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Original Article
Tularemia and plague survey in rodents in an earthquake zone in southeastern Iran
Behzad Pourhossein, Saber Esmaeili, Miklós Gyuranecz, Ehsan Mostafavi
Epidemiol Health. 2015;37:e2015050.   Published online November 17, 2015
DOI: https://doi.org/10.4178/epih/e2015050
  • 15,639 View
  • 125 Download
  • 9 Web of Science
  • 19 Crossref
AbstractAbstract PDF
Abstract
OBJECTIVES
Earthquakes are one the most common natural disasters that lead to increased mortality and morbidity from transmissible diseases, partially because the rodents displaced by an earthquake can lead to an increased rate of disease transmission. The aim of this study was to evaluate the prevalence of plague and tularemia in rodents in the earthquake zones in southeastern Iran.
METHODS
In April 2013, a research team was dispatched to explore the possible presence of diseases in rodents displaced by a recent earthquake magnitude 7.7 around the cities of Khash and Saravan in Sistan and Baluchestan Province. Rodents were trapped near and in the earthquake zone, in a location where an outbreak of tularemia was reported in 2007. Rodent serums were tested for a serological survey using an enzyme-linked immunosorbent assay.
RESULTS
In the 13 areas that were studied, nine rodents were caught over a total of 200 trap-days. Fortyeight fleas and 10 ticks were obtained from the rodents. The ticks were from the Hyalomma genus and the fleas were from the Xenopsylla genus. All the trapped rodents were Tatera indica. Serological results were negative for plague, but the serum agglutination test was positive for tularemia in one of the rodents. Tatera indica has never been previously documented to be involved in the transmission of tularemia.
CONCLUSIONS
No evidence of the plague cycle was found in the rodents of the area, but evidence was found of tularemia infection in rodents, as demonstrated by a positive serological test for tularemia in one rodent.
Summary

Citations

Citations to this article as recorded by  
  • The Epidemiological Investigation of Yersinia pestis, Francisella tularensis, and Arenavirus Infections in Small Mammals in Northwestern Iran
    Ehsan Mostafavi, Roya Mohammadpour, Saber Esmaeili, Ahmad Mahmoudi, Mostafa Salehi-Vaziri, Ahmad Ghasemi, Mahdi Rohani, Ali Mohammadi, Sana Eybpoosh, Neda Baseri, Christiane Denys, Max Maurin, Violaine Nicolas, Aude Lalis, Jean-Pierre Hugot
    Vector-Borne and Zoonotic Diseases.2024;[Epub]     CrossRef
  • Francisella and tularemia in western Asia, Iran: a systematic review
    Zahra Fooladfar, Farhad Moradi
    New Microbes and New Infections.2023; 52: 101092.     CrossRef
  • The source of the Black Death in fourteenth-century central Eurasia
    Maria A. Spyrou, Lyazzat Musralina, Guido A. Gnecchi Ruscone, Arthur Kocher, Pier-Giorgio Borbone, Valeri I. Khartanovich, Alexandra Buzhilova, Leyla Djansugurova, Kirsten I. Bos, Denise Kühnert, Wolfgang Haak, Philip Slavin, Johannes Krause
    Nature.2022; 606(7915): 718.     CrossRef
  • Analysis of the intellectual and social structure of health system response plan to earthquake studies adopting word co-occurrence and narrative approaches
    SeyedHossein Mousavi, Hamidreza Khankeh, Golrokh Atighechian, MohammadH Yarmohammadian, Mehrdad Memarzadeh
    Journal of Education and Health Promotion.2022; 11(1): 362.     CrossRef
  • Francisella tularensis survey among ranchers and livestock in western Iran
    Hossein Ahangari Cohan, Mahmoud Jamshidian, Mahdi Rohani, Meysam Moravedji, Ehsan Mostafavi
    Comparative Immunology, Microbiology and Infectious Diseases.2021; 74: 101598.     CrossRef
  • Vector-Borne Diseases in Iran: Epidemiology and Key Challenges
    Najmeh Parhizgari, Norair Piazak, Ehsan Mostafavi
    Future Microbiology.2021; 16(1): 51.     CrossRef
  • Rodent Ectoparasites in the Middle East: A Systematic Review and Meta-Analysis
    Md Mazharul Islam, Elmoubashar Farag, Khalid Eltom, Mohammad Mahmudul Hassan, Devendra Bansal, Francis Schaffner, Jolyon M. Medlock, Hamad Al-Romaihi, Zilungile Mkhize-Kwitshana
    Pathogens.2021; 10(2): 139.     CrossRef
  • Francisella tularensis human infections in a village of northwest Iran
    Saber Esmaeili, Mahdi Rohani, Ahmad Ghasemi, Mohammad Mehdi Gouya, Simin Khayatzadeh, Ahmad Mahmoudi, Hossein Ahangari Cohan, Anders Johansson, Max Maurin, Ehsan Mostafavi
    BMC Infectious Diseases.2021;[Epub]     CrossRef
  • Surveillance of Francisella tularensis in surface water of Kurdistan province, west of Iran
    Hossein Ahangari Cohan, Mahmoud Jamshidian, Mahdi Rohani, Meysam Moravedji, Ehsan Mostafavi
    Comparative Immunology, Microbiology and Infectious Diseases.2020; 69: 101419.     CrossRef
  • Wild Rodents and Their Ectoparasites in an Enzootic Plague Focus, Western Iran
    Ali Mohammadi, Mohammad Mehdi Sedaghat, Mohammad Reza Abai, Jamshid Darvish, Iraj Mobedi, Ahmad Mahmoudi, Ehsan Mostafavi
    Vector-Borne and Zoonotic Diseases.2020; 20(5): 334.     CrossRef
  • Cross-sectional sero-prevalence of tularemia among murine rodents of Nepal
    Narayan Acharya, Krishna Prasad Acharya, Ishwari Prasad Dhakal
    Comparative Clinical Pathology.2019; 28(2): 517.     CrossRef
  • A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance
    Shahyad Azari-Hamidian, Behzad Norouzi, Ralph E. Harbach
    Acta Tropica.2019; 194: 106.     CrossRef
  • Epidemiological survey of tularemia in Ilam Province, west of Iran
    Saber Esmaeili, Ahmad Ghasemi, Razi Naserifar, Ali Jalilian, Leila Molaeipoor, Max Maurin, Ehsan Mostafavi
    BMC Infectious Diseases.2019;[Epub]     CrossRef
  • Seroepidemiological study of Q fever, brucellosis and tularemia in butchers and slaughterhouses workers in Lorestan, western of Iran
    Saber Esmaeili, Fahimeh Bagheri Amiri, Hamid Mokhayeri, Mohammad Hassan Kayedi, Max Maurin, Mahdi Rohani, Ehsan Mostafavi
    Comparative Immunology, Microbiology and Infectious Diseases.2019; 66: 101322.     CrossRef
  • The fauna and perspective of rodentia ectoparasites in Iran relying on their roles within public health and veterinary characteristics
    Mousa khosravani
    Journal of Parasitic Diseases.2018; 42(1): 1.     CrossRef
  • Rodent-borne diseases and their public health importance in Iran
    Mohammad Hasan Rabiee, Ahmad Mahmoudi, Roohollah Siahsarvie, Boris Kryštufek, Ehsan Mostafavi, Peter J. Krause
    PLOS Neglected Tropical Diseases.2018; 12(4): e0006256.     CrossRef
  • Molecular Survey of Tularemia and Plague in Small Mammals From Iran
    Ehsan Mostafavi, Ahmad Ghasemi, Mahdi Rohani, Leila Molaeipoor, Saber Esmaeili, Zeinolabedin Mohammadi, Ahmad Mahmoudi, Mansour Aliabadian, Anders Johansson
    Frontiers in Cellular and Infection Microbiology.2018;[Epub]     CrossRef
  • A Field Study of Plague and Tularemia in Rodents, Western Iran
    Ehsan Mostafavi, Abdolrazagh Hashemi Shahraki, Alireza Japoni-Nejad, Saber Esmaeili, Jamshid Darvish, Mohammad Mehdi Sedaghat, Ali Mohammadi, Zeinolabedin Mohammadi, Ahmad Mahmoudi, Behzad Pourhossein, Ahmad Ghasemi, Miklós Gyuranecz, Elisabeth Carniel
    Vector-Borne and Zoonotic Diseases.2017; 17(4): 247.     CrossRef
  • Upsurge of Rodents’ Population in a Rural Area of Northeastern Iran Raised Concerns about Rodent-borne Diseases
    Ahmad Ghasemi, Saber Esmaeili, Abdolrazagh Hashemi Shahraki, Hamed Hanifi, Zeinolabedin Mohammadi, Ahmad Mahmoudi, Mahdi Rohani, Ehsan Mostafavi
    Journal of Medical Microbiology and Infectious Diseases .2017; 5(1): 21.     CrossRef
Review
Tularemia, a re-emerging infectious disease in Iran and neighboring countrie
Afsaneh Zargar, Max Maurin, Ehsan Mostafavi
Epidemiol Health. 2015;37:e2015011.   Published online February 22, 2015
DOI: https://doi.org/10.4178/epih/e2015011
  • 21,903 View
  • 204 Download
  • 33 Web of Science
  • 27 Crossref
AbstractAbstract PDF
Abstract
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 neighbors 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 southwest of Iran, and recent studies conducted among at-risk populations in the western, southeastern, and southwestern 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. Tularemia 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 established 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.
Summary

Citations

Citations to this article as recorded by  
  • Identification of zoonotic pathogenic bacteria from blood and ticks obtained from hares and long-eared hedgehogs (Hemiechinus megalofis) in eastern Iran
    Saeedeh Sarani, Ahmad Enferadi, Sayyed Jafar Hasani, Mohammad Younes Sarani, Mohammad Rahnama, Faroogh Sarani
    Comparative Immunology, Microbiology and Infectious Diseases.2024; 104: 102097.     CrossRef
  • Identifying key soil characteristics for Francisella tularensis classification with optimized Machine learning models
    Fareed Ahmad, Kashif Javed, Ahsen Tahir, Muhammad Usman Ghani Khan, Mateen Abbas, Masood Rabbani, Muhammad Zubair Shabbir
    Scientific Reports.2024;[Epub]     CrossRef
  • Epidemiology of tularemia in the countries of the WHO Eastern Mediterranean Region (EMRO): A systematic review and meta-analysis
    Mohammad Sholeh, Safoura Moradkasani, Saber Esmaeili, Sara I. Ruiz
    PLOS Neglected Tropical Diseases.2024; 18(5): e0012141.     CrossRef
  • The Epidemiological Investigation of Yersinia pestis, Francisella tularensis, and Arenavirus Infections in Small Mammals in Northwestern Iran
    Ehsan Mostafavi, Roya Mohammadpour, Saber Esmaeili, Ahmad Mahmoudi, Mostafa Salehi-Vaziri, Ahmad Ghasemi, Mahdi Rohani, Ali Mohammadi, Sana Eybpoosh, Neda Baseri, Christiane Denys, Max Maurin, Violaine Nicolas, Aude Lalis, Jean-Pierre Hugot
    Vector-Borne and Zoonotic Diseases.2024;[Epub]     CrossRef
  • Molecular investigation of Coxiella burnetii and Francisella tularensis infection in ticks in northern, western, and northwestern Iran
    Saber Esmaeili, Mina Latifian, Ahmad Mahmoudi, Ahmad Ghasemi, Ali Mohammadi, Alireza Mordadi, Seyyed Payman Ziapour, Saied Reza Naddaf, Ehsan Mostafavi, Maria Stefania Latrofa
    PLOS ONE.2023; 18(8): e0289567.     CrossRef
  • Small Mammals as Reservoir for Zoonotic Agents in Afghanistan
    Sandra Essbauer, Kathrin Baumann, Mathias Schlegel, Michael K Faulde, Jens Lewitzki, Sabine C Sauer, Dimitrios Frangoulidis, J M Riehm, Gerhard Dobler, Jens P Teifke, Hermann Meyer, Rainer G Ulrich
    Military Medicine.2022; 187(1-2): e189.     CrossRef
  • Bacterial and viral zoonotic infections: bugging the world
    Elham Sheykhsaran, Nima Hemmat, Hamed E. Leylabadlo, Hossein Bannazadeh Baghi
    Reviews in Medical Microbiology.2022; 33(1): e70.     CrossRef
  • The monitoring of Francisella tularensis in surface water of East Azerbaijan province, Iran
    Shadi Aghamohammad, Hossein Ahangari Cohan, Ahmad Ghasemi, Ehsan Mostafavi, Mahdi Rohani
    Comparative Immunology, Microbiology and Infectious Diseases.2022; 81: 101744.     CrossRef
  • Five Years of Surveillance for Tularemia Serovar B (Francisella tularensis holarctica) (Olsufjev) (Thiotrichales: Francisellaceae) Including Two Human Cases at an Endemic Site in San Mateo County, California
    Tara M Roth, Arielle Crews, Angie Nakano, Janet Foley
    Journal of Medical Entomology.2022; 59(5): 1787.     CrossRef
  • Tularemia: a re-emerging tick-borne infectious disease
    Derya Karataş Yeni, Fatih Büyük, Asma Ashraf, M. Salah ud Din Shah
    Folia Microbiologica.2021; 66(1): 1.     CrossRef
  • Francisella tularensis survey among ranchers and livestock in western Iran
    Hossein Ahangari Cohan, Mahmoud Jamshidian, Mahdi Rohani, Meysam Moravedji, Ehsan Mostafavi
    Comparative Immunology, Microbiology and Infectious Diseases.2021; 74: 101598.     CrossRef
  • Francisella tularensis human infections in a village of northwest Iran
    Saber Esmaeili, Mahdi Rohani, Ahmad Ghasemi, Mohammad Mehdi Gouya, Simin Khayatzadeh, Ahmad Mahmoudi, Hossein Ahangari Cohan, Anders Johansson, Max Maurin, Ehsan Mostafavi
    BMC Infectious Diseases.2021;[Epub]     CrossRef
  • Genetic Determinants of Antibiotic Resistance in Francisella
    Stephen J. Kassinger, Monique L. van Hoek
    Frontiers in Microbiology.2021;[Epub]     CrossRef
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    Parisa Soltan-Alinejad, Aboozar Soltani
    Travel Medicine and Infectious Disease.2021; 43: 102108.     CrossRef
  • Identification of Most Relevant Features for Classification of Francisella tularensis using Machine Learning
    Fareed Ahmad, Amjad Farooq, Muhammad Usman Ghani Khan, Muhammad Zubair Shabbir, Masood Rabbani, Irshad Hussain
    Current Bioinformatics.2021; 15(10): 1197.     CrossRef
  • Wild Rodents and Their Ectoparasites in an Enzootic Plague Focus, Western Iran
    Ali Mohammadi, Mohammad Mehdi Sedaghat, Mohammad Reza Abai, Jamshid Darvish, Iraj Mobedi, Ahmad Mahmoudi, Ehsan Mostafavi
    Vector-Borne and Zoonotic Diseases.2020; 20(5): 334.     CrossRef
  • Tularemia as a Mosquito-Borne Disease
    Zakaria Abdellahoum, Max Maurin, Idir Bitam
    Microorganisms.2020; 9(1): 26.     CrossRef
  • Rodent-borne and rodent-related diseases in Iran
    Vahid Kazemi-Moghaddam, Rouhullah Dehghani, Mostafa Hadei, Samaneh Dehqan, Mohammad Mehdi Sedaghat, Milad Latifi, Shamim Alavi-Moghaddam
    Comparative Clinical Pathology.2019; 28(4): 893.     CrossRef
  • A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance
    Shahyad Azari-Hamidian, Behzad Norouzi, Ralph E. Harbach
    Acta Tropica.2019; 194: 106.     CrossRef
  • Epidemiological survey of tularemia in Ilam Province, west of Iran
    Saber Esmaeili, Ahmad Ghasemi, Razi Naserifar, Ali Jalilian, Leila Molaeipoor, Max Maurin, Ehsan Mostafavi
    BMC Infectious Diseases.2019;[Epub]     CrossRef
  • Seroepidemiological study of Q fever, brucellosis and tularemia in butchers and slaughterhouses workers in Lorestan, western of Iran
    Saber Esmaeili, Fahimeh Bagheri Amiri, Hamid Mokhayeri, Mohammad Hassan Kayedi, Max Maurin, Mahdi Rohani, Ehsan Mostafavi
    Comparative Immunology, Microbiology and Infectious Diseases.2019; 66: 101322.     CrossRef
  • The fauna and perspective of rodentia ectoparasites in Iran relying on their roles within public health and veterinary characteristics
    Mousa khosravani
    Journal of Parasitic Diseases.2018; 42(1): 1.     CrossRef
  • Rodent-borne diseases and their public health importance in Iran
    Mohammad Hasan Rabiee, Ahmad Mahmoudi, Roohollah Siahsarvie, Boris Kryštufek, Ehsan Mostafavi, Peter J. Krause
    PLOS Neglected Tropical Diseases.2018; 12(4): e0006256.     CrossRef
  • Dermatological aspects of tularaemia: a study of 168 cases
    M. Polat, T. Karapınar, F. Sırmatel
    Clinical and Experimental Dermatology.2018; 43(7): 770.     CrossRef
  • Molecular Survey of Tularemia and Plague in Small Mammals From Iran
    Ehsan Mostafavi, Ahmad Ghasemi, Mahdi Rohani, Leila Molaeipoor, Saber Esmaeili, Zeinolabedin Mohammadi, Ahmad Mahmoudi, Mansour Aliabadian, Anders Johansson
    Frontiers in Cellular and Infection Microbiology.2018;[Epub]     CrossRef
  • A Field Study of Plague and Tularemia in Rodents, Western Iran
    Ehsan Mostafavi, Abdolrazagh Hashemi Shahraki, Alireza Japoni-Nejad, Saber Esmaeili, Jamshid Darvish, Mohammad Mehdi Sedaghat, Ali Mohammadi, Zeinolabedin Mohammadi, Ahmad Mahmoudi, Behzad Pourhossein, Ahmad Ghasemi, Miklós Gyuranecz, Elisabeth Carniel
    Vector-Borne and Zoonotic Diseases.2017; 17(4): 247.     CrossRef
  • Respiratory Tularemia: Francisella Tularensis and Microarray Probe Designing
    Reza Ranjbar, Payam Behzadi, Caterina Mammina
    The Open Microbiology Journal.2016; 10(1): 176.     CrossRef
Original Article
A Case of Ulceroglandular Tularemia Occurred In Korea.
Hyun Sul Lim, Hae Kwan Cheong, Woo Sup Ahn, Moon Youn Kim, Dong Hoon Kim
Korean J Epidemiol. 1998;20(1):32-38.
  • 5,566 View
  • 44 Download
AbstractAbstract PDF
Abstract
Tularemia is a zoonosis caused by Francisella tularensis. It is primarily a disease of wild animals. Human infection is incidental and usually results from interaction with biting or blood-sucking insect, wild or domestic animals or the environment. It is common in United States. An increasing number of cases have been reported from the Scandinavian countries, eastern Europe, Siberia, and Japan. But In Korea it has not been reported. A 40-year old male visited the department of Surgery on Jan 13, 1997 complaining multiple swollen lymph-nodes on his axillae and upper right arm for about ten days. On Dec 25, 1996, he found a dead wild rabbit at mountainside nearby, cooked it himself and ate it with his friends. He informed us that he got light injury on both hands while he was walking on the mountainside. On Dec 28, he started to suffer from high fever, fatigue and loss of appetite lasting for a day. After medication at a local clinic for several day, symptoms were somewhat relieved. A week later(Jan 4, 1997), several erythematous lesions developed on his both hands, which left ulcerations on the skin. Both axillary lymph nodes were swollen at both sides, but not tender. He visited the department of surgery on Jan 13 and he admitted on Jan 15. During hospitalization, the lymph nodes were surgically removed from both axillae and upper left arm. On microbiologic examination, small aerobic gram negative coccobacilli were grown on the chocolate agar plate in aerobic condition with 5% CO2 at 37 degrees centigrade. On Feb 10, fine needle aspiration from the liver abscess was done, drawing 3 ml of yellowish thick pustular material, but the microorganism was not isolated at the smear and culture of this material in the same condition as described above. After admission, he was treated with antibiotics(cefazole and marocin). His general conditions and laboratory results, including liver function, were markedly improved. He was discharged on Feb 12 and appears well on subsequent follow-ups. The microorganism and lymph nodes were sent to Centers for Disease Control and Prevention in the United States for further evaluation. A twostep indirect immunoalkaline phosphatase technique using an anti-F. tularensis antibody was performed on the lyph nodes having a positive reaction. The immunohistochemical stain demonstrated intense positivity in the stellate abscesses and fine granular reaction in some of the vessels in the paracortical region. Also F. tularensis was identified in the agar plug by culture morphology and immunofluorescence antibody test. We report a case of F. tularensis in Korea for the first time. Further studies were recommened for epidemiological characteristics and prevention of the disease.
Summary

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