A Molecular Screening of Mosquitoes (Diptera: Culicidae) for Flaviviruses in a Focus of West Nile Virus Infection in Northern Iran
-
Vahideh Moin-Vaziri
,
Remi N Charrel
,
Mehdi Badakhshan
,
Xavier de Lamballerie
,
Nourina Rahbarian
,
Mulood Mohammadi Bavani
,
Shahyad Azari-Hamidian
Abstract
Background: Mosquito-borne arboviruses such as West Nile (WN), dengue, Rift Valley fever, and Sindbis viruses are reported in Iran, but large-scale studies have not been performed on mosquitoes to find their vectors. A molecular study of the adult mosquitoes (Diptera: Culicidae) for flaviviruses was carried out in a focus of WN infection, Guilan Province, northern Iran.
Methods: Mosquito collections were carried out in five stations of two counties (Anzali and Rasht) using light traps, hand catch by manual aspirators and night landing catch during August–September 2013 and 2014. Molecular screening of WN virus and more widely for Flavivirus RNA was carried out using specific PCR technique.
Results: In total, 1015 adult mosquitoes were collected including 8 species representing four genera. The most prevalent species were Ae. vexans (33.2%), Cx. tritaeniorhynchus (22%), Cx. pipiens (20.7%), and An. maculipennis s.l. (15.6%). Molecular screening was carried out on the 1015 mosquitoes after they were organized as 38 pools according to sex, species and trapping location. None of the pools were positive.
Conclusion: Surveillance should be continued while increasing the sampling campaigns due to the presence of wetlands in the region and abundant species which are considered as vectors, feeding both on birds and humans.
1. Harbach RE (2018) Mosquito Taxonomic Inventory. Available at: http://mosquito-taxo¬nomic-inventory.info/ (Accessed 29 July 2018).
2. Hubálek Z (2008) Mosquito-borne viruses in Europe. Parasitol Res. 103: 29–43.
3. Schweitzer BK, Chapman NM, Iwen PC (2009) Overview of the Flaviviridae with an emphasis on the Japanese Een-cephalitis Group viruses. Lab Med. 40: 493–499.
4. Hubálek Z, Halouzka J (1999) West Nile fever--a reemerging mosquito-borne vi-ral dis¬ease in Europe. Emerg Infect Dis. 5: 643–650.
5. Azari-Hamidian S (2007) Checklist of Ira-nian mosquitoes (Diptera: Culicidae). J Vec¬tor Ecol. 32: 235–242.
6. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar lar¬vae of the mosquitoes of Iran (Diptera: Cu¬licidae). Zootaxa. 2078: 1–33.
7. Oshaghi MA, Yaghoobi-Ershadi MR, Shemshad Kh, Pedram M, Amani H (2008) The Anopheles superpictus complex: intro¬duction of a new malaria vector complex in Iran. Bull Soc Pathol Exot. 101: 429–434.
8. Harbach RE (2013) The Phylogeny and Clas¬sification of Anopheles. In: Manguin S (Ed) Anopheles Mosquitoes – New Insights into Malaria Vectors. InTech, Rijeka, Croatia, pp. 1–55.
9. Djadid ND, Jazayeri H, Gholizadeh S, Rad ShP, Zakeri S (2009) First record of a new member of Anopheles Hyrcanus Group from Iran: molecular identification, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Ento¬mol. 46: 1084–1093.
10. Doosti S, Yaghoobi-Ershadi MR, Schaffner F, Moosa-Kazemi SH, Ak-barzadeh K, Gooya MM, Vatandoost H, Shirzadi MR, Mostafavi E (2016) Mos-quito surveillance and the first record of the invasive mosquito species Aedes (Stegomyia) albopictus (Skuse) (Dip-tera: Culicidae) in southern Iran. Iran J Publ Health. 45: 1064–1073.
11. Yaghoobi-Ershadi MR, Doosti S, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Yaghoobi-Ershadi N (2017) Morpho-logi¬cal studies on adult mosquitoes (Diptera: Cu¬licidae) and first report of the potential Zika Virus vector Aedes (Stegomyia) unilineatus (Theobald, 1906) in Iran. Bull Soc Pathol Ex¬ot. 110: 116–121.
12. Azari-Hamidian S, Norouzi B, Noorallahi A (2017) Orthopodomyia pulcripalpis (Dip¬tera: Culicidae), a genus and spe-cies new to the Iranian mosquito fauna, with a review of bionomical infor-mation. Zootaxa. 4299: 141–145.
13. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distri-bution and ecology of mosquitoes in a focus of dirofilari¬asis in northwestern Iran, with the first find¬ing of filarial larvae in naturally infected local mos-quitoes. Med Vet Entomol. 23: 111–121.
14. Raeisi A, Nikpoor F, Ranjbar Kahkha M, Faraji L (2009) The trend of malaria in I.R. Iran from 2002 to 2007. Hakim Res J. 12: 35–41.
15. Naficy K, Saidi S (1970) Serological sur-vey on viral antibodies in Iran. Trop Geogr Med. 22: 183–188.
16. Saidi S, Tesh R, Javadian E, Nadim A (1976) The prevalence of human infection of West Nile in Iran. Iran J Pub Health. 5: 8–14.
17. Chinikar S, Shah-Hosseini N, Mostafavi E, Moradi M, Khakifirouz S, Jalili T, Goya MM, Shirzadi MR, Zainali M, Fooks AR (2013) Seroprevalevce of West Nile Virus in Iran. Vector Borne Zoonotic Dis. 13: 586–589.
18. Mardani M, Abbasi F, Aghahasani M, Ghavam B (2013) First Iranian import-ed case of Dengue. Int J Prev Med. 4: 1075–1077.
19. Aghaie A, Aaskov J, Chinikar S, Niedrig M, Banazadeh S, Khorsand Moham-madpour H (2014) Frequency of Den-gue Virus in¬fec¬tion in blood donors in Sistan and Ba¬luchestan Province in Iran. Transfus Apher Sci. 50: 59–62.
20. Fakour S, Naserabadi S, Ahmadi E (2017) The first positive serological study on Rift Valley fever in ruminants of Iran. J Vector Borne Dis. 54: 348–352.
21. World Health Organization (2004) Inte¬grated Vector Management. WHO Regional Of¬ficer for Eastern Mediterranean, Cai-ro.
22. Bagheri M, Terenius O, Oshaghi MA, Mota-zakker M, Ashari S, Dabiri F, Vatan-doost H, Mohammadi Bavani M, Chavshin AR (2015) West Nile Virus in mosquitoes of Iranian wetlands. Vector Borne Zoonotic Dis. 15: 750–754.
23. Shahhosseini N, Chinikar S, Moosa-Kazemi SH, Sedaghat MM, Kayedi MH, Lühken R, Schmidt-Chanasit J (2017) West Nile Virus lineage-2 in Culex specimens from Iran. Trop Med Inter Health. 22: 1343–1349.
24. Ahmadnejad F, Otarod V, Fallah MH, Low¬enski S, Sedighi-Moghaddam R, Zavareh A, Durand B, Lecollinet S, Sa-batier P (2011) Spread of West Nile Vi-rus in Iran: a cross-sectional serosurvey in equines, 2008–2009. Epidemiol In-fect. 139: 1587–1593.
25. Pourmahdi Borujeni M, Ghadrdan Mashadi AR, Seifi Abad Shapouri MR, Ze¬invand A (2013) A serological survey on an¬ti¬bodies against West Nile Virus in horses of Khuzestan Province. Iran J Vet Med. 7: 185–191.
26. Saidi S (1974) Viral antibodies in pre-school children from the Caspian area, Iran. Iran J Pub Health. 3: 83–91.
27. Sharifi Z, Mahmoodian Shooshtari M, Tal¬ebian A (2010) A study of West Nile Vi¬rus infection in Iranian blood donors. Arch Iran Med. 3: 1–4.
28. Chinikar S, Javadi A, Ataei B, Shakeri H, Moradi M, Mostafavi E, Ghiasi SM (2012) Detection of West Nile Virus genome and specific antibodies in Ira-nian encephalitis pa¬tients. Epidemiol Infect. 140: 1525–1529.
29. Shah-Hosseini N, Chinikar S, Ataei B, Fooks AR, Groschup MH (2014) Phylogenet¬ic analysis of West Nile Virus genome, Iran. Emerg Infect Dis. 20: 1419–1421.
30. Meshkat Z, Chinikar S, Shakeri M, Ma-navi¬far L, Moradi M, Mirshahabi H, Jalali T, Khakifirouz S, Shahhosseini N (2015) Preva¬lence of West Nile Virus in Mashhad, Iran: A population-based study. Asian Pac J Trop Med. 8: 203–205.
31. Fereidouni SR, Ziegler U, Linke S, Nie-drig M, Modirrousta H, Hoffmann B, Gro-schup MH (2011) West Nile Virus mon-itoring in migrating and resident water birds in Iran: are common coots the main reservoirs of the virus in wet-lands? Vector Borne Zoonotic Dis. 11: 1377–1381.
32. Charrel RN, Moureau G, Temmam S, Izri A, Marty P, Parola P, de Rosa AT, Tesh RB, de Lamballerie X (2009) Massilia virus, a novel Phlebovirus (Bunyaviri-dae) isolated from sandflies in the Med-iterranean. Vector Borne Zoonotic Dis. 9(5): 519–530.
33. Alkan C, Alwassouf S, Piorkowski G, Bichaud L, Tezcan S, Dincer E, Ergunay K, Ozbel Y, Alten B, de Lam-ballerie X, Charrel RN (2015) Isolation, genetic char¬acterization and seropreva-lence of Adana virus, a novel phlebo-virus belonging to the Salehabad virus complex, in Turkey. J Virol. 89(8): 4048–4091.
34. Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, de Lamballerie X (2007) A real-time RT-PCR method for the universal detection and identifica-tion of fla¬viviruses. Vector Borne Zoonotic Dis. 7: 467–478.
35. Azari-Hamidian S (2011) Larval habitat char¬acteristics of the genus Anopheles (Dip¬tera: Culicidae) and a checklist of mosquitoes in Guilan Province, north-ern Iran. Iran J Ar¬thropod Borne Dis. 5: 37–53.
36. Azari-Hamidian S, Joeafshani MA, Ras-saei A, Mosslem M (2002) Mosquitoes of the genus Aedes (Diptera: Culicidae) in Guilan. J Med Fac Guilan Univ Med Sci. 11: 29–39. (Persian).
37. Azari-Hamidian S (2007) Larval habitat characteristics of mosquitoes of the ge-nus Cu¬lex (Diptera: Culicidae) in Gui-lan Province, Iran. Iran J Arthropod Borne Dis. 1: 9–20.
38. Parreira R, Cook S, Lopes Â, de Matos AP, de Almeida APG, Piedade J, Es-teves A (2012) Genetic characterization of an in¬sect-specific flavivirus isolated from Cu¬lex theileri mosquitoes collect-ed in south¬ern Portugal. Virus Res. 167: 152–161.
39. Ergünay K, Litzba N, Brinkmann A, Günay F, Kar S, Öter K, Örsten S, Sari-kaya Y, Alten B, Nitsche A, Linton Y-M (2016) Isolation and genomic charac-terization of Cu¬lex theileri flaviviruses in field-col¬lect¬ed mosquitoes from Tur-key. Infect Genet Evol. 46: 138–147.
2. Hubálek Z (2008) Mosquito-borne viruses in Europe. Parasitol Res. 103: 29–43.
3. Schweitzer BK, Chapman NM, Iwen PC (2009) Overview of the Flaviviridae with an emphasis on the Japanese Een-cephalitis Group viruses. Lab Med. 40: 493–499.
4. Hubálek Z, Halouzka J (1999) West Nile fever--a reemerging mosquito-borne vi-ral dis¬ease in Europe. Emerg Infect Dis. 5: 643–650.
5. Azari-Hamidian S (2007) Checklist of Ira-nian mosquitoes (Diptera: Culicidae). J Vec¬tor Ecol. 32: 235–242.
6. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar lar¬vae of the mosquitoes of Iran (Diptera: Cu¬licidae). Zootaxa. 2078: 1–33.
7. Oshaghi MA, Yaghoobi-Ershadi MR, Shemshad Kh, Pedram M, Amani H (2008) The Anopheles superpictus complex: intro¬duction of a new malaria vector complex in Iran. Bull Soc Pathol Exot. 101: 429–434.
8. Harbach RE (2013) The Phylogeny and Clas¬sification of Anopheles. In: Manguin S (Ed) Anopheles Mosquitoes – New Insights into Malaria Vectors. InTech, Rijeka, Croatia, pp. 1–55.
9. Djadid ND, Jazayeri H, Gholizadeh S, Rad ShP, Zakeri S (2009) First record of a new member of Anopheles Hyrcanus Group from Iran: molecular identification, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Ento¬mol. 46: 1084–1093.
10. Doosti S, Yaghoobi-Ershadi MR, Schaffner F, Moosa-Kazemi SH, Ak-barzadeh K, Gooya MM, Vatandoost H, Shirzadi MR, Mostafavi E (2016) Mos-quito surveillance and the first record of the invasive mosquito species Aedes (Stegomyia) albopictus (Skuse) (Dip-tera: Culicidae) in southern Iran. Iran J Publ Health. 45: 1064–1073.
11. Yaghoobi-Ershadi MR, Doosti S, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Yaghoobi-Ershadi N (2017) Morpho-logi¬cal studies on adult mosquitoes (Diptera: Cu¬licidae) and first report of the potential Zika Virus vector Aedes (Stegomyia) unilineatus (Theobald, 1906) in Iran. Bull Soc Pathol Ex¬ot. 110: 116–121.
12. Azari-Hamidian S, Norouzi B, Noorallahi A (2017) Orthopodomyia pulcripalpis (Dip¬tera: Culicidae), a genus and spe-cies new to the Iranian mosquito fauna, with a review of bionomical infor-mation. Zootaxa. 4299: 141–145.
13. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distri-bution and ecology of mosquitoes in a focus of dirofilari¬asis in northwestern Iran, with the first find¬ing of filarial larvae in naturally infected local mos-quitoes. Med Vet Entomol. 23: 111–121.
14. Raeisi A, Nikpoor F, Ranjbar Kahkha M, Faraji L (2009) The trend of malaria in I.R. Iran from 2002 to 2007. Hakim Res J. 12: 35–41.
15. Naficy K, Saidi S (1970) Serological sur-vey on viral antibodies in Iran. Trop Geogr Med. 22: 183–188.
16. Saidi S, Tesh R, Javadian E, Nadim A (1976) The prevalence of human infection of West Nile in Iran. Iran J Pub Health. 5: 8–14.
17. Chinikar S, Shah-Hosseini N, Mostafavi E, Moradi M, Khakifirouz S, Jalili T, Goya MM, Shirzadi MR, Zainali M, Fooks AR (2013) Seroprevalevce of West Nile Virus in Iran. Vector Borne Zoonotic Dis. 13: 586–589.
18. Mardani M, Abbasi F, Aghahasani M, Ghavam B (2013) First Iranian import-ed case of Dengue. Int J Prev Med. 4: 1075–1077.
19. Aghaie A, Aaskov J, Chinikar S, Niedrig M, Banazadeh S, Khorsand Moham-madpour H (2014) Frequency of Den-gue Virus in¬fec¬tion in blood donors in Sistan and Ba¬luchestan Province in Iran. Transfus Apher Sci. 50: 59–62.
20. Fakour S, Naserabadi S, Ahmadi E (2017) The first positive serological study on Rift Valley fever in ruminants of Iran. J Vector Borne Dis. 54: 348–352.
21. World Health Organization (2004) Inte¬grated Vector Management. WHO Regional Of¬ficer for Eastern Mediterranean, Cai-ro.
22. Bagheri M, Terenius O, Oshaghi MA, Mota-zakker M, Ashari S, Dabiri F, Vatan-doost H, Mohammadi Bavani M, Chavshin AR (2015) West Nile Virus in mosquitoes of Iranian wetlands. Vector Borne Zoonotic Dis. 15: 750–754.
23. Shahhosseini N, Chinikar S, Moosa-Kazemi SH, Sedaghat MM, Kayedi MH, Lühken R, Schmidt-Chanasit J (2017) West Nile Virus lineage-2 in Culex specimens from Iran. Trop Med Inter Health. 22: 1343–1349.
24. Ahmadnejad F, Otarod V, Fallah MH, Low¬enski S, Sedighi-Moghaddam R, Zavareh A, Durand B, Lecollinet S, Sa-batier P (2011) Spread of West Nile Vi-rus in Iran: a cross-sectional serosurvey in equines, 2008–2009. Epidemiol In-fect. 139: 1587–1593.
25. Pourmahdi Borujeni M, Ghadrdan Mashadi AR, Seifi Abad Shapouri MR, Ze¬invand A (2013) A serological survey on an¬ti¬bodies against West Nile Virus in horses of Khuzestan Province. Iran J Vet Med. 7: 185–191.
26. Saidi S (1974) Viral antibodies in pre-school children from the Caspian area, Iran. Iran J Pub Health. 3: 83–91.
27. Sharifi Z, Mahmoodian Shooshtari M, Tal¬ebian A (2010) A study of West Nile Vi¬rus infection in Iranian blood donors. Arch Iran Med. 3: 1–4.
28. Chinikar S, Javadi A, Ataei B, Shakeri H, Moradi M, Mostafavi E, Ghiasi SM (2012) Detection of West Nile Virus genome and specific antibodies in Ira-nian encephalitis pa¬tients. Epidemiol Infect. 140: 1525–1529.
29. Shah-Hosseini N, Chinikar S, Ataei B, Fooks AR, Groschup MH (2014) Phylogenet¬ic analysis of West Nile Virus genome, Iran. Emerg Infect Dis. 20: 1419–1421.
30. Meshkat Z, Chinikar S, Shakeri M, Ma-navi¬far L, Moradi M, Mirshahabi H, Jalali T, Khakifirouz S, Shahhosseini N (2015) Preva¬lence of West Nile Virus in Mashhad, Iran: A population-based study. Asian Pac J Trop Med. 8: 203–205.
31. Fereidouni SR, Ziegler U, Linke S, Nie-drig M, Modirrousta H, Hoffmann B, Gro-schup MH (2011) West Nile Virus mon-itoring in migrating and resident water birds in Iran: are common coots the main reservoirs of the virus in wet-lands? Vector Borne Zoonotic Dis. 11: 1377–1381.
32. Charrel RN, Moureau G, Temmam S, Izri A, Marty P, Parola P, de Rosa AT, Tesh RB, de Lamballerie X (2009) Massilia virus, a novel Phlebovirus (Bunyaviri-dae) isolated from sandflies in the Med-iterranean. Vector Borne Zoonotic Dis. 9(5): 519–530.
33. Alkan C, Alwassouf S, Piorkowski G, Bichaud L, Tezcan S, Dincer E, Ergunay K, Ozbel Y, Alten B, de Lam-ballerie X, Charrel RN (2015) Isolation, genetic char¬acterization and seropreva-lence of Adana virus, a novel phlebo-virus belonging to the Salehabad virus complex, in Turkey. J Virol. 89(8): 4048–4091.
34. Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, de Lamballerie X (2007) A real-time RT-PCR method for the universal detection and identifica-tion of fla¬viviruses. Vector Borne Zoonotic Dis. 7: 467–478.
35. Azari-Hamidian S (2011) Larval habitat char¬acteristics of the genus Anopheles (Dip¬tera: Culicidae) and a checklist of mosquitoes in Guilan Province, north-ern Iran. Iran J Ar¬thropod Borne Dis. 5: 37–53.
36. Azari-Hamidian S, Joeafshani MA, Ras-saei A, Mosslem M (2002) Mosquitoes of the genus Aedes (Diptera: Culicidae) in Guilan. J Med Fac Guilan Univ Med Sci. 11: 29–39. (Persian).
37. Azari-Hamidian S (2007) Larval habitat characteristics of mosquitoes of the ge-nus Cu¬lex (Diptera: Culicidae) in Gui-lan Province, Iran. Iran J Arthropod Borne Dis. 1: 9–20.
38. Parreira R, Cook S, Lopes Â, de Matos AP, de Almeida APG, Piedade J, Es-teves A (2012) Genetic characterization of an in¬sect-specific flavivirus isolated from Cu¬lex theileri mosquitoes collect-ed in south¬ern Portugal. Virus Res. 167: 152–161.
39. Ergünay K, Litzba N, Brinkmann A, Günay F, Kar S, Öter K, Örsten S, Sari-kaya Y, Alten B, Nitsche A, Linton Y-M (2016) Isolation and genomic charac-terization of Cu¬lex theileri flaviviruses in field-col¬lect¬ed mosquitoes from Tur-key. Infect Genet Evol. 46: 138–147.
| Files | ||
| Issue | Vol 13 No 4 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i4.2235 | |
| Keywords | ||
| Aedes Anopheles Coquilletidia Culex Flaviviru | ||
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How to Cite
1.
Moin-Vaziri V, Charrel RN, Badakhshan M, Lamballerie X de, Rahbarian N, Mohammadi Bavani M, Azari-Hamidian S. A Molecular Screening of Mosquitoes (Diptera: Culicidae) for Flaviviruses in a Focus of West Nile Virus Infection in Northern Iran. J Arthropod Borne Dis. 2019;13(4):378-390.
