J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 27 http://jad.tums.ac.ir Published Online: April 27, 2019 Original Article The Potential of West Nile Virus Transmission Regarding the Environmental Factors Using Geographic Information System (GIS), West Azerbaijan Province, Iran Mojtaba Amini1; Ahmad Ali Hanafi-Bojd2; Sayyad Asghari3; *Ali Reza Chavshin1,4 1Department of Medical Entomology and Vector Control, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3Department of Geography, School of Humanities, University of Mohaghegh Ardabili, Ardabil, Iran 4Social Determinants of Health Research Center, Urmia University of Medical Sciences, Urmia, Iran (Received 2 Mar 2018; accepted 4 Dec 2018) 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 activi- ties, distribution, behavior and vectorial capacity could be affected by environmental factors. We determined the dis- tribution 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 Ge- ographical 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 transmis- sion-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 mos- quitoes (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. Keywords: Mosquitoes; Aedes caspius; Culex pipiens; Iran Introduction Due to notable problems caused by mos- quitoes and mosquito-borne diseases (MBDs), the studies of factors influencing the presence, activities, and distribution of mosquitoes and MBDs are important and form absolute parts of the epidemiology of MBDs, in which en- vironmental conditions and their changes are components of this process (1). In addition to biological factors, mosquitoes’ activities, distribution, behavior, and even their vecto- rial capacity could be affected by environmen- tal conditions (2-5). Mosquitoes’ feeding rates vary expressive- ly with temperature. Moreover, feeding behav- ior and host availability are affected by cli- mate. Additionally, length of the gonotrophic cycle as an important factor in diseases trans- mission could be influenced by precipitation patterns (6). Finally, a positive correlation be- tween temperature and West Nile and West *Corresponding author: Dr Ali Reza Chavshin, E- mail: chavshin@umsu.ac.ir, chavshin@gmail.com J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 28 http://jad.tums.ac.ir Published Online: April 27, 2019 Nile virus (WNV) incidence in mosquitoes have been reported (7, 8). Among the different tools used to identify the effects of environmental factors on MBDs and their epidemiology, is Geographical In- formation System (GIS) (9). In addition, global positioning systems (GPS), remote sensing, and spatial statistics could also play important role in MBDs research, surveillance, and con- trol programs (10). Among the MBDs, West Nile fever is an emerging zoonosis rapidly spread and caused expansive health threat in different parts of the world (11, 12). The transmission cycle of WNV includes a wide range of migratory birds as reservoirs (13), equines (14) and humans (15) as dead-end hosts, and numerous mos- quito species including different species e.g. Culex pipiens, Cx. restuans, Cx. salinarius, Cx. tarsalis, Aedes vexans, Ae. albopictus, and Coquillettidia perturbans as biological vec- tors (16-18). WNV has been isolated and iden- tified in numerous mosquito species includ- ing different species of Culex, Aedes, and Anopheles (19–21). Due to the wide use of GIS in the study of vector-borne diseases (includ- ing MBDs) (22, 23), several studies have em- ployed GIS across the world to predict, risk assessment (18), surveillance (25, 26) and the environmental factors influencing WNV trans- mission (27, 28). Because of the presence of theoretically favorable environments for the establishment of WNV across Iran, the presence of WNV has been investigated and showed the sero- prevalence rate of (1.3%) in human (29-33), 23.7% in equines (34), overall (15%) infec- tion in birds (35) and recently among the po- tential vector species, in which among them WNV has been isolated and reported from Ae. caspius (36) and Culex spp (37). Iranian West Azerbaijan Province in the northwestern part of the country, could be considered as one of the most suspicious ar- eas in Iran regarding the possibility of estab- lishment and transmission of WNV, because of its abundant water resources and wetlands for migratory birds from different parts around the world, which serve as reservoirs of WNV (38, 39) and also, the presence of potential vector species of mosquitoes in this region e.g. Culex pipiens s.l., Ae. caspius, Anopheles mac- ulipennis s.l., Culiseta longiareolata (40-42). As the first isolation of WNV from its poten- tial vectors was reported from this region (36), and this region borders several countries such as Turkey, Iraq, Armenia, and the Republic of Azerbaijan, more attention is needed at this area. Due to the special circumstances mentioned above about West Azerbaijan Province, we aimed to determine: 1) the distribution of prob- able WNV vectors, 2) the environmental fac- tors affecting WNV transmission and 3) the high-risk areas across the province regarding the potential of WNV transmission using GIS. Materials and Methods Study area West Azerbaijan Province is located in the northwest of Iran between latitudes 35° 58´– 39° 46´ N and longitudes 44° 3´–47° 23´ E. This province formally includes 17 counties. It is bordered by Turkey, Iraq, Armenia, and the Republic of Azerbaijan. In addition, it is also bordered by Iranian provinces such as East Azerbaijan, Zanjan and Kurdistan (Fig. 1). According to information obtained from Forests, Range and Watershed management organization, West Azerbaijan Province have five types of Micro-climates, including High- ly semi-arid (HSA), Moderate semi-arid (MSA), Slight semi-arid (SSA), semi-wet (SW) and wet (W). Distribution of potential West Nile Vectors in West Azerbaijan Province Mosquitoes were collected during May– Nov 2015 from 24 localities (wetlands) across the province (Table 1). Adults and larvae were J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 29 http://jad.tums.ac.ir Published Online: April 27, 2019 collected from different habitats using standard methods (43). Collected samples were quick- ly identified using a stereo microscope and a standard morphological key at the collection sites (44). Climatic and environmental data As distribution of mosquitoes and their transmitted diseases are notably dependent on environmental and climatic factors, the effec- tive climatic data, including maximum month- ly temperature, minimum monthly tempera- ture, mean monthly temperature, mean rela- tive humidity and rainfall data of decade (2004–2014) were obtained from 16 stations of West Azerbaijan Meteorological Organi- zation (Table 2). Datasets at district level were created in Excel sheets for further analysis by ArcGIS 10.3. The pattern of recent decade of Maximum, Mean and Minimum tempera- ture of different areas in West Azerbaijan Prov- ince was analyzed and mapped in Fig. 2 and summarized in Table 2. Spatial Analysis For proper analysis, the data regarding dis- tribution of mosquitoes across West Azerbai- jan Province were acquired from previous stud- ies (30, 33) and added to the findings of this survey in database created in ArcMap. Inverse distance weighted (IDW) interpolation analysis was conducted on the data of synoptic stations to find the climatic variables in the collection sites of different mosquito species. This anal- ysis interpolates a raster surface from points and estimates cell values by averaging the val- ues of nearby sample data points. The closer a point is to the center of the cell which is being estimated, the more weight it is given. The equation for IDW analysis is: where vˆ= value to be estimated vi= known value di..., dn= distances from the n data points to the point estimated n Layers of environmental factors that are important in transmitting the WNV were cat- egorized and weighted based on their effects on disease transmission, and important impact on vector-borne diseases (3, 45-47) (Table 3). The categorized and weighted environmental factors were overlaid with the vectors distri- bution across the West Azerbaijan Province for determination of high-risk areas for the establishment of the transmission cycle of WNV based on the mentioned environmental factors. As the five species (Ae. caspius, An. maculipennis, Cs. longiareolata, Cx. pipiens and Cx. theileri) reported from study area, al- so are known proven and suspected vectors of WNV in different parts of the world, they have been included in final analysis (Fig. 3). Ethics approval and consent to participate Prior to the approval of all projects by the Urmia University of Medical Sciences (UMSU), they are reviewed and endorsed by the Ethics Committee of the UMSU. Sample collection was carried out from private human and animal dwellings. At least one day prior to any sample collection, the owners were in- formed by the Local Health System officers. The whole process was coordinated, managed and documented by the “Local Health System officer” in the study areas. Results Overall, 2813 mosquito specimens from different regions of the province were collect- ed and identified (Table 1). Analysis of some climatic variables across the collection sites for different mosquito species is summarized in Table 4. The most frequent species in our study was Cx. pipiens (22 out of 24 collection J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 30 http://jad.tums.ac.ir Published Online: April 27, 2019 sites), while Ae. caspius was found only in 10 localities. The altitudinal activity of suspected vec- tors was determined across the areas with an average of 1214m for Ae. caspius to 1364m for Cs. longiareolata (Table 4). Considering the altitude of the study area which ranges from 605m to 3600m, the values of the altitude were classified into five categories, by overlying the presence of potential vectors and their distri- bution map on altitude values of the province, height less than 1615m (605–1500m), are more prepared and favored places for mosquitoes in the study areas. Finally using the scale of the most important environmental variables (Table 3), determination of high risk areas for WNV and distribution of potential vectors across the studied areas was analyzed and re- vealed in Fig. 3. The map of the mosquitoes including proven and suspected vectors of WNV, ie Cx. pipiens, Cx. theileri and Ae. caspius were collected mostly in hot spots, determined by the model (Fig. 3). Table 1. Collection sites of mosquitoes in West Azerbaijan Province, northwestern Iran, 2015 County Collection site Longitude Latitude Altitude A e . c a sp iu s A n . m a c u lip e n n is C x . p ip ie n s C x . th e ile ri C s. lo n g ia re o la ta Bazargan Bazargan 44.38944 39.38833 1400 0 25 1 13 0 Yarim-Ghiye 44.43656 39.44604 1409 175 65 0 420 0 Khoy Hashiyeh rood 45.06315 38.57117 1058 3 0 6 18 0 Mahabad Mahabad 45.71667 36.75 1351 0 10 89 25 4 Khoor-khooreh 45.72341 36.98732 1279 205 2 120 0 30 Kani barazan-wetland 45.77716 36.98689 1275 0 0 68 1 0 Hajib khosh 45.79718 36.90788 1288 0 0 136 0 0 Gapis 45.74795 36.93805 1286 0 0 4 7 0 Beytas 45.69427 36.67645 1396 3 0 28 39 0 Makoo Makoo 44.43333 39.3333 1411 6 7 82 23 3 Sangar 44.43429 39.31578 1355 288 132 100 169 90 Milan 44.4332 39.34351 1445 37 115 25 22 0 Keshmesh tappeh 44.40093 39.33351 1385 0 0 150 94 0 Glik gadim 44.66767 39.71264 807 31 0 26 0 0 Deim-Gheshlagh 45.07119 39.34766 784 0 58 0 0 0 Deimgeshlag 44.7987 39.62488 797 190 0 20 0 0 Miandoab Miandoab 46.06947 36.98592 1291 0 0 98 0 0 Naghadeh Naghadeh 45.41667 36.95 1338 0 56 0 0 7 Yadegarloo 45.52839 37.03822 1284 0 10 0 23 19 Plodasht Poldasht 45.07111 39.34778 788 0 10 55 89 0 Khol-kholeh 44.74524 39.67784 784 0 3 0 40 0 Ghooch-Ali 44.74391 39.66296 1401 0 25 1 5 0 Sardasht Sardasht 45.48333 36.15 1556 0 18 0 0 0 Urmia Urmia 45.05 37.66667 1328 0 128 151 163 246 Naz-loo 44.98442 37.65172 1358 0 0 441 67 10 Ghahraman-loo 45.17485 37.64896 1000 170 0 24 0 0 Koor-Abad 44.64239 37.72749 1545 0 68 34 0 6 Silvana 44.85142 37.42867 1577 0 120 0 0 0 Gojar 44.83373 39.48785 1736 0 7 15 19 7 Mavana 44.79643 37.56658 1617 0 13 0 32 24 Shaharchay dam 44.98628 37.4952 1433 0 11 0 10 3 Talebin 44.83398 37.54025 1608 0 0 0 149 0 J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 31 http://jad.tums.ac.ir Published Online: April 27, 2019 Table 2. Average of environmental variables in meteorological stations of West Azerbaijan Province of Iran, 1997– 2016 Localities Geographical properties Environmental variable Longitude Latitude Altitude Total Rainfall Mean Relative Humidity Mean Temp Min Temp Max Temp Bookan 46.21667 36.53333 1386.1 360.5 46 14.5 6.3 19.9 Chaldoran 44.38333 39.06667 1788 449.5 58 9.2 2.7 13.9 Ghareh Ziahadin 45.01667 38.9 1108 357.3 52 13.6 8 18 Khoy 44.96667 38.55 1103 289.2 59 12.1 5.5 18.6 Mahabad 45.71667 36.75 1351.8 403.8 53 13.0 6.9 19.15 Makoo 44.43333 39.3333 1411.3 302.8 57 10.6 5.5 15.6 Miandoab 46.05 36.96667 1300 303.8 53 14.4 5.6 20.0 Naghadeh 45.41667 36.95 1338 339.0 53 13.9 5.8 19.2 Oshnavie 45.13333 37.05 1415.9 437.3 52 13.5 4.5 18.6 Piranshahr 45.15 36.7 1443.5 672.7 52 12.0 6.2 17.9 Poldasht 45.07119 39.34778 787 198.8 51 14.7 4.8 20.2 Salmas 44.85 38.21667 1337 247.5 57 11.5 5.2 17.8 Sardasht 45.48333 36.15 1556.8 841.2 49 13.1 9.2 16.8 Shahindej 46.73333 36.6667 1395 334.8 47 14.9 6.7 20.4 Takab 47.1 36.4 1817.2 338.6 55 9.4 2.5 16.4 Urmia 45.05 37.66667 1328 338.9 61 11.6 5.4 17.7 Table 3. Categorizing the environmental factors based on their effects on disease transmission, and important impact on vector-borne diseases (3, 45–47) Environmental Factor Ratio Standard weight Category Group Effect on diseases Transmission 55 0.55 26–30 4 Very High Mean Temperature (˚Celsius) 20–26 3 High 18–20 2 Medium 14–18 1 Low 35 0.35 60< 4 Very High Relative Humidity (%) 50–60 3 High 40–50 2 Medium <40 1 Low 5 0.05 0–800 4 Very High Altitude (m) 800–1200 3 High 1200–2000 2 Medium <2000 1 Low 5 0.05 <8 3 Very High Slope (%) 8–15 2 Medium 15< 1 Low J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 32 http://jad.tums.ac.ir Published Online: April 27, 2019 Table 4. Average of some environmental and climatic variables in the collection sites of mosquitoes, West Azerbaijan Province, northwestern Iran, 2015 Species N o . o f c o lle c tio n site s P r e c ip ita tio n (m m ) A v e r a g e o f A ltitu d e (M ) A v e r a g e o f R e la tiv e H u m id ity (% ) A v e r a g e o f M a x im u m T e m p e r a tu r e ( oC ) A v e r a g e o f M in im u m T e m p e r a tu r e ( oC ) A v e r a g e o f M e a n T e m p e r a tu r e ( oC ) Ae. caspius 10 326.3 1214.7 56 17.21 5.61 11.74 An. maculipennis 20 347.3 1273.9 54.91 17.75 5.66 12.4 Cx. pipiens 22 328.6 1227.5 55.33 17.89 5.6 12.3 Cx. theileri 21 330.65 1275.1 55.78 17.65 5.6 12.1 Cs. longiareolata 12 345.1 1364.25 56.14 17.95 5.66 12.3 Fig. 1. Study area in northwestern Iran J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 33 http://jad.tums.ac.ir Published Online: April 27, 2019 Fig. 2. Environmental and meteorological variables affecting mosquito distribution in West Azerbaijan Province, northwestern Iran, (A): Altitude, (B): Slope, (C): Average of Mean Temperature, (D): Average of Minimum Temper - ature, (E): Average of Maximum Temperature, (F): Relative Humidity and (G): Total Precipitation. Fig. 3. Spatial distribution of mosquitoes and hot spots for vectors of West Nile virus in West Azerbaijan Province regarding environmental factors affecting the transmission of WNV, northwestern Iran, 2015 J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 34 http://jad.tums.ac.ir Published Online: April 27, 2019 Discussion The study area has a large number of wet- lands that host of migratory birds. Although WNV is an enzootic disease among birds (48), however, humans transmission is possible through bites of infected mosquitoes (49). WNV is responsible for disease outbreaks among human in the United States, Europe, and the Middle East (50). It has been detected in re- cent studies from birds, horse, human and mosquitoes in Iran (31–36). In the present study, environmental fac- tors affecting the transmission of WNV were studied and high-risk areas were determined (Fig. 3). Earlier study on the impact of cli- mate and environmental variables on WNV in Iran, using data from seropositive horses, found four studied factors that correlated with WNV infection in equine, these factors were tem- perature, distance to wetlands, and local and regional Normalized Difference Vegetation In- dex (NDVI) (27). Results from previous stud- ies also indicated the presence of WNV vec- tors (Cx. pipiens, Cx. theileri, Ae. caspius) in the region (36, 40) and their infection with WNV in Iran (36). In addition, the studied ar- eas have the potential for establishment of WNV transmission. The results of current study regarding the determination of the high-risk areas are interesting because they are in ac- cordance with results from previous study that isolated West Nile virus from vectors (36). The isolation of the virus in the men- tioned study has been reported from the high- risk areas identified in current study and this point shows the acceptable accuracy of the results of the current study which analyzed environmental factors (temperature, relative humidity, Altitude and Slope). These areas should be considered in planning of WNV ep- idemic control programs. Among the proba- ble reasons increasing the risk of establish- ing transmission cycle of WNV in these areas is the wide range of wetlands in the area and the presence of migratory birds as the reser- voirs of disease and also the appropriateness of environmental conditions for the presence and abundance of various species of mosqui- toes, as potential vectors of WNV. Also it seems northeastern areas of the province, which have lower altitudes and slopes with warmer temperatures and more water bodies, were found to have better condition for the activi- ty of mosquitoes. Diversity of environmental conditions in West Azerbaijan Province, which provides suit- able environment for the establishment of var- ious species of mosquitoes (Table 1) have been found in this current and related studies (36, 40, 42). Other results have shown the effect of temperature in transmission of WNV by Cx. pipiens, and the effect of temperature on the replication of the virus within the mosquito’s body and the incubation period, as well (51). WNV has the ability to replicate in mosqui- toes in wider range of temperatures between 14 °C in mosquitoes (52) to 45 °C in birds (53). By increasing the temperature, WNV propagation rate could be increased. The suitable temperature for WNV repli- cation is provided in the northeastern and south- ern parts of the provinces of Iran. Therefore, these areas need more investigation on blood feeding pattern of mosquitoes and their in- fection with WNV. Recent study on the feed- ing patterns of potential WNV vectors in South- West Spain showed that Cx. modestus, Cx. perexiguus and Cx. pipiens mainly feed on birds, while Cx. theileri and Ae. caspius main- ly feed on mammals. Cx. perexiguus had the highest potential for enzootic virus transmis- sion, followed by Cx. modestus and Cx. pipiens. According to results of the South-West Span- ish study, potential transmission risk to hu- mans was low for Cx. pipiens, Cx. theileri and Ae. caspius (54). The frequency of feeding on humans was only affected by season, while the low number of human blood meals was related to their study site. On the other hand, J Arthropod-Borne Dis, March 2019, 13(1): 27–38 M Amini et al.: The Potential of … 35 http://jad.tums.ac.ir Published Online: April 27, 2019 the researchers worked in natural areas with very low anthropic presence (54). Most of these mosquito species have been reported from our study area as well (36), therefore, they may have some roles in both avian to avian enzo- otic cycle and avian-to-mammal transmission. Certainly, the current study did not cover all important environmental factors affecting the potential of WNV transmission regarding the environmental factors and the effect of other important factors such as wetland, Nor- malized Difference Vegetation Index (NDVI) and land use should be analyzed and deter- mined in future studies. Conclusion The present study serves as a preliminary guide that shows the important effects of en- vironmental conditions on one of the important members (mosquitoes) in the transmission cy- cle of WNV and should be continued with sup- plementary studies. Taking into account the vector bio-ecologic conditions, other environ- mental factors and the interaction of the virus and the vectors as well as other important rings in the transmission of disease, the data ob- tained from this current study will be very useful and effective in knowing the exact na- ture of the disease transmission pathways and help in designing its control strategies. Acknowledgements This article is part of the results of the first author’s dissertation for fulfillment of MSc degree in Medical Entomology and Vector Control from the Department of Medical En- tomology and Vector Control, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran. This study was financially supported by Urmia University of Medical Sciences, Urmia, Iran (Project no. 1579). The authors would like to thank the health staff of the studied regions for their kind support and contributions. The authors declare that there is no con- flict of interests. References 1. 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