REVIEW PAPER
Zoonotic occupational diseases in forestry workers – Lyme borreliosis, tularemia and leptospirosis in Europe
 
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Institute for Work and Health, University of Lausanne, Switzerland
 
Ann Agric Environ Med. 2015;22(1):43–50
 
KEYWORDS
ABSTRACT
Introduction:
Forestry workers and other people who come into close contact with wild animals, such as hunters, natural science researchers, game managers or mushroom/berry pickers, are at risk of contracting bacterial, parasitological or viral zoonotic diseases. Synthetic data on the incidence and prevalence of zoonotic diseases in both animals and humans in European forests do not exist. It is therefore difficult to promote appropriate preventive measures among workers or people who come into direct or indirect contact with forest animals.

Objectives:
The objectives of this review are to synthesise existing knowledge on the prevalence of the three predominant bacterial zoonotic diseases in Europe, i.e. Lyme borreliosis, tularemia and leptospirosis, in order to draw up recommendations for occupational or public health.

Material and Methods:
88 papers published between 1995–2013 (33 on Lyme borreliosis, 30 on tularemia and 25 on leptospirosis) were analyzed.

Conclusions:
The prevalences of these three zoonotic diseases are not negligible and information targeting the public is needed. Moreover, the results highlight the lack of standardised surveys among different European countries. It was also noted that epidemiological data on leptospirosis are very scarce.

 
REFERENCES (83)
1.
Müller I, Freitag MH, Poggensee G, Scharnetzky E, Straube E, Schoerner CH, Hlobil H, Hagedorn HJ, Stanek G, Schubert-Unkmeir A, Norris DE, Gensichen J, Hunfeld , KP. Evaluating Frequency, Diagnostic Quality, and Cost of Lyme Borreliosis Testing in Germany: A Retrospective Model Analysis. Clin Dev Immunol. 2012; 13: 2012. doi:10.1155/2012/595427.
 
2.
Fritz CL. Emerging tick-Borne diseases. Vet Clin North America Small Animal Practice. 2009; 39: 265.
 
3.
Dutkiewicz J, Cisak E, Stroka J, Wojcik-Fatla A, Zajac V. Biological agents as occupational hazards – selected issues. Ann Agric Environ Med. 2011; 18: 286–293.
 
4.
Runge M, von Keyserlingk M, Berke O. Increased prevalence of Borrelia in ticks sampled within three forestry offices in Lower Saxony – a potential Borrelia hot-spot? J Cons Protect Food Saft. 2010; 5: 371–375.
 
5.
Huegli D, Moret J, Rais O, Moosmann Y, Erard P, Malinverni R, Gern L. Prospective study on the incidence of infection by Borrelia burgdorferi sensu lato after a tick bite in a highly endemic area of Switzerland. Ticks and Tick-borne Dis. 2011; 2: 129–136.
 
6.
Gern L. Life cycle of Borrelia burgdorferi sensu lato and transmission to humans. Curr Probl Dermatol. 2009; 37: 18–30.
 
7.
McGovern BH, Piesman JF. Microbiology and epidemiology of Lyme disease, UpToDate ® , 2010.
 
8.
Zhioua E, Postic D, Rodhain F, Perez-Eid C. Infection of Ixodes ricinus (Acari:Ixodae) by Borrelia burgdorferi in Ile de France. J Med Entomol. 1996; 33: 694–697.
 
9.
Cisak E, Chmielewska-Badora J, Zwolinski J, Wojcik-Fatla A, Polak J, Dutkiewicz J. Risk of tick-borne bacterial diseases among workers of Roztocze national park (south-eastern Poland). Ann Agric Environ Med. 2005; 12: 127–132.
 
10.
Cisak E, Chmielewska-Badora J, Zwolinski J, Wojcik-Fatla A, Zajac V, Skorska C, Dutkiewicz J. Study on Lyme borreliosis focus in the Lublin region (eastern Poland). Ann Agric Environ Med. 2008; 15: 327–332.
 
11.
Cinco M, Barbone F, Grazia Ciufolini M, Mascioli M, Anguero Rosenfeld M, Stefanel P, Luzzati R. Seroprevalence of tick-borne infections in forestry rangers from northeastern Italy. Clin Microbiol Infect. 2004; 10: 1056–1061.
 
12.
Thorin C, Rigaud E, Capek I, André-Fontaine G, Oster B, Gastinger G, Abadia G. Séroprévalence de la borréliose de Lyme et de l’encéphalite à tiques chez les professionnels exposés dans le Grand Est de la France. Médecine et maladies infectieuses. 2008; 38: 533–542 (in French).
 
13.
Chmielewska-Badora J, Seroepidemiological study on Lyme borreliosis in the Lublin Region. Ann Agric Environ Med. 1998; 5: 183–186.
 
14.
Cisak E, Wojcik-Fatla A, Zajac V, Stroka J, Dutkiewicz J. Risk of Lyme disease at various sites and workplaces of forestry workers in eastern Poland. Ann Agric Environ Med. 2012; 19:465–468.
 
15.
Sexton DJ. Diagnosis of Lyme disease, UpToDate ®. , 2010.
 
16.
Zhioua E, Rodhain F, Binet P, Perez-Eid C. Prevalence of antibodies to Borrelia burgdorferi in forestry workers of Ile de France, France. Europ J Epidemiol. 1997; 13: 959–962.
 
17.
Tomao P, Ciceroni L, D’Ovidio MC, De Rosa M, Vonesch N, Iavicoli S, Signorini S, Ciarrocchi S, Ciufolini MG, Fiorentini C, Papaleo B. Prevalence and incidence of antibodies to Borrelia burgdorferi and tick-borne encephalitis virus in agricultural and forestry workers from Tuscany, Italy. Eur J Clin Microbiol Infect Dis. 2005; 24: 457–463.
 
18.
Santino I, Cammarata E, Franco S, Galdiero F, Oliva B, Sessa R, Cipriani P, Tempera G, Del Piano M. Multicentric study of seroprevalence of Borrelia burgdorferi and Anaplasma phagocytophila in high risk groups in regions of central and southern Italy. Intern J Immunopathol Pharmacol. 2004; 17: 219–223.
 
19.
Bilski B. Occurrence of cases of borreliosis certified as an occupational disease in the province of Wielkopolska (Poland). Ann Agric Environ Med. 2009; 16: 211–217.
 
20.
Lewandowska A, Kruba Z, Filip R. Epidemiology of Lyme disease among workers of forest inspectorates in Poland. Ann Agric Environ Med. 2013; 20: 329–331.
 
21.
Hopla CE. The ecology of tularaemia. Ad Vet Sci Comp Med. 1974; 18: 25–53.
 
22.
Feldman KA. Tularemia. J Am Vet Med Ass. 2003; 222: 725–730.
 
23.
Vaissaire J, Mendy C, Le Doujet C, Le Coustumier A. La tularémie: la maladie et son épidémiologie en France. Médecine et maladies infectieuses 2005; 35: 273–280 (in French).
 
24.
Sjöstedt A. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann NY Acad Sci. 2007; 1105: 1–29.
 
25.
Foley JE, Nieto NC. Tularemia. Vet Microbiol. 2010; 140: 332–338.
 
26.
Keim P, Johansson A, Wagner DM. Molecular epidemiology, evolution and ecology of Francisella. Ann New York Ac Sci. 2007; 1105: 54–66.
 
27.
INRS (anonymous). Tularémie, rapport de l’Institut national de recherche et de sécurité pour la prévention des accidents du travail et des maladies professionnelles. INRS, 2005 (in French).
 
28.
Hazlett KRO, Cirillo KA. Environmental adaptation of Francisella tularensis. Microb Infect. 2009; 11: 828–834.
 
29.
Kaysser P, Seibold E, Mätz-Rensing K, Pfeffer M, Essbauer S, Splettstoesser WD. Re-emergence of tularaemia in Germany: Presence of Francisella tularensis in different rodent species in endemic areas. BMC Infect Dis. 2008; 8:157.
 
30.
Hofer E, Schildorfer H, Flatscher J, Müller M. Zum Nachweis der Tularämie bei Feldhasen (Lepus europaeus) in Österreich. Wien Tierärztl Monatsschr. 1997; 84: 301–306.
 
31.
Hoflechner-Poltl A, Hofer E, Awad-Masalmeh M, Muller M, Steineck T. Prevalence of tulareamia and brucellosis in European brown hares (Lepus europaeus) and red foxes (Vulpes vulpes) in Austria. Tieraerztl Umsch. 2000; 55: 264–268.
 
32.
Winkelmayer R, Vodnansky M, Paulsen P, Gansterer A, Treml F. Explorative study on the seroprevalence of Brucella-, Francisella- and Leptospira antibodies in the European hare (Lepus europaeus Pallas) of the Austrian-Czech border region. Vet Med Austria/Wien Tierärztl Mschr. 2005; 92: 131–135.
 
33.
Lopes de Carvalho I, Escudera R, Garcia-Amil C, Falcao H, Anda P, Nuncio MS. Francisella tularensis, Portugal. Emerg Infect Dis. 2007; 13: 666–667.
 
34.
Hubalek Z, Sixl W, Halouzka J. Francisella tularensis in Dermacentor reticulatus ticks from the Czech Republic and Austria. Wien Klin Wochenschr. 1998; 110: 909–910.
 
35.
Gurycova D, Vyrostekova V, Khanakah G, Kocianova E, Stamek G. Importance of surveillance of tularemia natural foci in the known endemic area of Central Europe 1991–1997. Wien Klin Wochenschr. 2001; 113: 433–438.
 
36.
Hubalek Z, Treml F, Halouzka J, Juricova Z, Hunady M, Janik V. Frequent isolation of Francisella tularensis from Dermacentor reticulates ticks in an epizootic focus of tularaemia. Med Vet Entomol. 1996; 10: 241–246.
 
37.
Wicki R, Sauter P, Mettler C, Natsch A, Enzler T, Pusterla N, Kuhnert P, Egli G, Bernasconi M, Lienhard R, Lutz H, Leutenegger CM. Swiss Army Survey in Switzerland to determine the prevalence of Francisella tularensis, members of Ehrlichia phagocytophila genogroup, Borrelia burgdorferi sensu lato, and tick-borne encephalitis virus in ticks. Eur J Clin Microbiol Infect Dis. 2000; 19: 427–432.
 
38.
Milutinovic M, Masuzawa T, Tomanovi S, Radulovic Z, Fukui T, Okamoto Y. Borrelia burgdorferi sensu lato, Anaplasma phago cytophilum, Francisella tularensis and their co-infection in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol. 2008; 45: 171–183.
 
39.
Jenzora A, Jansen A, Ranisch H, Lierz M, Wichmann O, Grunow R. Seroprevalence study of Francisella tularensis among hunters in Germany. FEMS Immunol Med Microbiol. 2008; 53: 183–189.
 
40.
Caron V. Leptospirose et milieu professionnel, rapport de l’INRS, Documents pour le Médecin du Travail. 2009;120: 485–489 (in French).
 
41.
Dale Everett E. Microbiology, epidemiology, clinical manifestations, and diagnosis of leptospirosis, UpToDate. 2010.
 
42.
Nardone A, Capek I, Baranton G, Campèse C, Postic D, Vaillant V, Liénard M, Desenclos JC. Risk Factors for Leptospirosis in Metropolitan France: Results of a National Case-Control Study, 1999–2000. Clin Infect Dis. 2004; 39: 751–753.
 
43.
Bessire N. La leptospirose – une maladie professionnelle, Schweiz. Med Forum. 2004; 4: 513–514.
 
44.
Jansen A, Schöneberg I, Frank C, Alpers K, Schneider T, Stark K. Leptospirosis in Germany, 1962–2003. Emerg Infect Dis. 2005; 11: 1048–1054.
 
45.
Levett PN. Leptospirosis: A forgotten zoonosis? Clinic App Immunol. Rev. 2004; 4: 435–448.
 
46.
Bharti AR, Nally JE, Ricaldi JN, Matthias MA, Diaz MM, Lovett MA, Levett PN, Gilman RH, Willig MR, Gotuzzo E, Vinetz JM. Leptospirosis: a zoonotic disease of global importance. The Lancet Infec Dis. 2003; 3: 757–771.
 
47.
Wasinski B, Dutkiewicz J. Leptospirosis – current risk factors connected with human activity and the environment. Ann Agric Environ Med. 2013; 20: 239–244.
 
48.
Vijayachari P, Sugunan AP, Shriram AN. Leptospirosis: an emerging global public health problem. Ind Ac Sci Biosci J. 2008; 33: 557–569.
 
49.
Adler B, De la Pena Moctezuma A. Leptospira and leptospirosis. Vet Microbiol. 2010; 140: 287–296.
 
50.
Ebani VV, Cerri D, Poli A, Andreani E. Prevalence of Leptospira and Brucella Antibodies un Wild Boars (sus scrofa) in Tuscany, Italy. J Wildlife Dis. 2003; 39: 718–722.
 
51.
Vengust G, Lindtner-Knific R, Zele D, Bidovec A. Leptospira antibodies in wild boars (sus scrofa) in Slovenia. Eur J Wildl Res. 2008; 54: 749–752.
 
52.
Treml F, Pikula J, Holesovska Z. Prevalence of antibodies against leptospires in the wild boar (Sus scrofa L., 1758). Vet Med Czech. 2003; 48: 66–70.
 
53.
Slavica A, Cvetnic Z, Milas Z, Janicky Z, Turk N, Konjevic D, Severin K, Toncic J, Lipej Z. Incidence of leptospiral antibodies in different game species over a 10-year period (1996–2005) in Croatia. Eur J Wildl Res. 2008; 5: 305–311.
 
54.
Cvetnic Z, Margaletic J, Toncic J, Turk N, Milas Z, Spicic S, Lojkic M, Terzic S, Jemersic L, Humski A, Mitak M, Habrun B, Krt B. A serological survey and isolation of leptospires from small rodents and wild boars in the Republic of Croatia. Vet Med Czech. 2003; 48: 321–329.
 
55.
Taseva E, Christova I, Gladnishka T. Epidemiological, clinical and serological features of human leptospirosis in Bulgaria in 2005. Int J Antimicrobial Agents. 2005; 29: S282-S282.
 
56.
Abgueguen P, Delbos V, Blanvillain J, Chennebault JM, Cottin J, Fanello S, Pichard E. Clinical aspects and prognostic factors of leptospirosis in adults. Retrospective study in France. J Infec. 2008; 57: 171–178.
 
57.
Cisak E, Wojcik-Fatla A, Zajac V, Dutkiewicz J. Repellents and acaricides as personal protection measures in the prevention of tick-borne diseases. Ann Agric Environ Med. 2012; 19:625–630.
 
58.
Hofmann F. Seroprevalence of infection with Borrelia burgdorferi s.l. in two adjacent regions of eastern France and southwestern Germany. Int J Med Microbiol. 2002; 291: 218–218.
 
59.
Christiann F, Rayet P, Patey O, Ngueodjibaye DB, Theron-le Gargasson JF, Lafaix C. Lyme borreliosis in central France: A sero-epidemiologic examination involving hunters. Europ J Epidemiol. 1997; 13: 855.
 
60.
Di Renzi S, Martini A, Binazzi A, Marinaccio A, Vonesch N, D’Amico W, Moro T, Fiorentini C, Ciufolini MG, Visca P, Tomao P. Risk of acquiring tick-borne infections in forestry workers from Lazio, Italy. Eur J Clin Microbiol Infect. Dis. 2010; 29: 1579–1581.
 
61.
Nübling M, Rieger MA, Wangerin W, Batsford S, Tiller FW, Hofmann F. Occupational risk of infections with Borrelia burgdorferi in agricultural and forestry workers. Zent Bl Bakteriol. 1999; 289: 720–724.
 
62.
Rath PM, Ibershoff B, Mohnhaupt A, Albig J, Eljaschewitsch B, Jürgens D, Horbach I, Fehrenbach FJ. Seroprevalence of Lyme borreliosis in forestry workers from Brandenburg, Germany. Eurp J Clin Microbiol Infect Dis. 1996; 15: 372–377.
 
63.
Moll van Charante AW, Groen J, Mulder PGH, Rijpkema SGT, Osterhaus ADME. Occupational risks of zoonotic infections in Dutch forestry workers and muskrat catchers. Europ J Epidemiol. 1998; 14: 109–116.
 
64.
Buczek A, Rudek A, Katarzyna B, Szymanska J, Wojcik-Fatla A. Seroepidemiological study of Lyme borreliosis among forestry workers in southern Poland. Ann Agric Environ Med. 2009; 16: 257–261.
 
65.
Niscigorska J, Skotarczak B, Wodecka B. Borrelia burgdoreferi infection among forestry workers-assessed with an immunoenzymatic method (ELISA), PCR, and correlated with the clinical state of the patients. Ann Agric Environ Med. 2003; 10: 15–19.
 
66.
Cisak E, Chmielewska-Badora J, Dutkiewicz J, Zwolinski J. Preliminary studies on the relationship between Ixodes ricinus activity and tick-borne infection among occupationally-exposed inhabitants of eastern Poland. Ann Agric Environ Med. 2001; 8: 293–295.
 
67.
Cisak E, Zajac V, Wojcik-Fatla A, Dutkiewicz J. Risk of tick-borne diseases in various categories of employment among forestry workers in eastern Poland. Ann Agric Environ Med. 2012, 19: 469–474.
 
68.
Rojko T, Ruzic-Sabjic E, Strle F, Lotric-Furlan S. Prevalence and incidence of Lyme borreliosis among Slovene forestry workers during period of tick activity. Wien Klin Wochenschr. 2005; 117: 219–225.
 
69.
Hristea A, Hristescu S, Ciufecu C, Vasile A. Seroprevalence of Borrelia Burgdorferi in Romania. Europ J Epidemiol. 2001; 17: 891–896.
 
70.
Kaya AD, Parlak AH, Ozturk CE, Behcet M. Seroprevalence of Borrelia burgdorferi infection among forestry workers and farmers in Duzce, north-western Turkey. New Microbiol. 2008; 31: 203–209.
 
71.
Lakos A, Igari Z, Solymosi N. Recent lesson from a clinical and seroepidemiological survey: low positive predictive value of Borrelia burgdorferi antibody testing in a high risk population. Ad Med Sci. 2012; 57: 356–363.
 
72.
Deutz A, Fuchs K, Nowotny N, Auer H, Schuller W, Stünzner D, Aspöck H, Kerbl U, Köfer J. Seroepidemiologische Untersuchungen von Jägern auf Zoonosen-Vergleich mit Untersuchungen bei Tierärzten, Landwirten und Schlachthofarbeitern. Wien Klin Wochenschr. 2003; 115: 61–67.
 
73.
Porsch-Ozcurumez M, Kischel N, Priebe H, Splettstosser W, Finkle EJ, Grunow R. Comparison of enzyme-linked immunosorbent assay, Western blotting, microagglutination, indirect immunofluorescence assay, and flow cytometry for serological diagnosis of tularaemia. Clin Diagn Lab Immun. 2004; 11: 1008–1015.
 
74.
Rastawicki W, Kurowska J, Hermanowska-Szpakowicz T, Pancewicz SA, Kondrusik M, Jagielski M. Prevalence of antibodies to Francisella tularensis in forest workers from different regions of Poland. Med Dosw Mikrobiol. 2006; 58: 207–215.
 
75.
Berdal BP, Mehl R, Meidell NK, Lorentzen-Styr AM, Scheel O. Field investigations of tularemia in Norway, Immunol. Med Microbiol. 1996: 13: 191–195.
 
76.
Treml F, Pikula J, Bandouchova H, Horakova J. European brown hare as potential source of zoonitc agents. Vet Med. 2007; 52: 451–456.
 
77.
Hubalek Z, Treml F, Juricova Z, Hunady M, Halouzka J, Janik V, Bill D. Serological survey of wild boar (Sus scrofa) for tularemia and brucellosis in South Moravia Czech Republic. Vet Med Czech. 2002; 47: 60–66.
 
78.
Vyrostekova V, Khanakah G, Kocianova E, Gurycova D, Stanek G. Prevalence of coinfection with Francisella tularensis in reservoir animals of Borrelia burgdorferi sensu lato. Wien Klin Wochenschr. 2002;114: 482–488.
 
79.
Dahouk SA, Nöckler K, Tomaso H, Splettstoesser WD, Jungersen G, Riber U, Petry T, Hoffmann D, Scholz HC, Hensel A, Neubauer H. Seroprevalence of Brucellosis, Tularemia, and Yersiniosis in Wild Boars (Sus scrofa) from North-Eastern Germany. J Vet Med B. 2005; 52: 444–455.
 
80.
Frölich K, Wisser J, Schmüser H, Fehlberg U, Neubauer H, Grunow R, Nikolaou K, Priemer J, Thiede S, Streich WJ, Speck S. Epizootiologic and ecologic investigations of European brown hares (Lepus europaeus) in selected populations from Schleswig-Holstein Germany. J Wildlife Dis. 2003; 39: 751–761.
 
81.
Schönberg A, Walburga L, Kämpe U. Untersuchung von Serumproben vom Schwarzwild (Sus scrofa L. 1758) auf Leptospirose. Z Jagdwiss. 1999; 45: 262–265.
 
82.
Slavica A, Dezdek D, Konjevic D, Cvetnic Z, Sindicic M, Stanin D, Habus J, Turk N. Prevalence of leptospiral antibodies in the red fox (Vulpes vulpes) population of Croatia. Vet Med. 2011; 56: 209–213.
 
83.
Oehme R, Hartelt K, Backe H, Brockmann S, Kimmig P, Foci of tick-borne diseases in Southwest Germany. Int J Med Microbiol. 2002; 291: 22–29.
 
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