Volume 15, Number 10—October 2009
Tick-borne Encephalitis from Eating Goat Cheese in a Mountain Region of Austria
We report transmission of tick-borne encephalitis virus (TBEV) in July 2008 through nonpasteurized goat milk to 6 humans and 4 domestic pigs in an alpine pasture 1,500 m above sea level. This outbreak indicates the emergence of ticks and TBEV at increasing altitudes in central Europe and the efficiency of oral transmission of TBEV.
Tick-borne encephalitis virus (TBEV) is a human pathogenic flavivirus that is endemic to many European countries and to parts of central and eastern Asia (1). Even though vaccination can effectively prevent TBE (2), >10,000 cases are reported annually for hospitalized persons in areas of Europe and Asia to which TBE is endemic. TBEV occurs in natural foci characterized by ecologic habitats favorable for ticks, especially in wooded areas within the 7°C isotherm (3). The major route of virus transmission is tick bites, but TBEV also can be transmitted during consumption of nonpasteurized milk and milk products from infected animals, primarily goats (3). Outbreaks resulting from oral virus transmission are rare in central Europe but more common in eastern Europe and the Baltic states (3). Our investigation of TBEV transmitted by milk from a goat in an alpine pasture in a mountainous region provides evidence for a changing TBEV epidemiology in central Europe and the expansion of ticks and TBEV to higher regions.
We investigated a TBE outbreak, comprising 6 cases, in a mountain region in western Austria in July 2008. The index case occurred in a 43-year-old shepherd who had stayed for 24 days at his alpine pasture (1,564 m above sea level) before he was hospitalized for nonbacterial urethritis and nonspecific influenza-like symptoms (including pain in the lower abdomen and legs), followed by clinical signs of meningitis. TBEV infection was confirmed serologically by ELISA demonstration of specific immunoglobulin (Ig) M and IgG in serum and cerebrospinal fluid. The patient did not remember a tick bite but had eaten self-made cheese prepared from a mixture of nonpasteurized goat milk and cow milk 8–11 days before illness onset; further investigation found 6 additional persons who had eaten the same cheese (Figure). For 5 of them, recent TBEV infection was serologically proven (Table). For 3 of these persons (2 men, 44 and 65 years of age; and 1 woman, 60 years of age), similar to the index patient, a typical biphasic course and symptoms of TBE (nonspecific flu-like symptoms followed by fever, cephalea, meningism, and ataxia after 4–10 days) developed and they were hospitalized. The 2 other persons who had eaten the cheese (female, 37 and 7 years of age) were clinically asymptomatic. The noninfected person had vomited shortly after eating the cheese because of a gastric banding. None of the infected persons had been vaccinated against TBEV.
The cheese was prepared from a mixture of fresh milk from 1 goat and 3 cows and was eaten shortly after production. Detection of TBEV-specific hemagglutination inhibiting (HI) and neutralizing antibodies in the goat’s serum proved infection in the goat; the 3 cows were seronegative for TBEV. At the time of this investigation (1 month after cheese production), TBEV was already undetectable by PCR in serum and milk of the goat. Cheese from the 3 batches produced after the contaminated batch was TBEV negative by PCR. The original cheese was no longer available for testing.
The 4 domestic pigs kept at the alpine pasture and fed with the whey and goat milk, however, were seropositive (TBEV HI- and neutralizing antibodies detected), which indicated TBEV infection, but no clinical signs were observed. Infection with TBEV has been reported in wild boars (4,5). Serum samples from 105 goats from pastures in the neighborhood also were investigated for TBEV-specific antibodies; all goats were seronegative.
Our analyses showed that the 6 humans and the 4 pigs were infected through the milk of 1 goat, which had been transported by car from a TBE–nonendemic valley to the alp 12 days before production of the TBEV-contaminated cheese. Experiments have demonstrated that infected domestic animals (i.e., goats, sheep, and cows) can excrete TBEV into milk for ≈3–7 days, beginning as early as the second or third day postinfection (6–9). In addition, although cheese was produced once or twice each week, only this ≈1-kg batch of cheese transmitted TBEV. Therefore, all the evidence indicates that the goat was infected at the alpine pasture at an altitude of 1,564 m. Indeed, some ticks were collected from cows that had stayed at this altitude during the entire summer. Analyses of these ticks for TBEV by PCR, however, yielded only negative results.
Our findings provide further evidence for the expansion of TBEV-endemic regions to higher altitudes in central Europe. For example, longitudinal studies in the Czech Republic, a country with similar climatic and ecologic conditions to those of Austria, showed a shift in Ixodes ricinus ticks and TBEV, from 700 m in 1981–1983 to 1,100 m altitude in 2001–2005 (10,11). Likewise, Zeman and Benes demonstrated that the maximum altitude at which TBEV is found in the Czech Republic gradually moved upward during 1970–2000, corresponding to the rise in temperature during the same period (12). In Scandinavia, a northward extension of the geographic range of I. ricinus ticks and TBEV since the mid-1980s has also been recognized (1,13–15). Climatic changes most likely are the major driving forces for the geographic changes in the distribution of TBEV and its main vector, I. ricinus, in Europe.
This report also emphasizes the efficiency of oral transmission of TBEV to humans and to pigs. Six of the 7 persons who ate the cheese and all 4 pigs fed residual milk or whey from the same cheese became infected. Given the excellent effectiveness of the TBE vaccine (2), vaccination probably could have prevented all 6 human cases.
Dr Holzmann is a virologist at the Clinical Institute of Virology, Medical University of Vienna, Austria. Her research interests focus on flaviviruses, hepatitis C virus, and antiviral vaccines.
We thank Jutta Hutecek and Cornelia Stöckl for expert technical assistance and Gabriel O’Riordain for critical reading of the manuscript.
- Lindquist L, Vapalahti O. Tick-borne encephalitis. Lancet. 2008;371:1861–71.
- Heinz FX, Holzmann H, Essl A, Kundi M. Field effectiveness of vaccination against tick-borne encephalitis. Vaccine. 2007;25:7559–67.
- Süss J. Epidemiology and ecology of TBE relevant to the production of effective vaccines. Vaccine. 2003;21(Suppl 1):S19–35.
- Borcić B, Raos B, Kranzelić D, Abu Eldan J, Filipović V. The role of large wildlife in the maintenance of natural foci of tick-borne meningoencephalitis in northern Croatia. Acta Med Iugosl. 1990;44:399–406.
- Zeman P, Januska J. Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endemic area. Comp Immunol Microbiol Infect Dis. 1999;22:247–60.
- Van Tongeren HA. Encephalitis in Austria. IV. Excretion of virus by milk of the experimentally infected goat. Arch Gesamte Virusforsch. 1955;6:158–62.
- Gresiková M. Excretion of tick-borne encephalitis virus in the milk of subcutaneously infected cows. Acta Virol. 1958;2:188–92.
- Gresiková M. Recovery of the tick-borne encephalitis virus from the blood and milk of subcutaneously infected sheep. Acta Virol. 1958;2:113–9.
- Gresiková M, Rehacek J. Isolation of the tick encephalitis virus from the blood and milk of domestic animals (sheep and cow) after infection by ticks of the family Ixodes ricinus L. Arch Gesamte Virusforsch. 1959;9:360–4.
- Daniel M, Danielová V, Kriz B, Kott I. An attempt to elucidate the increased incidence of tick-borne encephalitis and its spread to higher altitudes in the Czech Republic. Int J Med Microbiol. 2004;293(Suppl 37):55–62.
- Danielová V, Kliegrová S, Daniel M, Benes C. Influence of climate warming on tickborne encephalitis expansion to higher altitudes over the last decade (1997–2006) in the Highland Region (Czech Republic). Cent Eur J Public Health. 2008;16:4–11.
- Zeman P, Benes C. A tick-borne encephalitis ceiling in central Europe has moved upwards during the last 30 years: possible impact of global warming? Int J Med Microbiol. 2004;293(Suppl 37):48–54.
- Lindgren E, Gustafson R. Tick-borne encephalitis in Sweden and climate change. Lancet. 2001;358:16–8.
- Skarpaas T, Ljøstad U, Sundøy A. First human cases of tickborne encephalitis, Norway. Emerg Infect Dis. 2004;10:2241–3.
- Stjernberg L, Holmkvist K, Berglund J. A newly detected tick-borne encephalitis (TBE) focus in south-east Sweden: a follow-up study of TBE virus (TBEV) seroprevalence. Scand J Infect Dis. 2008;40:4–10.
Suggested citation for this article: Holzmann H, Aberle SW, Stiasny K, Werner P, Mischak A, Zainer B, et al. Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg Infect Dis [serial on the internet]. 2009 Oct [date cited]. Available from http://wwwnc.cdc.gov/eid/article/15/10/09-0743.htm
Comments to the Authors
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