The impact of climatic variables on the population dynamics of the main malaria vector, Anopheles stephensi Liston (Diptera: Culicidae), in southern Iran

ABSTRACT

Objective: To determine the significance of temperature, rainfall and humidity in the seasonal abundance of Anopheles stephensi in southern Iran. Methods: Data on the monthly abundance of Anopheles stephensi larvae and adults were gathered from earlier studies conducted between 2002 and 2019 in malaria prone areas of southeastern Iran. Climatic data for the studied counties were obtained from climatology stations. Generalized estimating equations method was used for cluster correlation of data for each study site in different years. Results: A significant relationship was found between monthly density of adult and larvae of Anopheles stephensi and precipitation, max temperature and mean temperature, both with simple and multiple generalized estimating equations analysis (P<0.05). But when analysis was done with one month lag, only relationship between monthly density of adults and larvae of Anopheles stephensi and max temperature was significant (P<0.05). Conclusions: This study provides a basis for developing multivariate time series models, which can be used to develop improved appropriate epidemic prediction systems for these areas. Long-term entomological study in the studied sites by expert teams is recommended to compare the abundance of malaria vectors in the different areas and their association with climatic variables. Abbasi Madineh 1 Deparment of Medical Entomology & Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran; Infectious and Tropical Diseases Research Center,Tabriz University of Medical Sciences, Tabriz Rahimi Foroushani Abbas 2 Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran Jafari-Koshki Tohid 3 Molecular Medicine Research Center; Department of Statistics and Epidemiology, Faculty of Health, Tabriz University of Medical Sciences, Tabriz Pakdad Kamran 4 Department of Parasitology & Mycology, Paramedical School, Shahid Beheshti University of Medical Sciences, Tehran Vatandoost Hassan 5 Deparment of Medical Entomology & Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran Hanafi-Bojd Ahmad 6 Deparment of Medical Entomology & Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran WHO. Malaria report 2019. Geneva WHO; 2019. Vatandoost H, Raeisi A, Saghafipour A, Nikpour F, Nejati J. Malaria situation in Iran 2002-2017. Malar J 2019; 18 200. Hanafi-Bojd AA, Azari-Hamidian S, Vatandoost H, Charrahy Z. Spatio-temporal distribution of malaria vectors (Diptera Culicidae) across different climatic zones of Iran. Asian Pac J Trop Med 2011; 6 498-504. Vatandoost H, Oshaghi MA, Abaie MR, Shahi M, Yaghoobi F, Baghaii M, et al. Bionomics of Anopheles stephensi Liston in the malarious area of Hormozgan Province, southern Iran. Acta Trop 2006; 97(2) 196-203. Faulde MK, Rueda LM, Khaireh BA. First record of the Asian malaria vector Anopheles stephensi and its possible role in the resurgence of malaria in Djibouti, Horn of Africa. Acta Trop 2014; 139 39-43. Gayan Dharmasiri G, Yashan Perera A, Harishchandra J, Herath H, Aravindan K, Jayasooriya HTR, et al. First record of Anopheles stephensi in Sri Lanka A potential challenge for prevention of malaria reintroduction. Malar J 2017; 16 326. Carter TE, Yared S, Gebresilassie A, Bonnell V, Damodaran L, Lopez K, et al. First detection of Anopheles stephensi Liston, 1901 (Diptera Culicidae) in Ethiopia using molecular and morphological approaches. Acta Trop 2018; 188 180-186. Zhou G, Munga S, Minakawa N. Spatial relationship between adult malaria vector abundance and environmental factors in western Kenya highlands. Am J Trop Med Hyg 2007; 77(1) 29-35. Bashar K, Tuno N. Seasonal abundance of Anopheles mosquitoes and their association with meteorological factors and malaria incidence in Bangladesh. Parasites Vectors 2014; 7 442. Gardiner LS. Climate change and vector-borne disease. University Corporation for Atmospheric Research. 2018. [Online]. Available from https//scied.ucar.edu/longcontent/climate-change-and-vector-borne- disease [Accessed on 9 June 2019]. Patz JA, Lindsay SW. New challenges, new tools The impact of climate change on infectious diseases. Curr Opin Microbiol 1999; 2(4) 445-451. Khormi HM, Kumar L. Future malaria spatial pattern based on the potential global warming impact in South and Southeast Asia. Geospat Health 2016; 11(3). doi 10.4081/gh.2016.416. Ren Z, Wang D, Ma A, Hwang J, Bennett A, Sturrock HJW, et al. Predicting malaria vector distribution under climate change scenarios in China Challenges for malaria elimination. Sci Rep 2016; 6 20604. Campbell-lendrum D, Woodruff R. Climate change Quantifying the health impact at national and local levels. Geneva World Health Organization; 2007. Hanafi-Bojd AA. Using of remote sensing and geographical information system for estabiling a malaria monitoring system in the Bashadgard endemic focus, Hormozgan Province, Iran. Ph.D. Thesis. Tehran University of Medical Sciences; 2010. No. 4526. Mohammadkhani M, Khanjani N, Bakhtiari B, Sheikhzadeh K. The relation between climatic factors and malaria incidence in Kerman, South East of Iran. Parasite Epidemiol Control 2016; 1 205-210. Statistical Center of Iran. Country statistical yearbook. 1st ed. Iran Management & Planning Organization; 2018, p.100-120. Basseri HR, Moosakazemi SH, Yosafi S. Mohebali M, Hajaran H, Jedari M. Anthropophily of malaria vectors in Kahnouj district, south of Kerman, Iran. Iran J Public Health 2005; 34(2) 27-35. Fathian M, Vatandoost H, Moosa-Kazemi H, Raeisi A, Yaghoobi-Ershadi MR, Oshaghi MA, et al. Susceptibility of Culicidae mosquitoes to some insecticides recommended by WHO in a malaria endemic area of Southeastern Iran. J Arthropod-Borne Dis 2015; 9(1) 22-34. Mojahedi A, Basseri HR, Raeisi A, Pakari A. Bioecological characteristics of malaria vectors in different geographical areas of Bandar Abbas County, 2014. J Prev Med 2016; 3(1) 18-25. Nedjati J. The study on some bioecological characteristics of malaria vectors and monitoring of their suseptibility levels to some insecticides in Sarbaz county, Sistan va Baluchestan province. MSc. Thesis. Tehran University of Medical Sciences; 2011. No. 5046. Poudat A. Epidemiological survey of malaria in Bandar Abbas County, 1998-2002. MSc. Thesis. Tehran University of Medical Sciences; 2003. No. 3375. Yeryan M, Basseri HR, Hanafi-Bojd AA, Raeisi A, Edalat H, Safari R. Bio-ecology of malaria vectors in an endemic area, Southeast of Iran. Asian Pac J Trop Med 2016; 9(1) 32-38. Iran Meteorological Organization. Specialized products and services weather. 2019. [Online]. Available from https//data.irimo.ir/ [Accessed on 10 April 2019]. Cui J. QIC program and model selection in GEE analyses. Stata J 2007; 7(2) 209-220. Aytekin S, Aytekin AM, Alten B. Effect of different larval rearing temperatures on the productivity (R0) and morphology of the malaria vector Anopheles superpictus Grassi (Diptera Culicidae) using geometric morphometrics. J Vec Ecol 2009; 34 32-42. Lardeux FJ, Tejerina RH, Quispe V, Chavez TK. A physiological time analysis of the duration of the gonotrophic cycle of Anopheles pseudopunctipennis and its implications for malaria transmission in Bolivia. Malar J 2008; 7 141. Simon-Oke IA, Olofintoye LK. The effect of climatic factors on the distribution and abundance of mosquito vectors in Ekiti State. J Biol Agri Healthcare 2015; 5(9) 142-146. Jemal Y, Al-Thukair AA. Combining GIS application and climatic factors for mosquito control in Eastern Province, Saudi Arabia. Saudi J Biol Sci 2016; 25(8)1593-1602. Msugh-Ter MM, Aondowase DA, Terese AE. Association of meteorological factors with two principal malaria vector complexes in the University of Agriculture Makurdi community, Central Nigeria. Am J Entomol 2017; 1(2) 31-38. [31 ]Kabbale FG, Akol AM, Kaddu JB, Ambrose W. Biting patterns and seasonality of Anopheles gambiae sensu lato and Anopheles funestus mosquitoes in Kamuli District, Uganda Onapa. Parasit Vectors 2013; 6 340. Paaijmans KP, Wandago OM, Githeko AK, Takken W. Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One 2007; 2(11) e1146. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. Effects of size and temperature on metabolic rate. Science 2001; 293 2248-2251. Koenraadt CJ, Paaijmans KP, Schneider P, Githeko AK, Takken W. Low level vector survival explains unstable malaria in the western Kenya highlands. Trop Med Int Health 2006; 11(8) 1195-1205. Munga S, Minakawa N, Zhou G, Githeko AK, Yan G. Survivorship of immature stages of Anopheles gambiae s.l. (Diptera Culicidae) in natural habitats in western Kenya highlands. J Med Entomol 2007; 44 758-764. Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Effects of microclimatic changes due to deforestation on the survivorship and reproductive fitness of Anopheles gambiae in Western Kenya Highlands. Am J Trop Med Hyg 2006; 74 772-778. Afrane YA, Githeko AK, Yan G. The Ecology of Anopheles mosquitoes under climate change Case studies from the effects of environmental changes in East Africa highlands. Ann Acad Sci 2012; 1249 204-210. Abbasi F, Babaeian I, Malboosi SH, Asmari M, Mokhtari LG. Climate change assessment over Iran during future decades, using statistical downscaling of ECHO-G model. J Geogr Res 2012; 104 205-230 (In Persian).