Detection of Coxiella burnetii and Francisella tularensis in Tissues of Wild-living Animals and in Ticks of North-west Poland

BIELAWSKA-DRÓZD, AGATA; CIEŚLIK, PIOTR; ŻAKOWSKA, DOROTA; GŁOWACKA, PATRYCJA; WLIZŁO-SKOWRONEK, BOŻENA; ZIĘBA, PRZEMYSŁAW; ZDUN, ARKADIUSZ

doi:10.21307/pjm-2018-059

Abstract

This work presents results of the research on the occurrence of Coxiella burnetii and Francisella tularensis in the tissues of wild-living animals and ticks collected from Drawsko County, West Pomeranian Voivodeship. The real-time PCR testing for the pathogens comprised 928 samples of animal internal organs and 1551 ticks. The presence of C. burnetii was detected in 3% of wild-living animals and in 0.45–3.45% (dependent on collection areas) of ticks. The genetic sequences of F. tularensis were present in 0.49 % of ticks (only in one location – Drawa) and were not detected in animal tissues. The results indicate respectively low proportion of animals and ticks infected with C. burnetii and F. tularensis.

References

Al Dahouk S, Nöckler K, Tomaso H, Splettstoesser WD, Jungersen G, Riber U, Petry T, Hoffmann D, Scholz HC, Hensel A, et al. 2005. Seroprevalence of brucellosis, tularemia, and yersiniosis in wild boars (sus scrofa) from north-eastern Germany. Vet Med. 52(10):444–455.
Search in Google Scholar Back to article
Andreassen A, Jore S, Cuber P, Dudman S, Tengs T, Isaken K, Hygen HO, Viljugrein H, Anestad G, Ottesen P, et al. 2012. Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Par Vect. 5:177.
Search in Google Scholar Back to article
Anusz Z. 1995. Q fever in humans and animals. Olsztyn (Poland): ART.
Search in Google Scholar Back to article
Artois M. 2003. Wildlife infectious disease control in Europe. J Mountain Ecol. 7:89–97.
Search in Google Scholar Back to article
Astobiza I, Barral M, Ruiz-Fons F, Barandika JF, Gerrikagoitia X, Hurtado A, García-Pérez AL. 2011. Molecular investigation of the occurrence of Coxiella burnetii in wildlife and ticks in an endemic area. Vet Microbiol. 147(1):190–194.
Search in Google Scholar Back to article
Bielawska-Drózd A, Cieślik P, Wlizło-Skowronek B, Zięba P, Pitucha G, Gaweł J, Knap J. 2016. Studies on the occurrrence of Coxiell burnetii infection in ticks in selected eastern and central regions of Poland. JMBFS. 5(4):355–357.
Search in Google Scholar Back to article
Bielawska-Drózd A, Cieślik P, Mirski T, Gaweł J, Michalski A, Niemcewicz M, Bartoszcze M, Żakowska D, Lasocki K, Knap J, et al. 2014. Prevalence of Coxiella burnetii in environmental samples collected from cattle farms in Eastern and Central Poland (2011– 2012). Vet Microbiol. 174(3–4):600–606.
Search in Google Scholar Back to article
Bielawska-Drózd A, Cieślik P, Mirski T, Bartoszcze M, Knap J, Gaweł J, Żakowska D. 2013. Q fever-selected issues. Ann Agric Environ Med. 20(2):222–232.
Search in Google Scholar Back to article
Bielawska-Drózd A, Niemcewicz M, Gaweł J, Bartoszcze M, Graniak G, Joniec J, Kołodziej M. 2010. Identyfikacja Francisella tularensis techniką real-time PCR z wykorzystaniem sond hybrydyzujących zaprojektowanych dla fragmentów sekwencji genów fopA i tul4. Med Dosw Mikrobiol. 4(62):351–360 [in Polish].
Search in Google Scholar Back to article
Bossi P, Tegnell A, Baka A, Van Loock F, Hendriks J, Werner A, Maidhof H, Gouvras G. 2004. Bichat guidelines for the clinical management of Q fever and bioterrorism-related Q fever. Euro Surveill. 9(12):1–5.
Search in Google Scholar Back to article
Chmielewski T, Tylewska-Wierzbanowska S. 2013. Q fever outbreaks in Poland during 2005–2011. Med Sci Monit. 19:1073–1079.
Search in Google Scholar Back to article
Daszak P, Cunnigham AA, Hyatt AD. 2000. Emerging infectious diseases of wildlife-threats of biodiversity and human health. Science. 287(5452):443–449.
Search in Google Scholar Back to article
Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Friedlander AM, Hauer J, Layton M, et al. 2001. Tularemia as a biological weapon: medical and public health management. JAMA. 285(21):2763–2773.
Search in Google Scholar Back to article
Emmanuel PA, Bell R, Dang JL, McClanahan R, David JC, Burgess RJ, Thompson J, Collins L, Hadfield T. 2003. Detection of Francisella tularensis within infected mouse tissues by using a handheld PCR thermocycler. J Clin Microbiol. 41(2):689–693.
Search in Google Scholar Back to article
ECDC. 2016. Annual Epidemiological Report 2016 – Tularemia [Internet]. Stockholm (Sweden): European Centre for Disease Prevention and Control; [cited 2018 Jul 12]. Available from http://ecdc.europe.eu/en/healthtopics/tularemia/Pages/Annual-epidemiological-report-2016.aspx
Search in Google Scholar Back to article
Faber M, Heuner K, Jacob D, Grunow R. 2018. Tularemia in Germany – A Re-emerging zoonosis. Front Cell Infect Microbiol. 8:40.
Search in Google Scholar Back to article
Fard SRN, Khalili M. 2011. PCR-detection of Coxiella burnetii in ticks collected from sheep and goats in Southeast Iran. Iran J Arthropod Borne Dis. 5(1):1–6.
Search in Google Scholar Back to article
Formińska K, Zasada AA, Rastawicki W, Śmietańska K, Bander D, Wawrzynowicz-Syczewska M, Yanushevych M, Niścigórska-Olsen J, Wawszczak M. 2015. Increasing role of arthropod bites in tularemia transmission in Poland – case reports and diagnostic methods. Ann Agric Environ Med. 22(3):443–446.
Search in Google Scholar Back to article
Franke J, Fritzsch J, Tomaso H, Straube E, Dorn W, Hildebrandt A. 2010. Coexistence of pathogens in host-seeking and feeding ticks within a single natural habitat in Central Germany. Appl Environ Microbiol. 76(20):6829–6836.
Search in Google Scholar Back to article
Fujita O, Tatsumi M, Tanabayashi K, Jamada A. 2006. Development of a real-time PCR assay for detection and quantification of Francisella tularensis. Jpn J Infect Dis. 59(1):46–51.
Search in Google Scholar Back to article
González-Barrio D, Maio E, Vieira-Pinto M, Ruiz-Fons F. 2015. European rabbits as reservoir for Coxiella burnetii. Emerg Infect Dis. 21(6):1055–1058.
Search in Google Scholar Back to article
Halos L, Jamal T, Vial L, Maillard R, Suau A, Le Menach A, Boulouis HJ, Vayssier-Taussat M. 2004. Determination of an efficient and reliable method for DNA extraction from ticks. Vet Res. 35(6):709–713.
Search in Google Scholar Back to article
Hestvik G, Warns-Petit E, Smith LA, Fox NJ, Uhlhorn H, Artois M, Hannant D, Hutchings MR, Mattsson R, Yon L, et. al. 2015. The status of tularemia in Europe in a one-health context: a review. Epidemiol Infect. 143:2137–2160.
Search in Google Scholar Back to article
Higgins JA, Hubalek Z, Halouzka J, Elkins KL, Sjöstedt A, Shipley M, Ibrahim MS. 2000. Detection of Francisella tularensis in infected mammals and vectors using a probe-based polymerase chain reaction. Am J Trop Med Hyg. 62(2):310–318.
Search in Google Scholar Back to article
Hildebrandt A, Straube E, Neubauer H, Schmoock G. 2011. Coxiella burnetii and coinfections in Ixodes ricinus ticks in Central Germany. Vector Borne Zoonotic Dis. 11(8):1205–1207.
Search in Google Scholar Back to article
Hukić M, Numanović F, Šiširak M, Moro A, Dervović E, Jakovac S, Salimović Bešić I. 2010. Surveillance of wildlife zoonotic diseases in the Balkans Region. Med. Glas (Zenica). 7(2):96–105.
Search in Google Scholar Back to article
Jain J, Bindu L, Aravindakshan TV, Hitaishi VN, Binu KM. 2017. Evaluation of DNA extraction protocols from Ixodid ticks. IJEST. 6(3):1912–1917.
Search in Google Scholar Back to article
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature. 451:990–993.
Search in Google Scholar Back to article
Klee SR, Tyczka J, Ellebrok H, Franz T, Linke S, Baljer G, Appel B. 2006. Highly sensitive real-time PCR for specific detection and quantification of Coxiella burnetii. BMC Microbiol. 6:2.
Search in Google Scholar Back to article
Kuehn A, Schulze C, Kutzer P, Probst C, Hlinak A, Ochs A, Grunow R. 2013. Tularaemia seroprevalence of captured and wild animals in Germany: the fox (Vulpes vulpes) as a biological indicator. Epidemiol Infect. 141(4):833–840.
Search in Google Scholar Back to article
Lopes de Carvalho I, Santos N, Soares T, Ze-Ze L, Nuncio S. 2010. Francisella-like endosymbiont in Dermacentor reticulatus collected in Portugal. Vector Borne Zoonotic Dis. 11(2):185–188.
Search in Google Scholar Back to article
Marrie TJ. 1990. Q fever – the disease. Boca Raton (USA): CRC Press.
Search in Google Scholar Back to article
Mediannikov O, Fenollar F, Socolovschi C, Diatta G, Bassene H, Molez JF, Sokhna C, Trape JF, Raoult D. 2010. Coxiella burnetii in humans and ticks in rural Senegal. PLoS Negl Trop Dis. 4(4):e654.
Search in Google Scholar Back to article
Michelet L, Jancour G, Devillers E, Torina A, Vayssier-Taussat M, Bonnet SI, Moutailler S. 2016. Tick species, tick-borne pathogens and symbionts in an insular environment off the coast of Western France. Ticks Tick Borne Dis. 7(6):1109–1115.
Search in Google Scholar Back to article
Ndeereh D, Muchemi G, Thaiyah A, Otiende M, Angelone-Alasaad S, Jowers MJ. 2017. Molecular survey of Coxiella burnetii in wildlife and ticks at wildlife – livestock interfaces in Kenya. Exp Appl Acarol. 72:277–289.
Search in Google Scholar Back to article
Niemczuk K, Szymańska-Czerwińska M, Zarzecka A, Konarska H. 2011. Q fever in a cattle herd and humans in the Southeastern Poland. Laboratory diagnosis of the disease using serological and molecular methods. Bulletin – Veterinary Institute in Pulawy. 55(4):593–598.
Search in Google Scholar Back to article
Norlander L. Q-fever epidemiology and pathogenesis. 2000. Microbes Infect. 2(4):417–424.
Search in Google Scholar Back to article
Ohtake S, Martin RA, Saxena A, Lechuga-Ballesteros D, Santiago A, Barry EM, Truong-Le V. 2011. Formulation and stabilization of Francisella tularensis live vaccine strain. J Pharm Sci. 100(8):3076–3087.
Search in Google Scholar Back to article
Otto P, Chaignat V, Klimpel D, Diller R, Melzer F, Müller W, Tomaso H. 2014. Serological investigation of wild boars (Sus scrofa) and red foxes (Vulpes vulpes) as indicator animals for circulation of Francisella tularensis in Germany. Vector Borne Zoonotic Dis. 14(1):46–51.
Search in Google Scholar Back to article
Oyston PCF, Sjöstedt A, Titball RW. 2004. Tularemia: bioterrorism defence renews interest in Francisella tularensis. Nature Rev Microbiol. 2(12):967–978.
Search in Google Scholar Back to article
Petersen JM, Carlson J, Yockey B, Pillai S, Kuske C, Garbalena G, Pottumarthy S, Chalcraft L. 2009. Direct isolation of Francisella spp. from environmental samples. Lett Appl Microbiol. 48(6):663–667.
Search in Google Scholar Back to article
Reis C, Cote M, Paul RE, Bonnet S. 2011. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis. 11(7):907–916.
Search in Google Scholar Back to article
Rodriguez I, Fraga J, Noda AA, Mayet M, Duarte Y, Echevarria E, Fernández C. 2014. An alternative and rapid method for the extraction of nucleic acids from Ixodid ticks by potassium acetate procedure. Braz Arch Biol Technol. 57(4):542–547.
Search in Google Scholar Back to article
Seshadri R, Paulsen TI, Eisen JA, Read TD, Nelson KE, Nelson WC, Ward NL, Tattelin H, Davidsen TM, Beanan MJ, et al. 2003. Complete genome sequence of the Q fever pathogen, Coxiella burnetii. Proc Natl Acad Sci. 100(9):5455–5460.
Search in Google Scholar Back to article
Smetanova K, Schwarzova K, Kocianova E. 2006. Detection of Anaplasma phagocytophilum, Coxiella burnetii, Rickettsia spp., and Borrelia burgdorferi s.I in ticks, and wild-living animals in western and middle Slovakia. Ann N Y Acad Sci. 1078(1):312–315.
Search in Google Scholar Back to article
Spitalska E, Kocianova E. Detection of Coxiella burnetii in ticks collected in Slovakia and Hungary. 2003. Eur J Epidemiol. 18:263–266.
Search in Google Scholar Back to article
Sprong H, Tijsse-Klasen E, Langelar E, De Bruin M, Fonville M, Gassner F, Takken W, Van Wieren S, Nijhof A, Jongejan F, et al. 2012. Prevalence of Coxiella burnetii in ticks after a large outbreak of Q fever. Zoonoses Public Health. 59(1):69–75.
Search in Google Scholar Back to article
Szymańska-Czerwińska M, Galińska EM, Niemczuk K, Zasepa M. 2013. Prevalence of Coxiella burnetii infection in foresters and ticks in south-eastern Poland and comparison of diagnostic methods. Ann Agric Environ Med. 20(4):699–704.
Search in Google Scholar Back to article
Tarnvik A, Berglund L. 2003. Tularemia. Eur Respir J. 21(2):361–373.
Search in Google Scholar Back to article
Taussing L, Landau L. 2008. Pediatric Respiratory Medicine 2nd Edition. Philadelphia (USA): Mosby Elsevier.
Search in Google Scholar Back to article
Toledo A, Jado I, Olmeda AS, Casado-Nistal MA, Gil H, Escudero R, Anda P. 2009. Detection of Coxiella burnetii in ticks collected from Central Spain. Vector Borne Zoonotic Dis. 9(5):465–468.
Search in Google Scholar Back to article
Tomanowić S, Radulowić Z, Masuzawa T, Milutinović M. 2010. Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia. Parasite. 17(3):211–217.
Search in Google Scholar Back to article
Tylewska-Wierzbanowska S, Kruszewska D, Chmielewski T, Zukowski K, Zabicka J. 1996. Ticks as a reservoir of Borrelia burgdorferi and Coxiella burnetii on Polish terrain. Przegl Epidemiol. 50(3):245–251.
Search in Google Scholar Back to article
Woldehiwet Z. 2004. Q fever (coxiellosis): epidemiology and pathogenesis. Res Vet Sci. 77(2):93–100.
Search in Google Scholar Back to article
Wójcik-Fatla A, Zając V, Sawczyn A, Cisak E, Sroka J, Dutkiewicz J. 2015. Occurrence of Francisella spp. in Dermacentor reticulatus and Ixodes ricinus ticks collected in eastern Poland. Ticks Tick Borne Dis. 6(3):253–257.
Search in Google Scholar Back to article
Zhang F, Liu W, Wu XM, Xin ZT, Zhao QM, Yang H, Cao WC. 2008. Detection of Francisella tularensis in ticks and identification of their genotypes using multiple-locus variable-number tandem repeat analysis. BMC Microbiol. 8:152.
Search in Google Scholar Back to article

Detection of Coxiella burnetii and Francisella tularensis in Tissues of Wild-living Animals and in Ticks of North-west Poland

Abstract

Paradigm

My account