Impact Factor 2017: 1.634 (@Clarivate Analytics)
5-Year Impact Factor: 1.677 (@Clarivate Analytics)
  • Users Online: 285
  • Print this page
  • Email this page


 
 
Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 11  |  Issue : 9  |  Page : 526-533

Distribution and ecological aspects of sand flies (Diptera: Psychodidae) species in Northeastern Iran


1 Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran
2 Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
3 Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran
4 Gonbad-e Kavoos Health Center, Golestan University of Medical Sciences, Gorgan, Iran
5 Ministry of Health, National Institute for Medical Research Development(NIMAD), Tehran, Iran

Date of Submission01-May-2018
Date of Decision20-Aug-2018
Date of Acceptance25-Aug-2018
Date of Web Publication27-Sep-2018

Correspondence Address:
Yavar Rassi
Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Po.Box:14155- 6446, Tehran
Iran
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1995-7645.242309

Get Permissions

  Abstract 

Objective: To determine both the distribution and the ecological characteristics of sand flies in Golestan Province, northeast of Iran in 2016. Methods: In this study, 34 villages were selected based on their geographical conditions. Sticky paper traps were used for collecting the sand flies. Sampling was carried out in each of villages from May to November. In each village, 60 traps for indoors and 60 for outdoors were monthly installed. The species of all collected sand flies were determined using approved morphological keys. Pearson coefficient correlation was used to find the relationship between the number of collected Phlebotomus papatasi from different villages and incidence rate of zoonotic cutaneous leishmaniasis as well as the number of positive cases of the disease. The altitude of the studied villages was extracted from digital elevation model of the area using GIS and vegetation cover density index of the province was extracted from Modis satellite imagery and distribution map of sand flies drown up. Results: Overall, 5 428 sand flies were collected and identified, belonging to 18 species. Phlebotomus wenyoni was reported for the first time from the area in this study. The frequency of sand flies in the villages located in northeast of the Golestan province (the plateau area, lower altitude, arid and semi-arid climates, and lower vegetation cover density), were more than other villages in this province. There was a significant correlation between the number of collected Phlebotomus papatasi and incidence rate of the zoonotic cutaneous leishmaniasis cases in different villages (r=0.837, P=0.019) as well as the number of positive cases of the disease (r=0.688, P<0.001). Conclusions: In the northeaster areas of Golestan Province which is known as the endemic foci of zoonotic cutaneous leishmaniasis, the abundance of sand flies were more and the conditions for their growth and development were more appropriate.

Keywords: Sand fly, Ecology, Zoonotic cutaneous leishmaniasis, Iran


How to cite this article:
Sofizadeh A, Rassi Y, Hanafi-Bojd AA, Shoraka HR, Mesgarian F, Rafizadeh S. Distribution and ecological aspects of sand flies (Diptera: Psychodidae) species in Northeastern Iran. Asian Pac J Trop Med 2018;11:526-33

How to cite this URL:
Sofizadeh A, Rassi Y, Hanafi-Bojd AA, Shoraka HR, Mesgarian F, Rafizadeh S. Distribution and ecological aspects of sand flies (Diptera: Psychodidae) species in Northeastern Iran. Asian Pac J Trop Med [serial online] 2018 [cited 2018 Oct 17];11:526-33. Available from: http://www.apjtm.org/text.asp?2018/11/9/526/242309

Foundation project: This study was supported by International Campus , Tehran University of Medical Sciences with project number: 92-03-103-24177.



  1. Introduction Top


Zoonotic cutaneous leishmaniasis is one of the most important vector-born diseases in Golestan Province and is endemic in north and northeast areas of the province; it may be regarded as one of the most important health problems in these areas[1],[2],[3]. The disease is transmitted by infected female sand flies (Diptera: Psychodidae) to animals and humans. Up to date, approximately 1 000 species of sand flies have been identified worldwide[4] and 98 species are known as proven or suspected vectors of human leishmaniases[5]. According to studies conducted in Iran since 1930 up to date, a total of 48 species of sand flies have been reported from two genera: Phlebotomus and Sergentomyia[6]. So far, approximately 18 species of sand flies have been reported in Golestan Province, northeast of Iran including: Phlebotomus papatasi (Ph. papatasi), Phlebotomus caucasicus (Ph. caucasicus), Phlebotomus mongolensis, Phlebotomus sergenti (Ph. sergenti), Phlebotomus alexandri, Phlebotomus kazeruni, Phlebotomus brevis (Ph. brevis), Phlebotomus adlerius sp, Sergentomyia sintoni (S. sintoni), Sergentomyia clydei (S. clydei), Sergentomyia sogdiana, Sergentomyia dentata, Sergentomyia hodegson, Sergentomyia antennata; Sergentomyia grekovi, Sergentomyia hodgsoni, Sergentomyia tiberiadis. Among the collected sand flies in the earlier studies, two species of Ph. papatasi and S. sintoni have been known as the dominant species sand flies, where Ph. papatasi was the major vector of zoonotic cutaneous leishmaniasis with an infection rate of 1% in the province[3],[7],[8],[9],[10],[11],[12],[13],[14].

In general, sand flies have different ecological and behavioral patterns. Some of them tend to rest in indoors places and others in outdoors. Some species of sand flies prefer to live within active burrows of rodents (reservoir of disease) across the plain areas, and the others in mountainous areas. Sand flies from Iran belong to three regions: the Afrotropical, the Oriental and the Palearctic[15]. However, due to influence of temperature and relative humidity on survival of these sand flies, they can be found in areas where conditions are appropriate in terms of temperature and relative humidity[15]. Other important factors have also contributed to distribution of the sand flies in different areas of the world. So many studies have been conducted around the world to identify these factors. The mean temperature of the wettest and driest quarters, the annual mean temperature and minimum temperature in the coldest month[16],[17] land cover type[18], the altitude from the sea level[19] and rainfall[19],[20],[21] have been reported as effective factors for distribution of different species of sand flies. Moreover, a study in Iran showed that among climate and geographic factors, the mean temperature of the wettest quarters played a more important role to distribution of Ph. papatasi[17]. A study in Golestan province[22] also indicated that some factors such as slope, annual mean temperature, the altitude from the free sea level and vegetation cover were known as the most important factors to distribution of sand fly species. Therefore, due to the fact that Golestan province has three different climatic areas, i.e. plateau, mountainous, forest and coastal zones, this study was carried out to determine distribution and ecological aspects of sand flies in Golestan province of Iran.


  2. Materials and methods Top


2.1. Study area

Golestan province with an area of 20 437.74 square kilometers covers about 1.3 percent of the total area of Iran. It is located in the northeast of the country and bordered from the north to the Republic of Turkmenistan, from the south to Alborz mountain range and Semnan province, from the east to the Khorassan-e Shomali province and from the west to the Caspian Sea and Mazandaran province. According to the latest divisions of the year 2011, this province consists of 14 counties, 25 cities, 60 districts and 1 764 villages. The province is widespread with diverse ecology and climate conditions. With regard to the sea, forest and mountainous areas climate conditions of province is classified to temperate mountain, cold mountain (3 000 meters high), a mild Mediterranean, arid and semi-arid conditions, so that as we move from southern to northern parts, the amount of rainfall and relative humidity decreases and degree of temperature increases. In regards to topography of the province, this region is divided into three distinct areas including mountainous, plain areas, and evenly posts. The mountainous areas are located in southern parts containing the highest peaks of the province. Mountain areas are located in the foothills of the southern and eastern parts of province with coarse sediments as alluvial fans make of this land. In mountain areas due to the high permeability of the soil, groundwater aquifers with water in wells and canals are exploited. Due to retreat of Caspian Sea post and plain regions were created with severe water erosion and compaction of alluvial rivers. The lowest parts of the province (Caspian Sea 32 meters below sea level) is located in this area where most of the province’s population living[23].

2.2. Villages selection

In this study, 34 villages were selected based on the wide range of different geographical zones including: 18 villages from wet zone including: 15 villages from hillside and mountainous areas and 3 villages from coastal areas. Also, 16 villages from arid and semiarid area including: 15 villages from plain areas and 1 village from hillside areas. Among the selected villages, seven were located in endemic areas of zoonotic cutaneous leishmaniasis and 27 villages in non-endemic areas.

2.3. Sand fly collection

This study was carried out during the activity period of sand flies from early May to November 2016. Sticky paper traps coated with castor oil were used to collect sand flies, so that for each month (May- November) 60 indoor and 60 outdoor sticky traps were installed before sunset and were collected the next morning before sunrise. All sand flies on traps were removed using an insulin needle and were placed for two minutes in acetone. Then, sand flies were preserved in 70% ethanol and delivered to the entomology laboratory. All specimens were mounted in Puris’ medium and identified using approved morphological keys[24],[25].

According to the results of previous studies in Golestan Province[3],[7],[8],[9],[10],[11],[12],[13],[14] that reported seasonal monthly activity of sand flies from May to November, we also sampled these months and for the other months, the number of collected specimens was considered zero.

2.4. Data analysis

Pearson coefficient correlation was used to find the relationship between the number of collected Ph. papatasi (primary and main vector of zoonotic cutaneous leishmaniasis) from different counties and disease incidence rate as well as the number of positive cases of the disease. To perform the test, first the average number of Ph. papatasi in different villages was calculated according to below formula:



Moreover, the disease incidence it was calculated by dividing the number of positive cases of the disease by the population at risk of this disease (population without scar of cutaneous leishmaniasis). Then the correlation between the entered data by entering the data in SPSS version 18.

Map of elevation layers, were obtained from the World-Clim database, version 1.4[26]. This database provides climate layers at a spatial resolution of 1 km2 derived from the data of weather stations from 1950 to 2000[27]. Also, map of normalized differentiated vegetation index (NDVI) was extracted from Modis satellite imagery for August 2014 in spatial resolution of 1000 m.


  3. Results Top


In this study, a total of 5 428 specimens of sand flies were collected and 2 407 (44.34%) specimen belonging to the Phlebotomus genus and the other species belonging to the Sergentomyia genus. In this study, a total of 18 species of sand flies were known in Golestan Province of which S. sintoni characterized as the dominant species in the region in relation to 52.19% of all species and Ph. papatasi (29.73%) was in lower ranking [Table 1]. Ph. wenyoni was also reported for the first time from Golestan Province.
Table 1: Sand flies collected in different zones of Golestan Province, 2016.

Click here to view


The most frequency of Ph. papatasi and Ph. caucasicus group were seen in northeast of Golestan Province and Ph. sergenti in Kalaleh County, east of this province [Figure 1]. Sand flies monthly activity extended from May to November, and they were active for 7 month of year in north, northeast and east of counties [Figure 2].
Figure 1: Geographical distribution of Ph. papatasi, Ph. sergenti and Ph. caucasicus group in Golestan Province, 2016.

Click here to view
Figure 2: Monthly activity of Ph. papatasi in different counties of Golestan province, Iran, 2016.

Click here to view


Visual comparison of satellite images of vegetation cover, altitude and distribution of Ph. papatasi in different counties of Golestan Province indicated that frequency of this species in northeast of Golestan Province with lower vegetation cover and altitude from sea level was higher than other areas [Figure 3],[Figure 4].
Figure 3: Geographical distribution of Ph. papatasi (No. per village) and NDVI in Golestan province, Iran, 2016.

Click here to view
Figure 4: Geographical distribution of Ph. papatasi (No. per village) and altitude of sea level in Golestan province, Iran, 2016.

Click here to view


From 15 villages sampled in the plateau areas of the Golestan Province, a total of 4 283 specimens of sand flies (285.5 sand flies per village) were collected, while 994 sand flies (62.1 sand flies per village) were collected from 16 villages of mountainous areas. In coastal areas, this figure was 50.3 per village [Table 1].

Sand flies were collected from an altitude of -23 m from the sea level to an altitude of 598 m. The highest number of sand flies were collected in a village with an altitude of 14 m from the sea level. No sand flies were collected in villages with an altitude above 900 m.

In this study, there was a significant relationship between the number of collected Ph. papatasi and the incidence rate of cutaneous leishmaniasis in different endemic and non-endemic counties of Golestan Province (r=0.837, P=0.019), as there was a significant relationship between the number of collected Ph. papatasi and number of positive cases of this disease (r=0.688, P< 0.001) [Table 2].
Table 2: Number of positive cases and incidence of zoonotic cutaneous leishmaniasis and collected of sand flies in counties of Golestan Province, 2016.

Click here to view


Foundation project: This study was supported by International Campus , Tehran University of

Medical Sciences with project number: 92-03-103-24177.

Comparing the species collected in this study with the previous studies in Golestan Province[3],[7],[8],[9],[10],[11],[12],[13],[14] Ph. wenyoni was also reported for the first time from Golestan Province. The abundance of sand flies in the villages located in the northeast of Golestan Province including plateau area, arid and semi-arid climates as well as lower vegetation cover density were more than other regions in this province.

The distribution of cutaneous leishmaniasis was very similar to distribution of sand flies, and the number of the positive cases of the disease and their incidence in the northeast villages of Golestan Province were significantly higher than other areas of the province. Similar to the results of this study, two studies conducted in Golestan Province[28],[29] showed distribution of cutaneous leishmaniasis in northeast of the province were higher than other areas. It was also reported that the number of collected sand flies in the Kalaleh County located in east of the province[10] was more than the number of collected sand flies in Aliabad-e Katool County located in central part of the province[14]. The presence probability of Ph. papatasi was reported in the northeast of the Golestan province more than other areas[22]. The association between the incidence of cutaneous leishmaniasis and vegetation cover density was investigated[29],[30] and results showed an inverse relationship between the incidence rate of cutaneous leishmaniasis and vegetation cover density which was consistent with our study. Similar to our study[31], others reported abundance of sand flies in plain area was more than mountainous and coastal areas; the abundance of sand flies in coastal area was more than mountainous areas. In another study[32], 56.8% sand flies had been collected from plain areas of Iranshahr County and mountainous areas, which was similar to the results of this study (81.2%). So we can conclude that situation in plain areas was more appropriate for growth and development of sand flies and distribution of sand flies in this areas are more than coastal and mountainous.

In this study, there was a significant relationship between the number of collected Ph. papatasi and the incidence rate of cutaneous leishmaniasis as well as the number of positive cases of the disease in different counties of the province. In the northeastern villages of the province with high frequency of Ph. papatasi, the incidence and number of positive cases of the disease were also high. A study conducted in Egypt[33] also showed there was an overlap between the geographical distribution of Ph. papatasi and distribution of zoonotic cutaneous leishmaniasis.

In the present study, the altitude of the sampling villages of sand flies from the sea level was also assessed. Sand flies were collected from an altitude of -23 m from the sea level to an altitude of 598 m. The highest number of sand flies were collected in a village with an altitude of 14 m from the sea level. No sand flies were collected in villages with an altitude above 900 m. In a conducted study in Turkey[34], which was similar to the results of our study, frequency of sand flies showed a negative correlation with the altitude and 56.1% of them were collected from areas with 0-199 m from sea level. According to our study, 68.7% of the sand flies in arid and semi-arid areas were collected from areas of 0-199 m. However, results of a study on the vectors of cutaneous leishmaniasis in Iran[17] showed that in areas with high potential for transmission of the disease, the presence probability of vectors (Ph. papatasi and Ph. sergenti) were higher than 60%, these areas had arid and semiarid climates and an average altitude in these areas was estimated 990 m and 1 235 m, respectively. In a study conducted in Golestan Province[28] approximately 97.8% of patients were reported from arid and semi-arid regions with an altitude below 725 m from the sea level. Ph. papatasi known as the vector of zoonotic cutaneous leishmaniasis in Golestan Province[9], it was previously reported by all studies in Iran’s different provinces[15]. This species was also collected from all counties of our studied areas, except the Bandar-e Gaz County, located in the west of the Golestan Province as well as villages which located in the mountainous and forest areas of the province. The abundance of this species in the northeast villages of Golestan Province, where had a geographic features including the plateau area, arid and semi-arid climate, was more than other areas of the province and 71.5% of all collected specimens of this species were collected from this area. In a study conducted in Libya[19] areas with an altitude of less than 600 m were identified as suitable areas to distribution of this species, as in our study the abundance of this species was also higher in areas with lower altitudes than those with higher altitudes. Monthly activity of Ph. papatasi in plateau areas of the province continued from May to November for 7 months, but in the counties located in the mountainous and forest areas, the activity duration of this species lasted from June to October. Similar results were reported in the previous study of the Golestan Province[10],[14]. In Iran[6], the activity of sand flies were estimated 10 months in the arid and semi-arid regions located in the southern part of the country and 7 to 8 months in the plateau areas located in center of Iran and 4 to 5 months in the cold regions located in the northwest areas of the country that was similar to the results of our study.

Another important species of sand flies in Golestan Province was Ph. caucasicus group known as the wild cycle vectors of Leishmania major[6],[35],[36] and also as the secondary vector of Leishmania major to human[36].

In the present study, Ph. sergenti represented 3% of all collected sand flies, which is known as the vector of anthroponotic cutaneous leishmaniasis in Iran[36],[37]. This species was reported in Iran from 26 provinces with three morphotypes[38] and is known as a mountainous species[6]. In our study, the frequency of this species in plain areas were more than other regions. In southeast of Iran[31],[32],[39], 96%, 97% and 98.5% of this species were collected from mountainous areas. In our study, this species was collected from villages with -3 to 598 m, but most of the specimens of this species were collected from Kalaleh County in the east of Golestan Province, so that 73.2% of the specimens of this species were collected from three villages in Kalaleh County, that located in hillside and plateau areas with 598 m, 424 m and 273 m from sea level. The abundance of this species has been very low at lower altitudes. In the studies conducted in Iran, this species has been collected from the height of 40-2 232 m, but the average altitude from the sea level for this species was estimated at 1 235 m[17]. In other countries, this species has also collected from the height of 1 600-2 000 m above sea level[34],[40].

Ph. alexandri, which is known as a probable vector of visceral leishmaniasis in the south part of the country, was almost 0.07% of all collected sand flies. In the various studies conducted in Iran[6], this species was reported mainly in the central regions of the country. However, in studies in Sistan-Baluchistan Province, 91.6%, 96.1% and 98% of this species were reported from mountainous areas[31],[32],[39], Therefore, it is necessary to was done more studies in mountainous areas of Golestan Province.

In the present study, collected san flies of Adlerius subgenus was in a low abundance. However, the abundance of this subgenus in areas with an altitude above 100 m was greater than those with a lower altitude. In other studies in Golestan Province, this species was also collected in a low abundance[10],[14]. Species of this subgenus are mostly found in wild form in mountainous areas above 1 200 m from sea level in northwest of Iran[41], as in our study, Ph. brevis is mostly collected in mountainous areas. There are about 20 species in this subgenus, known as primary or probably vectors of zoonotic visceral leishmaniasis in many parts of the world, however, some species of this subgenus are reported as the vestors of Leishmania tropica, Leishmania major and Leishmania donovani[42]. Six species of this subgenus has been reported in Iran[42].

In Iran, the sand flies of the subgenus Larroussius are considered as vectors of zoonotic visceral leishmaniasis[35]. From this subgenus, only the species Phlebotomus major has been reported before from this province[6].

Another species that was collected in the high abundance in Golestan Province was S. sintoni, known as a vector of lizard leishmaniasis in Afghanistan and Iran[6],[7],[15]. In most studies, this species has been collected[6] from Iran as well as Golestan province[6],[7],[8],[10],[14]. The distribution of this species was similar to Ph. papatasi in different areas of Golestan province, and were often collected in plain regions with low altitude and low vegetation[32],[39], But contrary of our result, in another study conducted in southeast of Iran[31], the abundance of this species in coastal areas was more than plain and mountainous areas.

Sergentomyia clydei and S. dentata, also considered as vectors of lizard leishmaniasis[6],[43],[44], were collected in a low abundance in this study. Both of these species were reported in previous studies of Golestan Province[10],[14]. Similar to the results of these studies, S. clydei was also reported from Aqqala, Gonad-e Kavus and Marāveh Tapeh Counties, located in the north and northeastern parts of Golestan Province.

Sergentomyia hodgsoni, previously reported only from the provinces such as West Azarbaijan, Sistan and Baluchestan and Aliabad-e Katul County in Golestan Province[14],[15], were collected in a low abundance in this study. It is a species that has been collected from mountainous areas (caves and gap of the rocks in mountains) but it was in a low abundance in plateau areas[15]. In the current study, this species was again collected from a village in Aliabad-e Katul County with an altitude of 221 m from the sea level and hillside areas and also from a village in Gonbad-e-Kavus County with 189 m altitude, hillside and arid and semi-arid areas.

Other species such as Sergentomyia sogdiana, S. grekovi, S. antennata and S.tiberiadis were also collected from the northeastern parts of Golestan Province in a low abundance which the villages of these areas were located in arid and semi-arid conditions with an altitude of less than 200 m. Because these species have been collected with low abundance, more studies are necessary for review their distribution and ecological characteristics.

Conflict of interest statement

We declare that we have no conflict of interest.

 
  References Top

1.
Cherabin M, Sofizadeh A, Palideh AR, Gharavi AH, Gharavi M. Epidemiological characteristics of cautaneous leishmaniasis in Maravehtapeh district, Golestan province during 2006-2010. J Zabol Uni Med Sci 2012; 4(1): 19-27. [Persian].  Back to cited text no. 1
    
2.
Sofizadeh A, Faraji Far AA, Cherabin M, Badiei F, Cherabin M, Sarli J, et al. Cutaneous leishmaniasis in Gonbad Kavoos, North of Iran (2009-11): an epidemiological study. J Gorgan Uni Med Sci 2013; 14(4): 100-106. [Persian].  Back to cited text no. 2
    
3.
Sofizadeh A, Ghorbani M, Gorganli Davaji A, Gharemeshk Gharavi A. Epidemiological status of cutaneous leishmaniasis and ecological characteristics of sand flies in Maraveh-Tapeh county, Golestan province, 2011-2012, Iran. Qom Univ Med Sci J 2015; 9(6): 53-65. [Persian].  Back to cited text no. 3
    
4.
Galati EAB, Galvis-Ovallos F, Lawyer P, Léger N, Depaquit J. An illustrated guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psychodidae). Parasite 2017; 24(26): 1-35.  Back to cited text no. 4
    
5.
Maroli M, feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. Phlebotomine sand flies and the spreading of leishmaniases and other disease of public health. Med & Vet Entomol 2013; 27: 123-147.  Back to cited text no. 5
    
6.
Karimi A, Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Akhavan AA, Ghezelbash Z. Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psychodidae), vectors of leishmaniasis, in Iran. Acta Tropica 2014; 132:131–139.  Back to cited text no. 6
    
7.
Seyedi-Rashti MA, Ataby A, Mohebali M. Natural promastigote infection of Sergentomyia sintoni, its seasonal variation and reservoir host in Turkmen sahra, Iran. Iran J Public Health 1994; 23(1-4): 41-50.  Back to cited text no. 7
    
8.
Parvizi P, Javadian E, Rassi Y, Amirkhani A. A study on vector and reservoir host of cutaneous leishmaniasis in Turkman-sahra, Golestan province, north-east of Iran. J Modarres Uni Med Sci 1999; 2(1): 125-129.  Back to cited text no. 8
    
9.
Rassi Y, Sofizadeh A, Abai MR, Oshaghi MA, Rafizadeh S, Mohebail M, et al. Molecular detection of Leishmania major in the vectors and reservoir hosts of cutaneous leishmaniasis in Kalaleh District, Golestan Province, Iran. Iran J Arthropod-Borne Dis 2008; 2(2): 21-27.  Back to cited text no. 9
    
10.
Sofizadeh A, Rassi Y, Abaei MR, Oshaghi MA, Salahi R, Rafizadeh S, et al. Ecological characters of leishmaniasis vectors in Kalaleh district, Golestan province, Iran (2006-2007). J Gorgan Uni Med Sci 2009; 11(3): 81-85.  Back to cited text no. 10
    
11.
Roshanghalb M, Parvizi P. Isolation and determination of Leishmania major and Leishmania turanikain, Phlebotomus papatasi main vector of zoonotic cutaneous leishmaniasis in Turkmen Sahra, Golestan province. J Mazandaran Uni Med Sci 2012; 21(Supplement 1): 74-83.  Back to cited text no. 11
    
12.
Bordbar A1, Parvizi P. High density of Leishmania major and rarity of other mammals’ Leishmania in zoonotic cutaneous leishmaniasis foci, Iran. Trop Med Int Health 2014; 19 (3): 355-363.  Back to cited text no. 12
    
13.
Agh-Ataby MD, Sofizadeh A, Ozbaki GM, Malaki-Ravasan N, Ghanbari MR, Mozafari O. Ecoepidemiological characteristics of a hypoendemic focus of zoonotic cutaneous leishmaniasis in north Iran (southeast of Caspian Sea). J Vector Borne Dis 2016; 53: 248–256.  Back to cited text no. 13
    
14.
Bagheri A, Sofizadeh A, Ghezel AH, Ghanbari MR, Fadaei E, Yapang Gharavi M, et al. Echological characters of sand flies (vectors of leishmaniasis) in Aliabad Katul District, Golestan Province, (2011-2012). J Gorgan Uni Med Sci 2014; 15(4): 84-88. [Persian].  Back to cited text no. 14
    
15.
Rassi Y, Hanafi-Bojd AA. Sand flies, vectors of leishmaniasis.1 ed. Tehran: Noavaran-e- Elm Publ; 2006, p. 2-156[Persian].  Back to cited text no. 15
    
16.
González C, Wang O, Strutz SE, González-Salazar C, Sánchez-Cordero. Climate change and risk of leishmaniasis in North America: Predictions from ecological niche models of vector and reservoir species. PLoS Negl Trop Dis 2010; 4(1): 1-16.  Back to cited text no. 16
    
17.
Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Haghdoost AA, Akhavan AA, Rassi Y, Karimi A, et al. Modeling the distribution of cutaneous leishmaniasis vectors (Psychodidae: Phlebotominae) in Iran: A potential transmission in disease prone areas. J Med Entomol 2015; 52(4): 557-565.  Back to cited text no. 17
    
18.
Colacicco-Mayhugh MG, Masuoka PM, Grieco J. Ecological niche model of Phlebotomus alexandri and P. papatasi (Diptera: Psychodidae) in the Middle East. Int J Health Geogr 2010; 9(2): 1-9.  Back to cited text no. 18
    
19.
Abdel-Dayem MS, Annajar BB, Hanafi HA, Obenauer PJ. The potential distribution of Phlebotomus papatasi (Diptera: Psychodidae) in Libya based on ecological niche model. J Med Entomol 2012; 49(3): 739-745.  Back to cited text no. 19
    
20.
Morrison AC, Ferro C, Pardo R, Torres M, Devlin B, Wilson ML, et al. Seasonal abundance of Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. J Med Entomol 1995; 32(4): 538-548.  Back to cited text no. 20
    
21.
Salomón OD, Wilson ML, Munstermann LE, Travi BL. Spatial and temporal patterns of phlebotomine sand flies (Diptera: Psychodidae) in a cutaneous leishmaniasis focus in northern Argentina. J Med Entomol 2004; 41(1): 33-39.  Back to cited text no. 21
    
22.
Sofizadeh A, Rassi Y, Vatandoost H, Hanafi-Bojd AA, Mollalo A, Rafizadeh S, et al. Predicting the distribution of Phlebotomus papatasi (Diptera: Psychodidae), the primary vector of zoonotic cutaneous leishmaniasis, in Golestan Province of Iran using ecological niche modeling: Comparison of MaxEnt and GARP Models. J Med Entomol 2017; 54(2): 312–320.  Back to cited text no. 22
    
23.
Golfiruzi S, Kh Kourdi, Abolhasani M. Statistics yearbook of health center in Golestan province (2010-2011). 1st ed. Gorgan: Noroozi Press; 2010, p. 6-92. [In persian].  Back to cited text no. 23
    
24.
Theodor O, Mesghali A. On the phlebotominae of Iran. J Med Entomol 1964; 1(3): 285-300.  Back to cited text no. 24
    
25.
Seyedi-Rashti MA, Nadim A. The genus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the Eastern Mediterranean Region. Iranian J Publ Health 1992; 21(1–4): 11–50.  Back to cited text no. 25
    
26.
European Space Agency. ESA: Mission, earthobservation: ENVISAT[Online]. Avaliable from: http://envisat.esa.int/[Accessed on 3rd July 2008].  Back to cited text no. 26
    
27.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005; 25: 1965–1978.  Back to cited text no. 27
    
28.
Mollalo AF, Alimohammadi A, Shahrisvand M, Shirzadi MR, Malek MR. Geographic information system-based analysis of the spatial and spatio-temporal distribution of zoonotic cutaneous leishmaniasis in Golestan Province, North-East of Iran. Zoonoses Public Health 2015; 62(1):18-28.  Back to cited text no. 28
    
29.
Mollalo AF, Alimohammadi A, Shahrisvand M, Shirzadi MR, Malek MR. Spatial and statistical analyses of the relations between vegetation cover and incidence of cutaneous leishmaniasis in an endemic province, northeast of Iran. Asian Pac J Trop Dis 2014; 4(3): 176-180.  Back to cited text no. 29
    
30.
Mozaffari Gh, Bakhshizadeh F, Gheibi M. Analysis relationship between vegetation cover and salak skin disease in Yazd-Ardakan Plain. Geography Environmental Planning J 2012; 44(4): 167-178 [Full text in Persian].  Back to cited text no. 30
    
31.
Kassiri H, Javadian E, Sharififard M. Monthly activity of Phlebotominae sand flies in Sistan-Baluchistan Province, Southeast Iran. J Insect Sci 2013; 13:153.  Back to cited text no. 31
    
32.
Kassiri H, Javadian EA, Sharififard M. Bionomics of phlebotomine sand flies (Diptera: Psychodidae) as vectors of leishmaniasis in the County of Iranshahr, Sistan-Baluchistan Province, Southeast of Iran. Iran J Clin Infect Dis 2011; 6(3): 112-116.  Back to cited text no. 32
    
33.
Samy AM, Camphell LP, Peterson AT. Leishmaniasis transmission: distribution and coarse-resolution ecology of two vectors and two parasites in Egypt. Rev Soc Bras Med Trop 2014; 47(1):57-62.  Back to cited text no. 33
    
34.
Simsek FM, Alten B, Caglar SS, Ozbel Y, Aytekin AM, Kaynaz S, et al. Distribution and altitudinal structuring of phlebotomine sand flies (Diptera: Psychodidae) in southern Antolia, Turkey: their relation to human cutaneous leishmaniasis. J Vector Ecol 2007; 32: 269-279.  Back to cited text no. 34
    
35.
Yaghoobi-Ershadi MR, Javadian E. Seasonal variation of Leishmania major infection rates in sand flies from rodent burrows in Isfahan province, Iran. Med Vet Entomol 1996; 10: 181–184.  Back to cited text no. 35
    
36.
Yaghoobi-Ershadi MR. Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their role on leishmania transmission. J Arthropod-Borne Dis 2012; 6: 1–17.  Back to cited text no. 36
    
37.
Oshaghi MA, Rasolian M, Shirzadi MR, Mohtarami F, Doosti S. First report on isolation of Leishmania tropica from sand flies of a classical urban cutaneous leishmaniasis focus in southern Iran. Exp Parasitol 2010; 126: 445–450.  Back to cited text no. 37
    
38.
Moin-Vaziri V, Depaquit J, Yaghoobi-Ershadi MR, Oshaghi MA, Derakhshandeh Peykar P, Ferte H, et al. Intraspecific variation within Phlebotomus sergenti Parrot (1917) (Diptera: Psychodidae) based on mtDNA sequences in Islamic Republic of Iran. Acta Trop 2007; 102: 29–37.  Back to cited text no. 38
    
39.
Kassiri H, Javadian E, Hanafi-Bojd AA. Species composition of Phlebotomine sandflies (Diptera: Psychodidae) in Nikshahr county, southeastern Iran. J Vector Borne Dis 2011; 48: 159-162.  Back to cited text no. 39
    
40.
Al-Zahrani MA, Peters W, Evans DA, ChingChin I, Smith V, Lane P. Phlebotomus sergenti, a vector of Leishmania tropica in Saudi Arabia. Trans R Soc Trop Med Hyg 1988; 82: 416.  Back to cited text no. 40
    
41.
Zahraei-Ramazani AR, Kumar D, Yaghoobi-Ershadi MR, Naghian A, Jafari R, Shirzadi MR, et al. Sand flies of the subgenus Adlerius (Diptera: Psychodidae) in an endemic focus of visceral leishmaniasis and introduction of Phlebotomus (Adlerius) comatus as a new record for Iran. J Arthropod-Borne Dis 2013; 7(1): 1–7.  Back to cited text no. 41
    
42.
Zahraei-Ramazani A, Kumar D, Mirhendi M, Sundar S, Mishra R, Moin-Vaziri V, et al. Morphological and genotypic variations among the species of the subgenus Adlerius (Diptera: Psychodidae, Phlebotomus) in Iran. J Arthropod-Borne Dis 2015; 9(1): 84–97.  Back to cited text no. 42
    
43.
Maleki Ravasan N, Javadian E, Mohebali M, Dalimi Asl A, Sadraei J, Zarei Z, et al. Natural infection of sand flies Sergentomyia dentata in Ardebil to lizard leishmaniasis. Modarres J Med Sci 2008; 10: 65–73.  Back to cited text no. 43
    
44.
Kassiri H, Jahanifard E. First report on Sergentomyia sintoni and Sergentomyia clydei (Diptera: Psychodidae): their natural promastigote infection and some aspects of biology in Sistan-Baluchistan Province, Southeastern Iran. Asian Pac J Trop Dis 2012; 2(1): S370–S373.  Back to cited text no. 44
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
[INLINE:1]
1. Introduction
2. Materials and...
3. Results
4. Discussion
1. Introduction
2. Materials and...
3. Results
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed99    
    Printed2    
    Emailed0    
    PDF Downloaded62    
    Comments [Add]    

Recommend this journal