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Study on species composition and seasonal activity of sand flies in a new focus of visceral leishmaniasis, Azarshahr district, East Azerbaijan province, Iran.


Sand flies belong to the family Psychodidae, wich is among the most primitive families of Diptera [24]. The family Psychodidae is characterized by their wing venation [the presence of numerous parallel veins running to wing margin), and the presence of dense hairs on the wings and thorax. Phlebotomine sand flies are classified within the subfamily Phlebotominae, and are differentiated from other subfamilies within Psychodidae by the presence of biting mouthparts that are longer than the head, five-segmented palps, nearly cylindrical antennae, a five-branched radial vein on the wing, and the absence of an eye-bridge [21]. There are three New World genera within subfamily Phlebotominae: Brumptomyia, Warileya and Lutzomyia [24]. There are two old world genera within the subfamily Phlebotominae: Sergentomyia and phlebotomus [10]. Sand flies in the genus Sergentomyia feed primarily on lizard, and may be the vectors of the agent of saurian leishmaniasis. Sand flies of the genus phlebotomus feed on mammals, and represent all of the medically important sand flies in the old world. Sand flies of the genus Phlebotomus can often be distinguished from those within Sergentomyia by the Cibarium. Phlebotomus dose not have a row of teeth and usually does not have a patch of pigment [10]. Sand flies of more than 30 species in the genus Lutzomyia and 40 species in the genus Phlebotomus are vectors of human pathogens. Phlebotomus sand flies are the vectors of several viruses, the bacterium Bartonella baciliformis, and most importantly, nearly 20 species of protozoan parasites in the genus Leishmania. Leishmania is a genus of heterogeneous parasites in the family Trypanosomatidae. Leishmania parasites are the etiological agents of a complex of disease with a broad clinical spectrum called Leishmaniasis. Nearly 20 species of Leishmania have been shown to cause human disease [3,11,13]. Worldwide, 2 million new cases of Leishmaniasis are believed to occur annually, and as many as 12 million people currently may be infected [22]. Since the first report of visceral leishmaniasis by Pouya in 1949, about 9000 cases have been reported in Iran [6]. There are four important foci of visceral Leishmaniasis in Iran, including Ardebil, East Azerbaijan, Fars and Bushehr provinces. The disease occurs sporadically in the other parts of the country in September onwards [19]. The recent reports were indicated of increasing new cases of disease in Azarshahr [East Azerbaijan province] has been reported to be endemic for VL [12,18]. In this area 5.3% rodents were shown to be seropositive [5]. Also in Azarshahr county more than 34 new cases of visceral leishmanisis [kala-azar] have been reported recently. The geographical distribution and development of insect vectors are strongly related to the climate factors such as temperature, rainfall, humidity, among which, temperature plays a prominent role in insect's development. It has a direct correlation with the insects, metabolic rates, egg production, survival of preimaginal stages, and adults longevity and frequency of blood feeding . On the other hands, climate factors have a direct impact on the development of the pathogens [8,9,13]. Study on the Phlebotomine vectors bionomics is an interesting tool. It makes for a better understanding of the planning for the prevention and control against Leishmaniasis particularly in the areas where the risk of Leishmaniasis extension is significant. This study is the first detailed research in terms of species composition and density of sand flies in an endemic focus of visceral leishamaniasis in Azarshahr County. The objective of this study was to determine the species composition, relative abundance, the activity periods of Phlebotomine sand flies, common sand flies in resting places and to specify the risk period of leishmaniasis in Azarshahr district, Eastern Azerbaijan province, Iran.

Material and Methods

Study Area:

The investigation was carried out from late April to late October 2010 in 5 villages, Almalodash, Jaragil, Segaiesh, Amirdizaj and Germezigol in Azarshahr, Eastern Azerbaijan province, in the northwest of Iran. Azarshahr county [37[degrees]30, 45[degrees]40 E] is situated in the northwest of Iran, 54 Km south of Tabriz at the altitude of 1,368 m above sea level. The mean annual precipitation is 303 mm and with 49% relative humidity, and the mean annual temperature is 15.2C[degrees]. The maximum and minimum average monthly temperatures are 27.7C[degrees] and 3.7C[degrees] respectively. The total population of Azarshahr was approximately 10664 in 2009. The main occupation of the population are farming and raising animals. On the basis of available epidemiologic data obtained from medical centers in Azarshahr district, villages that disease was recorded from them were selected for this study.

Sand Flies Collection and Identification:

Sand flies were collected using sticky traps [Castor Oil-Coated white papers 20 Cm x 30 Cm] biweekly from selected villages indoors [bedrooms, guest room, toilet and stable] and outdoors (rodent burrow). Traps (70 papers per village) were set at dusk and sand flies were collected at down [1,17, 23]. Sample collection began in late April and continued until late October 2010. When sand fly activities were reduced sharply, collected sand flies and were stored in 96% ethanol. In the laboratory for species identification, head, terminal abdomens of females and removed head of male with its body were mounted in puri's medium, produced at the medical entomology departement. Species identification after one week using keys of sand flies was carried out [19].

Data Analysis:

The density of sand flies collected by sticky traps was calculated using the formula number of specimens / [M.sup.2] of sticky traps and numbers of specimens/ number of traps. Logistic regression used to investigate the existence of a correlation between the abundance of the sand flies, and average monthly temperature in the study area using SAS software [9,15,20].

The density of species was corrected according to the formula:

Density = [square root of 1 + number of specimen / number of traps]

In order to reduce the dispersion of the variable without modifying the relative position of the species in the multidimensional space [4].


Totally, 5557 specimens comprising 16 species (14 phlebotomus and 2 sergentomyia) were identified including: Ph. papatasi (31.9%), ph. sergenti (22.5%), ph. mongolensis (17.3%), ph. ansarii (0,3%), ph. tobbi (3.4%), ph. kanelakii (4.2%), ph. halepensis (8.1%), ph. longiductus (0.8%), ph. anderjevi (2.9%), ph. Caucasicus (5%), Ph.mesghali (.5%) Ph.perfiliewi (.5%) ph. major (0.5%), ph. (Adlerius) spp (0.5%), S.hodgsoni (1.3%), S.pawlowskyi (0.3%) The activity of the species extended from April to October common sand flies in resting places were ph. papatasi, ph. sergenty and ph. mongolensis (Table 1). The monthly average density according to formula, number of specimens/ [M.sup.2] of sticky traps, was 37.60, 41.10, 40.23, 30.38 and 30.67 in Almalodash, Jaragil, Segaiesh, Amirdizaj and Germezigol respectively. Also according to formula, number of specimens/number of traps, corrected monthly average density in mentioned villages was 1.47, 1.51, 1.50, 1.39 and 1.40.Field survey on the population density of sand flies in the region showed that the first adult population occurred in late May and the highest population density was observed in the third week of August, followed by a sharp decrease in the first week of October.



Four sand flies species, namely ph. major, ph. kandelakii and ph. perfiliewi transcaucasicus have been suspected as the vectors of VL in Iran .Investigations on vectors of VL in Ardebil province, adjacent to eastern Azerbaijan showed two species of ph. kandelakii, ph. erfiliewi were main probable vectors of the disease as they were found naturally infected by promastigotes [16]. Also a recent study in Kaleybar, one of the foci of VL in East Azerbaijan province, Iran, which are based on PCR detection and sequencing of parasite ITS region of DNA, ph. perfiliewi transcaucosicus was found the only vector of the causative agent of VL found in that region [14]. So it seems that ph. kandelakii, ph. perfiliewi may play a role as vector in Azarshahr county. According to the results of previous studies, the vectors of viscerotropic Leishmania spp in old world mainly belong to the subgenera Larrousius, Adlerius, Euphlebotomus. In northwest of Iran ph. kandelakii and ph. perfiliewi are proven and probable vector of viscerotropic Leishmania spp [2]. Knowledge of spatial and seasonal trends will help decide both where and when to implement control programs [7]. The highest population density was observed in third week of August, but that in second week of October the population density decreased rapidly, with the adult population disappearing completely in third week of October. This study is the first detailed research in terms of species composition and density of sand flies in an endemic focus of visceral leishmaniasis in Azarshahr county. The population dynamics of sand flies in Azarshahr were greatly affected by climate factors. Our results suggest that the highest activity of the collected sand fly species occurs in third week of August that could help health authorities for prediction period of maximum risk of VL transmission and successful implementation of a control program.


The authors are grateful to Mohammadreza Abai, Ahmad ali Hanafi bojd [Academic member of Tehran University of medical sciences] and staff of Azarshahr center of disease control, Eastern Azerbaijan province, Iran for their contribution and help in sand fly collection or identification.


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(1) Teimour Hazratian, (1) Yavar Rassi, (1) Mohammad Ali Oshaghi, (1) Mohammad Reza Yaghoobi Ershadi, (2) Esmael Fallah and (3) Majid khanmohammadi

(1) Department of Medical Entomology and vector control, School of public health, Tehran University of Medical Sciences, Tehran, Iran.

(2) Departmemt of Parasitology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran.

(3) Department of Laboratory Sciences, Marand branch, Islamic Azad University, Marand, Iran.

Teimour Hazratian, Yavar Rassi, Mohammad Ali Oshaghi, Mohammad Reza Yaghoobi Ershadi, Esmael Fallah and Majid khanmohammadi: Study on Species Composition and Seasonal Activity of Sand Flies in A New Focus of Visceral Leishmaniasis, Azarshahr District, East Azerbaijan Province, Iran.

Corresponding Author

Yavar Rassi, Department of Medical Entomology and vector control, School of public health, Tehran University of Medical Sciences, Tehran, Iran.
Table 1: Species composition frequency
of sand flies in Azarshahr County,
East Azerbaijan, Iran, 2010.

     Species         No.     Rf.     %

   Ph. papatasi      1773   0.319   31.9
   Ph. sergenti      1250   0.255   22.5
 Ph. mongolensis     961    0.173   17.3
    Ph. ansari        17    0.003   0.3
    Ph. tobbi        189    0.034   3.4
  Ph. kandelakii     233    0.042   4.20
  Ph. halepensis     450    0.081   8.1
  Ph. logiductus      44    0.008   0.8
  Ph. anderjevi      161    0.029   2.9
  Ph. caucasicus     278    0.050    5
   Ph. mesghali       28    0.005   0.5
  Ph. perfiliewi      28    0.005   0.5
    Ph. major         28    0.005   0.5
Ph. [Adlerius] spp    28    0.005   0.5
    S.sodgsoni        72    0.013   1.3
   S.pawlowskyi       17    0.003   0.3
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Title Annotation:Original Article
Author:Hazratian, Teimour; Rassi, Yavar; Oshaghi, Mohammad Ali; Ershadi, Mohammad Reza Yaghoobi; Fallah, Es
Publication:Advances in Environmental Biology
Article Type:Report
Geographic Code:7IRAN
Date:Sep 1, 2011
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