Effect of Meteorological Factors on Hyalomma Species Composition and Their Host Preference, Seasonal Prevalence and Infection Status to Crimean-Congo Haemorrhagic Fever in Iran
-
Nayyereh Choubdar
,
Mohammad Ali Oshaghi
,
Javad Rafinejad
,
Mohammad Reza Pourmand
,
Naseh Maleki-Ravasan
,
Mostafa Salehi-Vaziri
,
Zakkyeh Telmadarraiy
,
Fateh Karimian
,
Mona Koosha
,
Abbas Rahimi-Foroushani
,
Safdar Masoomi
,
Kourosh Arzamani
,
Jalil 7 Nejati
,
Mohsen Karami
,
Ehsan Mozaffari
,
Yaser Salim-Abadi
,
Eslam Moradi-Asl
,
Behrooz Taghilou
,
Manouchehr Shirani
Abstract
Background: The impact of environmental factors and host on Hyalomma spp. community structure and abundance in the main Crimean-Congo haemorrhagic fever (CCHF) foci of Iran is largely unknown.
Methods: Biotic and abiotic factors, including host, temperature, humidity, altitude, Köppen-Geiger climate types, season, and precipitation on Hyalomma spp. community structure and abundances in 11 provinces of Iran were investigated. Additionally, the possible infection of ticks with CCHF virus was evaluated using reverse transcription PCR technique.
Results: Species analyses demonstrated the presence of Hyalomma anatolicum, H. marginatum, H. dromedarii, H. asiaticum, H. detritum and H. schulzei in the study area. Hyalomma anatolicum was the dominant species in the southern and northern parts, whereas H. dromedarii was distributed mostly in central parts of the country. The highest tick infestation was recognized in hot season. Spatial variation in tick relative density was observed between habitat types where more ticks were collected in deserts, semi-deserts, and Mediterranean habitats. Except for H. dromedarii, which was more prevalent on camel (P= 0.044), there were no significant variations in the frequencies of other Hyalomma species on different hosts. Hyalomma anatolicum, H. dromedarii frequencies had significant positive and negative association with temperature and precipitation respectively. Also humidity has positive impact on H. asiaticum frequency.
Conclusion: Data presented here will help improve ecological models to forecast the distribution of Hyalomma spp. ticks, to evaluate the risk of CCHF and other tick-borne diseases, and to design proper vector control measures to suppress Hyalomma populations in Iran.
1. de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: Ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 13: 6938–6946.
2. Gale P, Estrada‐Peña A, Martinez M, Ulrich RG, Wilson A, Capelli G, Phipps P, De La Torre A, Muñoz MJ, Dottori M, Mioulet V (2010) The feasibility of developing a risk assessment for the impact of climate change on the emergence of Crimean‐ Congo haemorrhagic fever in livestock in Europe: a Review. J Appl Microbiol. 108(6): 1859–1870.
3. Eldridge BF, Edman JD (2012) Medical entomology: a textbook on public health and veterinary problems caused by arthropods: Springer Science \and Business Media.
4. Chinikar S, Ghiasi SM, Moradi M, Goya MM, Shirzadi MR, Zeinali M, Meshkat M, Bouloy M (2010) Geographical distribution and surveillance of Crimean-Congo hemorrhagic fever in Iran. Vector Borne Zoonotic Dis. 10(7): 705–708.
5. Mostafavi E, Chinikar S, Bokaei S, Haghdoost A (2013) Temporal modeling of Crimean-Congo hemorrhagic fever in eastern Iran. Int J Infect Dis. 17(7): e524–e8.
6. Alavi-Naini R, Moghtaderi A, Koohpayeh HR, Sharifi-Mood B, Naderi M, Metanat M, Izadi M (2006) Crimean-Congo hemorrhagic fever in Southeast of Iran. J Infection. 52(5): 378–382.
7. Mardani M, Keshtkar-Jahromi M, Ataie B, Adibi P (2009) Crimean-Congo hemorrhagic fever virus as a nosocomial pathogen in Iran. Am J Trop Med Hyg. 81(4): 675–678.
8. Leblebicioglu H, Sunbul M, Guner R, Bodur H, Bulut C, Duygu F, Elaldi N, Senturk GC, Ozkurt Z, Yilmaz G, Fletcher TE (2016) Healthcare-associated Crimean-Congo haemorrhagic fever in Turkey, 2002–2014: a multicentre retrospective cross-sectional study. Clin Microbiol Infect. 22(4): 387–e1.
9. Al-Abri SS, Al Abaidani I, Fazlalipour M, Mostafavi E, Leblebicioglu H, Pshenichnaya N, Memish ZA, Hewson R, Petersen E, Mala P, Nguyen TMN (2017) Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. Int J Infect Dis. 58: 82–89.
10. Messina JP, Pigott DM, Golding N, Duda KA, Brownstein JS, Weiss DJ, Gibson H, Robinson TP, Gilbert M, William Wint GR, Nuttall PA (2015) The global distribution of Crimean-Congo hemorrhagic fever. Trans R Soc Trop Med Hyg. 109 (8): 503–513.
11. Chinikar S, Ghiasi SM, Hewson R, Mo¬ra-di M, Haeri A (2010) Crimean-Congo hemorrhagic fever in Iran and neighboring countries. J Clin Virol. 47(2): 110–114.
12. Ahmadkhani M, Alesheikh AA, Kha-kifirouz S, Salehi-Vaziri M (2018) Space-time epidemiology of Crimean-Congo hemorrhagic fever (CCHF) in Iran. Ticks Tick Borne Dis. 9(2): 207–216.
13. Haghdoost A, Chinikar S, Khakifirouz S, Mostafavi E (2013) Spatial Analysis of Crimean Congo Hemorrhagic Fever in Iran. Am J Trop Med Hyg. 89(6): 1135–1141.
14. Mostafavi E, Haghdoost AA (2014) Temporal Modeling of Crimean-Congo Hemorrhagic Fever in Iran. J Clin Microbiol Infect Dis. 2(1): 28–34.
15. Peyrefitte C, Marianneau P, Tordo N, Bouloy M (2015) Crimean-Congo haemorrhagic fever. Revue scientifique et technique (International Office of Epizootics). 34(2): 391–401.
16. Mertens M, Schmidt K, Ozkul A, Groschup MH (2013) The impact of Crimean-Congo hemorrhagic fever virus on public health. J Virol Antivir Res. 98(2): 248–260.
17. Ibrahim AM, Adam IA, Osman BT, Aradaib IE (2015) Epidemiological survey of Crimean Congo hemorrhagic fever virus in cattle in East Darfur State, Sudan. Ticks Tick Borne Dis. 6(4): 439–444.
18. Ince Y, Yasa C, Metin M, Sonmez M, Meram E, Benkli B, Ergonul O (2014) Crimean-Congo hemorrhagic fever infections reported by ProMED. Int J Infect Dis. 26: 44–46.
19. Saleem J, Usman M, Nadeem A, Sethi SA, Salman M (2009) Crimean-Congo hemorrhagic fever: a first case from Ab-bottabad, Pakistan. Int J Infect Dis. 13(3): e121–e3.
20. Keshtkar-Jahromi M, Sajadi MM, Ansari H, Mardani M, Holakouie-Naieni K (2013) Crimean-Congo hemorrhagic fever in Iran. Antiviral Res. 100(1): 20–28.
21. Hoogstraal H (1979) The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 15(4): 307–417.
22. Hosseini-Chegeni A, Hosseini R, Tavakoli M, Telmadarraiy Z, Abdigoudarzi M (2013) The Iranian Hyalomma (Acari: Ixodidae) with a key to the identification of male species. PJA. 2(3): 503–529
23. Hosseini-Chegeni A, Kayedi MH, Telmadarraiy Z, Hosseini R (2017) Multiplex-PCR differentiation of two Hyalomma and two Haemaphysalis species (Acari: Ixodidae). Persian J Acarol. 6(2): 103–112.
24. Hosseini-Chegeni A, Mostafavi E, Mohammadi A, Mahmoudi A, Kayedi MH (2018) The parasitism of Persian Jird by immature stages of Hyalomma asiaticum (Acari: Ixodidae) and its identification using molecular approaches in Iran. Persian J Acarol. 7(4): 313–392.
25. Estrada-Pea A, Aylln N, de la Fuente J (2012) Impact of Climate Trends on Tick-Borne Pathogen Transmission. Front Physiol. 3: 64.
26. McGarry JW (2011) Travel and disease vector ticks. Travel Med Infect Dis. 9(2): 49–59.
27. Raziei T (2017) Koppen-Geiger Climate Classification of Iran and Investigation of Its Changes during 20th Century.
28. Estrada-Pea A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region.
29. Burt F, Leman P, Smith J, Swanepoel R (1998) The use of a reverse transcription-polymerase chain reaction for the detection of viral nucleic acid in the diagnosis of Crimean-Congo haemorrhagic fever. J Virol Methods. 70(2): 129–137.
30. Rahbari S, Nabian S, Shayan P (2007) Primary report on distribution of tick fauna in Iran. Parasitol Res. 101(S2): 175–177.
31. Telmadarraiy Z, Vatandoost H, Chinikar S, Oshaghi MA, Moradi M, Ardakan EM, Hekmat S, Nasiri A (2010) Hard ticks on domestic ruminants and their seasonal population dynamics in Yazd Province, Iran. Iran J Arthropod Borne Dis. 4(1): 66–71
32. Ganjali M, Dabirzadeh M, Sargolzaie M (2014) Species diversity and distribution of ticks (Acari: Ixodidae) in Zabol County, eastern Iran. J Arthropod Borne Dis. 8 (2): 219–223.
33. Jafarbekloo A, Vatandoost H, Davari A, Faghihi F, Bakhshi H, Ramzgouyan MR, Nasrabadi M, Telmadarraiy Z (2014) Distribution of tick species infesting domestic ruminants in borderline of Iran-Afghanistan. J Biomed Sci Eng. 7(12): 982–987.
34. Sarani M, Telmadarraiy Z, Moghaddam AS, Azam K, Sedaghat MM (2014) Distribution of ticks (Acari: Ixodidae) infesting domestic ruminants in mountainous areas of Golestan Province, Iran. Asian Pac J Trop Biomed. 4: S246–S51.
35. Loui AM, Mahmoodi M, Fattahi R (2015) Prevalence of ixodid ticks on cattle, sheep and goats in Ilam County, Ilam Province, Iran. J Parasit Dis. 39(1): 37–40.
36. Sharifinia N, Rafinejad J, Hanafi-Bojd AA, Chinikar S, Piazak N, Baniardalan M, Biglarian A, Sharifinia F (2015) Hard ticks (Ixodidae) and Crimean-Congo hemorrhagic fever virus in south west of Iran. Acta Medica Iranica. 53(3): 177–181.
37. Ansari H, Mansournia MA, Izadi S, Zeinali M, Mahmoodi M, Holakouie-Naieni K (2015) Predicting CCHF incidence and its related factors using time-series analysis in the southeast of Iran: comparison of SARIMA and Markov switching models. Epidemiol Infect. 143(4): 839–850.
38. Estrada-Pena A, Zatansever Z, Gargili A, Aktas M, Uzun R, Ergonul O, Jongejan F (2007) Modeling the spatial distribution of Crimean-Congo hemorrhagic fever outbreaks in Turkey. Vector Borne Zoonotic Dis. 7(4): 667–678.
39. Vescio FM, Busani L, Mughini-Gras L, Khoury C, Avellis L, Taseva E, Rezza G, Christova I (2012) Environmental correlates of Crimean-Congo haemorrhagic fever incidence in Bulgaria. BMC Public Health. 12: 1116.
40. Ansari H, Shahbaz B, Izadi S, Zeinali M, Tabatabaee SM, Mahmoodi Ma (2014) Crimean-Congo hemorrhagic fever and its relationship with climate factors in southeast Iran: a 13-year experience. J Infect Dev Countr. 8(06): 749–757
41. Wilson ML, LeGuenno B, Guillaud M, Desoutter D, Gonzalez JP, Camicas JL (1990) Distribution of Crimean-Congo hemorrhagic fever viral antibody in Senegal: environmental and vectorial corre-lates. Am J Trop Med Hyg. 43(5): 557–566.
42. Davari B, Alam FN, Nasirian H, Nazari M, Abdigoudarzi M, Salehzadeh A (2017) Seasonal distribution and faunistic of ticks in the Alashtar county (Lorestan Province), Iran. Pan Afr Med J. 27: 284.
43. Izadi S, Holakouie-Naieni K, Majdzadeh SR, Chinikar S, Nadim A, Rakhshani F, Hooshmand B (2006) Seroprevalence of Crimean-Congo hemorrhagic fever in Sistan-va-Baluchestan Province of Iran. Jpn J Infect Dis. 59(5): 326–328.
44. Misonne X (1976) Notes sur la migration de printemps dans le Dasht-i-Lut et le Jaz Murian, Iran Oriental. Le Gerfaut. 66: 89–106.
45. Stone R (2018) Can Iran and Afghanistan cooperate to bring an oasis back from the dead? Available at: http://wwwsciencemagorg/news/2018/02/can-iran-and-afghanistan-cooperate-bring-oasis-back-dead.
46. De Liberato C, Frontoso R, Magliano A, Montemaggiori A, Autorino GL, Sala M, Bosworth A, Scicluna MT (2018) Monitoring for the possible introduction of Crimean-Congo haemorrhagic fever virus in Italy based on tick sampling on migratory birds and serological survey of sheep flocks. Prev Vet Med. 149: 47–52.
47. Moskvitina NS, Korobitsyn IG, Tyuten-kov OY, Gashkov SI, Kononova YV, Moskvitin SS, Romanenko VN, Mikryukova TP, Protopopova EV, Kartashov MY, Chausov EV (2014) The potential role of migratory birds in the spread of Tick-borne infections in Siberia and the Russian Far East. Achievements in the Life Sciences. 8(2): 118–120.
48. Kayedi MH, Chinikar S, Mostafavi E, Khakifirouz S, Jalali T, Hosseini-Chegeni A, Naghizadeh A, Niedrig M, Fooks AR, Shahhosseini N (2015) Crimean-Congo hemorrhagic fever virus clade iv (Asia 1) in ticks of western Iran. J Med Entomol. 52(5): 1144–1149.
49. Leblebicioglu H, Eroglu C, Erciyas-Yavuz K, Hokelek M, Acici M, Yilmaz H (2014) Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerg Infect Dis. 20(8): 1331–1334.
50. Telmadarraiy Z, Chinikar S, Vatandoost H, Faghihi F, Hosseini-Chegeni A (2015) Vectors of Crimean Congo hemorrhagic fever virus in Iran. J Arthropod Borne Dis. 9(2): 137–147.
51. Mohammadian M, Chinikar S, Telmadarraiy Z, Vatandoost H, Oshaghi MA, Hanafi-Bojd AA, Sedaghat MM, Noroozi M, Faghihi F, Jalali T, Khakifirouz S, Shahhosseini N, Farhadpour F (2016) Molecular assay on Crimean Congo hemorrhagic fever virus in ticks (Ixodidae) collected from Kermanshah Province, western Iran. J Arthropod Borne Dis. 10(3): 381–391.
2. Gale P, Estrada‐Peña A, Martinez M, Ulrich RG, Wilson A, Capelli G, Phipps P, De La Torre A, Muñoz MJ, Dottori M, Mioulet V (2010) The feasibility of developing a risk assessment for the impact of climate change on the emergence of Crimean‐ Congo haemorrhagic fever in livestock in Europe: a Review. J Appl Microbiol. 108(6): 1859–1870.
3. Eldridge BF, Edman JD (2012) Medical entomology: a textbook on public health and veterinary problems caused by arthropods: Springer Science \and Business Media.
4. Chinikar S, Ghiasi SM, Moradi M, Goya MM, Shirzadi MR, Zeinali M, Meshkat M, Bouloy M (2010) Geographical distribution and surveillance of Crimean-Congo hemorrhagic fever in Iran. Vector Borne Zoonotic Dis. 10(7): 705–708.
5. Mostafavi E, Chinikar S, Bokaei S, Haghdoost A (2013) Temporal modeling of Crimean-Congo hemorrhagic fever in eastern Iran. Int J Infect Dis. 17(7): e524–e8.
6. Alavi-Naini R, Moghtaderi A, Koohpayeh HR, Sharifi-Mood B, Naderi M, Metanat M, Izadi M (2006) Crimean-Congo hemorrhagic fever in Southeast of Iran. J Infection. 52(5): 378–382.
7. Mardani M, Keshtkar-Jahromi M, Ataie B, Adibi P (2009) Crimean-Congo hemorrhagic fever virus as a nosocomial pathogen in Iran. Am J Trop Med Hyg. 81(4): 675–678.
8. Leblebicioglu H, Sunbul M, Guner R, Bodur H, Bulut C, Duygu F, Elaldi N, Senturk GC, Ozkurt Z, Yilmaz G, Fletcher TE (2016) Healthcare-associated Crimean-Congo haemorrhagic fever in Turkey, 2002–2014: a multicentre retrospective cross-sectional study. Clin Microbiol Infect. 22(4): 387–e1.
9. Al-Abri SS, Al Abaidani I, Fazlalipour M, Mostafavi E, Leblebicioglu H, Pshenichnaya N, Memish ZA, Hewson R, Petersen E, Mala P, Nguyen TMN (2017) Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. Int J Infect Dis. 58: 82–89.
10. Messina JP, Pigott DM, Golding N, Duda KA, Brownstein JS, Weiss DJ, Gibson H, Robinson TP, Gilbert M, William Wint GR, Nuttall PA (2015) The global distribution of Crimean-Congo hemorrhagic fever. Trans R Soc Trop Med Hyg. 109 (8): 503–513.
11. Chinikar S, Ghiasi SM, Hewson R, Mo¬ra-di M, Haeri A (2010) Crimean-Congo hemorrhagic fever in Iran and neighboring countries. J Clin Virol. 47(2): 110–114.
12. Ahmadkhani M, Alesheikh AA, Kha-kifirouz S, Salehi-Vaziri M (2018) Space-time epidemiology of Crimean-Congo hemorrhagic fever (CCHF) in Iran. Ticks Tick Borne Dis. 9(2): 207–216.
13. Haghdoost A, Chinikar S, Khakifirouz S, Mostafavi E (2013) Spatial Analysis of Crimean Congo Hemorrhagic Fever in Iran. Am J Trop Med Hyg. 89(6): 1135–1141.
14. Mostafavi E, Haghdoost AA (2014) Temporal Modeling of Crimean-Congo Hemorrhagic Fever in Iran. J Clin Microbiol Infect Dis. 2(1): 28–34.
15. Peyrefitte C, Marianneau P, Tordo N, Bouloy M (2015) Crimean-Congo haemorrhagic fever. Revue scientifique et technique (International Office of Epizootics). 34(2): 391–401.
16. Mertens M, Schmidt K, Ozkul A, Groschup MH (2013) The impact of Crimean-Congo hemorrhagic fever virus on public health. J Virol Antivir Res. 98(2): 248–260.
17. Ibrahim AM, Adam IA, Osman BT, Aradaib IE (2015) Epidemiological survey of Crimean Congo hemorrhagic fever virus in cattle in East Darfur State, Sudan. Ticks Tick Borne Dis. 6(4): 439–444.
18. Ince Y, Yasa C, Metin M, Sonmez M, Meram E, Benkli B, Ergonul O (2014) Crimean-Congo hemorrhagic fever infections reported by ProMED. Int J Infect Dis. 26: 44–46.
19. Saleem J, Usman M, Nadeem A, Sethi SA, Salman M (2009) Crimean-Congo hemorrhagic fever: a first case from Ab-bottabad, Pakistan. Int J Infect Dis. 13(3): e121–e3.
20. Keshtkar-Jahromi M, Sajadi MM, Ansari H, Mardani M, Holakouie-Naieni K (2013) Crimean-Congo hemorrhagic fever in Iran. Antiviral Res. 100(1): 20–28.
21. Hoogstraal H (1979) The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 15(4): 307–417.
22. Hosseini-Chegeni A, Hosseini R, Tavakoli M, Telmadarraiy Z, Abdigoudarzi M (2013) The Iranian Hyalomma (Acari: Ixodidae) with a key to the identification of male species. PJA. 2(3): 503–529
23. Hosseini-Chegeni A, Kayedi MH, Telmadarraiy Z, Hosseini R (2017) Multiplex-PCR differentiation of two Hyalomma and two Haemaphysalis species (Acari: Ixodidae). Persian J Acarol. 6(2): 103–112.
24. Hosseini-Chegeni A, Mostafavi E, Mohammadi A, Mahmoudi A, Kayedi MH (2018) The parasitism of Persian Jird by immature stages of Hyalomma asiaticum (Acari: Ixodidae) and its identification using molecular approaches in Iran. Persian J Acarol. 7(4): 313–392.
25. Estrada-Pea A, Aylln N, de la Fuente J (2012) Impact of Climate Trends on Tick-Borne Pathogen Transmission. Front Physiol. 3: 64.
26. McGarry JW (2011) Travel and disease vector ticks. Travel Med Infect Dis. 9(2): 49–59.
27. Raziei T (2017) Koppen-Geiger Climate Classification of Iran and Investigation of Its Changes during 20th Century.
28. Estrada-Pea A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region.
29. Burt F, Leman P, Smith J, Swanepoel R (1998) The use of a reverse transcription-polymerase chain reaction for the detection of viral nucleic acid in the diagnosis of Crimean-Congo haemorrhagic fever. J Virol Methods. 70(2): 129–137.
30. Rahbari S, Nabian S, Shayan P (2007) Primary report on distribution of tick fauna in Iran. Parasitol Res. 101(S2): 175–177.
31. Telmadarraiy Z, Vatandoost H, Chinikar S, Oshaghi MA, Moradi M, Ardakan EM, Hekmat S, Nasiri A (2010) Hard ticks on domestic ruminants and their seasonal population dynamics in Yazd Province, Iran. Iran J Arthropod Borne Dis. 4(1): 66–71
32. Ganjali M, Dabirzadeh M, Sargolzaie M (2014) Species diversity and distribution of ticks (Acari: Ixodidae) in Zabol County, eastern Iran. J Arthropod Borne Dis. 8 (2): 219–223.
33. Jafarbekloo A, Vatandoost H, Davari A, Faghihi F, Bakhshi H, Ramzgouyan MR, Nasrabadi M, Telmadarraiy Z (2014) Distribution of tick species infesting domestic ruminants in borderline of Iran-Afghanistan. J Biomed Sci Eng. 7(12): 982–987.
34. Sarani M, Telmadarraiy Z, Moghaddam AS, Azam K, Sedaghat MM (2014) Distribution of ticks (Acari: Ixodidae) infesting domestic ruminants in mountainous areas of Golestan Province, Iran. Asian Pac J Trop Biomed. 4: S246–S51.
35. Loui AM, Mahmoodi M, Fattahi R (2015) Prevalence of ixodid ticks on cattle, sheep and goats in Ilam County, Ilam Province, Iran. J Parasit Dis. 39(1): 37–40.
36. Sharifinia N, Rafinejad J, Hanafi-Bojd AA, Chinikar S, Piazak N, Baniardalan M, Biglarian A, Sharifinia F (2015) Hard ticks (Ixodidae) and Crimean-Congo hemorrhagic fever virus in south west of Iran. Acta Medica Iranica. 53(3): 177–181.
37. Ansari H, Mansournia MA, Izadi S, Zeinali M, Mahmoodi M, Holakouie-Naieni K (2015) Predicting CCHF incidence and its related factors using time-series analysis in the southeast of Iran: comparison of SARIMA and Markov switching models. Epidemiol Infect. 143(4): 839–850.
38. Estrada-Pena A, Zatansever Z, Gargili A, Aktas M, Uzun R, Ergonul O, Jongejan F (2007) Modeling the spatial distribution of Crimean-Congo hemorrhagic fever outbreaks in Turkey. Vector Borne Zoonotic Dis. 7(4): 667–678.
39. Vescio FM, Busani L, Mughini-Gras L, Khoury C, Avellis L, Taseva E, Rezza G, Christova I (2012) Environmental correlates of Crimean-Congo haemorrhagic fever incidence in Bulgaria. BMC Public Health. 12: 1116.
40. Ansari H, Shahbaz B, Izadi S, Zeinali M, Tabatabaee SM, Mahmoodi Ma (2014) Crimean-Congo hemorrhagic fever and its relationship with climate factors in southeast Iran: a 13-year experience. J Infect Dev Countr. 8(06): 749–757
41. Wilson ML, LeGuenno B, Guillaud M, Desoutter D, Gonzalez JP, Camicas JL (1990) Distribution of Crimean-Congo hemorrhagic fever viral antibody in Senegal: environmental and vectorial corre-lates. Am J Trop Med Hyg. 43(5): 557–566.
42. Davari B, Alam FN, Nasirian H, Nazari M, Abdigoudarzi M, Salehzadeh A (2017) Seasonal distribution and faunistic of ticks in the Alashtar county (Lorestan Province), Iran. Pan Afr Med J. 27: 284.
43. Izadi S, Holakouie-Naieni K, Majdzadeh SR, Chinikar S, Nadim A, Rakhshani F, Hooshmand B (2006) Seroprevalence of Crimean-Congo hemorrhagic fever in Sistan-va-Baluchestan Province of Iran. Jpn J Infect Dis. 59(5): 326–328.
44. Misonne X (1976) Notes sur la migration de printemps dans le Dasht-i-Lut et le Jaz Murian, Iran Oriental. Le Gerfaut. 66: 89–106.
45. Stone R (2018) Can Iran and Afghanistan cooperate to bring an oasis back from the dead? Available at: http://wwwsciencemagorg/news/2018/02/can-iran-and-afghanistan-cooperate-bring-oasis-back-dead.
46. De Liberato C, Frontoso R, Magliano A, Montemaggiori A, Autorino GL, Sala M, Bosworth A, Scicluna MT (2018) Monitoring for the possible introduction of Crimean-Congo haemorrhagic fever virus in Italy based on tick sampling on migratory birds and serological survey of sheep flocks. Prev Vet Med. 149: 47–52.
47. Moskvitina NS, Korobitsyn IG, Tyuten-kov OY, Gashkov SI, Kononova YV, Moskvitin SS, Romanenko VN, Mikryukova TP, Protopopova EV, Kartashov MY, Chausov EV (2014) The potential role of migratory birds in the spread of Tick-borne infections in Siberia and the Russian Far East. Achievements in the Life Sciences. 8(2): 118–120.
48. Kayedi MH, Chinikar S, Mostafavi E, Khakifirouz S, Jalali T, Hosseini-Chegeni A, Naghizadeh A, Niedrig M, Fooks AR, Shahhosseini N (2015) Crimean-Congo hemorrhagic fever virus clade iv (Asia 1) in ticks of western Iran. J Med Entomol. 52(5): 1144–1149.
49. Leblebicioglu H, Eroglu C, Erciyas-Yavuz K, Hokelek M, Acici M, Yilmaz H (2014) Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerg Infect Dis. 20(8): 1331–1334.
50. Telmadarraiy Z, Chinikar S, Vatandoost H, Faghihi F, Hosseini-Chegeni A (2015) Vectors of Crimean Congo hemorrhagic fever virus in Iran. J Arthropod Borne Dis. 9(2): 137–147.
51. Mohammadian M, Chinikar S, Telmadarraiy Z, Vatandoost H, Oshaghi MA, Hanafi-Bojd AA, Sedaghat MM, Noroozi M, Faghihi F, Jalali T, Khakifirouz S, Shahhosseini N, Farhadpour F (2016) Molecular assay on Crimean Congo hemorrhagic fever virus in ticks (Ixodidae) collected from Kermanshah Province, western Iran. J Arthropod Borne Dis. 10(3): 381–391.
| Files | ||
| Issue | Vol 13 No 3 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i3.1537 | |
| Keywords | ||
| Hyalomma; Ticks; Climate; Host; Environment | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Choubdar N, Oshaghi MA, Rafinejad J, Pourmand MR, Maleki-Ravasan N, Salehi-Vaziri M, Telmadarraiy Z, Karimian F, Koosha M, Rahimi-Foroushani A, Masoomi S, Arzamani K, Nejati J, Karami M, Mozaffari E, Salim-Abadi Y, Moradi-Asl E, Taghilou B, Shirani M. Effect of Meteorological Factors on Hyalomma Species Composition and Their Host Preference, Seasonal Prevalence and Infection Status to Crimean-Congo Haemorrhagic Fever in Iran. J Arthropod Borne Dis. 2019;13(3):268-283.
