A Field Study of Plague and Tularemia in Rodents, Western Iran
Publication: Vector-Borne and Zoonotic Diseases
Volume 17, Issue Number 4
Abstract
Introduction: Kurdistan Province in Iran is a historical focus for plague and tularemia. This study aimed at assessing the current status of these two foci by studying their rodent reservoirs.
Materials and Methods: Rodents were trapped and their ectoparasites were collected. The genus and species of both rodents and ectoparasites were determined. Serological analyses of rodent blood samples were done by enzyme-linked immunosorbent assay for plague and by standard tube agglutination assay for tularemia. Rodent spleen samples were subjected to bacterial culture, microscopic examination, and real-time PCR to search for active plague or tularemia infection.
Results: During this study, 245 rodents were trapped, of which the most abundant genera were Apodemus (40%), Mus (24.49%), and Meriones (12.65%). One hundred fifty-three fleas, 37 mites, and 54 ticks were collected on these rodents. The results of all direct and indirect tests were negative for plague. Serological tests were positive for tularemia in 4.8% of trapped rodents.
Discussion: This study is the first report on the presence of tularemia infection in rodents in Western Iran. Since Meriones persicus is a known reservoir for plague and tularemia, and this rodent carried plague and tularemia vectors in Marivan and Sanandaj districts, there is a real potential for the occurrence of these two diseases in this region.
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References
Akalın H, Helvacı S, Gedikoğlu S. Re-emergence of tularemia in Turkey. Int J Infect Dis 2009; 13:547–551.
Amirova N, Pakizh V, Chepeliuk M, Suprun V, et al. [Ixodid ticks of Pavlodar Province and their participation in the circulation of tularemia infection]. Parazitologiia 1988; 23:267–274.
Arata A, Chamsa M, Farhang-Azad A, Meščerjakova I, et al. First detection of tularaemia in domestic and wild mammals in Iran. Bull World Health Organ 1973; 49:597.
Azizi MH, Azizi F. A history of the human plague in Iran. Arch Iran Med 2010; 13:563–569.
Bakanidze L, Imnadze P, Chubinidze S, Tsertsvadze N, et al. Surveillance on plague in natural foci in Georgia. In: O'Connell KP, Skowronski EW, Sulakvelidze A, Bakanidze L, eds. Emerging and Endemic Pathogens. Springer Netherlands, 2010:21–28.
Baltazard M, Bahmanyar M, Mofidi C, Seydian B. [Kurdistan plague focus]. Bull World Health Organ 1951; 5:441–472.
Baltazard M, Bahmanyar M, Mostachfi P, Eftekhari M, et al. [Research on plague in Iran]. Bull World Health Organ 1960; 23:141.
Bengis R, Leighton F, Fischer J, Artois M, et al. The role of wildlife in emerging and re-emerging zoonoses. Rev Sci Tech 2004; 23:497–512.
Bushon R, Kephart C, Koltun G, Francy D, et al. Statistical assessment of DNA extraction reagent lot variability in real-time quantitative PCR. Lett Appl Microbiol 2010; 50:276–282.
Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, et al. Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet 2003; 361:211–216.
Chin J. Control of Communicable Disease Manual. Washington: American Public Health Association, 2000.
Clark DV, Ismailov A, Seyidova E, Hajiyeva A, et al. Seroprevalence of tularemia in rural Azerbaijan. Vector Borne Zoonotic Dis 2012; 12:558–563.
Corbet GB. The Mammals of the Palaearctic Region: A Taxonomic Review. 1978:314, 322.
Dedeoğlu KG, Gürcan S, Eskiocak M, Kilic H, et al. [Investigation of tularemia seroprevalence in the rural area of Thrace region in Turkey]. Mikrobiyol Bul 2007; 41:411–418.
Dikid T, Jain S, Sharma A, Kumar A, et al. Emerging & re-emerging infections in India: An overview. Indian J Med Res 2013; 138:19–31.
Duplantier JM, Duchemin JB, Chanteau S, Carniel E. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res 2005; 36:437–453.
Emanuel PA, Bell R, Dang JL, McClanahan R, et al. Detection of Francisella tularensis within infected mouse tissues by using a hand-held PCR thermocycler. J Clin Microbiol 2003; 41:689–693.
Erdem H, Ozturk-Engin D, Yesilyurt M, Karabay O, et al. Evaluation of tularaemia courses: A multicentre study from Turkey. Clin Microbiol Infect 2014; 20:O1042–O1051.
Esmaeili S, Azadmanesh K, Naddaf SR, Rajerison M, et al. A serological survey of plague in animals in western Iran. Emerg Infect Dis 2013; 19:1549–1551.
Esmaeili S, Esfandiari B, Maurin M, Gouya M, et al. Serological survey of tularemia among butchers and slaughterhouse workers in Iran. Trans R Soc Trop Med Hyg 2014a; 108:516–518.
Esmaeili S, Gooya MM, Shirzadi MR, Esfandiari B, et al. Seroepidemiological survey of tularemia among different groups in western Iran. Int J Infect Dis 2014b; 18:27–31.
Guidelines on Tularemia. 2007, Geneva, Switzerland: World Health Organization. Available at: www.cdc.gov/tularemia/resources/whotularemiamanual.pdf
Gurbanov S, Akhmedova S. Especially dangerous infections in Azerbaijan. In: O'Connell KP, Skowronski EW, Sulakvelidze A, Bakanidze L, eds. Emerging and Endemic Pathogens. Springer Netherlands, 2010:39–43.
Gyuranecz M, Rigó K, Dán Á, Földvári G, et al. Investigation of the ecology of Francisella tularensis during an inter-epizootic period. Vector Borne Zoonotic Dis 2011; 11:1031–1035.
Hashemi Shahraki A, Carniel E, Mostafavi E. Plague in Iran: Its history and current status. Epidemiol Health 2016; 38:e2016033.
Hestvik G, Warns-Petit E, Smith L, Fox N, et al. The status of tularemia in Europe in a one-health context: A review. Epidemiol Infect 2015; 143:2137–2160.
Karimi Y. Conservation naturelle de la peste dans le sol. Bull Soc Pathol Exot 1963; 56:1183–1186.
Karimi Y. Plague and Its Epidemiology. Tehran: Pasteur Institute of Iran, 1976.
Karimi Y. Discovery of a new focus of zoonotic plague in eastern Azerbaijan, Iran. Bull Soc Pathol Exot Filiales 1980; 73:28–35.
Karimi Y, Salarkia F, Ghasemi MA. Tularemia: First human case in Iran. J Med Council Iran 1981; 8:134–141.
Kryštufek B, Vohralík V, Janžekovič F. Mammals of Turkey and Cyprus: Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae. Zgodovinsko društvo za južno Primorsko, American Society of Mammalogists, 2005.
Melikjanyan S, Vanyan A, Avetisyan A, Avetisyan A, et al. GIS analysis of tularemia outbreaks in Armenia, 1996–2013. Online J Public Health Inform 2014; 6:e45.
Morens DM, Fauci AS. Emerging infectious diseases: Threats to human health and global stability. PLoS Pathog 2013; 9:e1003467.
O'Connor FGS. Emerging and re-emerging infectious diseases. In: Zuckerman JN, ed. Principles and Practice of Travel Medicine. 2nd edition. Blackwell Publishing Ltd, 2013:146–164.
Perry RD, Fetherston JD. Yersinia pestis—Etiologic agent of plague. Clin Microbiol Rev 1997; 10:35–66.
Pourhossein B, Esmaeili S, Gyuranecz M, Mostafavi E. Tularemia and plague survey in rodents in an earthquake zone in southeastern Iran. Epidemiol Health 2015; 37:e2015050.
Prince F, McMahon M. Tularemia: Attempted transmission by each of two species of fleas: Xenopsylla cheopis (Roths.) and Diamanus montanus (Baker). Public Health Rep 1946; 61:79–85.
Saunders G, Giles J. A relationship between plagues of the house mouse, Mus musculus (Rodentia: Muridae) and prolonged periods of dry weather in South-Eastern Australia. Wildl Res 1977; 4:241–247.
Schlimmer JL. [Medical and pharmaceutical terminology alphabetical French-Persian. Indication of provenance of major animal and plant products, details on unique endemic diseases of the inhabitants of Persia]. Tehran: Lithographie d'Ali Gouli Khan, 1874.
Seyf A. The plague of 1877 and the economy of Gilan. Iran 1989:81–86.
Sjöstedt A. Tularemia: History, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci 2007; 1105:1–29.
Slack P. The black death: Past and present. Trans R Soc Trop Med Hyg 1989; 83:641–643.
Stewart A, Satterfield B, Cohen M, O'Neill K, Robison R. A quadruplex real-time PCR assay for the detection of Yersinia pestis and its plasmids. J Medi Microbiol 2008; 57:324–331.
Tarnvik A, Priebe HS, Grunow R. Tularaemia in Europe: An epidemiological overview. Scand J Infect Dis 2004; 36:350–355.
Taylor LH, Latham SM, Mark E. Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 2001; 356:983–989.
Theodorides J. [A great Franco-Mauritian epidemiologist: Joseph Désiré Tholozan (1820–1897)]. Bull Soc Pathol Exot 1998; 91:104–108.
Titball RW, Williamson ED. Vaccination against bubonic and pneumonic plague. Vaccine 2001; 19:4175–4184.
Versage JL, Severin DD, Chu MC, Petersen JM. Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J Clin Microbiol 2003; 41:5492–5499.
Xing Yuan M, Xian Guo G, Wen Ge D, Ai Qin N, et al. Ectoparasites of Chevrier's field mouse, Apodemus chevrieri, in a focus of plague in southwest China. Med Vet Entomol 2007; 21:297–300.
Zargar A, Maurin M, Mostafavi E. Tularemia, a re-emerging infectious disease in Iran and neighboring countrie. Epidemiol Health 2015; 37:e2015011.
Zhang F, Liu W, Chu MC, He J, et al. Francisella tularensis in rodents, China. Emerg Infect Dis 2006; 12:994.
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Vector-Borne and Zoonotic Diseases
Volume 17 • Issue Number 4 • April 2017
Pages: 247 - 253
PubMed: 28165869
Copyright
Copyright 2017, Mary Ann Liebert, Inc.
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Published in print: April 2017
Published online: 1 April 2017
Published ahead of print: 6 February 2017
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