The Potential of West Nile Virus Transmission Regarding the Environmental Factors Using Geographic Information System (GIS), West Azerbaijan Province, Iran
Abstract
Background: West Nile fever, as an expanding zoonotic disease, has been reported from different creatures involved in the disease from Iran. In addition to biological mosquito-associated factors, various elements such as their activities, distribution, behavior and vectorial capacity could be affected by environmental factors. We determined the distribution of West Nile virus (WNV) vectors, the environmental factors affecting WNV transmission and the high-risk areas across West Azerbaijan Province (Northwestern Iran), regarding the potential of WNV transmission using Geographical Information System (GIS).
Methods: Mosquitoes’ larvae and adults were collected from different habitats of the province in 2015 and identified using standard morphological keys. The data regarding the distribution of mosquitoes across the studied area were organized in ArcMap databases. Inverse Distance Weighted (IDW) interpolation analysis was conducted on the data of synoptic stations to find climatic variables in the collection sites of different mosquito species. Layers of transmission-related environmental factors were categorized and weighed based on their effects on disease transmission.
Results: Overall, 2813 samples of different mosquito species from different regions of the province were collected and identified. According to the GIS analysis, areas in the northeastern province, which have lower altitudes and slopes with higher temperatures and more water bodies, were found to have better condition for the activity of mosquitoes (as high-risk areas: hot spots).
Conclusion: The precision of our results was proven to be in line with previous study results that identified high-risk areas, where WNV-infected vectors were captured from these same areas.
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2. Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WM, Lemnge MM, Riley EM (2005) Altitude-dependent and indepen-dent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 191: 1589–1598.
3. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Charrahy Z, Haghdoost A, Zamani G, Abedi F, Sedaghat MM, Soltani M, Shahi M, Raeisi A (2012) Spatial ana-lysis and mapping of malaria risk in an endemic area, south of Iran: a GIS based decision making for planning of control. Acta Trop. 122(1): 132–137.
4. Afrane YA, Little TJ, Lawson BW, Githeko AK, Yan G (2008) Deforestation and vectorial capacity of Anopheles gambiae Giles mosquitoes in malaria transmission, Kenya. Emerg Infect Dis. 14(10): 1533–1538.
5. Paaijmans KP, Blanford S, Chan BH, Thomas MB (2011) Warmer tempera-tures reduce the vectorial capacity of malaria mosquitoes. Biol Lett: 8(3): 465–468 .
6. Ciota AT, Matacchiero AC, Kilpatrick AM, Kramer LD (2014) The effect of temperature on life history traits of Culex mosquitoes. J Med Entomol. 51: 55–62.
7. Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, Haramis L, Goldberg TL, Kitron UD (2010) Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors. 3(1): 19.
8. Hahn MB, Monaghan AJ, Hayden MH, Eisen RJ, Delorey MJ, Lindsey N, Nasci RS, Fischer M (2015) Meteorological conditions associated with increased in-cidence of West Nile virus disease in the United States, 2004–2012. Am J Trop Med Hyg. 92(5): 1013–1022.
9. Eisen L, Eisen RJ (2011) Using geographic information systems and decision support systems for the prediction, prevention, and control of vector-borne diseases. Annu Rev Entomol. 56: 41–61.
10. Kitron U (1998) Landscape ecology and epidemiology of vector-borne diseases: tools for spatial analysis. J Med En-tomol. 35: 435–445.
11. Hayes EB, Gubler DJ (2006) West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu Rev Med. 57: 181–194.
12. Mackenzie JS, Gubler DJ, Petersen LR (2004) Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 10: S98–S109.
13. Rappole JH, Derrickson SR, Hubálek Z (2000) Migratory birds and spread of West Nile virus in the Western Hemi-sphere. Emerg Infect Dis. 6: 319.
14. Autorino GL, Battisti A, Deubel V, Ferrari G, Forletta R, Giovannini A, Lelli R, Murri S, Scicluna MT (2002) West Nile virus epidemic in horses, Tuscany re-gion, Italy. Emerg Infect Dis. 8(12): 1372–1378.
15. Lindsey NP, Staples JE, Lehman JA, Fischer M (2010) Surveillance for hu-man West Nile virus disease-United States, 1999–2008. MMWR Surveill
Summ. 59(2): 1–17.
16. Hubalek Z, Halouzka J, Juricova Z, Se-besta O (1998) First isolation of mos-quito-borne West Nile virus in the Czech Republic. Acta Virol. 42: 119–120.
17. Hubalek Z, Rudolf I, Bakonyi T, Kazdova K, Halouzka J, Sebesta O, Sikutová S, Juricová Z, Nowotny N (2010) Mos-quito (Diptera: Culicidae) surveillance for arboviruses in an area endemic for West Nile (Lineage Rabensburg) and Tahyna viruses in Central Europe. J Med Entomol. 47(3): 466–472.
18. Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile virus from hu-man clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol. 38(11): 4066–4071.
19. Romi R, Pontuale G, Ciufolini M, Fiorentini G, Marchi A, Nicoletti L, Cocchi M, Tamburro A (2004) Poten-tial vectors of West Nile virus following an equine disease outbreak in Italy. Med Vet Entomol. 18(1): 14–19.
20. Turell MJ, Sardelis MR, Dohm DJ, O'Guinn ML (2001) Potential North American vectors of West Nile virus. Ann NY Acad Sci. 951: 317–324.
21. Ergünay K, Litzba N, Brinkmann A, Günay F, Sarıkaya Y, Kar S, Örsten S, Öter K, Domingo C, Erisoz Kasap Ö, Özkul A, Mitchell L, Nitsche A, Alten B, Linton YM (2017) Co-circulation of West Nile virus and distinct insect-specific flaviviruses in Turkey. Parasit Vectors. 10(1): 149.
22. Marcantonio M, Rizzoli A, Metz M, Rosà R, Marini G, Chadwick E, Neteler M (2015) Identifying the environmental conditions favouring West Nile Virus outbreaks in Europe. PLoS One. 10(3): e0121158.
23. Valiakos G, Papaspyropoulos K, Gian-nakopoulos A, Birtsas P, Tsiodras S, Hutchings MR, Spyrou V, Pervanidou D, Athanasiou LV, Papadopoulos N, Tsoka¬na C, Baka A, Manolakou K, Chatzopoulos D, Artois M, Yon L, Hannant D, Petrovska L, Hadjichris-todoulou C, Billinis C (2014) Use of wild bird surveillance, human case data and GIS spatial analysis for predicting spatial distributions of West Nile virus in Greece. PloS One. 9(5): e96935.
24. Sánchez-Gómez A, Amela C, Fernández-Carrión E, Martínez-Avilés M, Sánchez-Vizcaíno JM, Sierra-Moros MJ (2017) Risk mapping of West Nile virus cir-culation in Spain, 2015. Acta Trop. 169: 163–169.
25. Eisen RJ, Eisen L (2014) Use of geog-raphic information systems in infectious disease surveillance. In: M'ikanatha NM, Iskander J (Eds) Concepts and Methods in Infectious Disease Surveillance, Wiley-Blackwell, pp. 219–229.
26. Moore M (2014) Geographic Analysis of West Nile Virus in the Upper Minnesota River Valley: A GIS and Multi-temporal Remote Sensing Approach. [MSc dissertation]. Minnesota State University, Mankato Mankato, Minnesota, USA.
27. Ahmadnejad F, Otarod V, Fathnia A, Ahmadabadi A, Fallah MH, Zavareh A, Miandehi N, Durand B, Sabatier P (2015) Impact of climate and environ-men¬tal factors on West Nile virus cir-culation in Iran. J Arthropod Borne Dis. 10(3): 315–327.
28. Roiz D, Ruiz S, Soriguer R, Figuerola J (2015) Landscape effects on the pres-ence, abundance and diversity of mos-quitoes in Mediterranean Wetlands. PloS One. 10(6): e0128112.
29. Naficy K, Saidi S (1970) Serological survey on viral antibodies in Iran. Trop Geogr Med. 22: 183–188.
30. Saidi S, Tesh R, Javadian E, Nadim A (1976) The prevalence of human infec-tion with West Nile virus in Iran. Iran J Public Health. 5: 8–13.
31. Talebian A (2010) A study of West Nile virus infection in Iranian blood donors. Arch Iran Med . 13(1): 1–4
32. Chinikar S, Javadi A, Ataei B, Shakeri H, Moradi M, Mostafavi E, Ghiasi SM (2012) Detection of West Nile virus ge-nome and specific antibodies in Iranian encephalitis patients. Epidemiol Infect. 140(8): 1525–1529.
33. Meshkat Z, Chinikar S, Shakeri M, Ma-navifar L, Moradi M, Mirshahabi H, Jalali T, Khakifirouz S, Shahhosseini N (2015) Prevalence of West Nile virus in Mashhad, Iran: A population–based study. Asian Pac J Trop Med. 8(3): 203–205.
34. Ahmadnejad F, Otarod V, Fallah M, Lo-wenski S, Sedighi-Moghaddam R, Za-vareh 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(10): 1587–1593.
35. Fereidouni SR, Ziegler U, Linke S, Niedrig M, Modirrousta H, Hoffmann B, Gros-chup MH (2011) West Nile virus mo-nitoring in migrating and resident wa-ter birds in Iran: are common coots the main reservoirs of the virus in wet-lands? Vector Borne Zoonotic Dis. 11 (10): 1377–1381.
36. Bagheri M, Terenius O, Oshaghi MA, Motazakker M, Asgari S, Dabiri F, Va-tandoost H, Mohammadi Bavani M, Chavshin AR (2015) West Nile virus in mosquitoes of Iranian wetlands. Ve-tor Borne Zoonotic Dis. 15(12): 750–754.
37. 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 Int Health. 22(10): 1343–1349.
38. Salmanzadeh R, Majidi A, Jabbari H, Abbasnejad H, Saket A (2011) The Study of Mahabad’ s Kanibarazan Wetland Biodiversity Indexes, Iran. Int Proc Chem Biol Environ. 24: 73–77.
39. John R (2005) " Birds of Azerbaijan" by Michael Patrikeev (book review). Can field-nat. 119: 299.
40. Khoshdel-Nezamiha F, Vatandoost H, Azari-Hamidian S, Bavani MM, Dabiri F, Entezar-Mahdi M, Chavshin AR (2014) Fauna and larval habitats of mosquitoes (Diptera: culicidae) of west Azerbaijan Province, northwestern Iran. J Arthropod Borne Dis. 8(2): 163–173.
41. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol. 23(2): 111–121.
42. Khoshdel-Nezamiha F, Vatandoost H, Oshaghi MA, Azari-Hamidian S, Mian-roodi RA, Dabiri F, Bagheri M, Ter-enius O, Chavshin AR (2016) Molecular characterization of mosquitoes (Dip-tera: Culicidae) in Northwestern Iran by using rDNA-ITS2. Jpn J Infect Dis. 69(4): 319–322.
43. Silver JB (2008) Mosquito ecology: field sampling methods: Springer.
44. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 2078: 1–33-
45. Dohm DJ, O’Guinn ML, Turell MJ (2002) Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol. 39: 221–225.
46. Dohm DJ, Turell MJ (2001) Effect of incubation at overwintering temperatures on the replication of West Nile virus in New York Culex pipiens (Diptera: Culi-cidae). J Med Entomol. 46: 462–464.
47. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD (2008) Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 4: e1000092.
48. Malkinson M, Banet C (2002) The role of birds in the ecology of West Nile virus in Europe and Africa. In: Mackenzie JS, Barrett ADT, Deubel V (Eds) Japa-nese Encephalitis and West Nile Virus-es, Springer. pp. 309–322.
49. Murgue B, Murri S, Zientara S, Durand B, Durand JP, Zeller H (2001) West Nile outbreak in horses in southern France, 2000: the return after 35 years. Emerg Infect Dis. 7: 692–696.
50. Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annu Rev Ento-mol. 53: 61–81.
51. Hess A, Cherubin C, LaMotte L (1963) Relation of temperature to activity of western and St. Louis encephalitis vi-ruses. Am J Trop Med Hyg. 12: 657–667.
52. Cornel AJ, Jupp PG, Blackburn NK (1993) Environmental temperature on the vec-tor competence of Culex univittatus (Dip-tera: Culicidae) for West Nile virus. J Med Entomol. 30: 449–456.
53. Kinney RM, Huang CY-H, Whiteman MC, Bowen RA, Langevin SA, Miller BR, Brault AC (2006) Avian virulence and thermostable replication of the North American strain of West Nile virus. J Gen Virol. 87(Pt 12): 3611–3622.
54. Muñoz J, Ruiz S, Soriguer R, Alcaide M, Viana DS, Roiz D, Vázquez A, Fi-guerola J (2012) Feeding patterns of potential West Nile virus vectors in south-west Spain. PloS One. 7: e39549.
2. Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WM, Lemnge MM, Riley EM (2005) Altitude-dependent and indepen-dent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 191: 1589–1598.
3. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Charrahy Z, Haghdoost A, Zamani G, Abedi F, Sedaghat MM, Soltani M, Shahi M, Raeisi A (2012) Spatial ana-lysis and mapping of malaria risk in an endemic area, south of Iran: a GIS based decision making for planning of control. Acta Trop. 122(1): 132–137.
4. Afrane YA, Little TJ, Lawson BW, Githeko AK, Yan G (2008) Deforestation and vectorial capacity of Anopheles gambiae Giles mosquitoes in malaria transmission, Kenya. Emerg Infect Dis. 14(10): 1533–1538.
5. Paaijmans KP, Blanford S, Chan BH, Thomas MB (2011) Warmer tempera-tures reduce the vectorial capacity of malaria mosquitoes. Biol Lett: 8(3): 465–468 .
6. Ciota AT, Matacchiero AC, Kilpatrick AM, Kramer LD (2014) The effect of temperature on life history traits of Culex mosquitoes. J Med Entomol. 51: 55–62.
7. Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, Haramis L, Goldberg TL, Kitron UD (2010) Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors. 3(1): 19.
8. Hahn MB, Monaghan AJ, Hayden MH, Eisen RJ, Delorey MJ, Lindsey N, Nasci RS, Fischer M (2015) Meteorological conditions associated with increased in-cidence of West Nile virus disease in the United States, 2004–2012. Am J Trop Med Hyg. 92(5): 1013–1022.
9. Eisen L, Eisen RJ (2011) Using geographic information systems and decision support systems for the prediction, prevention, and control of vector-borne diseases. Annu Rev Entomol. 56: 41–61.
10. Kitron U (1998) Landscape ecology and epidemiology of vector-borne diseases: tools for spatial analysis. J Med En-tomol. 35: 435–445.
11. Hayes EB, Gubler DJ (2006) West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu Rev Med. 57: 181–194.
12. Mackenzie JS, Gubler DJ, Petersen LR (2004) Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 10: S98–S109.
13. Rappole JH, Derrickson SR, Hubálek Z (2000) Migratory birds and spread of West Nile virus in the Western Hemi-sphere. Emerg Infect Dis. 6: 319.
14. Autorino GL, Battisti A, Deubel V, Ferrari G, Forletta R, Giovannini A, Lelli R, Murri S, Scicluna MT (2002) West Nile virus epidemic in horses, Tuscany re-gion, Italy. Emerg Infect Dis. 8(12): 1372–1378.
15. Lindsey NP, Staples JE, Lehman JA, Fischer M (2010) Surveillance for hu-man West Nile virus disease-United States, 1999–2008. MMWR Surveill
Summ. 59(2): 1–17.
16. Hubalek Z, Halouzka J, Juricova Z, Se-besta O (1998) First isolation of mos-quito-borne West Nile virus in the Czech Republic. Acta Virol. 42: 119–120.
17. Hubalek Z, Rudolf I, Bakonyi T, Kazdova K, Halouzka J, Sebesta O, Sikutová S, Juricová Z, Nowotny N (2010) Mos-quito (Diptera: Culicidae) surveillance for arboviruses in an area endemic for West Nile (Lineage Rabensburg) and Tahyna viruses in Central Europe. J Med Entomol. 47(3): 466–472.
18. Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile virus from hu-man clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol. 38(11): 4066–4071.
19. Romi R, Pontuale G, Ciufolini M, Fiorentini G, Marchi A, Nicoletti L, Cocchi M, Tamburro A (2004) Poten-tial vectors of West Nile virus following an equine disease outbreak in Italy. Med Vet Entomol. 18(1): 14–19.
20. Turell MJ, Sardelis MR, Dohm DJ, O'Guinn ML (2001) Potential North American vectors of West Nile virus. Ann NY Acad Sci. 951: 317–324.
21. Ergünay K, Litzba N, Brinkmann A, Günay F, Sarıkaya Y, Kar S, Örsten S, Öter K, Domingo C, Erisoz Kasap Ö, Özkul A, Mitchell L, Nitsche A, Alten B, Linton YM (2017) Co-circulation of West Nile virus and distinct insect-specific flaviviruses in Turkey. Parasit Vectors. 10(1): 149.
22. Marcantonio M, Rizzoli A, Metz M, Rosà R, Marini G, Chadwick E, Neteler M (2015) Identifying the environmental conditions favouring West Nile Virus outbreaks in Europe. PLoS One. 10(3): e0121158.
23. Valiakos G, Papaspyropoulos K, Gian-nakopoulos A, Birtsas P, Tsiodras S, Hutchings MR, Spyrou V, Pervanidou D, Athanasiou LV, Papadopoulos N, Tsoka¬na C, Baka A, Manolakou K, Chatzopoulos D, Artois M, Yon L, Hannant D, Petrovska L, Hadjichris-todoulou C, Billinis C (2014) Use of wild bird surveillance, human case data and GIS spatial analysis for predicting spatial distributions of West Nile virus in Greece. PloS One. 9(5): e96935.
24. Sánchez-Gómez A, Amela C, Fernández-Carrión E, Martínez-Avilés M, Sánchez-Vizcaíno JM, Sierra-Moros MJ (2017) Risk mapping of West Nile virus cir-culation in Spain, 2015. Acta Trop. 169: 163–169.
25. Eisen RJ, Eisen L (2014) Use of geog-raphic information systems in infectious disease surveillance. In: M'ikanatha NM, Iskander J (Eds) Concepts and Methods in Infectious Disease Surveillance, Wiley-Blackwell, pp. 219–229.
26. Moore M (2014) Geographic Analysis of West Nile Virus in the Upper Minnesota River Valley: A GIS and Multi-temporal Remote Sensing Approach. [MSc dissertation]. Minnesota State University, Mankato Mankato, Minnesota, USA.
27. Ahmadnejad F, Otarod V, Fathnia A, Ahmadabadi A, Fallah MH, Zavareh A, Miandehi N, Durand B, Sabatier P (2015) Impact of climate and environ-men¬tal factors on West Nile virus cir-culation in Iran. J Arthropod Borne Dis. 10(3): 315–327.
28. Roiz D, Ruiz S, Soriguer R, Figuerola J (2015) Landscape effects on the pres-ence, abundance and diversity of mos-quitoes in Mediterranean Wetlands. PloS One. 10(6): e0128112.
29. Naficy K, Saidi S (1970) Serological survey on viral antibodies in Iran. Trop Geogr Med. 22: 183–188.
30. Saidi S, Tesh R, Javadian E, Nadim A (1976) The prevalence of human infec-tion with West Nile virus in Iran. Iran J Public Health. 5: 8–13.
31. Talebian A (2010) A study of West Nile virus infection in Iranian blood donors. Arch Iran Med . 13(1): 1–4
32. Chinikar S, Javadi A, Ataei B, Shakeri H, Moradi M, Mostafavi E, Ghiasi SM (2012) Detection of West Nile virus ge-nome and specific antibodies in Iranian encephalitis patients. Epidemiol Infect. 140(8): 1525–1529.
33. Meshkat Z, Chinikar S, Shakeri M, Ma-navifar L, Moradi M, Mirshahabi H, Jalali T, Khakifirouz S, Shahhosseini N (2015) Prevalence of West Nile virus in Mashhad, Iran: A population–based study. Asian Pac J Trop Med. 8(3): 203–205.
34. Ahmadnejad F, Otarod V, Fallah M, Lo-wenski S, Sedighi-Moghaddam R, Za-vareh 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(10): 1587–1593.
35. Fereidouni SR, Ziegler U, Linke S, Niedrig M, Modirrousta H, Hoffmann B, Gros-chup MH (2011) West Nile virus mo-nitoring in migrating and resident wa-ter birds in Iran: are common coots the main reservoirs of the virus in wet-lands? Vector Borne Zoonotic Dis. 11 (10): 1377–1381.
36. Bagheri M, Terenius O, Oshaghi MA, Motazakker M, Asgari S, Dabiri F, Va-tandoost H, Mohammadi Bavani M, Chavshin AR (2015) West Nile virus in mosquitoes of Iranian wetlands. Ve-tor Borne Zoonotic Dis. 15(12): 750–754.
37. 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 Int Health. 22(10): 1343–1349.
38. Salmanzadeh R, Majidi A, Jabbari H, Abbasnejad H, Saket A (2011) The Study of Mahabad’ s Kanibarazan Wetland Biodiversity Indexes, Iran. Int Proc Chem Biol Environ. 24: 73–77.
39. John R (2005) " Birds of Azerbaijan" by Michael Patrikeev (book review). Can field-nat. 119: 299.
40. Khoshdel-Nezamiha F, Vatandoost H, Azari-Hamidian S, Bavani MM, Dabiri F, Entezar-Mahdi M, Chavshin AR (2014) Fauna and larval habitats of mosquitoes (Diptera: culicidae) of west Azerbaijan Province, northwestern Iran. J Arthropod Borne Dis. 8(2): 163–173.
41. Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, Harbach RE (2009) Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol. 23(2): 111–121.
42. Khoshdel-Nezamiha F, Vatandoost H, Oshaghi MA, Azari-Hamidian S, Mian-roodi RA, Dabiri F, Bagheri M, Ter-enius O, Chavshin AR (2016) Molecular characterization of mosquitoes (Dip-tera: Culicidae) in Northwestern Iran by using rDNA-ITS2. Jpn J Infect Dis. 69(4): 319–322.
43. Silver JB (2008) Mosquito ecology: field sampling methods: Springer.
44. Azari-Hamidian S, Harbach RE (2009) Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa. 2078: 1–33-
45. Dohm DJ, O’Guinn ML, Turell MJ (2002) Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol. 39: 221–225.
46. Dohm DJ, Turell MJ (2001) Effect of incubation at overwintering temperatures on the replication of West Nile virus in New York Culex pipiens (Diptera: Culi-cidae). J Med Entomol. 46: 462–464.
47. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD (2008) Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 4: e1000092.
48. Malkinson M, Banet C (2002) The role of birds in the ecology of West Nile virus in Europe and Africa. In: Mackenzie JS, Barrett ADT, Deubel V (Eds) Japa-nese Encephalitis and West Nile Virus-es, Springer. pp. 309–322.
49. Murgue B, Murri S, Zientara S, Durand B, Durand JP, Zeller H (2001) West Nile outbreak in horses in southern France, 2000: the return after 35 years. Emerg Infect Dis. 7: 692–696.
50. Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annu Rev Ento-mol. 53: 61–81.
51. Hess A, Cherubin C, LaMotte L (1963) Relation of temperature to activity of western and St. Louis encephalitis vi-ruses. Am J Trop Med Hyg. 12: 657–667.
52. Cornel AJ, Jupp PG, Blackburn NK (1993) Environmental temperature on the vec-tor competence of Culex univittatus (Dip-tera: Culicidae) for West Nile virus. J Med Entomol. 30: 449–456.
53. Kinney RM, Huang CY-H, Whiteman MC, Bowen RA, Langevin SA, Miller BR, Brault AC (2006) Avian virulence and thermostable replication of the North American strain of West Nile virus. J Gen Virol. 87(Pt 12): 3611–3622.
54. Muñoz J, Ruiz S, Soriguer R, Alcaide M, Viana DS, Roiz D, Vázquez A, Fi-guerola J (2012) Feeding patterns of potential West Nile virus vectors in south-west Spain. PloS One. 7: e39549.
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| Issue | Vol 13 No 1 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i1.930 | |
| Keywords | ||
| Mosquitoes Aedes caspius Culex pipiens Iran | ||
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How to Cite
1.
Amini M, Hanafi-Bojd AA, Asghari S, Chavshin AR. The Potential of West Nile Virus Transmission Regarding the Environmental Factors Using Geographic Information System (GIS), West Azerbaijan Province, Iran. J Arthropod Borne Dis. 2018;13(1):27.
