The Open Public Health Journal




ISSN: 1874-9445 ― Volume 13, 2020
RESEARCH ARTICLE

Survey of Usutu Virus Potential Vectors and their Diversity in Iran: A Neglected Emerging Arbovirus



Mehdi Khoobdel1, Davoud Keshavarzi2, *
1 Health Research Center, Life style institute, Baqiyatallah University of Medical Sciences, Tehran, Iran
2 Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

Abstract

Introduction:

Usutu Virus (USUV) is a vector-borne flavivirus within the family of Flaviviridae; its reservoirs and vectors are birds and mosquitoes, respectively.

Methods:

At first, electronic databases were searched with a date range from 2000 to 2018 to find the Culex species that transmit the disease and then for determining the diversity of those, mosquito larvae were collected from six places in three main environmental categories using the dipping technique.

Results:

In total, 1369 specimens belonging to 10 different species were collected and identified, as follows: Cx. hortensis Ficalbi, Cx. laticinctus Edwards, Cx. mimeticus Noe, Cx. perxigus Theobald, Cx. pipiens Linnaeus, Cx. modestus Ficalbi, Cx. sinaiticus Kirkpatrick, Cx. theileri Theobald Cx. torrentium Martini and Cx. tritaeniorhynchus Giles. Four species involved as vectors of USUV in other countries are printed in bold. Cx.pipiens, as the main vector was the most frequent species in rural areas, share its larval habitats with Cx. torrentium (similarity > 0.9) and reached its peak in August. Overall, in the present study, there was a significant positive relationship between mean temperatures and abundance of mosquitoes (r = 0.75, P = 0.005).

Conclusion:

In the present study, some species involved as main vectors of USUV in other countries and their ecological features were recorded. Based on these results, the possibility of the emergence of USUV in Iran exists.

Keywords: Mosquitoes, Usutu virus, Species diversity, Flavivirus, Reservoirs, Rural areas.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 13
First Page: 114
Last Page: 118
Publisher Id: TOPHJ-13-114
DOI: 10.2174/1874944502013010114

Article History:

Received Date: 16/12/2019
Revision Received Date: 29/02/2020
Acceptance Date: 03/3/2020
Electronic publication date: 24/04/2020
Collection year: 2020

© 2020 Khoobdel and Keshavarzi.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran; Tel: 0098-0098-9374793951, Fax: 009871325254; E-mail: keshavarzd25@gmail.com, keshavarzid@razi.tums.ac.ir





1. INTRODUCTION

Usutu Virus (USUV) is a culicid-borne flavivirus within the family of Flaviviridae; its reservoirs and vectors are birds and Culex mosquitoes, respectively [1Vazquez A, Jiménez-Clavero M, Franco L, et al. Usutu virus: potential risk of human disease in Europe. Euro Surveill 2011; 16(31): 19935.
[PMID: 21871214]
]. Circulation and antigenic features of USUV is similar to West Nile Virus (WNV), since its identification in 1959 in Ndumu, South Africa, this culicid-borne virus has spread in Africa and Europe, reaching Austria in 2001 and countries of the Poland and Switzerland by 2006 [1Vazquez A, Jiménez-Clavero M, Franco L, et al. Usutu virus: potential risk of human disease in Europe. Euro Surveill 2011; 16(31): 19935.
[PMID: 21871214]
, 2Aberle SW, Kolodziejek J, Jungbauer C, et al. Increase in human West Nile and Usutu virus infections, Austria, 2018. Euro Surveill 2018; 23(43)1800545
[http://dx.doi.org/10.2807/1560-7917.ES.2018.23.43.1800545] [PMID: 30376913]
]. The virus has recently been identified in mosquitoes in northern Israel. [3Mannasse B, Mendelson E, Orshan L, et al. Usutu virus RNA in mosquitoes, Israel, 2014-2015. Emerg Infect Dis 2017; 23(10): 1699-702.
[http://dx.doi.org/10.3201/eid2310.171017] [PMID: 28930008]
]. USUV infection in human cases was reported in European countries [4Grottola A, Marcacci M, Tagliazucchi S, et al. Usutu virus infections in humans: a retrospective analysis in the municipality of Modena, Italy. Clin Microbiol Infect 2017; 23(1): 33-7.
[http://dx.doi.org/10.1016/j.cmi.2016.09.019] [PMID: 27677699]
]. Some migratory infected bird species such as; Passer domesticus (house sparrows), Gallus gallus, and Turdus merula (the common blackbird) are responsible for the dissemination of USUV from Europe to other countries [5Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap? Trans R Soc Trop Med Hyg 2015; 109(10): 609-18.
[http://dx.doi.org/10.1093/trstmh/trv066] [PMID: 26286946]
]. USUV had been detected in some culicid species from different parts of the world (i.e. Culex pipiens and Cx. perexigus in Israel and Spain, Cx. torrentium in Germany, and Ae. albopictus in Israel), Cx. pipiens and Cx. neavei are considered as the main vectors for this virus [3Mannasse B, Mendelson E, Orshan L, et al. Usutu virus RNA in mosquitoes, Israel, 2014-2015. Emerg Infect Dis 2017; 23(10): 1699-702.
[http://dx.doi.org/10.3201/eid2310.171017] [PMID: 28930008]
, 6Nikolay B, Diallo M, Faye O, Boye CS, Sall AA. Vector competence of Culex neavei (Diptera: Culicidae) for Usutu virus. Am J Trop Med Hyg 2012; 86(6): 993-6.
[http://dx.doi.org/10.4269/ajtmh.2012.11-0509] [PMID: 22665607]
-8Jöst H, Bialonski A, Maus D, et al. Isolation of usutu virus in Germany. Am J Trop Med Hyg 2011; 85(3): 551-3.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0248] [PMID: 21896821]
]. These reservoirs and vectors have been reported from Iran [9Keshavarzi D, Soltani Z, Ebrahimi M, et al. Monthly prevalence and diversity of mosquitoes (Diptera&58; Culicidae) in Fars Province, Southern Iran. Asian Pac J Trop Dis 2017; 7(2): 112-20.
[http://dx.doi.org/10.12980/apjtd.7.2017D6-369]
, 10Khaleghizadehi A, Sehhatisabet ME. Avifaunal surveys of the Latian Dam and Lashgarak Area, an important IBA for migrants in Iran. Sandgrouse 2007; 29(1): 53.]. Co- transmission of USUV and WNV was reported in different countries, because of some bird/mosquito species are potential reservoirs/vectors for both viruses [5Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap? Trans R Soc Trop Med Hyg 2015; 109(10): 609-18.
[http://dx.doi.org/10.1093/trstmh/trv066] [PMID: 26286946]
]. Sero-survey of WNV in the equine populations in Iran indicated the circulation of the virus in southwestern provinces [11Ahmadnejad F, Otarod V, Fallah MH, et al. Spread of West Nile virus in Iran: a cross-sectional serosurvey in equines, 2008-2009. Epidemiol Infect 2011; 139(10): 1587-93.
[http://dx.doi.org/10.1017/S0950268811000173] [PMID: 21396143]
]. Common coot (Fulica atra) was reported as a competent host for WNV in Iran [12Fereidouni SR, Ziegler U, Linke S, et al. West Nile virus monitoring in migrating and resident water birds in Iran: are common coots the main reservoirs of the virus in wetlands? Vector Borne Zoonotic Dis 2011; 11(10): 1377-81.
[http://dx.doi.org/10.1089/vbz.2010.0244] [PMID: 21923253]
]. As Iran experiences regional climate change, mosquitoes are possible to flourish better through expected conditions. Mosquito vectors are ectothermic and are thus specifically susceptible to climatic factors. Survival, behavior, and reproduction of vectors are affected by weather conditions and it can strongly affect pathogen development within vectors and also influence the availability of breeding sites for culicid vectors, because of their immature aquatic stages [13Rogers DJ, Randolph SE. Climate change and vector-borne diseases. Adv Parasitol 2006; 62: 345-81.
[http://dx.doi.org/10.1016/S0065-308X(05)62010-6] [PMID: 16647975]
]. Therefore, the study on the dynamic of mosquitoes and surveillance for probable importation of vector-borne disease is essential.

Some culicid-borne viruses comprise the WNV‚ Sindbis virus‚ and the Dengue virus have been reported from Iran [14Chinikar S, Shah-Hosseini N, Mostafavi E, et al. Seroprevalence of West Nile virus in Iran. Vector Borne Zoonotic Dis 2013; 13(8): 586-9.
[http://dx.doi.org/10.1089/vbz.2012.1207] [PMID: 23697768]
, 15Naficy K, Saidi S. Serological survey on viral antibodies in Iran. Trop Geogr Med 1970; 22(2): 183-8.
[PMID: 4317129]
]. According to a report from WHO, the risk of Japanese encephalitis and Rift Valley fever in the Eastern Mediterranean Region, comprising Iran, is remarkable [16WHO. Integrated Vector Management 2004.]. Before USUV arrives in Iran, we should build upon information on the diversity of common mosquito’s species. For this reason, the present study aims to gather baseline data on species richness and diversity of potential vectors of USUV in Iran.

2. MATERIALS AND METHODS

2.1. Search Strategy

Electronic databases (PubMed, Scopus, Google Scholar, EMBASE, the Chinese National Knowledge Infrastructure database (CNKI), the Chinese Biological Medical Literature database (CBM), were searched with a date range from 2000 to 2018 to find the vector species that transmits the disease using the free combinations of the terms “Usutu virus,” “Mosquitoes,” and “Culex”.

2.2. Study Area

To develop the study, six sites were selected in the different areas [Urban Areas (UA), Rural Areas (RA) and uninhabited area (UNA)] of the north of Bushehr province (50° 31' 1E, 29° 34' 45N), in the Southwest of Iran. Two sites for each of these areas were selected. During this period of study (January – December 2017), maximum and minimum temperatures were 48 ˚C and 1˚C in July and February, respectively. The distance between urban and rural areas, uninhabited and rural areas and between urban and uninhabited areas were 30,17, and 12 km, respectively.

2.3. Sampling Methods and Taxonomic Identification

To study the ecology of mosquitoes, sampling was carried out by dipping technique with a metal dipper for collecting larvae. Four dips were taken from each breeding site (350 ml each). Larval investigation was conducted two times a month during the study period.

All samples were brought to the laboratory of the Entomology department, Tehran University of Medical Sciences, Iran. The mosquito larvae were preserved in 75% ethanol and the microscopic slides were prepared using the chloral gum mounting. The microscope was used for the taxonomic study and identification, up to the species level using taxonomic keys available in the literature [17Azari-Hamidian S, Harbach RE. Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa 2009; 2078(1): 1-33.
[http://dx.doi.org/10.11646/zootaxa.2078.1.1]
].

2.4. Biodiversity and Statistical Analysis

Diversity studies (alpha diversity) were conducted separately for each category (rural, urban and uninhabited areas) by calculating classic diversity indexes like Margalef’s (S-1) / lnN [S= total number of species and N= total number of individuals) and Simpson’s indexes (λ =1-Σpi2, where pi = ni/N [ni is the number of individuals of taxon i]) [18Jochmann R, Lipkow E, Blanckenhorn WU. A field test of the effect of spiked ivermectin concentrations on the biodiversity of coprophagous dung insects in Switzerland. Environ Toxicol Chem 2016; 35(8): 1947-52.
[http://dx.doi.org/10.1002/etc.3081] [PMID: 26013817]
]. Dominance = 1-Simpson index. Ranges from 0 (all taxa are equally present) to 1 (one taxon dominates the community completely). Shannon diversity index (H’ = -[Σ(pi lnpi)]) is commonly used to characterize species diversity in a community, accounting for both abundance and evenness of the species present [9Keshavarzi D, Soltani Z, Ebrahimi M, et al. Monthly prevalence and diversity of mosquitoes (Diptera&58; Culicidae) in Fars Province, Southern Iran. Asian Pac J Trop Dis 2017; 7(2): 112-20.
[http://dx.doi.org/10.12980/apjtd.7.2017D6-369]
, 18Jochmann R, Lipkow E, Blanckenhorn WU. A field test of the effect of spiked ivermectin concentrations on the biodiversity of coprophagous dung insects in Switzerland. Environ Toxicol Chem 2016; 35(8): 1947-52.
[http://dx.doi.org/10.1002/etc.3081] [PMID: 26013817]
]. The equitability index measures the evenness with which individuals are divided among the taxa present.

Jaccard’s and Whittaker indices were used to illustrate similarity and dissimilarity [18Jochmann R, Lipkow E, Blanckenhorn WU. A field test of the effect of spiked ivermectin concentrations on the biodiversity of coprophagous dung insects in Switzerland. Environ Toxicol Chem 2016; 35(8): 1947-52.
[http://dx.doi.org/10.1002/etc.3081] [PMID: 26013817]
]. Data were analyzed using PAST software version 3.14 (Paleontological Statistics Software Package). Non -parametric tests were used to evaluate differences in species abundances and weather-related variables between months.

3. RESULTS

3.1. Monthly Abundance

A total of 1369 specimens belonging to 10 different mosquito species were collected and identified. Viz.; Cx. hortensis Ficalbi, Cx. laticinctus Edwards, Cx. mimeticus Noe, Cx. perexiguus Theobald, Cx. pipiens Linnaeus, Cx. modestus Ficalbi, Cx. sinaiticus Kirkpatrick, Cx. theileri Theobald Cx. torrentium Martini, and Cx. tritaeniorhynchus Giles. Four species involved as vectors of USUV in other countries are printed in bold. Culex theileri (28.0%), Cx. pipiens (26.1%), Cx. tritaeniorhynchus (23.1%) were predominated, respectively. The greatest number of mosquitoes were collected from RA (723 specimens) and the lowest in the UA (209 specimens), Cx. pipiens and Cx. torrentium were more frequent in RA, while Cx. hortensis was only caught in UNA and Cx.perexigus was more frequent in UNA (Fig. 1). The greatest number of mosquitoes were collected in August (379) and September (370 specimens). Culex pipiens, Cx. torrentium,and Cx. hortensis were more active in Aguste, while Cx. perexigus was in October (Fig. 2). Depending on the month, the difference was not significant in mosquito abundances according to the Kruskal-Wallis test (P = 0.44). Analysis with Kruskal-Wallis and Mann-Whitney tests showed that the difference between environments (UA, RA, and UNA) and abundance of mosquitoes was not significant (P = 0.33). Overall, in the present study, there was a significant positive relationship between mean temperatures and abundance of mosquitoes (r = 0.75, P = 0.005). In contrast, abundance of mosquitoes decreased with increasing precipitation (r = - 0.42, P = 0.16).

Among the four species mentioned above, Cx. torrentium and Cx. hortensis prefers mostly permanent water resources without vegetation.

Fig. (1)
Abundance of Usutu virus potential vector species found in rural (RA), urban (UA), and uninhabited (UNA) areas in southwest Iran.


Fig. (2)
Monthly abundance of Usutu virus potential vector species in southwest Iran, in 2017. Notes: January (Jan)-February (Feb)-March (Mar)- April (Apr)- May (May)-June (Jun)- July (Jul)- August (Aug)- September (Sep)- October (Oct)- November (Nov)-December (Dec).


3.2. Mosquito Species Diversity

Greater species richness was found in RA (M=1/21), while UA has the lowest (M=0.93) (Table 1). The average diversity indices for the three environment types ranged from 1.50 to 1.64 for the Shannon index and from 0.730 to 0.738 for the Simpson index. Shannon index was highest in UNA and lowest in UA. While Simpson index in UA was highest (Table 1). The T-test showed no statistically significant difference between the Shannon index (t=1.17, p=0.24) and Simpson index (t=0.39, p=0.69) in RA and UA. Similarly, there was also no statistically significant difference between the Shannon index (t=-1.36, p=0.17) and Simpson index (t=0.20, p=0.83) in RA and UNA. But, there was a significant difference between the Shannon index in UNA and UA (t=-2.26, p=0.024). However, the difference between the Simpson index was not significant in these areas (t=-0.15, p=0.87). Greater evenness was observed in UA because the most dominant species do not show such a strong influence as in the two other environments. Where, Cx. theileri in UNA and Cx. pipiens and Cx. tritaeniorhynchus in RA were dominant and showed a strong influence.

The analysis of β biodiversity shows that RA and UNA are the closest categories in their specific composition (Whittaker index= 0.17), while UNA and UA are the farthest categories (Whittaker index= 0.28). Culex pipiens and Cx. torrentium share their larval habitatswith each other and similarity was more than 0.9 according to the Jaccard’s index, while Cx. hortensis had little similarity to other species.

Table 1
Alpha biodiversity estimators for rural (RA), urban (UA), and uninhabited (UNA) areas.


4. DISCUSSION

In the present investigation, 10 species of mosquitoes were identified. Among them, four species (Cx. pipiens, Cx. hortensis, Cx. torrentium, Cx.perexigus) involved as vectors of USUV in other countries [3Mannasse B, Mendelson E, Orshan L, et al. Usutu virus RNA in mosquitoes, Israel, 2014-2015. Emerg Infect Dis 2017; 23(10): 1699-702.
[http://dx.doi.org/10.3201/eid2310.171017] [PMID: 28930008]
, 6Nikolay B, Diallo M, Faye O, Boye CS, Sall AA. Vector competence of Culex neavei (Diptera: Culicidae) for Usutu virus. Am J Trop Med Hyg 2012; 86(6): 993-6.
[http://dx.doi.org/10.4269/ajtmh.2012.11-0509] [PMID: 22665607]
-8Jöst H, Bialonski A, Maus D, et al. Isolation of usutu virus in Germany. Am J Trop Med Hyg 2011; 85(3): 551-3.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0248] [PMID: 21896821]
, 19Reusken C, De Vries A, Ceelen E, et al. A study of the circulation of West Nile virus, Sindbis virus, Batai virus and Usutu virus in mosquitoes in a potential high-risk area for arbovirus circulation in the Netherlands,“De Oostvaardersplassen. Eur Mosq Bull 2011; 29: 66-81.].

Culex pipiens have two biotypes: the molestus and the pipiens, these two biotypes are morphologically indiscernible, both forms have been recorded from Iran [20Martínez-de la Puente J, Ferraguti M, Ruiz S, Roiz D, Soriguer RC, Figuerola J. Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malar J 2016; 15(1): 589.
[http://dx.doi.org/10.1186/s12936-016-1643-5] [PMID: 27931226]
, 21Amirkhanian JD. The salivary gland chromosomes of Culex pipiens molestus. Iranian J Publ Hlth 1974; 3: 40-54.]. The pipiens biotype feeds mainly on birds, prefer aboveground habitats and frequently found in rural areas [20Martínez-de la Puente J, Ferraguti M, Ruiz S, Roiz D, Soriguer RC, Figuerola J. Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malar J 2016; 15(1): 589.
[http://dx.doi.org/10.1186/s12936-016-1643-5] [PMID: 27931226]
, 22Fritz ML, Walker ED, Miller JR, Severson DW, Dworkin I. Divergent host preferences of above- and below-ground Culex pipiens mosquitoes and their hybrid offspring. Med Vet Entomol 2015; 29(2): 115-23.
[http://dx.doi.org/10.1111/mve.12096] [PMID: 25600086]
]. We found similar findings in our research, and this species mostly caught from rural areas with aboveground habitats. In the present study, Shannon and equitability indices show that in RA, Cx. pipiens intensely dominate the rest of the species present in the community. Something similar occurs in the case of UNA, where Cx. theileri develop a strong influence. Passer domesticus, Turdus migratorius, and Zenaida macroura are the most common feeding sources for Cx. pipiens [23Hamer GL, Kitron UD, Brawn JD, et al. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. J Med Entomol 2008; 45(1): 125-8.
[http://dx.doi.org/10.1093/jmedent/45.1.125] [PMID: 18283952]
]. Culex pipiens are considered as a major vector for USUV in Israel, Spain and Germany [3Mannasse B, Mendelson E, Orshan L, et al. Usutu virus RNA in mosquitoes, Israel, 2014-2015. Emerg Infect Dis 2017; 23(10): 1699-702.
[http://dx.doi.org/10.3201/eid2310.171017] [PMID: 28930008]
, 6Nikolay B, Diallo M, Faye O, Boye CS, Sall AA. Vector competence of Culex neavei (Diptera: Culicidae) for Usutu virus. Am J Trop Med Hyg 2012; 86(6): 993-6.
[http://dx.doi.org/10.4269/ajtmh.2012.11-0509] [PMID: 22665607]
-8Jöst H, Bialonski A, Maus D, et al. Isolation of usutu virus in Germany. Am J Trop Med Hyg 2011; 85(3): 551-3.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0248] [PMID: 21896821]
]. Co-occurrence of this virus and WNV in Cx. pipiens have been reported from Europe [5Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap? Trans R Soc Trop Med Hyg 2015; 109(10): 609-18.
[http://dx.doi.org/10.1093/trstmh/trv066] [PMID: 26286946]
, 7Vázquez A, Ruiz S, Herrero L, et al. West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. Am J Trop Med Hyg 2011; 85(1): 178-81.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0042] [PMID: 21734145]
]. The same reservoir and vector for both flaviviruses represent that USUV has the potential to import to other countries where only WNV exists. Therefore, Iran is in threat of entering because WNV has already been reported from the country [12Fereidouni SR, Ziegler U, Linke S, et al. West Nile virus monitoring in migrating and resident water birds in Iran: are common coots the main reservoirs of the virus in wetlands? Vector Borne Zoonotic Dis 2011; 11(10): 1377-81.
[http://dx.doi.org/10.1089/vbz.2010.0244] [PMID: 21923253]
]. Although no study has been conducted to verify the presence or absence of this virus in Iran.

The high temperature accompanied by rainfall is desirable for Cx. pipiens and affect on vector competence to WNV [24Bravo-Barriga D, Gomes B, Almeida APG, et al. The mosquito fauna of the western region of Spain with emphasis on ecological factors and the characterization of Culex pipiens forms. J Vector Ecol 2017; 42(1): 136-47.
[http://dx.doi.org/10.1111/jvec.12248] [PMID: 28504431]
]. Temporary water sources are its favor and could explain why this species is related to precipitation [25Roiz D, Vazquez A, Rosà R, et al. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol 2012; 37(1): 20-8.
[http://dx.doi.org/10.1111/j.1948-7134.2012.00196.x] [PMID: 22548533]
]. This is similar to the present study. Therefore, water resources are vital for both birds and Cx. pipiens and it may increase the risk of disease transmission [24Bravo-Barriga D, Gomes B, Almeida APG, et al. The mosquito fauna of the western region of Spain with emphasis on ecological factors and the characterization of Culex pipiens forms. J Vector Ecol 2017; 42(1): 136-47.
[http://dx.doi.org/10.1111/jvec.12248] [PMID: 28504431]
]. In the present study, we caught this species from March to December and a peak in Aguste was observed, when the mean temperature was 37.1˚C and there was no rain. However, in this research, the presence of irrigation canals had created favorable habitats.

Culex hortensis has been reported as another vector of USUV in Central Europe [19Reusken C, De Vries A, Ceelen E, et al. A study of the circulation of West Nile virus, Sindbis virus, Batai virus and Usutu virus in mosquitoes in a potential high-risk area for arbovirus circulation in the Netherlands,“De Oostvaardersplassen. Eur Mosq Bull 2011; 29: 66-81.]. This species feeds on both birds (ornithophilic) and reptiles (herpetophilic) [25Roiz D, Vazquez A, Rosà R, et al. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol 2012; 37(1): 20-8.
[http://dx.doi.org/10.1111/j.1948-7134.2012.00196.x] [PMID: 22548533]
]. This mosquito tends to grow in permanent water resources, in contrast to the Cx. pipiens species [25Roiz D, Vazquez A, Rosà R, et al. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol 2012; 37(1): 20-8.
[http://dx.doi.org/10.1111/j.1948-7134.2012.00196.x] [PMID: 22548533]
]. This is similar to the present study. The two above-mentioned mosquitoes had similar dynamics in Italy [25Roiz D, Vazquez A, Rosà R, et al. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol 2012; 37(1): 20-8.
[http://dx.doi.org/10.1111/j.1948-7134.2012.00196.x] [PMID: 22548533]
]. This is in contrast to our study and Cx.hortensis was caught only from July to September. The attempt to isolate WNV from Cx.hortensis in Iran was not successful, but it was detected from Ae. (Och.) caspius [26Bagheri M, Terenius O, Oshaghi MA, et al. West Nile virus in mosquitoes of Iranian wetlands. Vector Borne Zoonotic Dis 2015; 15(12): 750-4.
[http://dx.doi.org/10.1089/vbz.2015.1778] [PMID: 26565610]
]. Culex hortensis is an endemic species in Iran, and more studies are needed on its hosting preferences and other behavioral features.

Culex torrentium is an ornithophagous species and involved in the transmission of both WNV and USUV [8Jöst H, Bialonski A, Maus D, et al. Isolation of usutu virus in Germany. Am J Trop Med Hyg 2011; 85(3): 551-3.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0248] [PMID: 21896821]
, 27Balenghien T, Vazeille M, Grandadam M, et al. Vector competence of some French Culex and Aedes mosquitoes for West Nile virus. Vector Borne Zoonotic Dis 2008; 8(5): 589-95.
[http://dx.doi.org/10.1089/vbz.2007.0266] [PMID: 18447623]
]. According to several studies, this species breeding in artificial sites and found it to be more frequent in clean water to turbid breeding sites [28Weitzel T, Jawień P, Rydzanicz K, Lonc E, Becker N. Culex pipiens s.l. and Culex torrentium (Culicidae) in Wrocław area (Poland): occurrence and breeding site preferences of mosquito vectors. Parasitol Res 2015; 114(1): 289-95.
[http://dx.doi.org/10.1007/s00436-014-4193-1] [PMID: 25339516]
, 29Lühken R, Steinke S, Leggewie M, et al. Physico-chemical characteristics of Culex pipiens sensu lato and Culex torrentium (Diptera: Culicidae) breeding sites in Germany. J Med Entomol 2015; 52(5): 932-6.
[http://dx.doi.org/10.1093/jme/tjv070] [PMID: 26336210]
], which is supported by this study. This species may be sharing its larval habitatswith Cx. pipiens [29Lühken R, Steinke S, Leggewie M, et al. Physico-chemical characteristics of Culex pipiens sensu lato and Culex torrentium (Diptera: Culicidae) breeding sites in Germany. J Med Entomol 2015; 52(5): 932-6.
[http://dx.doi.org/10.1093/jme/tjv070] [PMID: 26336210]
]. This is similar to this study and similarity was more than 0.9 according to the Jaccard’s index.

Culex perexigus is considered a vector of both WNV and USUV [4Grottola A, Marcacci M, Tagliazucchi S, et al. Usutu virus infections in humans: a retrospective analysis in the municipality of Modena, Italy. Clin Microbiol Infect 2017; 23(1): 33-7.
[http://dx.doi.org/10.1016/j.cmi.2016.09.019] [PMID: 27677699]
]. It is a common species in Iran and breeding in a wide range of places such as seepages, irrigation ditches and temporary ponds [9Keshavarzi D, Soltani Z, Ebrahimi M, et al. Monthly prevalence and diversity of mosquitoes (Diptera&58; Culicidae) in Fars Province, Southern Iran. Asian Pac J Trop Dis 2017; 7(2): 112-20.
[http://dx.doi.org/10.12980/apjtd.7.2017D6-369]
]. In the present study, it was more frequent in clean and temporary water. Birds are favor for feeding of Cx.perexigus and it is more frequent between June and August in Spain, where both WNV and USUV have been reported [7Vázquez A, Ruiz S, Herrero L, et al. West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. Am J Trop Med Hyg 2011; 85(1): 178-81.
[http://dx.doi.org/10.4269/ajtmh.2011.11-0042] [PMID: 21734145]
]. This contrasts with our study, in the present study, Cx.perexigus showed two peaks in June and October, while it was not caught in August and July.

In the end, it can be said that species that have been introduced as a vector of virus are indigenous in Iran. Thus, isolation of the virus from the Fulica atra, other migratory birds, culicid species mentioned above and also Ae. (Och.) caspius is essential.

CONCLUSION

In our research, some possible vectors of USUV were identified. In the present study, Cx. pipiens as the main vector of the disease was more active between May and August. Potential reservoirs and vectors of USUV have been reported from Iran, therefore, the possibility of the emergence of the virus in Iran exists. Biodiversity analysis indicated that species diversity in rural, urban, and uninhabited areas is somewhat similar. Therefore, attention to all areas in vector control programs is essential.

ETHICAL APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.

HUMAN AND ANIMAL RIGHTS

Not applicable

CONSENT FOR PUBLICATION

Not applicable.

AVAILABILITY OF DATA AND MATERIALS

The datasets generated and/or analyzed during the current study are available at Baqiyatallah University of Medical Sciences at https://www.bmsu.ac.ir.

FUNDING

This study was financially supported by Baqiyatallah University of Medical Sciences (Project No.: 95-10-001069).

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

ACKNOWLEDGEMENT

We would like to thank “Clinical Research Development Center of Baqiyatallah Hospital” for their kind cooperation.

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