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Tularaemia, a disease caused by the bacterium , is a re-emerging zoonosis in the Netherlands. After sporadic human and hare cases occurred in the period 2011 to 2014, a cluster of -infected hares was recognised in a region in the north of the Netherlands from February to May 2015. No human cases were identified, including after active case finding. Presence of was investigated in potential reservoirs and transmission routes, including common voles, arthropod vectors and surface waters. was not detected in common voles, mosquito larvae or adults, tabanids or ticks. However, the bacterium was detected in water and sediment samples collected in a limited geographical area where infected hares had also been found. These results demonstrate that water monitoring could provide valuable information regarding spread and persistence, and should be used in addition to disease surveillance in wildlife.


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  1. Hestvik G, Warns-Petit E, Smith LA, Fox NJ, Uhlhorn H, Artois M, et al. The status of tularemia in Europe in a one-health context: a review. Epidemiol Infect. 2015;143(10):2137-60.  https://doi.org/10.1017/S0950268814002398  PMID: 25266682 
  2. Sissonen S, Rossow H, Karlsson E, Hemmilä H, Henttonen H, Isomursu M, et al. Phylogeography of Francisella tularensis subspecies holarctica in Finland, 1993-2011. Infect Dis (Lond). 2015;47(10):701-6.  https://doi.org/10.3109/23744235.2015.1049657  PMID: 26004621 
  3. Karadenizli A, Forsman M, Şimşek H, Taner M, Öhrman C, Myrtennäs K, et al. Genomic analyses of Francisella tularensis strains confirm disease transmission from drinking water sources, Turkey, 2008, 2009 and 2012. Euro Surveill. 2015;20(21):21136.  https://doi.org/10.2807/1560-7917.ES2015.20.21.21136  PMID: 26062561 
  4. Karlsson E, Svensson K, Lindgren P, Byström M, Sjödin A, Forsman M, et al. The phylogeographic pattern of Francisella tularensis in Sweden indicates a Scandinavian origin of Eurosiberian tularaemia. Environ Microbiol. 2013;15(2):634-45.  https://doi.org/10.1111/1462-2920.12052  PMID: 23253075 
  5. World Health Organization (WHO). WHO Guidelines on Tularaemia. Geneva: WHO; 2007. Available from: http://www.who.int/csr/resources/publications/deliberate/WHO_CDS_EPR_2007_7/en/
  6. Rossow H, Forbes KM, Tarkka E, Kinnunen PM, Hemmilä H, Huitu O, et al. Experimental Infection of voles with Francisella tularensis indicates their amplification role in tularemia outbreaks. PLoS One. 2014;9(10):e108864.  https://doi.org/10.1371/journal.pone.0108864  PMID: 25271640 
  7. Desvars A, Furberg M, Hjertqvist M, Vidman L, Sjöstedt A, Rydén P, et al. Epidemiology and ecology of tularemia in Sweden, 1984-2012. Emerg Infect Dis. 2015;21(1):32-9.  https://doi.org/10.3201/eid2101.140916  PMID: 25529978 
  8. Broman T, Thelaus J, Andersson AC, Backman S, Wikstrom P, Larsson E, et al. Molecular Detection of Persistent Francisella tularensis Subspecies holarctica in Natural Waters. International Journal of Microbiology. 2011;2011: 851946.  https://doi.org/http://dx.doi.org/10.1155/2011/851946 
  9. Abd H, Johansson T, Golovliov I, Sandström G, Forsman M. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol. 2003;69(1):600-6.  https://doi.org/10.1128/AEM.69.1.600-606.2003  PMID: 12514047 
  10. Maraha B, Hajer G, Sjodin A, Forsman M, Paauw A, Roeselers G, et al. Indigenous Infection with Francisella tularensis holarctica in The Netherlands. Case Reports in Infectious Diseases. 2013;2013:916985.  https://doi.org/http://dx.doi.org/10.1155/2013/916985 
  11. Koene MG, Rijks JM, Maas M, De Rosa M, Broens E, Vellema P, et al. Tularemie in Nederland, terug van weggeweest? [Tulaeremia in the Netherlands, out of hiding?]. Nederlands Tijdschrift voor Diergeneeskunde. 2015;140(8):4. Dutch. Available from: www.dwhc.nl/wp-content/uploads/2016/04/ARTIKEL_TULAREMIE_TVD_08_2015.pdf
  12. Pijnacker R, Koene M, Rijks JM, Swaan C, Maas M, De Rosa M, et al. Tularemie in Nederland, terug van weggeweest? [Tulaeremia in the Netherlands, out of hiding?]. Nederlands Tijdschrift voor Medische Microbiologie. 2016;24(2):4. Dutch. Available from: http://www.nvmm.nl/media/1330/2016-2-24e-jaargang-juni-2016-nummer-2.pdf
  13. Leenders ACAP, Essink AHPM, Notermans D, Koene MG, Schimmer B, Swaan CM, et al. Tularemie na 60 jaar terug in Nederland? [Tulaeremia back in the Netherlands after 60 years?]. Tijdschrift voor Infectieziekten. 2015;10:194-9. Dutch. Available from: http://www.ariez.nl/DownloadFile.lynkx?guid=5748c7a0-74ac-474f-8a73-609495832a4a
  14. The Minister of Health, Welfare and Sport and the Minister of Safety and Justice. Besluit van 23 augustus 2016, houdende aanpassing van het Besluit publieke gezondheid vanwege een meldingsplicht voor tularemie en zikavirusinfectie. [Decision of 23 August 2016, adaptation of the Decision Public Health because of a notification requirement for tularaemia and Zika virus infection]. The Hague: Staatsblad. 5 Sep 2016: Nr. 308. Available from: https://zoek.officielebekendmakingen.nl/stb-2016-308.html
  15. Rijks JM, Kik M, Koene MG, Engelsma MY, van Tulden P, Montizaan MG, et al. Tularaemia in a brown hare (Lepus europaeus) in 2013: first case in the Netherlands in 60 years. Euro Surveill. 2013;18(49):20655.  https://doi.org/10.2807/1560-7917.ES2013.18.49.20655  PMID: 24330941 
  16. van de Wetering D, Oliveira dos Santos C, Wagelaar M, de Kleuver M, Koene MG, Roest HI, et al. A cluster of tularaemia after contact with a dead hare in the Netherlands. Neth J Med. 2015;73(10):481-2. PMID: 26687265 
  17. Janse I, Hamidjaja RA, Bok JM, van Rotterdam BJ. Reliable detection of Bacillus anthracis, Francisella tularensis and Yersinia pestis by using multiplex qPCR including internal controls for nucleic acid extraction and amplification. BMC Microbiol. 2010;10:314. PMID: 21143837 
  18. Decors A, Lesage C, Jourdain E, Giraud P, Houbron P, Vanhem P, et al. Outbreak of tularaemia in brown hares (Lepus europaeus) in France, January to March 2011. Euro Surveill. 2011;16(28):19913. PMID: 21794224 
  19. Gyuranecz M, Reiczigel J, Krisztalovics K, Monse L, Szabóné GK, Szilágyi A, et al. Factors influencing emergence of tularemia, Hungary, 1984-2010. Emerg Infect Dis. 2012;18(8):1379-81.  https://doi.org/10.3201/eid1808.111826  PMID: 22840419 
  20. Luque-Larena JJ, Mougeot F, Roig DV, Lambin X, Rodríguez-Pastor R, Rodríguez-Valín E, et al. Tularemia Outbreaks and Common Vole (Microtus arvalis) Irruptive Population Dynamics in Northwestern Spain, 1997-2014. Vector Borne Zoonotic Dis. 2015;15(9):568-70.  https://doi.org/10.1089/vbz.2015.1770  PMID: 26333034 
  21. Petersen JM, Mead PS, Schriefer ME. Francisella tularensis: an arthropod-borne pathogen. Vet Res. 2009;40(2):7.  https://doi.org/10.1051/vetres:2008045  PMID: 18950590 
  22. van Hoek ML. Biofilms: an advancement in our understanding of Francisella species. Virulence. 2013;4(8):833-46.  https://doi.org/10.4161/viru.27023  PMID: 24225421 
  23. Sinclair R, Boone SA, Greenberg D, Keim P, Gerba CP. Persistence of category A select agents in the environment. Appl Environ Microbiol. 2008;74(3):555-63.  https://doi.org/10.1128/AEM.02167-07  PMID: 18065629 
  24. Schulze C, Heuner K, Myrtennäs K, Karlsson E, Jacob D, Kutzer P, et al. High and novel genetic diversity of Francisella tularensis in Germany and indication of environmental persistence. Epidemiol Infect. 2016;144(14):3025-36.  https://doi.org/10.1017/S0950268816001175  PMID: 27356883 
  25. Barns SM, Grow CC, Okinaka RT, Keim P, Kuske CR. Detection of diverse new Francisella-like bacteria in environmental samples. Appl Environ Microbiol. 2005;71(9):5494-500.  https://doi.org/10.1128/AEM.71.9.5494-5500.2005  PMID: 16151142 
  26. Berrada ZL, Telford SR 3rd. Diversity of Francisella species in environmental samples from Martha’s Vineyard, Massachusetts. Microb Ecol. 2010;59(2):277-83.  https://doi.org/10.1007/s00248-009-9568-y  PMID: 19669828 
  27. Trung TT, Hetzer A, Göhler A, Topfstedt E, Wuthiekanun V, Limmathurotsakul D, et al. Highly sensitive direct detection and quantification of Burkholderia pseudomallei bacteria in environmental soil samples by using real-time PCR. Appl Environ Microbiol. 2011;77(18):6486-94.  https://doi.org/10.1128/AEM.00735-11  PMID: 21803915 
  28. Kahler AM, Haley BJ, Chen A, Mull BJ, Tarr CL, Turnsek M, et al. Environmental surveillance for toxigenic Vibrio cholerae in surface waters of Haiti. Am J Trop Med Hyg. 2015;92(1):118-25.  https://doi.org/10.4269/ajtmh.13-0601  PMID: 25385860 
  29. Otto P, Kohlmann R, Müller W, Julich S, Geis G, Gatermann SG, et al. Hare-to-human transmission of Francisella tularensis subsp. holarctica, Germany. Emerg Infect Dis. 2015;21(1):153-5.  https://doi.org/10.3201/eid2101.131837  PMID: 25531286 
  30. Anda P, Segura del Pozo J, Díaz García JM, Escudero R, García Peña FJ, López Velasco MC, et al. Waterborne outbreak of tularemia associated with crayfish fishing. Emerg Infect Dis. 2001;7(7):575-82.  https://doi.org/10.3201/eid0707.017740  PMID: 11485678 
  31. Bäckman S, Näslund J, Forsman M, Thelaus J. Transmission of tularemia from a water source by transstadial maintenance in a mosquito vector. Sci Rep. 2015;5(1):7793.  https://doi.org/10.1038/srep07793  PMID: 25609657 
  32. Thelaus J, Andersson A, Broman T, Bäckman S, Granberg M, Karlsson L, et al. Francisella tularensis subspecies holarctica occurs in Swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding. Microb Ecol. 2014;67(1):96-107.  https://doi.org/10.1007/s00248-013-0285-1  PMID: 24057273 
  33. Lundström JO, Andersson AC, Bäckman S, Schäfer ML, Forsman M, Thelaus J. Transstadial transmission of Francisella tularensis holarctica in mosquitoes, Sweden. Emerg Infect Dis. 2011;17(5):794-9.  https://doi.org/10.3201/eid1705.100426  PMID: 21529386 
  34. Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, et al. Tularemia as a biological weapon: medical and public health management. JAMA. 2001;285(21):2763-73.  https://doi.org/10.1001/jama.285.21.2763  PMID: 11386933 

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