Volume 18, Number 8—August 2012
Factors Influencing Emergence of Tularemia, Hungary, 1984–2010
To the Editor: Francisella tularensis, the etiologic agent of tularemia, is a highly infectious zoonotic agent. F. tularensis subsp. holarctica (type B) is found throughout the Northern Hemisphere and is the only subspecies found in Europe (1). Lagomorphs and rodents probably serve as the primary mammalian reservoir hosts, and hematophagous arthropods, such as ticks, play a role as vectors and hosts (2,3). Although F. tularensis is a potential agent of biological warfare and several emergences and reemergences of tularemia have been reported around the world (1,4), the epizootiology of the disease is only partially understood. The aim of our study was to analyze factors that influence the emergence of tularemia in Hungary.
The study area (15,475 km2) included 3 counties in eastern Hungary. The analyzed data represented a period of 25 years, March 1984–February 2010. Annual F. tularensis–specific seroprevalence data for the European brown hare (Lepus europaeus) population were obtained by slide agglutination testing during the winter (December and January) screening of 2,500–25,000 animals (Technical Appendix). Population density data (animals/km2) for hares were based on February line transect counts and were obtained from the Hungarian Game Management database (www.vvt.gau.hu/vadgazdalkodasi_statisztikak.htm). Common vole (Microtus arvalis) densities (calculated from the number of active burrows/hectare during November) for 1996–2010 were obtained from the Central Agriculture Office, Budapest, Hungary. Vole density was scaled from 0 (absent) to 10 (peak population). The annual number of tularemia cases in humans (based on clinical history and tube agglutination test results) was obtained from the National Center for Epidemiology, Budapest.
The data were regrouped according to the yearly biologic cycle (March–February) for hares and voles (Figure), and relationships between these yearly data were quantified by using the Spearman rank correlation coefficient (5) at county and regional levels. A 2–3 year cycle was characteristic for the analyzed data. A significant positive correlation was found among the number of tularemia cases in humans and the seroprevalence of F. tularensis among European brown hares (Spearman ρ = 0.73; p<0.0001) and the population density of common voles (Spearman ρ = 0.77; p = 0.0081). A significant negative correlation was found between the population density of hares and the seroprevalence of F. tularensis in hares (Spearman ρ = −0.41; p = 0.0365).
The comprehensive and long-term annual data used in this study provide clues regarding the factors shaping the intraannual epizootiology and emergence or reemergence of tularemia. The European brown hare is moderately sensitive to F. tularensis subsp. holarctica. The hares produce a heterogeneous response to infection, which means that some die of overwhelming bacteremia and others survive with a protracted course of infection, thereby contributing to the maintenance of tularemia over longer periods and serving as useful sentinels of disease activity. Other studies have concluded that hares, together with infected ticks, may serve as disease reservoirs between epizootics (2,3,6,7).
However, we instead hypothesize that the 2–3 year cycling feature of the population dynamics for the common vole (2) determines the ecology of F. tularensis subsp. holarctica in eastern Hungary. The common vole is highly susceptible to F. tularensis subsp. holarctica (3,8). When population densities among voles are high, F. tularensis disease transmission and spillover to hares may be facilitated by stress-related aggression, cannibalism, and F. tularensis contamination of the environment by infectious body discharges (2). Enhanced transmission and spillover can expand local outbreaks to epizootic proportions, and infected hares may, in turn, further enhance the spread of disease through bacterial shedding in urine (6,7).
The disease in hares often results in septicemia and death (7), thus decreasing the population density of these animals. Hares and especially voles are also hosts for different stages of several tick species (2,6), so it can be expected, that higher numbers of infected rodents and lagomorphs result in an increased proportion of infected ticks and, thus, increased transmission of F. tularensis subsp. holarctica. It can be concluded that a higher number of infection sources in the environment results in elevated numbers of cases in humans, mainly through the handling and skinning of hares, but also through tick bites and, potentially, the inhalation of infectious aerosols originating from, for example, hay or grain.
This study was supported by the Lendület program of the Hungarian Academy of Sciences and the Hungarian Scientific Research Fund (grant OTKA-78139). K.E. is a Bolyai János Research Fellow of the Hungarian Academy of Sciences.
- Petersen JM, Schriefer ME. Tularemia: emergence/re-emergence. Vet Res. 2005;36:455–67.
- Friend M. Tularemia, 1st ed. Reston (VA): US Geological Survey, circular 1297; 2006 [cited 2011 Feb 4]. http://www.nwhc.usgs.gov/publications/tularemia
- Mörner T, Addison E. Tularemia. In: Williams ES, Barker IK, editors. Infectious diseases of wild mammals, 3rd ed. Ames (IA): Iowa University Press; 2001. p. 303–12.
- Kaysser P, Seibold E, Matz-Rensing K, Pfeffer M, Essbauer S, Splettstoesser WD. Re-emergence of tularemia in Germany: presence of Francisella tularensis in different rodent species in endemic areas. BMC Infect Dis. 2008;8:157.
- R program. R Foundation for Statistical Computing, version 2.13.1. 2011 [cited 2011 Feb 4]. http://ftp5.gwdg.de/pub/misc/cran
- Gyuranecz M, Rigó K, Dán Á, Földvári G, Makrai L, Dénes B, Investigation of the ecology of Francisella tularensis during an inter-epizootic period. Vector Borne Zoonotic Dis. 2011;11:1031–5.
- Gyuranecz M, Szeredi L, Makrai L, Fodor L, Ráczné Mészáros Á, Szépe B, Tularemia of European brown hare (Lepus europaeus): a pathological, histopathological and immunhistochemical study. Vet Pathol. 2010;47:958–63.
- World Health Organization. WHO guidelines on tularemia. 2007 [cited 2011 Feb 4]. http://www.cdc.gov/tularemia/resources/whotularemiamanual.pdf
- Figure. . Correlation between the seroprevalence of Francisella tularensis in the European brown hare (Lepus europaeus) population, the population density of European brown hares and common voles (Microtus arvalis), and the...
- Technical Appendix. . Detailed data of the annual Francisella tularensis–specific seroprevalence in the European brown hare (Lepus europaeus) population, the annual population density of European brown hares and common voles (Microtus... 46 KB
Suggested citation for this article: Gyuranecz M, Reiczigel J, Krisztalovics K, Monse L, Kükedi Szabóné G, Szilágyi A, et al. Factors influencing emergence of tularemia, 1984–2010, Hungary [letter]. Emerg Infect Dis [serial on the Internet]. 2012 Aug [date cited]. http://dx.doi.org/10.3201/eid1808.111826
Please use the form below to submit correspondence to the authors or contact them at the following address:
Miklós Gyuranecz, Institute for Veterinary Medical Research, Centre for Agricultural Research–Hungarian Academy of Sciences, Hungária krt. 21, Budapest, H-1143, Hungary
Comment submitted successfully, thank you for your feedback.
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
- Page created: July 20, 2012
- Page last updated: July 20, 2012
- Page last reviewed: July 20, 2012
- Centers for Disease Control and Prevention,
National Center for Emerging and Zoonotic Infectious Diseases (NCEZID)
Office of the Director (OD)