Tularemia, a Re-Emerging Infectious Disease in Iran and Neighboring Countries

Epidemiology and Health Volume: 37, Article ID: e2015011, 6 pages Epidemiology and Health http://dx.doi.org/10.4178/epih/e2015011 REVIEW Open Access Tularemia, a re-emerging infectious disease in Iran and neighboring countries Afsaneh Zargar1,2, Max Maurin3,4, Ehsan Mostafavi1,2 1Department of Epidemiology, Pasteur Institute of Iran, Tehran; 2Research Centre for Emerging and Reemerging Infectious Diseases, Pasteur Institute of Iran, Akanlu, Kabudar-Ahang, Hamadan, Iran; 3Centre National de Référence des Francisella, Laboratoire de Bactériologie, Département des Agents Infectieux, Institut de Biologie et Pathologie, Centre Hospitalier Universitaire de Grenoble, Université Joseph Fourier, Grenoble; 4Laboratoire Adaptation et Pathogénie des Microorganismes, CNRS UMR 5163, Grenoble, France OBJECTIVES: Tularemia is a zoonotic disease transmitted by direct contact with infected animals and through arthropod bites, inhalation of contaminated aerosols, ingestion of contaminated meat or water, and skin contact with any infected material. It is widespread throughout the northern hemisphere, including Iran and its neigh- bors to the north, northeast, and northwest. METHODS: In this paper, the epidemiology of tularemia as a re-emerging infectious disease in the world with a focus on Iran and the neighboring countries is reviewed. RESULTS: In Iran, positive serological tests were first reported in 1973, in wildlife and domestic livestock in the northwestern and southeastern parts of the country. The first human case was reported in 1980 in the south- west of Iran, and recent studies conducted among at-risk populations in the western, southeastern, and south- western parts of Iran revealed seroprevalences of 14.4, 6.52, and 6%, respectively. CONCLUSIONS: Several factors may explain the absence of reported tularemia cases in Iran since 1980. Tula- remia may be underdiagnosed in Iran because Francisella tularensis subspecies holarctica is likely to be the major etiological agent and usually causes mild to moderately severe disease. Furthermore, tularemia is not a disease extensively studied in the medical educational system in Iran, and empirical therapy may be effective in many cases. Finally, it should be noted that laboratories capable of diagnosing tularemia have only been estab- lished in the last few years. Since both recent and older studies have consistently found tularemia antibodies in humans and animals, the surveillance of this disease should receive more attention. In particular, it would be worthwhile for clinical researchers to confirm tularemia cases more often by isolating F. tularensis from infected humans and animals. KEY WORDS: Tularemia, Francisella tularensis, Bacterial infections, Rodentia INTRODUCTION ough direct contact with infected wildlife or domestic animals, arthropod bites (mostly ticks, but also flies and mosquitoes), in- Tularemia is a zoonotic disease caused by Francisella tularen- halation of contaminated aerosols, ingestion of contaminated sis, a gram-negative, intracellular bacterium [1] transmitted thr- meat or water, and touching infected material. Direct human- to-human transmission has never been reported [2]. Tularemia Correspondence: Ehsan Mostafavi has been isolated from 200 species of mammals, birds, reptiles, Department of Epidemiology, Pasteur Institute of Iran, 69 Pasteur Ave., Tehran 1316943551, Iran and fishes [2]. Tel/Fax: +98-21-66496448, E-mail: [email protected] Laboratory workers, farmers, veterinarians, hunters, foresters, cooks, and butchers are at risk of tularemia infection [3]. F. tu- Received: Jan 15, 2015, Accepted: Feb 22, 2015, Published: Feb 22, 2015 This article is available from: http://e-epih.org/ larensis is widespread in soil and water environments, where it 2015, Korean Society of Epidemiology can survive for up to 140 days [4]. However, no agreement ex- This is an open-access article distributed under the terms of the Creative Commons ists about whether water can be considered a reservoir for this Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original bacterium [5,6]. Since F. tularensis is highly virulent and can be work is properly cited. spread via aerosols, causing severe pneumonia, it is a potential 1 Epidemiology and Health 2015;37:e2015011 biological weapon [1]. ed aerosols. Mosquito bites are considered the main route of The aim of this paper is to review the epidemiology of tulare- transmission in Russia and Scandinavia [15,16]. Mosquitoes mia as a re-emerging infectious disease, with a focus on Iran and can be infected with F. tularensis during their life as larvae in its neighboring countries. stagnant water, and then transmit the disease as adults [11]. F. tularensis subsp. novicida is not considered an etiological Clinical manifestations of tularemia agent of tularemia. However, it has been occasionally associat- The infectious dose of F. tularensis in humans is 25 bacteria ed with severe systemic disease in immunosuppressed patients for aerosol transmission and 100 bacteria for oral transmission [17]. It has been isolated from contaminated water, mainly in [7,8]. After infection, the latent phase depends on the virulence the US, and more rarely in Europe, Japan, China, and Australia and number of bacteria that entered the body, but most often [1,17,18]. lasts between three and six days [1]. The clinical manifestations F. tularensis subsp. mediasiatica has only been isolated in Ka- of tularemia depend on the route through which the bacterium zakhstan and Turkmenistan. Only a few studies have been con- entered the body and are usually ulceroglandular or typhoidal, ducted on this subsp. [19], but experiments in hares have shown although oculoglandular, oropharyngeal, and pneumonic forms that it is less virulent than subsp. holarctica (type B) [20]. have also been reported [2]. The ulceroglandular form, which represents 75 to 85% of all tularemia cases, corresponds to a The geographic distribution of tularemia worldwide regional lymphadenopathy with a painful maculopapular lesion Tularemia is widespread in the northern hemisphere, mostly that evolves to an eschar at sites of skin infection; it can also occurring in forests and mountainous regions [21]. The main occasionally develop into systemic disease with a 5 to 15% endemic foci of the disease are Russia, Kazakhstan, Turkmeni- case fatality rate. The typhoidal form, which is an acute form stan, Finland, and Sweden [22,23], and annual reports of tula- that occurs in 5 to 15% of all cases of tularemia, is a febrile sys- remia incidence are published in the eastern European coun- temic disease that can include gastrointestinal and respiratory tries. Tularemia is considered a rare disease in western Europe- symptoms. It is associated with a case fatality rate of approxi- an countries, but recent outbreaks have occurred in Spain, in- mately 35%. Early diagnosis of tularemia can help prevent fatal volving hundreds of cases. The disease is also prevalent in Japan outcomes [9]. and in the northwest and northeast of China. Tularemia cases have been systematically reported in recent decades in Sweden, Francisella tularensis subspecies the US, and Canada (Figure 1) [24-27]. An outbreak of tulare- F. tularensis currently includes four subspecies ([subsp.] tular- mia also occurred in South Korea in 1998 [28]. ensis, holarctica, mediasiatica, and novicida) with different phe- During an outbreak occurring in 1966 in Sweden, more than notypic traits, virulence, and geographical distributions [7]. Only 600 tularemia cases were reported after the inhalation of con- two subsp. (tularensis [type A] and holarctica [type B]) are taminated aerosols on a farm [29]. In 2000 and 2003, following causative agents of human tularemia. the war in Kosovo, outbreaks were seen in Kosovo in areas un- Type A strains are highly virulent in humans. They are pre- der the control of the United Nations, with 300 reported cases. dominantly found in North America, where mice, rats, hares, The areas in question were not previously known as areas where and squirrels are natural reservoirs of these bacteria [10,11]. tularemia was endemic [30]. The case fatality rate of type A infections is 5 to 15% without Between 1997 and 2008, outbreaks were reported in America, antibiotic therapy (30 to 60% in cases involving severe pneu- Spain, Yugoslavia, Russia, Kosovo, Turkey, Switzerland, Ukraine, monia or septicemia), and < 2% with antibiotic therapy. Type A France, Canada, Bulgaria, Germany, Norway, Czech, Finland, strains have been separated into genotypes (AI and AII) and Japan, and Slovakia [31]. subtypes (e.g., AIa and AIb). In the US, type AI predominates in the central and eastern parts of the country, whereas type AII The status of tularemia in countries neighboring Iran predominates in the western part [3,12]. The subtype AIb is In addition to the countries that were formerly part of the So- currently considered the most virulent. viet Union, tularemia has been reported in Asia in Turkey, Chi- Type B strains are usually associated with less severe forms of na, Japan, and Iran [32]. tularemia, with a case fatality rate < 1% in Europe and Asia. Tularemia has been reported to the west of Iran (Turkey), as However, a 7% fatality rate was recently reported for type B well as in countries bordering Iran to the north (Turkmenistan, infections in the US [13,14]. Tularemia is mostly transmitted Kazakhstan, and Azerbaijan) and to the east

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