Original Article

Spatial Modelling of Malaria in South of Iran in Line with the Implementation of the Malaria Elimination Program: A Bayesian Poisson-Gamma Random Field Model

Abstract

Background: Malaria is the third most important infectious disease in the world. WHO propose programs for control­ling and elimination of the disease. Malaria elimination program has begun in first phase in Iran from 2010. Climate factors play an important role in transmission and occurrence of malaria infection. The main goal is to investigate the spatial distribution of incidence of malaria during April 2011 to March 2018 in Hormozgan Province and its association with climate covariates.Methods: The data included 882 confirmed cases gathered from CDC in Hormozgan University of Medical Sciences. A Poisson-Gamma Random field model with Bayesian approach was used for modeling the data and produces the smoothed standardized incidence rate (SIR).Results: The SIR for malaria ranged from 0 (Abu Musa and Haji Abad districts) to 280.57 (Bandar–e-Jask). Based on model, temperature (RR= 2.29; 95% credible interval: (1.92–2.78)) and humidity (RR= 1.04; 95% credible interval: (1.03–1.06)) had positive effect on malaria incidence, but rainfall (RR= 0.92; 95% credible interval: (0.90–0.95)) had negative impact. Also, smoothed map represent hot spots in the east of the province and in Qeshm Island.Conclusion: Based on the analysis of the study results, it was found that the ecological conditions of the region (tem­perature, humidity and rainfall) and population displacement play an important role in the incidence of malaria. There­fore, the malaria surveillance system should continue to be active in the region, focusing on high-risk areas of malaria.
1. World Health Organization (2019) World Ma¬laria Report 2019. Geneva, Switzer-land.
2. Zakeri S, Mehrizi AA, Mamaghani S, Nooriza¬deh S, Snounou G, Djadid ND (2006) Population structure analysis of Plas¬modium vivax in areas of iran with different malaria endemicity. Am J Trop Med Hyg. 74(3): 394–400.
3. Vatandoost H, Raeisi A, Saghafipour A, Nik¬pour F, Nejati J (2019) Malaria situ-ation in Iran: 2002–2017. Malar J. 18 (1): 200.
4. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Haghdoost AA, Shahi M, Sedaghat MM (2012) Entomological and epide¬miological attributes for malaria trans¬mission and implementation of vector con¬trol in southern Iran. Acta Trop. 121(2): 85–92.
5. Mesdaghinia AR, Vatandoost H, Hanafi-Bojd AA, Majdzadeh R, Raeisi A (2013) Con¬ducting International Diplo-ma Course on Malaria Program Plan¬ning and Manage¬ment (1996–2012). J Arthropod Borne Dis. 7(2): 100–112.
6. Zaim M (1993) Malaria. Ministry of Health and Medical Education, Tehran.
7. Schapira A, Zaim M, Raeisi A, Ranjbar M, Kolifarhood G, Nikpour F (2018) Histo-ry of the successful struggle against ma-laria in the Islamic Republic of Iran. Neek¬pey Press, Tehran.
8. Turki H, Soltani A (2016) Follow-Up and Monitoring of Malaria Treated Cases To-ward Malaria Elimination Program in Ba¬shagard District, Hormozgan Prov-ince, Iran, in 2016. Jundishapur J Mi-crobiol. 12 (2): 1–6.
9. Rashid G, Soltani A, Eftekhar E, Shafiei R, Turki H (2020) Immigrants: Big Chal-lenge and Silent Threat to Implement Ma¬laria Elimination Program in Hor-mozgan Province, Iran. Jundishapur J Microbiol. 13(1): 1-6.
10. Ebrahimzadeh A, Nouri Dalir S, Mirahmadi H, Mehravaran A, Salimi Khorashad A, Turki H (2017) The Inci-dence of Current Infection with Differ-ent Human Malaria Species by Poly-merase Chain Reaction for Diagnosis of Suspicious Malaria Pa¬tients on Elimina-tion Region Sistan and Baluchistan Province, Southeast of Iran. Jundishapur J Microbiol. 10(10): 1–7.
11. Nkurunziza H, Gebhardt A, Pilz J (2010) Bayes¬ian modelling of the effect of cli-mate on malaria in Burundi. Malar J. 9(1): 114.
12. Loha E, Lindtjorn B (2010) Model vari-ations in predicting incidence of Plas¬modium fal¬ciparum malaria using 1998–2007 morbid¬ity and meteorological data from south Ethiopia. Malar J. 9(1): 166.
13. Sriwattanapongse W, Kuning M (2009) Mod¬eling Malaria Incidence in North-West¬ern Thailand. Chiang Mai J Sci. 36(3): 403–410.
14. Gaudart J, Toure O, Dessay N, Dicko Al, Ranque S, Forest L (2009) Modeling ma¬laria incidence with environmental depend¬ency in a locality of Sudanese savannah area, Mali. Malar J. 8(1): 61.
15. Haghdoost AA, Alexander N, Cox J (2008) Modeling of malaria temporal variations in Iran. Trop Med Inter Health. 13(12): 1501–1508.
16. Briët OJT, Vounatsou P, Gunawardena DM, Galappaththy GNL, Amerasinghe PH (2008) Models for short term malar¬ia pre¬diction in Sri Lanka. Malar J. 7(1): 76.
17. Pascual M, Cazelles B, Bouma MJ, Chaves LF, Koelle K (2008) Shifting patterns: ma¬laria dynamics and rainfall variability in an African highland. Pro-ceedings of the Roy¬al Society B: Bio-logical Sciences. 275(1631): 123–132.
18. Teklehaimanot H, Schwartz J, Tekleha¬ima-not A, Lipsitch M (2004) Weather-based prediction of Plasmodium falcipa¬rum ma¬laria in epidemic-prone regions of Ethio¬pia II. Weather-based prediction systems perform comparably to early detection sys¬tems in identifying times for interventions. Malar J. 3(1): 44.
19. Hoshen M, Morse A (2004) A weather-driv¬en model of malaria transmission. Malar J. 3(1): 32.
20. Besag J, York J, Mollié A (1991) Bayesian image restoration, with two applications in spatial statistics. Ann Inst Stat. 43(1): 1–20.
21. Clayton D, Bernardinelli L (1992) Bayesian methods for mapping disease risk. Geo¬graphical and Environmental Epidemi¬ol¬ogy. In: Elliot P, Cuzick J, English D, Stern R: Methods for Small-area Studies, Oxford University Press, Oxford, UK, pp. 220–240.
22. Wolpert RL, Ickstadt K (1998) Pois¬son/ gamma random field models for spatial statistics. Biometrika. 85(2): 251–267.
23. Clayton D, Kaldor J (1978) Empirical Bayes estimates of age-standardized rel-ative risks for use in disease mapping. Biometrics. 43(3): 671–681.
24. Best N, Richardson S, Thomson A (2005) A comparison of Bayesian spa¬tial models for disease mapping. Stat Methods Med Res. 14(1): 35–59.
25. Manouchehri A, Zaim M, Emadi A (1990) A review of malaria in Iran. J Am Mosq Control Assoc. 8(4): 381–385.
26. Taddese AA, Baraki AG, Gelaye KA (2019) Spatial modeling, prediction and season¬al variation of malaria in north-west Ethi¬opia. BMC Res Notes. 12(1): 273.
27. Saita S, Silawan T, Parker DM, Sriwichai P, Phuanukoonnon S, Suda¬thip P (2019) Spatial Heterogeneity and Temporal Trends in Malaria on the Thai–My¬an¬mar Border (2012–2017): A Retrospective Ob¬servational Study. Trop Med Infect Dis. 4(2): 62–77.
28. Bui Q-T, Nguyen Q-H, Pham VM, Pham MH, Tran AT (2019) Understand¬ing spa¬tial variations of malaria in Vi¬etnam us¬ing remotely sensed data inte¬grated into GIS and machine learning classifiers. Ge¬ocarto Int. 34(12): 1300–1314.
29. Gwitira I, Murwira A, Masocha M, Zengeya FM, Shekede MD, Chirenda J (2018) GIS-based stratification of ma-laria risk zones for Zimbabwe. Geocarto Int. 34(11): 1163–1176.
30. Sasane SA, Jadhav A, Barik RK, Krish¬na-kumar G, Raghavswamy V (2019) Appli¬cation of spatial technology in ma-laria in¬formation infrastructure mapping with cli¬mate change perspective in Ma-harashtra, India. MAUSAM. 70(4): 787–806.
31. Nur R, Nuryati, Marko Ferdian S, Syairaji M, Ismil Khairi L (2019) The implemen-tation of spatial weighted re¬gression on de¬tecting the risk factors of malaria incidenc¬es in Kulonprogo Dis¬trict. KnE Social Sci¬ences. 3(23): 148.
32. Hast M, Searle KM, Chaponda M, Lu¬piya J, Lubinda J, Sikalima J (2019) The use of GPS data loggers to describe the im-pact of spatio-temporal movement patterns on malaria control in a high-trans¬mission area of northern Zambia. Int J Health Ge¬ogr. 18(1): 19–25.
33. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Charrahy Z, Haghdoost AA, Zamani G (2012) Spatial analysis and mapping of malaria risk in an en¬demic area, south of Iran: A GIS based decision making for planning of control. Acta Tropica. 122 (1): 132–137.
34. Ostovar A, Haghdoost AA, Rahimi-foroushani A, Raeisi A, Majdzadeh R (2016) Time Series Analysis of Meteor-ological Factors Influencing Malaria in South Eastern Iran. J Arthropod Borne Dis. 10(2): 222–237
35. Mohammadkhani M, Khanjani N, Bakhtiari B, Sheikhzadeh K (2016) The relation be¬tween climatic factors and malaria inci¬dence in Kerman, South East of Iran. Par¬asite Epidemiol Control. 1(3): 205–210.
36. Ikeda T, Behera SK, Morioka Y, Mina-kawa N, Hashizume M, Tsuzuki A (2017) Sea¬sonally lagged effects of cli-matic factors on malaria incidence in South Africa. Sci Rep. 7(1): 2458.
37. Kang SY, Battle KE, Gibson HS, Ratsim-basoa A, Randrianarivelojosia M, Ram-boarina S (2018) Spatio-temporal map-ping of Madagascar’s Malaria Indi¬cator Survey results to assess Plasmodi¬um fal-ciparum endemicity trends be¬tween 2011 and 2016. BMC Med. 16(1): 71.
38. Laneri K, Cabella B, Prado PI, Mendes Coutinho R, Kraenkel RA (2019) Cli-mate drivers of malaria at its southern fringe in the Americas. PLoS One. 14(7): e0219249.
39. Ssempiira J, Nambuusi B, Kissa J, Agaba B, Makumbi F, Kasasa S (2017) Geosta-tistical modelling of malaria indi¬cator sur¬vey data to assess the effects of interven¬tions on the geographical distri-bution of malaria prevalence in children less than 5 years in Uganda. PLoS One. 12(4): e0174948.
40. Herekar F, Iftikhar S, Nazish A, Rehman S (2020) Malaria and the cli¬mate in Ka-rachi: An eight year review. Pakistan J Med Sci. 36(1): S33–S7.
41. Liu J, Wu X, Li C, Zhou S (2018) De¬cline in malaria incidence in a typical county of China: Role of climate vari¬ance and anti-malaria intervention measures. Environ Res. 167: 276–282.
42. M'Bra RK, Kone B, Soro DP, N'Krumah RTAS, Soro N, Ndione JA (2018) Im-pact of climate variability on the trans-mis¬sion risk of malaria in northern Côte d'Ivoire. PloS One. 13(6): e0182304
43. Santos-Vega M, Lowe R, Anselin L, De-sai V, Vaishnav KG, Naik A, Pascual M (2019) Local climate and social ine¬qual-ity drive spatio-temporal variation in ma-laria risk across a complex urban land-scape. Available at: https://www.biorxiv.org/content/10.1101/583880v1.
44. Simple O, Mindra A, Obai G, Ovuga E, Odongo-Aginya EI (2018) Influence of climatic factors on malaria epidemic in Gulu District, northern Uganda: A 10-Year Retrospective Study. Mal Res Ttreat. 2018: 1–8.
45. Adigun AB, Gajere EN, Oresanya O, Vounatsou P (2015) Malaria risk in Ni-ge¬ria: Bayesian geostatistical modelling of 2010 malaria indicator survey data. Ma¬lar J. 14: 156.
46. Millar J, Psychas P, Abuaku B, Ahorlu C, Amratia P, Koram K, (2018) Detect¬ing local risk factors for residual malaria in northern Ghana using Bayesian mod¬el av¬eraging. Malar J. 17(1): 343.
47. Matthew OJ (2020) Investigating cli¬mate suit¬ability conditions for malaria transmis¬sion and impacts of climate var-iability on mosquito survival in the hu-mid tropical region: a case study of Obafemi Awolowo University Campus, Ile-Ife, south-west¬ern Nigeria. Inter J Biomet. 64(3): 355–365.
48. Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF (2018) Present and future Köppen-Geiger cli¬mate classification maps at 1km resolution. Sci¬entific Data. 5: 180214.
49. Vatandoost H, Shahi H, Abai MR, Hanafi-Bojd AA, Oshaghi MA, Zamani G (2015) Larval habitats of main malaria vectors in Hormozgan Province and their suscepti¬bility to differentlarvicides. Se Asian J Trop Med. 35 Suppl 2: 22–25.
50. Vatandoost H, Mashayekhi M, Abai MR, Af¬latoonian MR, Hanafi-Bojd AA, Sharifi I (2005) Monitoring of insecti-cides re¬sistance in main malaria vectors in a ma¬larious area of Kahnooj District, Kerman Province, southeastern Iran. J Vector Borne Dis. 42(3): 100–108.
51. Davari B, Vatandoost H, Ladonni H, Shaeghi M, Oshaghi M, Basseri HR (2006) Com¬parative efficacy of different imagicides against different strains of Anopheles ste¬phensi in the malarious ar¬eas of Iran, 2004–2005. Pak J Biol Sci. 9(5): 885–892.
52. Hanafi-Bojd AA, Vatandoost H, Jafari R (2006) Susceptibility status of Anophe¬les dthali and An. fluviatilis to common¬ly used larvicides in an endemic focus of malar¬ia, southern Iran. J Vector Borne Dis. 43 (1): 34–38.
53. Davari B, Vatandoost H, Oshaghi M, La-donni H, Enayati A, Shaeghi M (2007) Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spec¬trum to pyrethroids and fipronil. Pes¬tic Biochem Physiol. 89(2): 97–103.
54. Abai MR, Mehravaran A, Vatandoost H, Oshaghi MA, Javadian E, Mashayekhi M (2008) Comparative performance of ima¬gicides on Anopheles stephensi, main ma¬laria vector in a malarious area, southern Iran. J Vector Borne Dis. 45(4): 307–312.
55. Vatandoost H, Hossein ZA (2010) Re-spon¬siveness of Anopheles maculipennis to dif¬ferent imagicides during resurgent ma¬laria. Asian Pac J Trop Med. 3(5): 360–363.
56. Vatandoost H, Hanafi-Bojd AA (2012) In¬dication of pyrethroid resistance in the main malaria vector, Anopheles ste¬phen¬si from Iran. Asian Pac J Trop Med. 5 (9): 722–726.
57. Soltani A, Vatandoost H, Oshaghi MA, Enayati AA, Raeisi A, Eshraghian MR (2013) Baseline susceptibility of differ-ent geographical strains of Anopheles stephen¬si (Diptera: Culicidae) to Temephos in ma¬larious Areas of Iran. J Arthropod Borne Dis. 7(1): 56–65.
58. Lak SS, Vatandoost H, Entezarmahdi M, Ashraf H, Abai M, Nazari M (2002) Mon¬itoring of insecticide resistance in Anoph¬eles sacharovi (Favre, 1903) in borderline of Iran, Armenia, Naxcivan and Turkey, 2001. Iran J Public Health. 31(3–4): 96–99.
59. Enayati AA, Vatandoost H, Ladonni H, Town¬son H, Hemingway J (2003) Mo-lec¬ular evidence for a kdr-like pyre¬throid re¬sistance mechanism in the ma¬laria vector mosquito Anopheles ste¬phensi. Med Vet Entomol. 17(2): 138–144.
60. Naddaf SR, Oshaghi MA, Vatandoost H, Ass¬mar M (2003) Molecular characteri-zation of Anopheles fluviatilis species com¬plex in the Islamic Republic of Iran. East¬ern Mediterr Health J. 9(3): 257–265.
61. Oshaghi MA, Sedaghat MM, Vatandoost H (2003) Molecular characterization of the Anopheles maculipennis complex in the Islamic Republic of Iran. Eastern Medi¬terr Health J. 9(4): 659–666.
62. Sedaghat MM, Linton YM, Oshaghi MA, Vatandoost H, Harbach RE (2003) The Anopheles maculipennis complex (Dip-tera: Culicidae) in Iran: molecular char-acter¬i¬za¬tion and recognition of a new species. Bull Entomol Res. 93(6): 527–535.
63. Azari-Hamidian S, Abai MR, Ladonni H, Vatandoost H, Akbarzadeh K (2006) Anoph¬eles peditaeniatus (Leicester) new to the Iranian mosquito fauna with notes on Anopheles hyrcanus group in Iran. J Am Mosq Control Assoc. 22(1): 144–146.
64. Oshaghi MA, Shemshad K, Yaghobi-Er-shadi MR, Pedram M, Vatandoost H, Abai MR (2007) Genetic structure of the ma¬laria vector Anopheles superpictus in Iran using mitochondrial cytochrome oxidase (COI and COII) and morpho-logic mark¬ers: a new species complex? Acta Trop. 101(3): 241–248.
65. Mehravaran A, Oshaghi MA, Vatandoost H, Abai MR, Ebrahimzadeh A, Roodi AM (2011) First report on Anopheles fluviatilis U in southeastern Iran. Acta Trop. 117(2): 76–81.
66. Naddaf SR, Oshaghi MA, Vatandoost H (2012) Confirmation of two sibling spe-cies among Anopheles fluviatilis mos¬qui-toes in south and southeastern Iran by anal¬ysis of Cytochrome Oxidase I Gene. J Ar¬thropod Borne Dis. 6(2): 144–150.
67. Dezfouli SR, Oshaghi MA, Vatandoost H, Assmar M (2003) rDNA-ITS2 based spe¬cies diagnostic polymerase chain re-ac¬tion assay for identification of sibling species of Anopheles fluviatilis in Iran. Southeast Asian J Trop Med Public Health. 34(2): 56–60.
68. Soltani A, Vatandoost H, Jabbari H, Mes-daghinia A, Mahvi A, Younesian M (2008) Use of expanded polystyrene (EPS) and shredded waste polystyrene (SWAP) beads for control of mosqui-toes. Iran J Ar¬thropod Borne Dis. 2(2): 12–20.
69. Omrani SM, Vatandoost H, Oshaghi MA, Shokri F, Guerin PM, Yaghoobi-Ershadi MR (2010) Fabrication of an olfactome-ter for mosquito behavioral studies. J Vec¬tor Borne Dis. 47(1): 17–25.
70. Omrani SM, Vatandoost H, Oshaghi M, Shokri F, Yaghoobi-Ershadi MR, Rassi Y (2010) Differential responses of Anophe¬les stephensi (Diptera: Cu¬licidae) to skin emanations of a man, a cow, and a guinea pig in the olfactome¬ter. Iran J Arthropod Borne Dis. 4(1): 1–16.
71. Omrani SM, Vatandoost H, Oshaghi MA, Rahimi A (2012) Upwind responses of Anopheles stephensi to carbon dioxide and L-lactic acid: an olfactometer study. East¬ern Mediterr Health J. 18(11): 1134–1142.
72. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA (2012) Identification of bacterial micro¬flora in the midgut of the larvae and adult of wild caught Anopheles ste-phensi: a step toward finding suitable paratransgenesis candidates. Acta Trop. 121(2): 129–134.
73. Soltani A, Vatandoost H, Jabbari H, Mes-daghinia AR, Mahvi AH, Younesian M (2012) Field efficacy of expanded poly-styrene and shredded waste polystyrene beads for mosquito control in artificial pools and field trials, Islamic Republic of Iran. Eastern Mediterr Health J. 18 (10): 1042–1048.
74. Moosa-Kazemi S, Vatandoost H, Ni-kookar H, Fathian M (2009) Culicinae (Diptera: culicidae) mosquitoes in chabahar coun¬ty, Sistan and Baluchistan Province, south¬eastern Iran. Iran J Ar-thropod Borne Dis. 3(1): 29–35.
75. Oshaghi MA, Vatandoost H, Gorouhi A, Abai MR, Madjidpour A, Arshi S (2011) Anopheline species composition in bor-derline of Iran-Azerbaijan. Acta Trop. 119 (1): 44–49.
76. Hadjiakhoondi A, Aghel N, Zamanizadeh-Nadgar N, Vatandoost H (2008) Chemi-cal and biological study of Mentha spi-catal essential oil from Iran. Daru J Phar-maceut Sci. 8(1–2): 19–21.
77. Hadjiakhoondi A, Vatandoost H, Jamshidi A, Amiri EB (2003) Chemical Constitu¬ents of Efficacy of Cymbopogon Olivieri (Boiss) bar essential oil against malaria vec¬tor, Anopheles stepensi Daru J Phar¬maceut Sci. 11(3): 125–128.
78. Oshaghi M, Ghalandari R, Vatandoost H, Shayeghi M, Kamali-Nejad M, Tourabi-Khaledi H (2003) Repellent effect of ex-tracts and essential oils of Citrus limon (Ru¬taceae) and Melissa officinalis (La¬bi-atae) against main malaria vector, Anoph¬eles stephensi (Diptera: Cu-licidae). Iran J Public Health. 32(4): 47–52.
79. Vatandoost H, Moein-Vaziri V (2004) Lar¬vicidal activity of a neem tree extract (Neema¬rin) against mosquito larvae in the Islamic Republic of Iran. Eastern Medi¬terr Health J. 10(4–5): 573–581.
80. Hadjiakhoondi A, Vatandoost H, Khanavi M, Abai MR, Karami M (2005) Bio-chem¬ical investigation of different ex-tracts and larvicidal activity of Tagetes minuta L. on Anopheles stephensi lar¬vae. Iran J Phar¬maceut Sci. 1(2): 81–84.
81. Hadjiakhoondi A, Vatandoost H, Khanavi M, Sadeghipour Roodsari HR, Vosoughi M, Kazemi M (2006) Fatty acid compo-sition and toxicity of Melia azedarach L. fruits against malaria vector Anophe¬les stephensi. Iran J Pharmaceut Sci. 2(2): 97–102.
82. Sadat Ebrahimi S, Hadjiakhoondi A, Re-zazadeh S, Fereidunian N, Vatandoost H, Abai M (2005) The components of Taget¬es minuta L. and its biological ac-tivities against malaria vector, Anophe¬les stephen¬si in Iran. J Med Plants Res. 4(16): 43–47.
83. Shahi M, Hanafi-Bojd AA, Iranshahi M, Vatandoost H, Hanafi-Bojd MY (2010) Larvicidal efficacy of latex and extract of Calotropis procera (Gentianales: As-cle¬piadaceae) against Culex quinquefas-ci¬a¬tus and Anopheles stephensi (Diptera: Cu¬licidae). J Vector Borne Dis. 47(3): 185–188.
84. Khanavi M, Toulabi PB, Abai MR, Sadati N, Hadjiakhoondi F, Hadjiakhoondi A (2011) Larvicidal activity of marine al-gae, Sargassum swartzii and Chondria da¬syphylla, against malaria vector Anophe¬les stephensi. J Vector Borne Dis. 48(4): 241–244.
85. Sedaghat MM, Sanei-Dehkordi AR, Abai M, Khanavi M, Mohtarami F, Abadi YS (2011) Larvicidal activity of essential oils of apiaceae plants against malaria vec¬tor, Anopheles stephensi. Iran J Ar-thro¬pod Borne Dis. 5(2): 51–59.
86. Sedaghat MM, Sanei-Dehkordi AR, Kha-navi M, Abai MR, Mohtarami F, Vatan-doost H (2011) Chemical composition and larvicidal activity of essential oil of Cu¬pressus arizonica E.L. Greene against ma¬laria vector Anopheles ste¬phensi Liston (Diptera: Culicidae). J Pharmacogn Res. 3(2): 135–139.
87. Khanavi M, Vatandoost H, Khosravi Dehaghi N, Sanei-Dehkordi A, Sedaghat MM, Hadjiakhoondi A (2013) Larvicid¬al activities of some Iranian native plants against the main malaria vector, Anophe¬les stephensi. Acta Med Iran. 51(3): 141–147.
88. Vatandoost H, Sanei-Dehkordi AR, Sadeghi SM, Davari B, Karimian F, Abai MR (2012) Identification of chem-ical constit¬uents and larvicidal activity of Kelussia odoratissima Mozaffarian essential oil against two mosquito vec-tors Anopheles stephensi and Culex pipiens (Diptera: Cu¬licidae). Exp Parasi-tol. 132(4): 470–474.
89. Vatandoost H, Dehakia M, Djavadia E, Abai MR, Duchson S (2006) Compara-tive study on the efficacy of lambda-cyhalothrin and bifenthrin on torn nets against the malaria vector, Anopheles stephensi as as¬sessed by tunnel test method. J Vector Borne Dis. 43(3): 133–135.
90. Moosa-Kazemi S, Vatandoost H, Raeisi A, Akbarzadeh K (2007) Deltamethrin im¬pregnated bed nets in a malaria con-trol program in Chabahar, Southeast Ba-lu¬chi¬stan, Iran. Iran J Arthropod Borne Dis. 1 (1): 43–51.
91. Rafinejad J, Vatandoost H, Nikpoor F, Abai MR, Shaeghi M, Duchen S (2008) Effect of washing on the bioefficacy of insecti¬cide-treated nets (ITNs) and long-lasting insecticidal nets (LLINs) against main ma¬laria vector Anopheles stephen¬si by three bioassay methods. J Vector Borne Dis. 45(2): 143–150.
92. Soleimani-Ahmadi M, Vatandoost H, Shaeghi M, Raeisi A, Abedi F, Eshraghi-an MR (2012) Effects of educa¬tional in-tervention on long-lasting insec¬ticidal nets use in a malarious area, southeast Iran. Acta Med Iran. 4: 279–287.
93. Soleimani-Ahmadi M, Vatandoost H, Shaeghi M, Raeisi A, Abedi F, Eshraghi-an MR (2012) Field evaluation of per-methrin long-lasting insecticide treated nets (Olyset ((R)) for malaria con¬trol in an endemic area, southeast of Iran. Acta Trop. 123(3): 146–153.
94. Vatandoost H, Mamivandpoor H, Abai MR, Shayeghi M, Rafi F, Raeisi A (2013) Wash Resistance and Bioefficacy of Alpha-cy¬permethrin Long Lasting Impregnated Nets (LLIN-Interceptor((R))) against Anoph¬e¬les ste-phensi using Tunnel Test. J Arthro¬pod Borne Dis. 7(1): 31–45.
95. Vatandoost H, Ramin E, Rassi Y, Abai M (2009) Stability and wash resistance of lo¬cal made mosquito bednets and deter-gents treated with pyrethroids against suscep¬tible strain of malaria vector Anopheles stephensi. Iran J Arthropod Borne Dis. 3 (1): 19–28.
96. Emami SN, Vatandoost H, Oshaghi MA, Mohtarami F, Javadian E, Raeisi A (2007) Morphological method for sex¬ing anophe¬line larvae. J Vector Borne Dis. 44(4): 245–249.
97. Doosti S, Azari-Hamidian S, Vatandoost H, Hosseini MOM (2006) Taxonomic dif¬ferentiation of Anopheles sacharovi and An. maculipennis sl (Diptera: Cu-licidae) larvae by seta 2 (antepalmate hair). Acta Medica Iranica. 44(1): 21–27.
98. Doosti S, Vatandoost H, Oshaghi MA, Hos¬seini M, Sedaghat MM (2007) Ap-plying morphometric variation of seta 2 (Ante¬palmate Hair) among the larvae of the members of the Maculipennis Sub-group (Diptera: Culicidae) in Iran. J Ar-thropod Borne Dis. 1(1): 28–37.
99. Vatandoost H, Ashraf H, Lak SH, Mahdi RE, Abai MR, Nazari M (2003) Factors involved in the re-emergence of malaria in borderline of Iran, Armenia, Azerbai-jan and Turkey. The Southeast Asian J Trop Med Public Health. 34 Suppl 2: 6–14.
100. Hanafi-Bojd AA, Vatandoost H, Philip E, Stepanova E, Abdi A, Safari R (2010) Ma¬laria situation analysis and stratifica¬tion in Bandar Abbas County, southern Iran, 2004–2008. Iran J Arthropod Borne Dis. 4(1): 31–41.
101. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Eshraghian MR, Haghdoost AA, Abedi F (2011) Knowledge, attitudes and practices regarding malaria control in an endemic area of southern Iran. Southeast Asian J Trop Med Public Health. 42(3): 491–501.
102. Hemami MR, Sari AA, Raeisi A, Vatan-doost H, Majdzadeh R (2013) Malaria elimination Iran, importance and chal-lenges. Int J Prevent Med. 4(1): 88–94.
103. Vatandoost H, Oshaghi MA, Abai MR, Shahi M, Yaaghoobi F, Baghaii M (2006) Bionomics of Anopheles ste-phensi Lis¬ton in the malarious area of Hormozgan Province, southern Iran, 2002. Acta Trop. 97(2): 196–203.
104. Vatandoost H, Shahi M, Hanafi-Bojd AA, Abai M, Oshaghi M, Rafii F (2007) Ecol¬ogy of Anopheles dthali Patton in Ban¬dar abbas District, Hormozgan Province, southern Iran. Iran J Arthro-pod Borne Dis. 1(1): 21–27.
105. Hanafi-Bojd AA, Azari-Hamidian S, Vatan¬doost H, Charrahy Z (2011) Spa-tio-tem¬poral distribution of malaria vec-tors (Dip¬tera: Culicidae) across different climatic zones of Iran. Asian Pacific J Trop Med. 4(6): 498–504.
106. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Charrahy Z, Haghdoost AA, Seda¬ghat MM (2012) Larval habitats and bi¬odiversity of anopheline mosquitoes (Dip¬tera: Culicidae) in a malarious area of southern Iran. J Vector Borne Dis. 49 (2): 91–100.
107. Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Haghdoost AA, Shahi M, Sedaghat MM (2012) Entomological and epide¬miological attributes for malaria trans¬mission and implementation of vector control in southern Iran. Acta Trop. 121 (2): 85–92.
108. Mehravaran A, Vatandoost H, Oshaghi MA, Abai MR, Edalat H, Javadian E (2012) Ecology of Anopheles stephensi in a ma¬larious area, southeast of Iran. Acta Med Iran. 50(1): 61–65.
109. Soleimani-Ahmadi M, Vatandoost H, Hanafi-Bojd AA, Zare M, Safari R, Mo-jahedi A (2013) Environmental charac-teristics of anopheline mosquito larval hab¬itats in a malaria endemic area in Iran. Asian Pacific J Trop Med. 6(7): 510–515.
110. Soleimani-Ahmadi M, Vatandoost H, Shaeghi M, Raeisi A, Abedi F, Eshraghi-an MR (2012) Vector ecology and sus-ceptibility in a malaria-endemic focus in southern Islamic Republic of Iran. East-ern Mediterr Health J. 18(10): 1034–1041.
111. Vatandoost H, Emami SN, Oshaghi MA, Abai MR, Raeisi A, Piazzak N (2011) Ecol¬ogy of malaria vector Anopheles cu-licifacies in a malarious area of Sistan va Baluchestan Province, south-east Is¬lam¬ic Republic of Iran. Eastern Mediterr Health J. 17(5): 439–445.
112. Oshaghi MA, Chavshin AR, Vatandoost H, Yaaghoobi F, Mohtarami F, Noorjah N (2006) Effects of post-ingestion and phys¬ical conditions on PCR amplifica-tion of host blood meal DNA in mosqui-toes. Exp Parasitol. 112(4): 232–236.
113. Nikookar S, Moosa-Kazemi S, Oshaghi M, Yaghoobi-Ershadi M, Vatandoost H, Kia¬ninasab A (2010) Species composi-tion and diversity of mosquitoes in Neka County, Mazandaran Province, northern Iran. Iran J Arthropod Borne Dis. 4(2): 26–34.
114. Vatandoost H, Abai MR, Abbasi M, Shaeghi M, Abtahi M, Rafie F (2009) De¬signing of a laboratory model for evalua¬tion of the residual effects of del-tame¬thrin (K-othrine WP 5%) on differ-ent surfaces against malaria vector, Anopheles stephen¬si (Diptera: Cu-licidae). J Vector Borne Dis. 46(4): 261–267.
115. Vatandoost H, Hanafi-Bojd AA (2008) Laboratory evaluation of 3 repellents against Anopheles stephensi in the Is-lamic Republic of Iran. Eastern Mediterr Health J. 14(2): 260–267.
116. Oshaghi MA, Chavshin AR, Vatandoost H (2006) Analysis of mosquito blood-meals using RFLP markers. Exp Parasi-tol. 114(4): 259–264.
117. Vatandoost H, Mesdaghinia AR, Zamani G, Madjdzadeh R, Holakouie K, Sadriza¬deh B (2004) Development of Training the Regional Malaria Centre in Bandar-e Abbas, Islamic Republic of Iran. Eastern Mediterr Health J. 10(1): 215–224.
118. Khoshdel-Nezamiha F, Vatandoost H, Azari-Hamidian S, Bavani MM, Dabiri F, Entezar-Mahdi R (2014) Fauna and lar¬val habitats of mosquitoes (diptera: cu¬licidae) of West Azerbaijan Province, north¬western Iran. J Arthropod Borne Dis. 8(2): 163–173.
119. Chavshin AR, Oshaghi MA, Vatandoost H, Hanafi-Bojd AA, Raeisi A, Nikpoor F (2014) Molecular characterization, bi-olog¬ical forms and sporozoite rate of Anoph¬eles stephensi in southern Iran. Asian Pa¬cific J Trop Biomed. 4(1): 47–51.
120. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Terenius O (2014) Isolation and identification of cul¬turable bacteria from wild Anopheles cu¬licifacies, a first step in a para¬transgen-esis approach. Parasite Vectors. 7: 419–424.
121. Karimian F, Oshaghi MA, Sedaghat MM, Waterhouse RM, Vatandoost H, Hanafi-Bojd AA (2014) Phylogenetic analysis of the Oriental-Palearctic-Afrotropical mem¬bers of Anopheles (Culicidae: Diptera) based on nuclear rDNA and mitochon¬drial DNA charac-teristics. Jpn J Infect Dis. 67(5): 361–367.
122. Chavshin AR, Oshaghi MA, Vatandoost H, Yakhchali B, Zarenejad F, Terenius O (2015) Malpighian tubules are im-portant determinants of Pseudomonas transstadi¬al transmission and longtime persistence in Anopheles stephensi. Par-asite Vectors. 8: 36–42.
123. Khoshdel-Nezamiha F, Vatandoost H, Oshaghi MA, Azari-Hamidian S, Mian-roodi RA, Dabiri F (2016) Molecular char¬acterization of mosquitoes (Diptera: Cu¬licidae) in Northwestern Iran by Us-ing rDNA-ITS2. Jpn J Infect Dis. 69(4): 319–322.
124. Shayeghi M, Vatandoost H, Gorouhi A, Sanei-Dehkordi AR, Salim-Abadi Y, Kara¬mi M (2014) Biodiversity of aquat¬ic in¬sects of Zayandeh Roud River and its branch¬es, Isfahan Province, Iran. J Ar-thropod Borne Dis. 8(2): 197–204.
125. Gezelbash Z, Vatandoost H, Abai MR, Raeisi A, Rassi Y, Hanafi-Bojd AA (2014) Laboratory and field evaluation of two for¬mulations of Bacillus thurin-giensis M-H-14 against mosquito larvae in the Islam¬ic Republic of Iran, 2012. Eastern Medi¬terr Health J. 20(4): 229–235.
126. Anjomruz M, Oshaghi MA, Pourfatollah AA, Sedaghat MM, Raeisi A, Vatan-doost H (2014) Preferential feeding suc-cess of laboratory reared Anopheles ste-phensi mos¬quitoes according to ABO blood group status. Acta Trop. 140: 118–123.
127. Anjomruz M, Oshaghi MA, Sedaghat MM, Pourfatollah AA, Raeisi A, Vatan-doost H (2014) ABO blood groups of residents and the ABO host choice of malaria vectors in southern Iran. Exp Parasitol. 136: 63–67.
128. Soleimani-Ahmadi M, Vatandoost H, Za¬re M (2014) Characterization of lar¬val habitats for anopheline mosquitoes in a malarious area under elimination program in the southeast of Iran. Asian Pacific J Trop Biomed. 4(Suppl 1): S73–80.
129. Soleimani-Ahmadi M, Vatandoost H, Za¬re M, Alizadeh A, Salehi M (2014) Com¬munity knowledge and practices regarding malaria and long-lasting in-secticidal nets during malaria elimina¬tion pro¬gramme in an endemic area in Iran. Malar J. 13: 511–518.
130. Soleimani-Ahmadi M, Vatandoost H, Zare M, Turki H, Alizadeh A (2015) Topo¬graph¬ical distribution of anophe¬line mos¬quitoes in an area under elimi¬nation pro¬gramme in the south of Iran. Malar J. 14: 262.
131. Ataie A, Moosa-Kazemi SH, Vatandoost H, Yaghoobi-Ershadi MR, Bakhshi H, Anjom¬ruz M (2015) Assessing the sus-ceptibility status of mosquitoes (Diptera: Culicidae) in a Dirofilariasis focus, north¬western Iran. J Arthropod Borne Dis. 9 (1): 7–21.
132. Fathian M, Vatandoost H, Moosa-Kazemi SH, Raeisi A, Yaghoobi-Ershadi MR, Oshaghi MA (2015) Sus¬ceptibility of cu¬licidae mosquitoes to some insecticides recommended by WHO in a malaria en¬demic area of southeastern Iran. J Ar¬thropod Borne Dis. 9(1): 22–34.
133. Soltani A, Vatandoost H, Oshaghi MA, Ravasan NM, Enayati AA, Asgarian F (2015) Resistance mechanisms of Anoph¬eles stephensi (Diptera: Cu¬licidae) to Temeph¬os. J Arthropod Borne Dis. 9(1): 71–83.
134. Golfakhrabadi F, Khanavi M, Ostad SN, Saeidnia S, Vatandoost H, Abai MR (2015) Biological activities and compo-sition of Ferulago carduchorum Essen-tial Oil. J Arthropod Borne Dis. 9(1): 104–115.
135. Nikookar SH, Moosa-Kazemi SH, Oshaghi MA, Vatandoost H, Yaghoobi-Ershadi MR, Enayati AA (2015) Biodi-versity of culicid mosquitoes in rural Neka town¬ship of Mazandaran Prov¬ince, northern Iran. J Vector Borne Dis. 52(1): 63–72.
136. Nikookar SH, Moosa-Kazemi SH, Yaghoobi-Ershadi MR, Vatandoost H, Oshaghi MA, Ataei A (2015) Fauna and larval habitat characteristics of mosqui-toes in Neka County, Northern Iran. J Ar¬thropod Borne Dis. 9(2): 253–266.
137. Chavshin AR, Dabiri F, Vatandoost H, Ba¬vani MM (2015) Susceptibility of Anophe¬les maculipennis to different classes of insecti¬cides in West Azarbaijan Province, Northwestern Iran. Asian Pacific J Trop Biomed. 5(5): 403–406.
138. Shayeghi M, Nejati J, Shirani-Bidabadi L, Koosha M, Badakhshan M, Bavani MM, (2015) Assessing the fauna of aquatic in¬sects for possible use for ma-laria vector control in large river, central Iran. Acta Medica Iranica. 53(9): 523–532.
139. Pirmohammadi M, Shayeghi M, Vatan-doost H, Abai MR, Mohammadi A, Bagheri A (2016) Chemical composition and repellent activity of Achillea ver-miculata and Satureja hortensis against Anopheles stephensi. J Arthropod Borne Dis. 10(2): 201–210.
140. Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H (2015) Current susceptibility status of Anopheles stephensi (Diptera: Cu¬licidae) to different imagicides in a ma¬larious ar-ea, southeastern Iran. J Arthro¬pod Borne Dis. 10(4): 493–500.
141. Abai MR, Hanafi-Bojd AA, Vatandoost H (2015) Laboratory Evaluation of Temeph¬os against Anopheles stephensi and Cu¬lex pipiens larvae in Iran. J Ar-thropod Borne Dis. 10(4): 510–518.
142. Sanei-Dehkordi A, Vatandoost H, Abai MR, Davari B, Sedaghat MM (2016) Chemical Composition and larvicidal ac-tivity of Bunium persicum essential oil against two important mosquitoes vec-tors. J Essent Oil Bear Pl. 19(2): 349–357.
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IssueVol 15 No 1 (2021) QRcode
SectionOriginal Article
Published2021-03-31
DOI https://doi.org/10.18502/jad.v15i1.6490
Keywords
Bayesian; Spatial; Poisson-Gamma; Hormozgan; Malaria elimination

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How to Cite
1.
Ghanbarnejad A, Turki H, Yaseri M, Raeisi A, Rahimi-Foroushani A. Spatial Modelling of Malaria in South of Iran in Line with the Implementation of the Malaria Elimination Program: A Bayesian Poisson-Gamma Random Field Model. J Arthropod Borne Dis. 2021;15(1):108-125.