroprevalence of Q fever among 1,036 participants [15]. They identified a seroprevalence of 7.5 % (ranging from 0-18 % in the tested municipalities), a value in good accordance with our results. Realizing that a survey based on serological data from routine specimens is inevitably biased toward overestimation, we nevertheless consider the endeavour Austrian Voluntary Q Fever Surveillance Group a valid approach in view of absence of alternatives. 4 Previously, Q fever was primarily considered an occupational hazard in persons in contact with domestic animals such as cattle, sheep, and, less frequently, goats. Persons at risk from Q fever included farmers, veterinarians, abattoir workers, and those in contact with dairy products. Antibodies against C. burnetii were detected in 6 % of 1,026 sheep of 435 farms tested in Tyrol in 1994 [16]. In 2004, Wagner et al. reported C. burnetii seropositivity at 2 of 70 Styrian sheep farms tested, postulating a herd prevalence of 0.4-9.9 % based on a confidence interval of 95 %; antibodies to C. burnetii were detected at 5 of the 30 goat farms inspected, postulating a herd prevalence of 5.6 - 34.7 % [17]. Cat or dog ownership is not related to an increased incidence of antibodies against C. burnetii in Austria [12]. In the above mentioned study by Brockmann et al., close contact to goats, close contact to rats, being a waste control worker, being a farmer, close contact to cattle, and living in sight of a goat or sheep stable were – in this order – associated with seropositivity [15]. Even though the role of rodents in a natural cycle involving ticks is established, their role as a direct source for human Q fever infection has not yet been proven [15,18]. Occurrence of Q fever always should prompt investigations for a source of infection (contact with sheep, cattle goats or parturient cats; consumption of raw milk) [19]. Although cases of miscarriage among cattle had reportedly occurred at the farm of the patient in the weeks before her hospitalization for Q-fever in Vorarlberg in 2009, to our knowledge no attempt was made to verify the presence of C. burnetii in this herd. Also in the case of the female patient from Tyrol, to the best of our knowledge no attempt was made to identify C. burnetii in her sheep herd. Current epidemiologic studies indicate, that Q fever should be considered a public health problem in many countries, including the Netherlands, Germany, France, United Kingdom, Italy, Spain, Israel, and Greece [20,21]. In 2007, Slovenia experienced two outbreaks. The first was detected among high school students and students who worked on a sheep farm in the southwest part of Slovenia. Q fever was serologically confirmed in 83 patients [22]. In the second outbreak, a family from Slovenia working on a sheep farm in Croatia was infected. Q fever was serologically confirmed in three patients [23]. An estimated 2,300 people contracted Q fever in the Netherlands in 2009, up from 1,000 in 2008 and 168 in 2007 [4,24,25,26]. Still in 1955 the Netherlands were considered to be free from Q fever; according to Kaplan and Bertagna, it seems, that the traffic of infected ruminants may be one of the most important, if not the most important means for the geographical spread of Q fever [11]. One theory as to why the outbreak has been so severe in the Netherlands is the large number of animals per farm (especially on large dairy goat farms), combined with the density of the Dutch human population, which is one of the highest in the world. In all there are around 1.2 million sheep and 400,000 goats on 350 farms in the Netherlands, a country of 16 million people. In Austria (total population 8.3 Mio. inhabitants) there were (per 1.4.2008) 389,379 sheep on 15,276 farms and 77,655 goats on 10,278 farms. This significant difference - seven goats per Austrian farm versus 1142 goats per Dutch farm – may explain the absence of the “new Q fever problem” in Austria. However, also in Austria an ongoing suburbanization could bring more people into closer proximity with animals [15]. Directive 2009/99/EC on the monitoring of zoonotic agents requires EU Member States to monitor and report on cases of Q fever in animals warranted by the epidemiological 5 situation. Furthermore, Commission Decision 2000/96/EC, as amended by Decision 2003/534/EC, lists Q fever in humans as a communicable disease to be monitored and controlled in the EU [27]. That Q fever is not a statutorily notifiable disease constitutes an inherent weakness of the surveillance of human Q fever in Austria. Whether global warming plays a role in the increasing prevalence of this desiccation-resistant organisms as recently hypothesized by various experts still has to be answered, a challenge which asks for valid data on human Q fever in Austria too. A travel-warning against Europe, issued by the USA [http://wwwnc.cdc.gov/travel/content/in-the-news/q-fever-netherlands.aspx] in view of the outbreaks in the Netherlands, drastically underlines the considerable role that this infection could play in the upcoming future. References: [1] Heymann DL: Control of Communicable Diseases Manual. 19th edt. American Public Health Association, Washington DC. 2008. [2] Maurin M, Raoult D. Q fever. Clin Microbiol Rev. 1999;12:518-553. [3] Cilla G, Montes M, Pérez-Trallero E. Q fever in the Netherlands – what matters is seriousness of disease rather than quantity . Euro Surveill. 2008;13(37):pii=18975. 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BMC Infectious Diseases 2009; http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=1618839&blobtype=pdf DOI: doi:10.1186/1471-23346-147 [22] Grilc E, Socan M, Koren N, Ucakar V, Avsic T, Pogacnik M, Kraigher A. Outbreak of Q fever among a group of high school students in Slovenia, March-April 2007. Euro Surveill. 2007;12(29):pii=3237. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3237 [23] European Centre for Disease Prevention and Control. Annual Epidemiological Report on Communicable Diseases in Europe 2009. Stockholm, European Centre for Disease Prevention and Control ISBN 978-92-9193196-5 [24] Karagiannis I, Morroy G, Rietveld A, Horrevorts AM, Hamans M, Francken P, Schimmer B. A Q fever outbreak in the Netherlands: a preliminary report. Euro Surveill. 2007;12(32):pii=3247. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3247 [25] Schimmer B, Dijkstra F, Vellema P, Schneeberger PM, Hackert V, ter Schegget R, Wijkmans C, van Duynhoven Y, van der Hoek W. Sustained intensive transmission of Q fever in the south of the Netherlands, 2009. Euro Surveill. 2009;14(19):pii=19210. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19210 [26] Karagiannis I, Schimmer B, Van Lier A, Timen A, Schneeberger P, Van Rotterdam B, De Bruin A, Wijkmans C, Rietveld A, Van Duynhoven Y. 2009, Investigation of a Q fever outbreak in a rural area of The Netherlands Epidemiol Infect, 2009; 137:1283-1294. [27] Anonymous in ProMED-mail (2010) Available online: http://www.promedmail.org/pls/apex/f?p=2400:1001:1965956696361779::::F2400_P1001_BACK_PAGE,F2400 _P1001_ARCHIVE_NUMBER,F2400_P1001_USE_ARCHIVE:1202,20100204.0380,Y 7