УДК 578.4(470.22)
ARTHROPOD-BORNE AND ARTHROPOD-RELATED VIRUSES
IN IRAN AND NEIGHBORING COUNTRIES
© 2023 S. Azari-Hamidiana,b*, R. E. Harbachc
aResearch Center of Health and Environment, School of Health,
Guilan University of Medical Sciences, Rasht, Iran
bDepartment of Medical Parasitology, Mycology and Entomology, School of Medicine,
Guilan University of Medical Sciences, Rasht, Iran
cDepartment of Life Sciences, Natural History Museum, London, UK
Correspondence: Prof. Dr. Shahyad Azari-Hamidian, Research Center of Health
and Environment, School of Health, Guilan University of Medical Sciences,
Rasht, Iran, P.O. Box: 3391, Rasht, Iran, Tel./Fax: 0098 13 33822877
The present article is dedicated to my wife Elaheh and my son Arvin who have patiently
supported me during my professional currier, especially providing this article
*e-mail: azari@gums.ac.ir
Received May 07, 2023
Revised August 30, 2023
Accepted September 20, 2023
Arthropods are very significant for human and veterinary medicine and health because of the
burden of diseases caused by the pathogens they transmit. Databases, including the Web of Science,
PubMed, Scopus, Google Scholar, CABI, Scientific Information Database, IranMedex and Magiran
were searched to the end of December 2022 for publications concerning infections in Iran caused
by arboviruses. Pertinent information was extracted and analyzed. Thirty-three viral infections occur
in Iran, which are biologically or mechanically known or assumed to be transmitted by arthropods.
Information about agents (viruses), distribution (in 31 Iranian provinces), hosts (human and animals)
and known vectors in Iran was obtained for each disease. Also, a list of arboviruses was provided for
the countries neighboring Iran, including Afghanistan, Armenia, Azerbaijan, Bahrain, Iraq, Kuwait,
Oman, Pakistan, Qatar, Saudi Arabia, Turkey, Turkmenistan and the United Arab Emirates, as well
as Djibouti, Somalia, Sudan, Syria and Yemen, which do not neighbor Iran but, like Iran, occur in
the World Health Organization Eastern Mediterranean Region. This list includes 40 viruses which
are not formally recorded in Iran. The viruses are members of 19 genera representing 14 families
in which three, four, 20 and 29 viruses are sandfly-borne, biting midge-borne, mosquito-borne and
tick-borne, respectively.
Keywords: arboviruses, biological transmission, mechanical transmission, mobovirus, reservoirs,
vectors, zoonoses
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DOI: 10.31857/S0031184723050010; EDN: PTKYLO
About 17% of the global burden of infectious and parasitic diseases is caused by
vector-borne pathogens. After lower respiratory infections, diarrhoeal diseases, HIV/AIDS
and tuberculosis, malaria displays the fifth highest burden among infectious and parasitic
diseases (World Health Organization, 2008). Traditionally, malaria and leishmaniasis are
major diseases in the World Health Organization (WHO) Eastern Mediterranean Region,
caused by vector-borne malarial protozoa (mosquito-borne) and trypanosomes (sandfly-
borne), respectively. Many other arthropod-borne viral (arboviral) infections, such as
Crimean-Congo hemorrhagic fever, dengue fever, Japanese encephalitis, Rift Valley fever,
sandfly fever, West Nile fever and yellow fever, are of lesser or more local importance
(World Health Organization, 2004). While, the burden of malaria has decreased and the
burden of leishmaniasis has not changed during recent years in the region (World Health
Organization, 2004, 2008, 2017), some arboviral infections, such as Crimean-Congo
hemorrhagic fever, Chikungunya fever, dengue fever, Rift Valley fever and West Nile
fever, which are classified as neglected, emerging or reemerging infectious diseases (EIDs
or RIDs), have been introduced into the region or Iran (World Health Organization, 2010;
Parhizgari et al., 2017; Pouriayevali et al., 2019). It has been estimated that the majority of
EIDs are zoonotic (60.3%) and 71.8% of these are caused by pathogens that originated from
wildlife, such as Ebola virus, Nipah virus and severe acute respiraotory syndrome (SARS)
virus. While 25.4% of EIDs are caused by viral and prion pathogens, 22.8% of EIDs
are vector-borne (Jones et al., 2008). Some arthropod-borne viruses (arboviruses) are not
pathogenic for humans but they are for domesticated animals; thus, they are very important
in view of food production and/or have economical importance because of loss of eggs,
milk or meat production, unhealthy offspring and loss of herds or fowl populations due to
diseases such as African horse sickness (Dennis et al., 2019), African swine fever (Dixon et
al., 2019), bluetongue (Maclachlan et al., 2015), bovine ephemeral fever (Walker, Klement,
2015), fowl pox (Della-Porta, 2001), rinderpest (Roeder et al., 2013) and Schmallenberg
virus infection (Collins et al., 2019). Also, the possible use of some arthropods infected with
certain arboviruses as weapons or bioterrorism is mentioned in published literature, such
as mosquitoes infected with dengue, Rift Valley fever and yellow fever viruses and ticks
infected with Colorado fever and Crimean-Congo hemorrhagic fever viruses (Lockwood,
2012). There are more than 600 known arboviruses (Conway et al., 2014) and about 100
of these infect humans and some 40 infect livestock (Hart, 2001). Fifty arboviruses are
known to cause disease in homeotherm (endotherm) wild and domestic mammals and birds
(Hubálek et al., 2014a).
Iran is located in the Middle East and southwestern Asia where the Afrotropical,
Oriental and Palaearctic Regions converge. Iran is connected with Central Asia through
Turkmenistan in the northeast, with southern Asia and the Oriental Region through Pakistan
in the southeast and with the Afrotropical Region through the Arabian Peninsula in the
south. For this reason, the region is interesting in view of biodiversity while at the same
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time complicating interventions for vector control and integrated vector management (IVM)
aimed at reducing the transmission of vector-borne pathogens and parasites and the burden
of diseases. Iran also resides in the WHO Eastern Mediterranean Region along with 21
other countries: Afghanistan, Bahrain, Djibouti, Egypt, Iraq, Jordan, Kuwait, Lebanon,
Lybia, Morocco, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, Somalia, Sudan, Syria,
Tunisia, the United Arab Emirates and Yemen (World Health Organization, 2004).
There are some recent and useful reviews of different arboviruses that occur in some
of the aforementioned countries, such as Failloux et al. (2017) who reviewed arboviruses
in the Mediterranean and Black Sea Regions, Atkinson and Hewson (2018) who reviewed
arboviruses in Central Asia and Braack et al. (2018) who reviewed mosquito-borne viruses
(moboviruses) in Africa. Also, there are some useful reviews on specific infections that
occur in the region, such as African horse sickness (Dennis et al., 2019), African swine
fever (Dixon et al., 2019), Akabane virus infection (Kirkland, 2015), Bhanja virus infection
(Hubálek, 1987), bluetongue virus infection (Maclachlan et al., 2015), bovine ephemeral
fever (Walker, Klement, 2015), bovine herpes (Chatterjee et al., 2016), Chikungunya virus
infection (Silva et al., 2018), Crimean-Congo hemorrhagic fever (Nasirian, 2019), Hantaan
virus infection (Bi et al., 2008), Rift Valley fever (Kenawy et al., 2018), rinderpest (Roeder
et al., 2013), sandfly fever (Depaquit et al., 2010), Schmallenberg virus infection (Collins
et al., 2019), West Nile fever (Eybpoosh et al., 2019) and Zika virus infection (Epelboin
et al., 2017), as well as reviews for specific countries, such as Afghanistan (Wallace et al.,
2002), Pakistan (Hayes, Burney, 1981), Sudan (Ahmed et al., 2020) and Turkey (Ergunay
et al., 2011; Inci et al., 2013, 2016, 2018; Düzlü et al., 2020).
Recently, Azari-Hamidian et al. (2019) reviewed 14 mosquito-borne pathogens and
parasites in Iran, including six viral infections (avian or fowl pox, bovine ephemeral
fever, dengue, Rift Valley fever, Sindbis and West Nile fever), two bacterial infections
(anthrax and tularemia), four helminthoses (Deraiophoronema evansi infection, dirofilariasis,
lymphatic filariasis and setariasis) and two protozoal infections (avian and human malarias)
and updated the checklist of Iranian mosquitoes. Also, Parhizgari et al. (2021) reviewed
some selected diseases in Iran caused by vector-borne pathogens. They reviewed, for
example, four arboviruses: Crimean-Congo hemorrhagic fever, dengue fever, sandfly fever
and West Nile fever.
In the present article, we provide a comprehensive review of infections caused by
arboviruses in Iran. We also provide a list of arboviruses in the countries neighboring
Iran, as well as Djibouti, Somalia, Sudan, Syria and Yemen, which, like Iran, located in
the WHO Eastern Mediterranean Region, and have not received much attention in recent
reviews of arboviruses (Failloux et al., 2017; Braack et al., 2018). Thus, the present review
includes 19 countries. Additionally, it includes some viruses that are not (true) arboviruses
or are arthropod-related viruses which arthropods may mechanically transmit to humans
and domestic animals, and were not included in the aforementioned reviews of arboviruses.
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METHODS
Iran, with an area of approximately 1,648,195 km2, is located between 25-40o N latitude
and 44-63o E longitude and formally includes 31 provinces (Fig. 1). Iran is bordered by
Armenia, Azerbaijan and Turkmenistan in the north, Afghanistan and Pakistan in the east,
Iraq and Turkey in the west and the Persian Gulf and Oman Sea in the south, across
which lie the countries of Bahrain, Kuwait, Oman, Qatar, Saudi Arabia and the United
Arab Emirates. Hereafter, Iran, the aforementioned countries and five countries of the
WHO Eastern Mediterranean Region, including Djibouti, Somalia, Sudan, Syria and Yemen,
are referred to as “the region”. Most parts of Iran and many countries in “the region”
have arid climate based on different climate classifications. This investigation is based on
publications listed in the Web of Science (Clarivate), PubMed, Scopus, Google Scholar,
CABI, Scientific Information Database (SID), IranMedex and Magiran databases prior
to December 2022. Firstly, principal textbooks on medical and veterinary entomology
(for example Harwood, James, 1979; Lane, Crosskey, 1993; Mullen, Durden, 2019) were
reviewed for information on diseases caused by arboviruses. Secondly, we searched the
aforementioned databases using terms such as “arthropod-borne diseases”, “arboviruses”,
“mosquito-borne viruses” and “moboviruses” to identify the names of viral infections
associated with arthropods. Afterwards, the databases were searched to obtain literature
reporting the occurrence of those diseases in animals and humans in Iran, Central Asia,
the Middle East, southwestern Asia and the WHO Eastern Mediterranean Region (Harbach,
1988; World Health Organization, 2004). Finally, the searches were conducted using the
keywords “extracted arthropod-borne viral disease names, Iran, Iranian” and “extracted
arthropod-borne virus names, Iran, Iranian”. Also, the searches were conducted with the
names of the countries neighboring Iran and the five additional countries of the WHO
Eastern Mediterranean Region. The names of diseases or infections comprised more than
73 keywords (names or terms) which were mentioned in the search results (Table 1,
Fig. 2). It should be mentioned that there were more than one name or term for some
infections or diseases. The generic names of arthropod-borne and arthropod-related viruses
included Alphavirus, Asfavirus, Avipoxvirus, Bandavirus, Capripoxvirus, Deltaretrovirus,
Ephemerovirus, Flavivirus, Lentivirus, Morbillivirus, Orbivirus, Orthobunyavirus,
Orthohantavirus, Orthonairovirus, Phlebovirus, Thogotovirus, Varicellovirus, Vesiculovirus
and Zamolirhabdovirus. Additionally, references cited in the retrieved publications were
also reviewed to increase the coverage of the literature. Likewise, unpublished documents
such as the Centers for Disease Control and Prevention (CDC) Arthropod-Borne Virus
coverage. With few exceptions, only information obtained from books and peer-reviewed
articles was used to prepare this review. Information about infectious agents (viruses),
distribution (in 31 Iranian provinces) (Fig. 1), reservoirs or hosts (human and animals) and
known vectors in Iran was obtained for each infection. Six mosquito-borne viral infections,
which were recently reviewed by Azari-Hamidian et al. (2019), were mentioned only for
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distributional records in the region or possible new data in Iran. Maes et al. (2018) was
consulted for the latest classification of arboviruses of the order Bunyavirales. The capital
letter abbreviations used for the names of viruses are based on the “International catalog
of arboviruses including certain other viruses of vertebrates” (available at https://wwwn.
cdc.gov/arbocat/VirusBrowser.aspx). There is one exception: all sandfly-borne phleboviruses
were mentioned in one keyword “Sandfly fever”. Those are abbreviated SFN-SV because
the most common viruses among them are Naples (SFNV) and Sicilian (SFSV) viruses,
and also to distinguish them from Semliki Forest virus (SFV). Also, sheep pox virus (SPV)
and goat pox virus (GPV) were mentioned in one search result. Though they are different
viruses, their clinical diseases are similar. The abbreviations of mosquito and sandfly genera
and subgenera follow Reinert (2009) and Galati et al. (2017), respectively. For the valid
species names of different arthropod taxa, the following references and webpages were
consulted: biting midges (Borkent, Dominiak, 2020), horseflies (Moucha, 1976), mosquitoes
(Azari-Hamidian et al., 2019, 2020; Harbach, 2023), sandflies (Secombe et al., 1993) and
ticks (Gugliemone et al., 2010, 2014; Hosseni-Chegeni et al., 2019).
Figure 1. Map of Iran and its 31 provinces.
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Figure 2. Map showing the arthropod-borne and arthropod-related viruses in the countries
included in the present review and the highlighted countries of the World Health Organization
Eastern Mediterranean Region. Abbreviations for viruses: AH = Abu Hammad, AHS = African
horse sickness, AINO = Aino, AKA = Akabane, AMT = Arumowot, ARTS = Artashat,
ASF = African swine fever, BAK = Bakau, BAKU = Baku, BAN = Banzi, BAR = Barur,
BAT = Batai, BEF = Bovine ephemeral fever, BHA = Bhanja, BH = Bovine herpes,
BJ = Barkedji, BKN = Batken, BL = Bovine leukemia, BLU = Bluetongue, CAS = Caspiy,
CCHF = Crimean-Congo hemorrhagic fever, CHIK = Chikungunya, CNU = Chenuda,
DEN = Dengue, DGK = Dera Ghazi Khan, DHO = Dhori, EHD = Epizootic haemorrhagic
disease, EIA = Equine infectious anaemia, FP = Fowl pox, GA = Grand Arbaud, GF = Gabek
Forest, GER = Geran, HAZ = Hazara, HTN = Hantaan, ISF = Isfahan, ISK = Issyk-Kul,
ITM = Israel turkey meningoencephalitis, JE = Japanese encephalitis, KAD = Kadam,
KFD = Kyasanur Forest disease, KSI = Karshi, LI = Louping ill, LSD = Lumpy skin disease,
MAL = Malakal, MWA = Manawa, NRI = Ngari, NSD = Nairobi sheep disease,
OBO = Obodhiang, ONN = O'nyong-nyong, PAL = Palyam, QRF = Quaranfil, RAZ = Razdan,
RF = Royal farm, RP = Rinderpest, RVF = Rift Valley fever, SB = Schmallenberg,
SFN-S = Sandfly fever, SF = Semliki Forest, SIN = Sindbis, SP-GP = Sheep pox-goat pox,
TAH = Tahyna, TBE = Tick-borne encephalitis, TDY = Tamdy, THO = Thogoto, USU = Usutu,
UUK = Uukuniemi, WAN = Wanowrie, WM = Wad Medani, WN = West Nile, YF = Yellow
fever, ZAR = Zahedan rhabdovirus, ZIKA = Zika, ZIR = Zirqa.
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Viruses
Iran
Afghanistan
Armenia
Azerbaijan
Bahrain
Djibouti
Iraq
Kuwait
Oman
Pakistan
Qatar
Saudi Arabia
Somalia
Sudan
Syria
Turkey
Turkmenistan
UAE
Yemen
Viruses
Iran
Afghanistan
Armenia
Azerbaijan
Bahrain
Djibouti
Iraq
Kuwait
Oman
Pakistan
Qatar
Saudi Arabia
Somalia
Sudan
Syria
Turkey
Turkmenistan
UAE
Yemen
Viruses
Iran
Afghanistan
Armenia
Azerbaijan
Bahrain
Djibouti
Iraq
Kuwait
Oman
Pakistan
Qatar
Saudi Arabia
Somalia
Sudan
Syria
Turkey
Turkmenistan
UAE
Yemen
Viruses
Iran
Afghanistan
Armenia
Azerbaijan
Bahrain
Djibouti
Iraq
Kuwait
Oman
Pakistan
Qatar
Saudi Arabia
Somalia
Sudan
Syria
Turkey
Turkmenistan
UAE
Yemen
Infections in Iran caused by arthropod-borne viruses or the viruses
which may be mechanically transmitted by arthropods
Asfaviridae
African swine fever
African swine fever is caused by the African swine fever virus (ASFV) (Asfaviridae:
Asfavirus), the only DNA arbovirus that is pathogenic for animals. There are four antigenic
types and 22 genotypes of ASFV. The disease occurs in Africa, America, Asia and Europe.
Infections occur in Armenia and Azerbaijan. The virus infects all members of the pig
family (Suidae). The disease is transmitted via direct route and also by the bite of soft ticks
of the genus Ornithodoros (Parasitiformes: Argasidae) (Gibbs, 2001; Labuda, Nuttall,
2008; Hubálek, Rudolf, 2012; Vlasova et al., 2012; Hubálek et al., 2014a; Beltrán-Alcrudo
et al., 2017; Dixon et al., 2019). The principal vectors are O. erraticus (Lucas), species
of the O. moubata (Murray) complex (such as O. moubata and O. porcinus Walton),
O. savignyi (Audouin) and O. sonrai Sautet et Witkowski in Africa, O. erraticus in Europe
and O. coriaceus Koch, O. puertoricensis Fox and O. turicata (Dugès) in the Americas.
Transovarial, transstadial and sexual (venereal) transmission of the virus occur throughout
the life of the ticks (Plowright et al., 1970; Hoogstraal, 1985; Hess et al., 1987; Gibbs, 2001;
Boinas et al., 2004, 2011; de la Fuente et al., 2008; Ravaomanana et al., 2010; Gallardo
et al., 2011; Hubálek et al., 2014a; Beltrán-Alcrudo et al., 2017). There is some evidence
that the stable fly Stomoxys calcitrans (Linnaeus) (Diptera: Muscidae) may be involved
in mechanical transmission while feeding, or infection is due to ingestion of an infected
fly by the host (Mellor et al., 1987; Baldacchino et al., 2013; Olsen et al., 2018a, b).
The virus has been found in wild boars in East and West Azerbaijan Provinces of Iran
(Rahimi et al., 2010; Beltrán-Alcrudo et al., 2017). At least 11 species of soft ticks,
including four species of Ornithodoros, one being O. erraticus, occur in Iran (Hosseni-
Chegeni et al., 2019; Hosseini-Chegeni, Tavakoli, 2020), however there is no information
about the vector(s) of the virus in the country.
Flaviviridae
Dengue fever
Dengue fever, caused by the dengue fever virus (DENV) (Flaviviridae: Flavivirus),
was reviewed by Azari-Hamidian et al. (2019). Some published documents which might
be added to the Iranian literature are Baniasadi et al. (2016), Salehi-Vaziri et al. (2016),
Heydari et al. (2018), Tavakoli et al. (2020) and Firooziyan et al. (2022). The virus has
also been found in Afghanistan (Arsenʼeva, 1982; Wallace et al., 2002; Elyan et al., 2014),
Djibouti (World Health Organization, 2004; Andayi et al., 2014; Braak et al., 2018), Kuwait
(Mustafa et al., 2001; Pacsa et al., 2003), Oman (Al-Abri et al., 2015), Pakistan (Hayes,
Burney, 1981; World Health Organization, 2004; Afzal et al., 2015; Khan et al., 2016;
Yaqub et al., 2017; Ahmad et al., 2020), Qatar (Humphrey et al., 2019), Saudi Arabia
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(World Health Organization, 2004; Khan et al., 2008; Zaki et al., 2008; Memish et al., 2011;
Shibl et al., 2012; Ahmed, 2015), Somalia (Oldfield et al., 1993; World Health Organization,
2004; Braak et al., 2018), Sudan (Watts et al., 1994; World Health Organization, 2004;
Farnon et al., 2010; Braak et al., 2018; Ahmed et al., 2020), Turkey (Ergunay et al., 2011)
and Yemen (World Health Organization, 2004; Shibl et al., 2012; Ciccozzi et al., 2014;
Rezza et al., 2014; Alghazali et al., 2019; Al-Samadi, Ali, 2020; Abdul-Ghani et al., 2021).
There are no recent reports of Aedes aegypti (Linnaeus) [Stegomyia aegypti] (Diptera:
Culicidae), the main vector, in Iran (Azari-Hamidian et al., 2019). The other important
vector, Ae. albopictus Skuse [Stegomyia albopicta], was recorded just one time in Iran
based on five larvae and six adults found in Sistan and Baluchistan Province (Doosti
et al., 2016). The species has not been recorded since and there is no evidence for
indigenous transmission of DENV in the country.
Japanese encephalitis
Japanese encephalitis, caused by the Japanese encephalitis virus (JEV) (Flaviviridae:
Flavivirus), is known from Asia and Australia. The virus has been isolated from different
domesticated and wild mammals, such as bats, cattle, dogs, donkeys, monkeys, horses,
pigs, rodents and water buffaloes, and also birds, including chickens, ducks, egrets, herons
and water hens; however, important amplifying hosts in the epidemiology of the disease
seem to be pigs and aquatic birds. The virus has been identified in different mosquito
species of the genera Aedes, Anopheles, Armigeres, Culex and Mansonia, however the
most important vector is Culex tritaeniorhynchus Giles, the rice field mosquito. Vertical
(transovarial) transmission and sexual (venereal) transmission are also known for mosquito
vectors (Barrett, 2001; Hubálek et al., 2014a; Gould et al., 2017). The virus has also
been isolated from the biting midge Forcipomyia (Lasiohelea) taiwana Shiraki (Diptera:
Ceratopogonidae) (Linley et al., 1983) and the hard ticks Dermacentor marginatus (Sulzer)
(Parasitiformes: Ixodidae) and Ixodes ricinus (Linnaeus), as reported by Anastos (1957).
Also, Hoogstraal (1966) listed a number of hard tick species of the genera Dermacentor,
Ixodes, Haemaphysalis, Hyalomma and Rhipicephalus which might serve as JEV hosts
in nature. The virus is known in Pakistan and is suspected to be present in Afghanistan
(Arsen'eva, 1982; Darwish et al., 1983a; Igarashi et al., 1994; Wallace et al., 2002; World
Health Organization, 2004; Khan et al., 2016). Also, one febrile patient who entered
China from Bahrain was positive for JEV-specific IgM antibody (Shi et al., 2016).
Japanese encephalitis virus has been isolated from a number of mosquitoes, including
Aedes albopictus, Ae. curtipes (Edwards) [Cancraedes curtipes], Ae. vexans (Meigen)
[Aedimorphus vexans], Anopheles barbirostris van der Wulp, An . sinensis Wiedemann,
An. subpictus Grassi s. l., An. vagus Dönitz, Armigeres obturbans (Walker), Ar. subalbatus
(Coquillett), Culex annulus Theobald, Cx. annulirostris Skuse, Cx. bitaeniorhynchus Giles,
Cx. epidesmus Theobald, Cx. fuscocephala Theobald, Cx. gelidus Theobald, Cx. modestus
Ficalbi, Cx. pipiens Linnaeus, Cx. pseudovishnui Colless, Cx. quinquefasciatus Say,
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Cx. sitiens Wiedemann, Cx. theileri Theobald, Cx. vishnui Theobald, Cx. whitmorei (Giles),
Mansonia annulifera (Theobald), Ma. bonneae Edwards, Ma. dives (Schiner), Ma. indiana
Edwards and Ma. uniformis (Theobald), according to Simpson et al. (1970, 1974), Peiris
et al. (1994), Reuben et al. (1994), Dhanda et al. (1997), Barrett (2001) and Wang et al.
(2007). According to unpublished data in Iran, the antibodies for the virus have been found
in humans (3.4%) using the neutralization test (the CDC Arthropod-Borne Virus Information
published documentation about the occurrence of the virus in the country. The main vector,
Culex tritaeniorhynchus, has been found in at least 17 Iranian provinces (Zaim, 1987;
Sofizadeh et al., 2018). The species is very abundant in three northern provinces, Golestan,
Guilan and Mazandaran, with vast rice fields (Azari-Hamidian et al., 2018; Nikookar
et al., 2018; Sofizadeh et al., 2018). Other mosquito species in Iran from which the virus
has been isolated elsewhere include Aedes albopictus, Culex bitaeniorhynchus, Cx. pipiens,
Cx. pseudovishnui, Cx. quinquefasciatus, Cx. sitiens, Cx. theileri and Mansonia uniformis
(Reuben et al., 1994; Barrett, 2001; Wang et al., 2007; Azari-Hamidian et al., 2019, 2020).
Also, the aforementioned hard ticks occur in Iran (Hosseni-Chegeni et al., 2019).
Tick-borne encephalitis
Tick-borne encephalitis, caused by tick-borne encephalitis virus (TBEV) (Flaviviridae:
Flavivirus), has been found in Asia and Europe. TBEV is the most important tick-borne
pathogenic flavivirus in humans. The virus consists of three subtypes, also called clusters,
including the western European subtype (formerly central European encephalitis virus -
CEEV), the Siberian subtype (formerly West Siberian encephalitis virus - WSEV) and
the far-eastern subtype (formerly Russian spring-summer encephalitis virus - RSSEV).
The main reservoirs of the virus are small mammals, such as rodents and insectivores,
and some wild carnivores, such as foxes, however the virus has also been isolated from
chamois (Rupicapra rupicapra), dogs, horses and sheep. The main route of transmission
is the bite of hard ticks; however, some local epidemics have been caused by consumption
of unpasteurized milk or milk products. Ixodes ricinus is the main vector in Europe
(the western European subtype) and I. persulcatus Schulze is the main vector in Asia
(the Siberian and the far-eastern subtypes). Transovarial and transstadial transmission have
been observed in both main vectors (Heinz, Holzmann, 2001; de la Fuente et al., 2008;
Labuda, Nuttall, 2008; Wójcik-Fatla et al., 2011; Hubálek, Rudolf, 2012; Valarcher et al.,
2015). According to Anastos (1957), TBEV [as (Russian) spring-summer encephalitis virus]
has been isolated, in addition to Ixodes ricinus and I. persulcatus, from the following ticks
(in the former USSR): Dermacentor marginatus, D. nuttalli Olenev, D. silvarum Olenev,
Haemaphysalis concinna Koch, H. japonica Warburton, Hyalomma dromedarii Koch,
H. excavatum Koch and Ixodes trianguliceps Birula. Additionally, the virus has been isolated
from Dermacentor reticulatus (Fabricius) in Germany (Chitimia-Dobler et al., 2019),
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Poland (Wójcik-Fatla et al., 2011) and Russia (Kislenko et al., 1987), Ixodes hexagonus
Leach in the Czech Republic (Krivanec et al., 1988) and Croatia (Jemeršić et al., 2014),
Haemaphysalis punctata Canstrini et Fanzago in the Czech Republic (Hubálek et al., 1989),
Ixodes ovatus Neumann in Japan (Takeda et al., 1998), Haemaphysalis flava Neumann,
H. japonica, H. longicornis Neumann and I. nipponensis Kitaoka et Saito in South Korea
(Kim et al., 2009; Yun et al., 2012), Hyalomma marginatum Koch in Crimea (Hubálek,
Rudolf, 2012), Ixodes gibbosus Nuttall in the Mediterranean (Hubálek, Rudolf, 2012),
Dermacentor silvarum, Ixodes pavlovskyi Pomerantzev and I. lividus Koch (as I. plumbeus
Leach) in Russia (Mikryukova et al., 2014; Pukhovskaya et al., 2018). Also, TBEV has
been shown experimentally to be vectored by Dermacentor marginatus, Haemaphysalis
inermis Birula and Ixodes arboricola Schulze et Schlottke (Lichard, Kozuch, 1967; Nosek
et al., 1972; Nosek, Kožuch, 1985). The virus has also been isolated from fleas, including
Ceratophyllus indages (Rothschild) (synonym: Ceratophyllus tamias Wagner) (Siphonaptera:
Ceratophyllidae), Palaeopsylla soricis (Dale) (Siphonaptera: Hystrichopsyllidae), gamasid
mites (Federov et al., 1959; Sotnikova, Soldatov, 1964; Naumov, Gutova, 1984),
the horsefly Hybomitra lundbecki Lynborg (Diptera: Tabanidae) (Krinsky, 1976), the poultry
red mite Dermanyssus gallinae (De Geer) (Mesostigmata: Dermanyssidae) (Sparagano et al.,
2014) and the mosquito Aedes vexans (Pukhovskaya et al., 2018). The virus has been found
in Afghanistan, Armenia, Azerbaijan, Djibouti, Turkey and Turkmenistan (Gromashevsky,
Nikimorov, 1973; Heinz, Holzmann, 2001; de la Fuente et al., 2008; Ergunay et al., 2011;
Inci et al., 2013, 2016; Elyan et al., 2014; Failloux et al., 2017; Atkinson, Hewson, 2018;
Im et al., 2020). The disease was recently recorded in Mazandaran Province of northern
Iran using ELISA. Among 448 serum samples, 3.6% were positive (Salehi-Vaziri et al.,
2020). There is no information about the vector(s) in Iran, however Ixodes ricinus,
the main vector, is a prevalent hard tick in northern areas of the country, especially
the Caspian Sea littoral. Dermacentor marginatus, Haemaphysalis concinna, H. inermis,
H. punctata, Hyalomma dromedarii, H. excavatum and H. marginatum also occur in Iran
(Rahbari et al., 2007; Hosseni-Chegeni et al., 2019).
West Nile fever
West Nile fever, caused by West Nile fever virus (WNV) (Flaviviridae: Flavivirus)
(synonyms or subtypes: Kunjin and Rabensburg viruses), was reviewed for Iran by Azari-
Hamidian et al. (2019) and for the WHO Eastern Mediterranean Region by Eybpoosh
et al. (2019). Information in the following publications might be added to those reviews:
Shamsizadeh et al. (2015), Shahhosseini, Chinikar (2016), Ziyaeyan et al. (2018), Adham
et al. (2019), Amini et al. (2019), Amini et al. (2020), Dehghani et al. (2020), Shahhosseini
et al. (2020), Bakhshi et al. (2021) and Staji et al. (2021). The virus has also been found in
Afghanistan (Arsenʼeva, 1982; Wallace et al., 2002; Elyan et al., 2014), Armenia (Failloux
et al., 2017), Azerbaijan (Gromashevsky, Nikimorov, 1973; Mirzoeva et al., 1974), Djibouti
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(Andayi et al., 2014), Iraq (Barakat et al., 2016), Pakistan (Hayes, Burney, 1981; Hayes
et al., 1982; Reisen et al., 1982; Darwish et al., 1983a; Sugamata, 1988; Sugamata et al.,
1988; Igarashi et al., 1994; Bryan et al., 1996; Zohaib et al., 2015; Khan et al., 2016;
Niazi et al., 2017; Yaqub et al., 2017), Qatar (DeCarlo et al., 2017; Dargham et al.,
2021), Saudi Arabia (Al-Ghamdi, 2014; Hemida et al., 2019; Alqahtani, 2020), Somalia
(Henderson et al., 1968; Cahill, 1971; Oldfield et al., 1993), Sudan (Salim, Porterfield,
1973; Watts et al., 1994; McCarthy et al., 1996; Depoortere et al., 2004; Farnon et al.,
2010; Yousof et al., 2018; Ahmed et al., 2020), Syria (Azmi et al., 2017), Turkey (Inci et
al., 2013; Failloux et al., 2017; Düzlü et al., 2020; Yildirim et al., 2021), Turkmenistan
(Atkinson, Hewson, 2018), the United Arab Emirates (Wernery et al., 2007; Alfaresi,
Elkoush, 2008) and Yemen (Qassem, Jaawal, 2014). Three mosquito species are known
vectors of WNV in Iran: Aedes caspius (Pallas) s. l. [Ochlerotatus caspius s. l.] (Bagheri
et al., 2015), Culex pipiens (Shahhosseini et al., 2017) and Cx. theileri (Shahhosseini
et al., 2020). Other species which are known principal vectors in other countries that also
occur in Iran include Aedes albopictus, Coquillettidia richiardii (Ficalbi), Cx. modestus,
Cx. perexiguus Theobald, Cx. pipiens, Cx. quinquesfasciatus, Cx. tritaeniorhynchus and
Mansonia uniformis (see Hubálek et al., 2014a; Azari-Hamidian et al., 2019, 2020).
Hantaviridae
Hantaan infection
Hantaviruses (Hantaviridae: Orthohantavirus), which cause haemorrhagic fever with
renal syndrome (HFRS) in the Old World and hantavirus pulmonary syndrome (HPS) or
hantavirus cardiopulmonary syndrome (HCPS) in the New World, are distributed worldwide.
The main reservoirs of rural epidemiological pattern are the rodents of the genera Apodemus
and Clethrionomys in Asia and Europe and Microtus and Peromyscus in the Americas,
whereas in urban pattern domestic rodents (Rattus species) are reservoirs and in animal
houses (vivaria) colonized experimental rats are reservoirs. The viruses that cause HFRS in
the Old World include Dobrava (DOBV), Hantaan (HTNV), Puumala (PUUV), Saaremaa
(SAAV) and Seoul (SEOV). Dobrava virus is found primarily in the Balkans. Haantan virus
is widely distributed in eastern Asia, particularly in China, Russia and Korea. Puumala virus
is found in Scandinavia, western Europe and western Russia. Saaremaa is found in central
Europe and Scandinavia. Seoul virus is found worldwide. The virus is usually transmitted
by contamination of wounds by the saliva, urine or faeces of rodents or by rodent bite
(Xu, 2001; Bi et al., 2008; Zowghi et al., 2008; Kassiri, Dehghani, 2020). The virus has
been found in Kuwait (Pacsa et al., 2002, 2003), Sudan (Ibrahim et al., 2017) and Turkey
(Oncul et al., 2011; Gozalan et al., 2013). There is some evidence for transmission of the
virus by the tropical rat mite Ornithonyssus bacoti (Hirst) (Mesostigmata: Macronyssidae),
trombiculid mites (Prostigmata: Trombiculidae), such as Eutrombicula splendens (Ewing),
Leptotrombidium scutellare (Nagayo, Miyagawa, Mitamura, Tamiya et Tenjin), L. subpalpale
Vercammen-Grandjean et Langston, an unidentified ixodid tick (Houck et al., 2001; Xu,
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2001) and the gamasid mites Haemolaelaps glasgowi (Ewing) and Eulaelaps stabularis
(Koch) (Mesostigmata: Haemogamasidae) (Li, 1986). The first verified record of Hantaan
virus in Iran was among street cleaners (4.5%) in Isfahan Province using ELISA and
molecular tests as an EID (Chinikar et al., 2014). Later, positive sera were detected in
10 provinces of the country, East Azerbaijan, Fars, Ilam, Isfahan, Kerman, Mazandaran,
Razavi Khorasan, South Khorasan, Tehran and Yazd, based on the results of ELISA (Salehi-
Vaziri et al., 2019, 2021). Parhizgari et al. (2017) recognized the disease in Iran as an
EID, and it was reviewed by Kassiri and Dehghani (2020). However, the aforementioned
references mentioned that IgG to hantaviruses has been identified in Iran, which are genus-
specific due to the close antigenic relationship of the Old World hantaviruses causing HFRS.
In fact, HFRS is caused by various hantaviruses, not necessarily by Hantaan. The Hantaan
virus itself circulates in the Far East and is unlikely to be detected in Iran. Ornithonyssus
bacoti has been found on various rodents in different areas of Iran (Kamali et al., 2001)
and at least 85 species of the mite family Trombiculidae are known to be present in the
country (Stekolnikov et al., 2019), however there is no information about the possible role
of mites in the transmission of Hantaan virus in Iran.
Herpesviridae
Bovine herpes
Bovine herpes, caused by the bovine herpes virus (BHV) (Herpesviridae: Varicellovirus),
has a worldwide distribution. The virus has been found in different wild and domesticated
ruminants, especially camels, cattle, goats and sheep. The disease generally displays two
clinical syndromes, respiratory and genital. The disease causes significant financial losses
because of a drop in milk production, abortion and deaths in cattle. The virus is mostly
transmitted through respiratory infection and less importantly via genital tract infection
(Wentink et al., 1993; Chatterjee et al., 2016). However, there is some evidence that the
stable fly Stomoxys calcitrans, the face fly Musca autumnalis De Geer (Diptera: Muscidae)
and the soft tick Ornithodoros coriaceus may be involved in mechanical transmission
(Gibbs et al., 1972, 1973a, b; Taylor et al., 1982; Johnson et al., 1991; Baldacchino et al.,
2013). Bovine herpes virus has been found in Oman (Hedger et al., 1980). The virus has
been detected in bufalloes, camels, cattle, dogs, horses, humans, Indian gazelles and pigs,
using serological and molecular tests, in the following provinces of Iran: Chaharmahal
and Bakhtiari, Fars, Guilan, Hamedan, Isfahan, Kerman, Khorasan, Khuzistan, Kurdistan,
Qazvin, Semnan, Tehran and Zanjan (Afshar, Tadjbakhsh, 1970; Hazrati et al., 1981; Kargar
Moakhar et al., 2001, 2003; Sakhaee et al., 2009; Raoofi et al., 2012a; Sadri, 2012b;
Shirvani et al., 2012; Bahari et al., 2013; Ezzi et al., 2013; Safarpoor Dehkordi et al.,
2013; Nikbakht et al., 2015; Sharifzadeh et al., 2015; Hemmatzadeh et al., 2016; Seyfi
Abad Shapouri et al., 2016; Adeli et al., 2017; Kaveh et al., 2017; Erfani et al., 2019;
Noaman, Nabinejad, 2020; Hashemi et al., 2022). There is no information about possible
transmission of the virus by arthropods in the country.
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Nairoviridae
Abu Hammad virus
Abu Hammad virus (AHV) (Nairoviridae: Orthonairovirus) was first found in the soft
tick Argas hermanni Audouin (Parasitiformes: Argasidae) in Egypt (Converse et al., 1974;
Darwish et al., 1976; Casals, Tignor, 1980; Hoogstraal, 1985; Labuda, Nuttall, 2008; Kuhn
et al., 2016). It has also been isolated from A. hermanni in Dormian Village of Isfahan
Province in central Iran (Tesh, 1976, personal communication, cited by the CDC Arthropod-
Argas hermanni is not mentioned in the most recent checklist of the soft ticks (10
species) in Iran (Hosseni-Chegeni et al., 2019). Although Hosseni-Chegeni and Tavakoli
(2020) recently recorded the species in Lorestan Province in western Iran, there is no new
information about AHV in Iran.
Crimean-Congo hemorrhagic fever
Crimean-Congo hemorrhagic fever (CCHF), caused by CCHF virus (CCHFV)
(Nairoviridae: Orthonairovirus), occurs in Africa, Asia and Europe and is the most widely
distributed medically important arboviral disease after dengue fever. The disease is the
most significant tick-borne viral disease in humans. The virus has been found in different
wild and domestic animals (birds and mammals). It has been isolated from more than
30 species of hard and soft ticks, however the main vector is Hyalomma marginatum.
CCHFV is biologically transmitted to humans by the bite of an infected tick (horizontal
transmission) or by direct contact with infected blood, body fluid, tissues and, possibly,
crushed ticks (direct transmission). The virus can be transmitted via different routes in
certain ticks, including transovarial, trans-stadial and sexual (venereal) transmission
(Hoogstraal, 1979, 1981, 1985; Nuttall, 2001; Labuda, Nuttall, 2008; Chinikar et al., 2010b;
Hubálek, Rudolf, 2012; Bente et al., 2013; Spengler et al., 2016; Al-Abri et al., 2017;
Contigiani et al., 2017; Blair et al., 2019; Saleem et al., 2020). Also, as reported by
Hoogstraal (1979) and Nuttall (2001), the virus has been isolated from species of Culicoides
(Diptera: Ceratopogonidae). CCHFV occurs in Afghanistan (Hoogstraal, 1979; World Health
Organization, 2004), Armenia (Karapetyan et al., 1974; Hoogstraal, 1979; Lvov, 1994;
Failloux et al., 2017; Gevorgyan et al., 2019), Azerbaijan (Gromashevsky, Nikimorov, 1973;
Semashko et al., 1974; Hoogstraal, 1979; Lvov, 1994), Iraq (Al-Tikriti et al., 1981; World
Health Organization, 2004; Abul-Eis et al., 2012), Kuwait (Al-Nakib et al., 1984), Oman
(Scrimgeour et al., 1996, 1999; Williams et al., 2000; Al-Zadjali et al., 2013; Body et al.,
2016; Al-Abri et al., 2019), Pakistan (Begum et al., 1970a, d; Hoogstraal, 1979; Hayes,
Burney, 1981; Darwish et al., 1983b; World Health Organization, 2004; Kasi et al., 2020),
Saudi Arabia (El-Azazy, Scrimgeour, 1997; Hassanein et al., 1997; Memish et al., 2011),
Somalia (Spengler et al., 2016), Sudan (Watts et al., 1994; Aradaib et al., 2011; Elata
et al., 2011; Osman et al., 2013; Ibrahim et al., 2015; Spengler et al., 2016; Suliman et al.,
2017; Ahmed et al., 2020), Syria (Blair et al., 2019), Turkey (Inci et al., 2013, 2016; Düzlü
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et al., 2020), Tukmenistan (Aristova et al., 1973; Hoogstraal, 1979; Lvov, 1994; Atkinson,
Hewson, 2018), the United Arab Emirates (Suleiman et al., 1980; Baskerville et al., 1981;
Khan et al., 1997; Rodriguez et al., 1997; Schwarz et al., 1997; Al-Dabal et al., 2016;
Aijazi et al., 2020; Camp et al., 2020; Khalafalla et al., 2021) and Yemen (Cecaro et al.,
2013). Historically, Jorjani (Gorgani) (1042-1136 AD), in his monumental book “Treasure
of the Khwarazm Shah” (Zakhireye Kharazmshahi), a Persian medical encyclopedia,
described a hemorrhagic and arthropod caused disease about one thousand years ago that
seemed to be CCHF (Hoogstraal, 1979; Jorjani, 2001). The first scientific reports of clinical
signs of CCHF in humans in Iran date back to the 1960s (Aminol-Achrafi, Noraniyan,
1966a, b). The first records of antibodies to the virus in different domesticated and wild
animals were identified in the early 1970s using the agar gel diffusion precipitation (AGDP)
test (Chumakov et al., 1970; Chumakov, Smirnova, 1972; Saidi et al., 1975). Also, the first
records of CCHFV antibodies in humans were identified in 4% of individuals tested in the
Caspian Sea littoral provinces of Golestan, Guilan and Mazandaran using the
hemagglutination inhibition (HI) test (Saidi, 1974) and 13% of people tested in six
provinces of the country using the AGDP test (Saidi et al., 1975). Phylogenetic analysis
showed that CCHFV in Iran includes at least five genomic variants (Senegalese, Pakistani,
Iraqi, Afghani and Russian) and seven genotypes of six clades or lineages: clades I (Africa
3), III (Africa 1), IV (Asia 1 and 2), V (Europe 1), VI (Europe 2) and a new clade VII
(Iran) (Chinikar et al., 2004, 2013b, 2016a, b; Morovvati et al., 2012; Kayedi et al., 2015;
Al-Abri et al., 2017; Nasirian, 2020). Saidi et al. (1975), using the AGDP test, found
positive antibodies in different domesticated and wild mammals in six provinces, East
Azerbaijan, Golestan, Guilan, Razavi Khorasan, Isfahan and Tehran as follow: 38% of
sheep, 36% of gaots, 18% of cattle and 3% of small mammals such as Myotis blyti,
Nyctalus noctula, Allactaga williamsoni, Mus musculus and Meriones crassus. CCHFV
was also serologically detected in a number of mammals and birds using ELISA, including
goats (46%) and sheep (77.5%) in North Khorasan, Razavi Khorasan and South Khorasan
Provinces (Bokaie et al., 2008; Chinikar et al., 2012b); in cattle (30%), goats (33.3%) and
sheep (41.9%) in Ardebil Province (Telmadarraiy et al., 2010); in cattle (5.9%) in five
Iranian provinces (Chaharmal and Bakhtiari, Razavi Khorasan, Semnan, Sistan and
Baluchistan and South Khorasan) (Lotfollahzadeh et al., 2011); in sheep (15.5%) in East
Azerbaijan Province (Rezazadeh et al., 2012, 2013); in cattle (25%), goats (24.8%) and
sheep (58.7%) in differenet areas of Iran (Mostafavi et al., 2013a); in ostriches (20%) and
sheep (54.2%) in Isfahan Province (Izadi et al., 2007; Mostafavi et al., 2013b); in sheep
(0.8%) in Kohgiluyeh and Boyerahmad Province (Ghasemian et al., 2021); in sheep (3.7%)
(Mostafavi et al., 2012) and (38.7%) (Faghihi et al., 2015) in Mazandaran Province; in
cattle (9.6%) in Razavi Khorasan and South Khorasan Provinces (Lotfollahzade et al.,
2009); and in camels (5.29%) in North Khorasan, Razavi Khorasan and South Khorasan
Provinces (Champour et al., 2014). In general, infections of CCHFV in humans have been
reported in at least 25 Iranian provinces (out of 31), with the highest rates in Sistan and
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Baluchistan, Isfahan and Fars Provinces (Chinikar, 2003; Chinikar et al., 2002, 2005, 2008,
2009, 2010a, c; Mostafavi et al., 2013a). Specific documents have been published about
human cases of the disease in different provinces, including Ardebil (Asefi, 1974, 1977;
Adham et al., 2021; Habibzadeh et al., 2021; Abazari et al., 2022), Chaharmahal and
Bakhtiari (Mahzounieh et al., 2012), East Azerbaijan (Aminol-Achrafi, Noraniyan, 1966a,
b; Asefi, 1974; Saidi et al., 1975; Ardoin, Karimi, 1982; Ardalan et al., 2006), Fars (Raoofi
et al., 2012b; Rezaei et al., 2012), Golestan (Saidi, 1974; Saidi et al., 1975; Abbasi, Moradi,
2005); Guilan (Saidi, 1974; Saidi et al., 1975; Asefi, 1977), Hormozgan (Fazlalipour et al.,
2019), Isfahan (Saidi et al., 1975; Chinikar et al., 2012a), Khuzistan (Sharififard et al.,
2016), Kohgiluyeh and Boyerahmad (Hadinia et al., 2012), Kurdistan (Firouzmanesh et al.,
2017; Shahbazi et al., 2019), Mazandaran (Saidi, 1974; Sadeghi et al., 2013), North
Khorasan, Razavi Khorasan and South Khorasan (Saidi et al., 1975; Bokaie et al., 2008;
Ebadiazar et al., 2011; Ziyaei et al., 2011; Chinikar et al., 2013a; Heydari, Movahed
Danesh, 2013; Naderi et al., 2013; Shahhosseini et al., 2018); also co-infections of
brucellosis and CCHF (Hashemian, Ebrahimi, 2010), Qazvin (Nikoonejad, Bijani, 2016),
Qom (Saghafipour et al., 2012a, b; Farzinnia et al., 2013), Semnan (Arab-Ameree,
Mirshafee, 2006), Sistan and Baluchistan (Izadi et al., 2003, 2004, 2006; Alavi-Naini
et al., 2006; Sharifi Mod, Metanat, 2006; Owaysee Oskooei et al., 2008; Sharifi-Mood
et al., 2014; Mostafavi et al., 2017; Nili et al., 2020); also co-infections of malaria and
CCHF (Sharifi-Mood et al., 2011) and Tehran (Saidi et al., 1975). Some 53 to 154 human
cases of CCHF were found in at least 24 provinces of Iran during 2006-2011, with highest
number of cases in Sistan and Baluchistan, Isfahan, Razavi Khorasan, Khuzistan and Fars
Provinces (Ramezankhani, Kaveh, 2014). Blair et al. (2019) reported that the total number
of confirmed human cases of the virus in the country was 1256, with total deaths being
177 during 1999-2017 and cases per year ranging from 18 and 150. At least 47 species
of ticks (11 species of soft ticks and 36 species of hard ticks) occur in Iran (Hosseni-
Chegeni et al., 2019; Hosseini-Chegeni, Tavakoli, 2020). CCHFV has been isolated from
different tick species using RT-PCR in various provinces, including Ardebil (28% of tested
ticks were positive) (Telmadarraiy et al., 2010); East Azerbaijan (5.0%) (Shafei et al.,
2016); Fars (4.5%) (Farhadpour et al., 2015); Golestan (5.3%) (Sedaghat et al., 2017);
Hamedan (16.4%) (Telmadarraiy et al., 2008) (19.3%) (Tahmasebi et al., 2010); Ilam (6.6%)
(Sharifinia et al., 2015); Kermanshah (3.8%) (Mohammadian et al., 2016); Kurdistan (5.6%)
(Fakoorziba et al., 2012); Lorestan (6.7%) (Kayedi et al., 2015); Mazandaran (9.52%)
(Faghihi et al., 2015); Qom (7.9%) (Telmadarraiy et al., 2012); Razavi Khorasan (3.8%)
(Fakoorziba et al., 2015), (5%) (Maghsood et al., 2020); Semnan (4.3%) (Faghihi et al.,
2018); Sistan and Baluchistan (4.3%) (Mehravaran et al., 2013); South Khorasan (15.9%)
(Jafari et al., 2020); West Azerbaijan (8.33%) (Morovvati et al., 2012) and Yazd (5.71%)
(Salim Abadi et al., 2011). The virus was isolated from the following species of ticks:
Alveonasus lahorensis (Neumann), Dermacentor marginatus, Haemaphysalis inermis,
H. punctata, Hyalomma anatolicum Koch, H. asiaticum Schulze et Schlottke, H. scupense
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Schulze (synonym: H. detritum Schulze), H. dromedarii, H. marginatum, H. schulzei
Olenev, Rhipicephalus bursa Canstrini et Fanzago, Rh. sanguineus (Latreille) and
Rh. turanicus Pomerantsev, Matikashvili et Lotosky (Sureau, Klein, 1980; Sureau et al.,
1980; Fakoorziba et al., 2015; Telmadarraiy et al., 2015). Fakoorziba et al. (2015) reported
finding CCHFV in Rhipicephalus appendiculatus Neumann collected in Razavi Khorasan
Province, however the record of this Afrotropical species in Iran is doubtful and the species
is not mentioned in the checklist of Iranian ticks (Hosseni-Chegeni et al., 2019). Among
the ticks from which the virus has been isolated in other countries, the following species
occur in Iran: Argas persicus (Oken), Dermacentor niveus Neumann, Ixodes ricinus,
Rhipicephalus annulatus (Say) and Rh. rossicus Yakimov et Kol-Yakimova (Hoogstraal,
1979; Hoogstraal, Valdez, 1980; Hosseni-Chegeni et al., 2019). A number of reviews of
CCHF in Iran (Emadi-Kouchak et al., 2003; Chinikar et al., 2010b; Keshtkar-Jahromi et
al., 2013; Keshtkar Jahromi, 2014; Mostafavi et al., 2014; Kouhpayeh, 2019; Mardani,
2019; Kassiri et al., 2020c), including two mata-analyses (Nasirian, 2019, 2020), have been
published.
Orthomyxoviridae
Quaranfil virus
Quaranfil virus (QRFV) (Orthomyxoviridae: Thogotovirus) was first isolated from
humans, the soft ticks Argas arboreus Kaiser, Hoogstraal et Kohls and A. hermanni and
pigeon squabs in Egypt (Taylor et al., 1966b; Mourya et al., 2019). The virus has been
found in several African and Asian countries. It has been isolated from the soft ticks
Argas arboreus, A. reflexus (Fabricius), A. hermanni, A. vulgaris Filippova and the hard
tick Hyalomma dromedarii (Hoogstraal, 1966, 1981, 1985; Taylor et al., 1966b; Williams
et al., 1970; Converse, Moussa, 1982; Labuda, Nuttall, 2008; Presti et al., 2009). The virus
has been found in Afghanistan, Iraq, Kuwait and Yemen (Williams et al., 1970; Converse,
Moussa, 1982). One isolation of Quaranfil virus was obtained from Argas vulgaris collected
near pigeon and sparrow nests in Razavi Khorasan Province of Iran (Klein et al., 1979;
Sureau, Klein, 1980). Eleven species of soft ticks, including A. hermanni and 36 species
of hard ticks, as well as Hyalomma dromedarii, are listed in the most recent checklist
of Iranian ticks (Hosseni-Chegeni et al., 2019; Hosseini-Chegeni, Tavakoli, 2020), however
there is no recent verification of Argas vulgaris in the country and it is not listed in
the checklist. Nothing more is known about the virus in Iran.
Thogoto virus
Thogoto virus (THOV) (Orthomyxoviridae: Thogotovirus) is known to occur in Africa,
Europe (Italy and Portugal) and Asia (Iran and Japan). The virus infects livestock (camels,
cattle, goats and sheep), migratory birds and occasionally humans. The virus is transmitted
by a number of species of hard ticks of the genera Amblyomma, Haemaphysalis, Hyalomma
and Rhipicephalus and can cause abortion in sheep (Haig et al., 1965; Albanese et al.,
1972; Williams et al., 1973; Filipe, Calisher, 1984; Woodall, 2001c; Labuda, Nuttall, 2008;
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Hubálek, Rudolf, 2012; Hubálek et al., 2014a; Yoshii et al., 2015). The virus has been
isolated from Amblyomma variegatum (Fabricius), Haemaphysalis longicornis, Hyalomma
anatolicum, H. truncatum Koch, Rhipicephalus annulatus, Rh. appendiculatus, Rh. bursa,
Rh. decoloratus Koch, Rh. evertsi Neumann and Rh. sanguineus (see Haig et al., 1965;
Albanese et al., 1972; Williams et al., 1973; Johnson et al., 1980; Filipe, Calisher, 1984;
Jones et al., 1989; Woodall, 2001c; Hubálek et al., 2014a; Yoshii et al., 2015). There is just
one record of Thogoto virus in Iran, which was found in Hyalomma anatolicum collected
from cattle in Razavi Khorasan Province (Sureau, Klein, 1980; Sureau et al., 1980). Among
other ticks from which the virus has been isolated, Rhipicephalus annulatus, Rh. bursa and
Rh. sanguineus occur in Iran (Hosseni-Chegeni et al., 2019).
Paramyxoviridae
Rinderpest (cattle plague)
Rinderpest (cattle plague), caused by the rinderpest virus (RPV) (Paramyxoviridae:
Morbillivirus), has sometimes been found in Africa, Asia, Australia, Europe and South
America. The virus affected various mammals, including humans, but especially ruminants,
primilarily buffaloes and cattle. The disease was economically very important. In the 1990s,
Afghanistan, Iran, Iraq, Pakistan, Saudi Arabia, Somalia, Sudan, Turkey, Yemen and some
other African and Asian countries were identified as the last active foci of rinderpest.
Finally, after about 65 years and a global eradication program involving vaccinations and
zoosanitory procedures, the disease was officially declared eradicated in 2011. Rinderpest is
only the second disease to be eradicated and the greatest veterinary achievement of our time
(Njeumi et al., 2012; Roeder et al., 2013). This disease is mentioned here as a historical
example of successful international collaboration and acheivment, and the importance of
a One Health approach. Rinderpest was not considered to be an arbovirus and was mainly
transmitted via direct route, however there was some evidence, natural and experimental,
for its mechanical transmission by horseflies, for example Tabanus orientis Walker (Krinsky,
1976; Foil, 1989). There is no historical information with regard to what the vector of
virus may have been in Iran.
Peribunyaviridae
Akabane virus
Akabane virus (AKAV) (Peribunyaviridae: Orthobunyavirus) has been found in Africa,
Asia and Australia. The virus infects various wild and domesticated mammals, including
buffaloes, camels, cattle, elephants, giraffes, goats, horses, pigs and sheep. Infections in
pregnant cattle, goats or sheep causes a variety of abnormalities in the fetus, principally
arthrogryposis and hydranencephaly. Epizootics may cause a significant economical loss.
Infections in adult animals are entirely subclinical. Certain species of Culicoides are the
biological vectors of AKAV. The virus has also been isolated from a number of mosquitoes,
for example Aedes vexans, Anopheles funestus Giles, An. vagus, Culex tritaeniorhynchus
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and Cx. vishnui; however, they do not biologically transmit the virus and are of lesser
importance as vectors (Oya et al., 1961; Wirth, Hubert, 1989; Mellor et al., 2000; Mellor,
2001c; Bryant et al., 2005; Hubálek et al., 2014a; Kirkland, 2015; Contigiani et al., 2017).
The virus has been found in Iraq (Alsaad et al., 2017; Al-Salihi, Al-Dabhawi, 2019), Oman
(Al-Busaidy, Mellor, 1991b), Saudi Arabia (Abu Elzein et al., 1998b), Sudan (Mohamed
et al., 1996), Syria (Taylor, Mellor, 1994) and Turkey (Taylor, Mellor, 1994; Dagalp
et al., 2021). The main vectors are Culicoides brevitarsis Kieffer and C. wadai Kitaoka
in Australia, C. oxystoma Kieffer in Japan, C. imicola Kieffer and C. milnei Austen in
Africa and C. imicola in Oman (St George et al., 1978; Kurogi et al., 1987; Al-Busaidy,
Mellor, 1991b; Mellor, 2001c; Hubálek et al., 2014a). Also, C. nubeculosus (Meigen) and
C. variipennis (Coquillett) have been shown to be capable of experimentally transmitting
the virus (Jennings, Mellor, 1989). Serological tests, such as hemagglutination inhibition
(HI) and enzyme-linked immunosorbent assay (ELISA), have been used to identify the
virus in Iran: in Charmahal and Bakhtiari Province (15% in goats and 5.88% in sheep)
(Kojouri et al., 2015), Golestan Province (10% in sheep, 80% in cattle) (Ahourai et al.,
1992), Khuzistan Province (39.72% in sheep, 85.87% in cattle) (Ahi et al., 2015; Karami
Boldaji et al., 2016), Semnan Province (23.3% in cattle) (Mohajer et al., 2019) and Tehran
Province (56.52% in cattle) (Dehghan Rahimabadi et al., 2020). There are at least four
genera of biting midges (Ceratopogonidae), Atrichopogon (three species), Culicoides
(43 species), Dasyhelea (four species) and Forcipomyia (one species), with at least
51 species in Iran (Navai, 1974; Dominiak, Alwin, 2013; Pilvari et al., 2016), however
there is no information about the vectors of the virus in the country. Among known possible
vectors, Culicoides nubeculosus occurs in Iran (Jennings, Mellor, 1989; Abdigoudarzi,
2016). Two mosquito species, Aedes vexans and Culex tritaeniorhynchus, from which
the virus was first isolated in Japan, also occur in Iran (Oya et al., 1961; Azari-Hamidian
et al., 2019).
Schmallenberg virus
Schmallenberg virus (SBV) (Peribunyaviridae: Orthobunyavirus) occurs in Africa, Asia
and Europe. SBV, as a newly emerging virus, was first detected in Germany (Schmallenberg
City) and the Netherlands in 2011 (Gibbens, 2012; Hoffmann et al., 2012). The virus
RNA or antibodies have been identified in a wide range of wild and domestic ruminants,
including cattle, goats, sheep, buffaloes, camels, chamois, deer, llamas, moufflons and
reindeer, and also non-ruminant species such as dogs, elephants, horses, pigs, wild boars
and zebras. SBV infection is economically very important. Infections in adult cattle,
goats and sheep are mild or subclinical or with clinical signs such as fever, drop in milk
production and diarrhea; however, infections in pregnant cattle, goats or sheep may cause
abortions or serious congenital malformation in offspring, such as arthrogryposis and
hydranencephaly. Infection is not considered a zoonosis. The virus is biologically vectored
by certain species of Culicoides biting midges (Gibbens, 2012; Hoffmann et al., 2012;
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Nekoei et al., 2015b; Collins et al., 2019; Asadolahizoj et al., 2021). Infections have been
found in Azerbaijan (Zeynalova et al., 2019), Iraq (Al-Barawary, 2018; Al-Baroodi, 2021),
Pakistan (Wernery et al., 2013), Saudi Arabia (Taha et al., 2015), Sudan (Wernery et al.,
2013) and Turkey (Azkur et al., 2013; Yilmaz et al., 2014; Tonbak et al., 2016). SBV
has been isolated from C. chiopterus (Meigen), C. dewulfi Goetghebuer and C. obsoletus
(Meigen) in Belgium (De Regge et al., 2012), from C. chiopterus, C. obsoletus and
C. scoticus Downes et Kettle in the Netherlands (Elbers et al., 2013), from C. obsoletus and
C. punctatus (Meigen) in Poland (Larska et al., 2013), from C. imicola (experimentally)
and C. obsoletus in Spain (Pages et al., 2018) and from C. chiopterus, C. deltus Edwards
(synonym: C. lupicaris Downes et Kettle), C. dewulfi, C. imicola, C. newsteadi Austen,
C. nubeculosus, C. obsoletus, C. pulicaris (Linnaeus) and C. scoticus in France (Segard
et al., 2018). Additionally, the Nearctic C. sonorensis Wirth et Jones has experimentally
been shown to be an efficient vector (Veronesi et al., 2013). Transovarial transmission
is also known for Culicoides vectors (Larska et al., 2013). Rasekh et al. (2018) detected
SBV-specific antibodies in 5% of samples from horses using ELISA in North Khorasan
and Razavi Khorasan Provinces. This was the first time that antibodies against SBV were
detected in horses. However, the results should be verified using virus neutralization tests,
PCR and SBV RNA isolation (Collins et al., 2019). Also, Rasekh et al. (2022) detected
SBV-specific antibodies in 12.45% of samples from cattle using ELISA in Razavi Khorasan,
South Khorasan and Sistan, Baluchistan Provinces. Among known vectors of the virus,
C. nubeculosus, C. pulicaris and C. punctatus occur in Iran (Navai, 1974; Larska
et al., 2013; Abdigoudarzi, 2016; Segard et al., 2018). Although at least 43 species
of Culicoides are found in Iran (Navai, 1974), there is no information about the vector(s)
of Schmallenberg virus in the country.
Tahyna virus
Tahyna virus (TAHV) (Valtice fever) (Peribunyaviridae: Orthobunyavirus) (synonyms:
Lumbo, Trojica) is known to occur in Africa, Asia and Europe (Labuda, 2001; Bennett
et al., 2011). The virus has been found in Armenia (Failloux et al., 2017), Azerbaijan
(Gromashevsky, Nikimorov, 1973; Lvov, 1994), Iraq (Barakat et al., 2016) and Turkey
(Hubálek, 2008). It has been isolated from different domestic and wild mammals, such as
rodents and insectivores, however it seems that the main reservoirs in Europe are hares and
rabbits. Infection causes a non-fatal flu-like illness in humans. Infections in endemic areas,
such as Central Asia, seem to be very frequent based on serological tests. The virus has
been isolated from different mosquito species of the genera Aedes, Anopheles, Culex and
Culiseta. Transovarial transmission has been documented (Labuda, 2001; Hubálek, 2008;
Atkinson, Hewson, 2018). It seems Aedes vexans is the most important vector. Other known
vectors are Ae. cantans (Meigen) [Ochlerotatus cantans], Ae. caspius s. l., Ae. cinereus
Meigen, Ae. communis (De Geer) [Ochlerotatus communis], Ae. excrucians (Walker)
[Ochlerotatus excrucians], Ae. detritus (Haliday) [Ochlerotatus detritus], Ae. flavescens
(Muller) [Ochlerotatus flavescens], Ae. punctor (Kirby) [Ochlerotatus punctor], Ae. sticticus
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(Meigen) [Ochlerotatus sticticus], Anopheles hyrcanus (Pallas), Culex modestus, Cx. pallens
Coquillett, Cx. pipiens and Culiseta annulata (Schrank) (Labuda, 2001; Hubálek, 2008;
Li et al., 2010; Hubalek et al., 2014b; Sonnleitner et al., 2014). According to Hannoun
and Rau (1970), the virus has been experimentally transmitted in chickens by the soft
tick Argas reflexus. Based on unpublished data, antibodies for the virus have been found
in humans in Azerbaijan Province of Iran using the serological test (the CDC Arthropod-
there is no verified and published information about the occurrence of the virus in the
country. Among known vectors of the virus, Aedes caspius s. l., Ae. detritus, Ae. flavescens,
Ae. vexans, Anopheles hyrcanus, Culex modestus, Cx. pipiens and Culiseta annulata occur
in Iran (Labuda, 2001; Hubálek, 2008; Li et al., 2010; Azari-Hamidian et al., 2019).
Phenuiviridae
Bhanja virus
Bhanja virus (BHAV) (Phenuiviridae: Phlebovirus) (synonym or subtype: Palma virus)
occurs in Africa, Asia and Europe. Isolation of the virus from mammals is rare, however
serological surveys indicate the highest prevalence of antibodies in domestic mammals, such
as camels, cattle, dogs, goats, horses and sheep, and also antibodies have been detected in
different wild mammals, birds and reptiles (Shah, Work, 1969; Hubálek et al., 1982, 2014a;
Hubálek, 1987; Filipe et al., 1994; Labuda, Nuttall, 2008; Hubálek, Rudolf, 2012; Matsuno
et al., 2013). The virus has been identified in Armenia, Azerbaijan, Pakistan, Somalia and
Turkmenistan (Chunikhin, Karaseva, 1971; Semashko et al., 1973; Matevosyan et al., 1974;
Hubálek et al., 1982, 2014a; Hubálek, 1987; Darwish et al., 1983b; Lvov, 1994; Hubálek,
Rudolf, 2012; Failloux et al., 2017; Atkinson, Hewson, 2018). It has been isolated from
at least 15 species of hard ticks of the genera Amblyomma, Dermacentor, Haemaphysalis,
Hyalomma and Rhipicephalus (Shah, Work, 1969; Hoogstraal, Valdez, 1980; Johnson
et al., 1980; Hoogstraal, 1981; Hubálek et al., 1982, 2014a; Hubálek, 1987; Filipe et al.,
1994; Hubálek, Rudolf, 2012). It seems that the only record of BHAV in Iran is based on
a serological survey of 3000 humans and domestic and wild mammls. A “small proportion”
showed antibodies to BHAV (Saidi, 1975). Also, Arata (1975) mentioned the presence
of BHAV in Iran and listed it as a “representative rodent born [sic] disease”. There are
at least 36 species of hard ticks representing five genera (Dermacentor, Haemaphysalis,
Hyalomma, Ixodes and Rhipicephalus) in Iran (Hosseni-Chegeni et al., 2019), however
there is no more recent information about the virus and its possible vector(s) in the country.
The following 10 species, which are known vectors in other countries, occur in Iran:
Dermacentor marginatus, Haemaphysalis parva (Neumann) (synonym: H. intermedia
Nuttall et Warburton), H. punctata, H. sulcata Canstrini et Fanzago, Hyalomma asiaticum,
H. dromedarii, H. marginatum, H. scupense (synonym: H. detritum), Rhipicephalus
annulatus, Rh. bursa (Hoogstraal, Valdez, 1980; Hubálek et al., 1982, 2014a; Hubálek,
1987; Hubálek, Rudolf, 2012; Hosseni-Chegeni et al., 2019).
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Rift Valley fever
Rift Valley fever, caused by the Rift Valley fever virus (RVFV) (Phenuiviridae:
Phlebovirus) (synonym: Zinga virus), was reviewed by Azari-Hamidian et al. (2019) and
Kassiri et al. (2020b). Information provided by Fakour et al. (2021) might be added to
those reviews. In addition to Iran, the virus has also been recorded in Djibouti (Andayi et
al., 2014), Iraq (Muhsen, 2012), Saudi Arabia (World Health Organization, 2004; Memish
et al., 2011; Ahmed, 2015; Taha et al., 2015; Kenawy et al., 2018), Somalia (Oldfield
et al., 1993; World Health Organization, 2004; Braak et al., 2018), Sudan (Watts et al.,
1994; McCarthy et al., 1996; Braak et al., 2018; Ahmed et al., 2020), Turkey (Tezcan-Ulger
et al., 2019) and Yemen (World Health Organization, 2004; Kenawy et al., 2018). Among
known principal mosquito vectors, the following species (see Hubálek et al., 2014a and
Azari-Hamidian et al., 2019, 2020) occur in Iran: Aedes caspius s. l., Ae. vexans, Culex
antennatus (Becker), Cx. perexiguus, Cx. pipiens, Cx. theileri, Cx. tritaeniorhynchus and
Mansonia uniformis, however there is no evidence for indigenous transmission of the virus
in the country.
Sandfly fever (papatasi fever, Phlebotomus fever, three-day fever)
Sandfly fever, caused by different sandfly-borne phleboviruses (SFN-SV) (Phenuiviridae:
Phlebovirus), which are transmitted in the Old World by species of the genus Phlebotomus
(Diptera: Psychodidae, Phlebotominae), and probably also the genus Sergentomyia in the
Mediterranean region, Africa, the Indian subcontinent, the Middle East and Central Asia,
and in the New World by species of the genus Lutzomyia. Different vertebrates including
bats, carnivora, insectivora, rodents and sheep, may serve as hosts in nature. Sandfly
fever caused by most of the sandfly-borne phleboviruses is a self-limiting influenza-like
disease without mortality, however acute meningitis or meningo-encephalitis has been
reported for Toscana virus (TOSV) in several European countries (Adler, Theodor, 1957;
Barnett, Suyemoto, 1961; Ashford, 2001; Depaquit et al., 2010; Ready, 2013; Dehghani
et al., 2021). In addition to Iran, viruses that cause sandfly fever have also been found in
Aghanistan, Azerbaijan, Djibouti, Iraq, Pakistan, Saudi Arabia, Somalia, Sudan, Turkey and
Turkmenistan (Tesh et al., 1975, 1976b; Hayes, Burney, 1981; Arsen'eva, 1982; Darwish
et al., 1983b; Tesh, 1989; Gaidamovich et al., 1990a, b; Nikolaev et al., 1991; Lvov,
1994; Watts et al., 1994; Bryan et al., 1996; McCarthy et al., 1996; Wallace et al., 2002;
Riddle et al., 2008; Depaquit et al., 2010; Inci et al., 2013; Andayi et al., 2014; Alkan et
al., 2015; Barakat et al., 2016; Failloux et al., 2017; Atkinson, Hewson, 2018; Ahmed et
al., 2020). The main vector is Phlebotomus papatasi (Scopoli), the distribution of which
coincides closely with the distribution of the disease. Dashli virus (DASHV), Karimabad
virus (KARV), sandfly fever Naples virus (SFNV), sandfly fever Sicilian virus (SFSV) and
Tehran virus (THEV) have been isolated from Ph. papatasi (Tesh et al., 1977; Ashford,
2001; Depaquit et al., 2010; Alkan et al., 2017). Also, SFSV was isolated from Ph. ariasi
Tonnoir in Algeria (Izri et al., 2008). Corfou virus (CFUV), closely related to SFSV, was
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isolated from Ph. neglectus Tonnoir (as Ph. major Annandale) in Greece (Rodhain et al.,
1985). In Europe, Arbia virus (ARBV), closely related to Salehabad virus (SALV), SFNV
and TOSV were isolated from Ph. perfiliewi Parrot (Ashford, 2001) and Ph. perniciosus
Newstead (Verani et al., 1988; Ashford, 2001). TOSV has been isolated from Sergentomyia
minuta Roundani (Charrel et al., 2006b) and Massilia virus (MASV), closely related to
SFNV, has been isolated from Phlebotomus perniciosus (Charrel et al., 2009). Historically,
the first reports of sandfly fever infection in Iran were by foreign investigators in the
1940s and 1950s (Hertig, Sabin, 1955; Barnett, Suyemoto, 1961; Hyams et al., 1995).
Eight sandfly fever viruses have been found in Iran: DASHV, KARV, SFNV, SALV, SFSV,
THEV, TOSV and sandfly fever Cyprus virus (SFCV). It seems that while Naples and
Sicilian viruses are the most prevalent viruses in most studied areas, Karimabad virus is
most abundant in Isfahan Province, in central Iran, and is also very common in Razavi
Khorasan Province, in northeastern Iran, according to seroepidemiological studies (Saidi,
1974; Tesh et al., 1975, 1976a, b, 1977; Javadian et al., 1977; Saidi et al., 1977; Tesh, 1988,
1989; Mehrabi-Tavana, 1999, 2001; Mehrabi-Tavana et al., 2000; Alkan et al., 2017; Shiraly
et al., 2017). There is doubt about the occurrence of SFCV and TOSV in Iran because
of the rarity of cases and probable cross-reaction between viral serotypes (Shiraly et al.,
2017). Saidi (1974) found seropositive antibodies for KARV in 3% of preschool children
in the Caspian area using hemagglutination inhibition (HI) tests. Tesh et al. (1976a, b)
reported positive neutralization tests for humans in different urban and rural areas of seven
Iranian provinces: East Azerbaijan: SFSV (12%), SFNV (26%), KARV (1%); Guilan: SFSV
(12.9%), SFNV (21.5%); Isfahan: SFSV (14.1-20%), SFNV (6.3-10%), KARV (50-75%);
Kermanshah: SFSV (9.4%), SFNV (28.1%); Khorasan: SFSV (4.1-19%), SFNV (4.2-
33.8%), KARV (1.0-31.1%); Khuzistan: SFSV (9.1-34.2%), SFNV (3.0-42.9%), KARV
(0.8%); Tehran: SFSV (10.8-27.4%), SFNV (19.4-36.6%), KARV (5.9-11.8%). Tesh et al.
(1977) isolated SFSV and KARV from Phlebotomus papatasi and possibly Ph. caucasicus
Marzinowsky in Isfahan Province. Saidi et al. (1977) reported positive neutralization tests
in Isfahan Province for humans: SFNV (17.2%), SFSV (25.4%) and KARV (66.4%); for
sheep: SFSV (5.2%) and for the gerbil Rhombomys opimus: SFSV (34.2%) and KARV
(31.6%). Mehrabi-Tavana (2001) reported positive HI tests for SFSV (60%) and SFNV
(46%) in Ilam Province and SFSV (100%) and SFNV (33.3%) in Kermanshah Province
in limited samples. Seroprevalence of indirect fluorescent antibody (IFA) tests in humans
in Ilam Province gave positive results for SFSV (10.9%), SFNV (5%), SFCV (1.5%) and
TOSV (1%) (Shiraly et al., 2017). Karimabad virus (KARV) and Salehabad virus (SALV)
were found in Phlebotomus species and Tehran virus (THEV) was found in Phlebotomus
papatasi for the first time in Iran in 1959 (International catalog of arboviruses including
aspx). Dashli virus (DASHV) was first isolated and described from Sergentomyia species
and Ph. papatasi collected in Dashliboroun of Golestan Provine, in northern Iran (Alkan
et al.,
2017). Additionally, there are many notes, letters and reviews on sandfly fever
381
in Iran (Mehrabi-Tavana, 2007, 2012, 2015, 2017a, b, c, d, e, f; Khoobdel et al., 2008;
Azari-Hamidian et al., 2023). The most recent checklist of Iranian sandflies (Kasiri et
al., 2000) includes 54 species, 31 species of the genus Phlebotomus and 23 species of
the genus Sergentomyia. While at least 62 species of sandflies occur in Iran (Javadian,
Mesghali, 1975; Artemiev, 1978; Secombe et al., 1993; Kasiri et al., 2000; Badakhshan et
al., 2011; Akhoundi et al., 2012; Zahraei-Ramazani et al., 2013, 2015; Norouzi et al., 2020),
the occurrence of some species and the number of species in Iran are controversial, with
44 to 50 species recorded by different investigators, for example Yaghoobi-Ershadi (2012),
Karimi et al. (2014) and Moradi-Asl et al. (2019).
Poxviridae
Avian (fowl) pox
Avian (fowl or poultry) pox, caused by the avian (fowl) pox virus (FPV) (Poxviridae:
Avipoxvirus), was reviewed by Azari-Hamidian et al. (2019). The papers by Ebrahimi et
al. (2012), Khalesi et al. (2019), Sadat Mousavi et al. (2019), Zarifi et al. (2019), Khalili
Gheidariy et al. (2020), Mehrabadi et al. (2020), Alemian et al. (2021), Mirzazadeh et al.
(2021), Zamani et al. (2021) and Ghodsian et al. (2022) might be added to the Iranian
literature pertaining to the virus. The virus has also been found in Bahrain (Samour et al.,
1996), Iraq (Tantawi et al., 1981), Kuwait (Tarello, 2008), Saudi Arabia (Tarello, 2004)
and the United Arab Emirates (Tarello, 2008), and has been isolated from the poultry red
mite Dermanyssus gallinae in Iran (Eram et al., 2020).
Lumpy skin disease
Lumpy skin disease, caused by the lumpy skin disease virus (LSDV) (Poxviridae:
Capripoxvirus), has been found in Africa, Asia and Europe. The virus infects cattle and
water buffaloes. The infection causes huge economic losses in the livestock industry (Weiss,
1968; Hunter, Wallace, 2001; Tuppurainen, Oura, 2012; Al-Salihi, 2014; Tuppurainen
et al., 2015; Namazi, Khodakaram Tafti, 2021). The disease is known in Azerbaijan,
Bahrain, Djibouti, Iraq, Kuwait, Oman, Saudi Arabia, Somalia, Sudan, Syria, Turkey, the
United Araba Emirates and Yemen (Kumar, 2011; Tuppurainen, Oura, 2012; Al-Salihi,
2014; Tageldin et al., 2014; Tuppurainen et al., 2015; Inci et al., 2016; Sevik, Dogan,
2017). To date, the main route of transmission of LSDV is mechanical, not biological,
through the bites of haematophagous arthropods, therefore it has not been considered an
arbovirus (Hunter, Wallace, 2001; Chihota et al., 2003; Tuppurainen, Oura, 2012; Al-Salihi,
2014; Sprygin et al., 2019). Recently, evidence was found for the biological transmission
of LSDV by Culicoides punctatus in Turkey (Sevik, Dogan, 2017). Mechanical transmission
of LSDV has been reported for different biting, or even non-biting, arthropods, including the
stable fly Stomoxys calcitrans (Weiss, 1968; Baldacchino et al., 2013), the mosquito Aedes
aegypti (Chihota et al., 2001), the hard ticks Amblyomma hebraeum Koch, Rhipicephalus
appendiculatus and Rh. decoloratus (Lubinga et al., 2013a, b, 2014a, b; Tuppurainen
382
et al., 2013a, b), the horn fly Haematobia irritans Linnaeus (Diptera: Muscidae) (Kahana-
Sutin et al., 2017), the house fly Musca domestica Linnaeus (Diptera: Muscidae) (Sprygin
et al., 2018) and Musca (Biomyia) confiscata Speiser (junior homonym: M. fasciata Stein)
(Diptera: Muscidae) (Weiss, 1968; as Biomyia fasciata). Also, transovarial and transtadial
transmission of the virus in ticks has been reported (Lubinga et al., 2013b, 2014a).
In Iran, the disease has been found in Alborz, East Azerbaijan, Fars, Guilan, Ilam, Kerman,
Kermanshah, Khorasan, Khuzistan, Kurdistan, Mazandaran, Qom and West Azerbaijan
Provinces (Norian et al., 2016; Jalili et al., 2017; Sameea Yousefi et al., 2017, 2018;
Karimpour Somedel et al., 2019; Ghalyanchilangeroudi et al., 2021; Hedayati et al., 2021).
There is no information about the possible role that arthropods may play in transmission
in the country.
Sheep and goat pox
Sheep and goat pox is caused, respectively, by the sheep pox virus (SPV) and the
goat pox virus (GPV) (Poxviridae: Capripoxvirus). While, sheep pox is clinically similar
to goat pox, recent molecular findings have shown that these are two separate viruses.
Most strains are host specific and cause severe clinical disease in either sheep or goats,
while some strains have equal virulence in both of these animals. The disease occurs in
Africa, Asia, Europe and the western USA. The virus infects ruminants (especially cattle,
goats and sheep). The main route of transmission is close contact with infected animals
(Rao, Bandyopadhyay, 2000; World Organisation for Animal Health, 2013; Mirzaei et al.,
2015; Tuppurainen et al., 2015; Yune, Abdela, 2017). The stable fly Stomoxys calcitrans
and the sheep head fly Hydrotaea irritans are assumed to play a role via mechanical
transmission (Kitching, Mellor, 1986; Mellor et al., 1987). Infections have occurred in
Afghanistan, Azerbaijan, Djibouti, Iraq, Oman, Pakistan, Somalia, Sudan, Syria, Turkey and
Yemen (Hedger et al., 1980; Kitching, Mellor, 1986; Rao, Bandyopadhyay, 2000; World
Organisation for Animal Health, 2013; Mirzaei et al., 2015; Tuppurainen et al., 2015).
A disease control vaccination program has been ongoing for about 70 years in Iran (Rafyi,
Mirchamsy, 1956; Rafyi, Ramyar, 1959; Ramyar et al., 1974; Sadri, Fallahi, 2010; Ghorani,
Esmaeili, 2022). Despite this, some severe outbreaks still occur in the country with high
morbidity and mortality. Sheep pox outbreaks mostly occur in the northwestern, northeastern
and central provinces of Iran, including Azerbaijan, Hormozgan, Kermanshah, Qom, Fars,
Bushehr, Kerman, Khorasan and Yazd Provinces, and goat pox outbreaks mostly occur in
southern provinces, including Fars, Hormozgan, Kerman and Khorasan Provinces (Mirzaei
et al., 2015; Karimpour Somedel et al., 2019). SPV pathology has been studied in Fars
Province (Khoda Karam Tafti, Namdari, 2000). During a study in six Iranian provinces,
including Azerbaijan, Fars, Hormozgan, Kerman, Khorasan and Khuzistan, 20.75% of goats
were positive for GPV (Sadri, 2012c). A high rate of mortality due to a SPV outbreak was
reported in Qom Province (Mirzaei et al., 2015). There is no information about the possible
vector(s) of the viruses in the country.
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Reoviridae
African horse sickness
African horse sickness is a non-contagious infection caused by African horse sickness
virus (AHSV) (Reoviridae: Orbivirus). Nine distinct serotypes of the virus are known
(Sailleau et al., 2000; Mellor, 2001a; Mellor, Hamblin, 2004). Equids such as horses, mules,
donkeys and zebras are the most important vertebrate hosts. Dogs may occasionally be
infected, however they do not have an important role in the epidemiology of the disease
and are considered dead-end hosts. The disease is not considered a zoonosis. Infections are
widely distributed in Africa south of the Sahara, including Sudan, and are also enzootic in
Yemen, both countries of the WHO Eastern Mediterranean Region (Mellor, 1994, 2001a;
Mellor, Hamblin, 2004; Tkubet et al., 2016; Carpenter et al., 2017; Dennis et al., 2019). The
mortality rates are 50-95, 50, 5-10% for horses, mules and Europran and Asian donkeys,
respectively; however, mortality is rare in African donkeys and zebras (Tkubet et al., 2016).
The disease is rarely seen as far northward as Algeria, Egypt, Libya, Morocco, Palestine,
Portugal, Spain and Tunisia and eastward to Afghanistan, Cyprus, India, Iran, Iraq, Jordan,
Oman, Pakistan, Saudi Arabia, Syria and Turkey (Rafyi, 1961; Hazrati, Taslimi, 1964;
Hazrati, 1967; Mirchamcy, Hazrati, 1973; Hedger et al., 1980; Anderson et al., 1989;
Mellor et al., 1990a; Mellor, 1994, 2001a). AHSV is biologically and exclusively vectored
by certain species of Culicoides (Mellor et al., 2000), athough different haematophagous
arthropods may be implicated in transmission, such as the mosquitoes Aedes aegypti,
Anopheles stephensi Liston and Culex pipiens, the hard ticks Hyalomma dromedarii and
Rhipicephalus sanguineus (Mellor, 1994) and the horsefly Tabanus pluto Walker (Krinsky,
1976). The only confirmed principal vector is Culicoides imicola, which is present in Africa,
Asia and Europe (Mellor et al., 1990b, 2000; Mellor, 2001a). The species occurs in Bahrain,
Iraq, Oman, Saudi Arabia, Turkey and the United Arab Emirates (Boorman, 1989), however
it has not been reported in Iran (Navai, 1974). Also, C. bolitinos Meiswinkel is considered
as a secondary vector and the North American C. variipennis has been experimentally
found to be an efficient vector (Mellor et al., 1975, 2000; Mellor, 2001a). Two species,
C. obsoletus and C. pulicaris, may be involved in transmission in Europe (Mellor et al.,
1990b; Mellor, Hamblin, 2004). In summer 1959, infections were found in southern Iran
following the outbreak in the Arabian Peninsula, which rapidly spread throughout the
region, including Afghanistan, Cyprus, Iraq, Jordan, Libya, Pakistan, Syria, Turkey and
India, over a period of three years (1959-1961). During the outbreak, the region lost more
than 300,000 equines (Rafyi, 1961; Hazrati, Taslimi, 1964; Mirchamsy, Hazrati, 1973). The
virus was isolated from horses (32.5%), mules (40.0%) and donkeys (20.0%) in Iran during
the outbreak (Hazrati, Taslimi, 1964). After the outbreak, scientists in the Razi Institute
of Iran studied the virus and produced a vaccine, as reviewed by Mirchamsy and Hazrati
(1973). There is no recent record of the disease in Iran. At least 43 species of Culicoides
are known to occur in Iran (Navai, 1974); However, there is no information about
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the possible vector(s) of AHSV in Iran. Among known vectors, C. pulicaris occurs in
the country (Navai, 1974; Mellor, Hamblin, 2004).
Bluetongue
Bluetongue virus (BLUV) (Reoviridae: Orbivirus) causes the disease of bluetongue,
which has a worldwide distribution. Infections have been found in wild and domestic
ruminants, especially sheep. The virus consists of 26, more likely 27, serotypes. The
BLUV serotypes 1-24 are transmitted almost entirely and biologically by certain species
of Culicoides biting midges, however there is not such certainty about the role of these
midges in the transmission of BLUV-25 and BLUV-26 (Afshar et al., 1989; Wirth, Hubert,
1989; Afshar, 1994; Mellor, 2001d; Hubálek et al., 2014a; Maclachlan et al., 2015). Also,
the sheep ked Melophagus ovinus (Linnaeus) (Diptera: Hippoboscidae) (Gray, Bannister,
1961; Luedke et al., 1965) and a number of mosquitoes, such as Aedes lineatopennis
(Ludlow) [Neomelaniconion lineatopenne], Ae. vigilax (Skuse) [Ochlerotatus vigilax] and
Culex annulirostris, are believed to be possible secondary or mechanical vectors (Weir
et al., 1997; Hubálek et al., 2014a). In addition to biological transmission, BLUV may
be occasionally and directly transmitted via semen and embryo transfer from infected
countries to virus-free regions (Mellor, 2001d). Infections have been found in Aghanistan
(Hassani, Madadgar, 2021), Iraq (Hafez et al., 1978), Kuwait (Maan et al., 2011a, b), Oman
(Hedger et al., 1980; Al-Busaidy, Mellor, 1991a, b), Pakistan (Akhtar et al., 1997), Saudi
Arabia (Hafez, Taylor, 1985; Abu Elzein et al., 1998a; Taha et al., 2015), Sudan (Abu
Elzein, Tageldin, 1985; Abu Elzein, 1986; Mohammad, Taylor, 1987; Mohammad, Mellor,
1990), Syria (Mellor et al., 2008; Hubálek et al., 2014a), Turkey (Gür, 2008; Failloux
et al., 2017) and Yemen (Stanley, 1990). The principal verified vectors are Culicoides
insignis Lutz and species of the C. variipennis complex in the Americas, C. imicola in
Africa and Europe and C. actoni Smith, C. brevitarsis, C. fulvus Sen et Das Gupta and
C. wadai in Australasia and Indonesia (Mohammad, Mellor, 1990; Mellor et al., 2000,
2009). Additionally, the virus has been isolated from C. milnei and C. tororoensis Khamala
et Kettle in Kenya (Walker, Davies, 1971), C. pusillus Lutz in Central America and the
Caribbean (Mo et al., 1994), C. peregrinus Kieffer in Indonesia (Sendow et al., 1996)
and C. dewulfi, C. newsteadi, C. obsoletus, C. pulicaris, C. punctatus and C. scoticus
in Italy (Caracappa et al., 2003; Goffredo et al., 2015; Federici et al., 2019). Afshar and
Kayvanfar (1974) identified precipitating antibodies to BLUV in sera of farm animals
in Iran for the first time. Kargar Moakhar et al. (1988) found the international serotypes
3, 7, 20 and 22 in sheep in different areas of Iran using the agar gel immunodiffusion
(AGID) and microneutralization tests. Serological surveys, using ELISA, found positive
antibodies to BLUV in East Azerbaijan Province (in sheep, 67-76.44%) (Hasanpour
et al., 2008; Imandar et al., 2014), Fars Province (in cattle, 19.77%, in goats, 55.70-85.3%
and in sheep, 70.93-74.4%) (Mohammadi et al., 2012; Oryan et al., 2014; Manavian
et al., 2017; Hashemi et al., 2018), Hamedan Province (in sheep, 46%) (Yavari et al., 2018),
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Ilam Province (in sheep, 43.88%) (Khezri, Azimi, 2012b), Isfahan Province (in cattle,
2.69%, in goats, 49.19% and in sheep, 53.37%) (Noaman et al., 2008, 2013), Kerman
Province (in camels, 100%, in cattle, 2.13%, in goats, 67.7% and in sheep 6.57%) (Mahdavi
et al., 2006; Mozaffari, Khalili, 2012; Mozaffari et al., 2012, 2014), Khuzistan Province
(in sheep, 55.9%) (Noroozikia et al., 2014), Kohgiluyeh and Boyerahmad Province (in sheep,
77.48%) (Sabaghan et al., 2014), Kurdistan Province (in sheep, 19.3-51.85%) (Khanbabaie
et al., 2011; Khezri, 2012; Khezri, Azimi, 2012a, b; Khezri, Bakhshesh, 2014), Razavi
Khorasan Province (in goats, 87.6% and in sheep, 90.0%) (Najarnezhad, Rajae, 2013), West
Azerbaijan Province (in sheep, 34.7-55.9%) (Jafari-Shoorijeh et al., 2010; Sadri, 2012a;
Hasanpour et al., 2014) and Yazd Province (in camels, 67.8%) (Mozaffari et al., 2013).
In a study conducted in eight Iranian provinces, the total prevalence of BLUV antibodies
found in sheep was 34.9%: the provinces included Ardebil (23.7%), East Azerbaijan
(39.8%), Fars (25.3%), Ilam (42.6%), Khuzistan (15%), Kurdistan (41.7%), Qom (12.1%)
and West Azerbaijan (64.8%) (Khezri, Azimi, 2013). In a study in seven provinces, Ardebil,
East Azerbaijan, Fars, Ilam, Khuzistan, Kurdistan and Qom, the infection was investigated
using RT-PCR for the first time in Iran and 10% of total samples were both seropositive and
RT-PCR positive in sheep (Azimi et al., 2009). During another investigation in nine
provinces, Ardebil, East Azerbaijan, Golestan, Isfahan, Markazi, Qazvin, Qom, West
Azerbaijan and Yazd, 66.43% of all samples were serologically positive in sheep (Fallahi
et al., 2013). In an investigation in three provinces of southeastern Iran, Hormozgan,
Kerman and Sistan and Baluchistan, the total prevalence of BLUV antibodies was 92.67%
in goats and 48.72% in sheep (Ezatkhah et al., 2014). In a study on wild ruminants in
different areas of Iran, 12% of viral serological tests (ELISA) and 8% of PCR results were
positive for BLUV in mouflon (Ovis orientalis) (Hemmatzadeh et al., 2016). Momtaz et al.
(2011) compared the results of ELISA and RT-PCR for BLUV in sheep in Chaharmahal
and Bakhtiari, Isfahan and Khuzistan Provinces. Another study in Chaharmahal and
Bakhtiari Province indicated a significant relationship between seropositivity and topography
(plains or mountains), sex (male or female) and abortion history (Noaman, Arzani, 2017).
Bakhshesh et al. (2020) studied the large-scale seroprevalence and risk factors associated
with the virus in the country. Khezri and Bakhshesh (2014), Oryan et al. (2014) and
Hassani and Madadgar (2021) reviewed infections in Iran. Among known vectors of
the virus, Culicoides pulicaris and C. punctatus occur in the country (Navai, 1974; Goffredo
et al., 2015; Abdigoudarzi, 2016). Although at least 43 species of Culicoides are known to
be present in Iran (Navai, 1974), there is no information about the vector(s) of bluetongue
virus in the country.
Wad Medani virus
Wad Medani virus (WMV) (Reoviridae: Orbivirus) is distributed in Africa and Asia.
The virus has been found in numerous species of hard ticks of the genera Amblyomma,
Dermacentor, Hyalomma and Rhipicephalus. Serological tests have identified infections in
cattle, camels, pigs, buffaloes and rodents (Taylor et al., 1966a; Hoogstraal, Valdez, 1980;
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Labuda, Nuttall, 2008; Belaganahalli et al., 2015; Atkinson, Hewson, 2018; Dedkov et al.,
2021). The virus has been found in Armenia, Pakistan, Sudan and Turkmenistan (Taylor
et al., 1966a; Lvov et al., 1967; Begum et al., 1970a, d; Skvortsova et al., 1975; Hayes,
Burney, 1981; Darwish et al., 1983b; Lvov, 1994; Alkhovsky et al., 2014c; Atkinson,
Hewson, 2018). It has been isolated from the following ticks: Amblyomma cajennense
(Fabricius) s. l., Dermacentor nuttalli, Hyalomma anatolicum, H. asiaticum, Rhipicephalus
guilhoni Morel et Vassiliades, Rh. microplus (Canstrini), Rh. sanguineus and Rh. turanicus
(see Taylor et al., 1966a; Lvov et al., 1967; Begum et al., 1970d; Hoogstraal, Valdez, 1980;
Hayes, Burney, 1981; Voltsit, 1982; Alkhovsky et al., 2014c; Yadav et al., 2019; Dedkov
et al., 2021). There is a unique record of Wad Medani virus in Iran, which was found in
Hyalomma anatolicum collected from cattle in Razavi Khorasan Province (Sureau, Klein,
1980; Sureau et al., 1980). Among known vectors, Hyalomma asiaticum, Rhipicephalus
sanguineus and Rh. turanicus occur in Iran (Taylor et al., 1966a; Hayes, Burney, 1981;
Hoogstraal, Valdez, 1980; Hosseni-Chegeni et al., 2019).
Retroviridae
Bovine leukemia
Bovine leukemia, caused by the bovine leukemia virus (BLV) (Retroviridae:
Deltaretrovirus), occurs worldwide. The virus consists of ten genotypes. The disease
causes economical losses due to reduction in milk production, reproductive performance
and length of life (Polat et al., 2017). The disease is mainly directly transmitted among
cattle, however there is some evidence for mechanical transmission by horseflies (Tabanus
fuscicostatus Hine, T. nigrovittatus Macquart, T. nipponicus Murdoch et Takahasi and
T. trigeminus Coquillett), the stable fly Stomoxys calcitrans and the hard tick Rhipicephalus
microplus (Foil, 1989; Foil et al., 1988; Foil, Issel, 1991; Baldacchino et al., 2013).
Infections have been found in Saudi Arabia (Hafez et al., 1990) and Turkey (Burgu
et al., 2005). The disease has been found in cattle in the following provinces of Iran based
on ELISA and PCR tests: Alborz (45%) (Kazemimanesh et al., 2012), Ardebil (9.5%)
(Kazemimanesh et al., 2012), Chaharmahal and Bakhtiari (18.4%) (Nekoei et al., 2015a),
East Azerbaijan (50%) (Kazemimanesh et al., 2012), Guilan (100%) (Kazemimanesh
et al., 2012), Isfahan (23.8-81.9%) (Morovati et al., 2012; Nekoei et al., 2015a), Kerman
(15.5%) (Mohammadabadi et al., 2011), Markazi (53.3%) (Kazemimanesh et al., 2012),
North Khorasan (1.5%) (Mousavi et al., 2014), Qom (57%) (Kazemimanesh et al., 2012),
Razavi Khorasan (2.3-29.8%) (Kazemimanesh et al., 2012; Mousavi et al., 2014) and
Tehran (17-88.8%) (Nikbakht Brujeni et al., 2010; Mohammadi et al., 2011; Kazemimanesh
et al., 2012). The virus has also been found in sheep in Chaharmahal and Bakhtiari Province
(2.7%) and Isfahan Province (6.7%) (Nekoei et al., 2015a). Recently, an investigation in
Iran proposed the possible association between the human breast cancer and the BLV
infection in cattle using the nested PCR technique (Khalilian et al., 2019). There is no
information about possible transmission of the virus by arthropods in the country.
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Equine infectious anaemia (swamp fever)
Equine infectious anaemia, caused by the equine infectious anaemia virus (EIAV)
(Retroviridae: Lentivirus), has a worldwide distribution. The disease is the most important
viral infection in horses. Although EIAV is not an arbovirus, it does not replicate in
the vector and is not vectored biologically, haematophagous insects play an important
role in its transmission and the epidemiology of infection (Issel, 2001; Issel, Foil, 2015).
The virus has been found in Oman (Body et al., 2011), Saudi Arabia (Alnaeem, Hemida,
2019), Sudan (Wegdan et al., 2017) and Turkey (Marenzoni et al., 2013). Horseflies, such as
Chrysops flavidus Wiedemann, Hybomitra frontalis (Walker), H. lasiophthalma (Macquart),
Tabanus fuscicostatus and T. sulcifrons Macquart, and the stable fly Stomoxys calcitrans
(less important), play an important role in mechanical transmission of the virus to horses,
whereas mosquitoes, such as Aedes aegypti and Psorophora columbiae (Dyar et Knab), are
linked to subclinical or inapparent infections (Hawkins et al., 1973; Krinsky, 1976; Foil
et al., 1983; Foil, 1989; Foil, Issel, 1991; Green et al., 1996; Issel, 2001; Baldacchino
et al., 2013). In Iran, the disease has been found in the provinces of Ardebil, East
Azerbaijan, Isfahan, Kurdistan and Tehran (Hazrati et al., 1978; Momtaz, Nejat, 2010;
Rezazadeh et al., 2016). There is no information about the possible role of arthropods in
transmission of the virus in Iran.
Rhabdoiviridae
Bovine ephemeral fever
Bovine ephemeral fever, caused by the bovine ephemeral fever virus (BEFV)
(Rhabdoviridae: Ephemerovirus), was reviewed by Azari-Hamidian et al. (2019). The papers
by Bakhshesh et al. (2018), Pasandideh et al. (2018a, b, c, 2019a, b), Almasi, Bakhshesh
(2019a, b), Mollazadeh et al. (2022) and Rezatofighi et al. (2022) might be added to
the Iranian literature pertaining to the infection. The virus has also been found in
Afghanistan (St George, 1988), Iraq, Kuwait, Pakistan, Saudi Arabia, Somalia, Sudan,
Syria, Turkey, Turkmenistan and Yemen (St George, 1988; Lvov, 1994; Hubálek et al.,
2014a; Walker, Klement, 2015), as well as Iran (Azari-Hamidian et al., 2019).
Isfahan virus
Isfahan virus (ISFV) (Rhabdoviridae: Vesiculovirus) was isolated from pools of
Phlebotomus papatasi for the first time in Isfahan Province of Iran (Tesh et al., 1977;
Calisher et al., 1989). The virus has also been isolated from humans in the provinces of
Isfahan (66.9%), Khuzistan (5.4%) and Tehran (3.3%), and from the rodents Rhombomys
opimus in Isfahan Province (79%) and Tatera indica in Khuzistan Province (8.6%) using
the neutralization test (Tesh et al., 1977). Additionally, the virus has been isolated from
the mosquito Aedes caspius s. l. and the hard tick Hyalomma asiaticum, see Alkhutova
et al. (1981), Alkhutova, Sadykov (1982), Labuda, Nuttall (2008) and Atkinson, Hewson
(2018). Aedes caspius and Hyalomma asiaticum both occur in Iran (Azari-Hamidian et al.,
388
2019; Hosseni-Chegeni et al., 2019). Some isolations of the virus, or its antibodies, have
been made in Central Asia (Tajikistan, Turkmenistan and Uzbekistan) (Gaidamovich et al.,
1980; Lvov, 1994; Atkinson, Hewson, 2018).
Zahedan rhabdovirus
Zahedan rhabdovirus (ZARV) (Rhabdoviridae: Zamolirhabdovirus) was first recovered
and described from the hard tick Hyalomma anatolicum anatolicum collected in Zahedan in
Sistan and Baluchistan Province, southeastern Iran. The virus is lethal for mice and possibly
pathogenic for other mammals. The mammalian host is not known (Dilcher et al., 2015).
Togaviridae
Chikungunya infection
Chikungunya infections caused by Chikungunya virus (CHIKV) (Togaviridae:
Alphavirus) occur widely in sub-Saharan Africa and southern Asia. The virus has been
isolated from different species of monkey, as well as bats and birds. It seems that non-
human primates and humans are the main vertebrate hosts in Africa and Asia, respectively.
The virus has been isolated from different mosquito species of the genera Aedes, Anopheles,
Coquillettidia, Culex and Mansonia, as well as species of soft ticks (Ornithodoros sonrai)
and hard ticks. It is probable that sylvan species of Aedes in Africa, for example Aedes
africanus (Theobald) [Stegomyia africana] and Ae. furcifer (Edwards) [Diceromyia furcifer],
and urban Ae. aegypti and Ae. albopictus in Asia are the main vectors (Hoogstraal, 1985;
McCarthy et al., 1996; Diallo et al., 1999; Woodall, 2001a; Nsoesie et al., 2016; Failloux
et al., 2017; Gould et al., 2017; Wahid et al., 2017; Silva et al., 2018; Simo et al., 2019).
The virus may have been isolated from the tropical bed bug Cimex hemipterus (Fabricius)
(Hemiptera: Cimicidae) (Rao, 1964). Other possible mosquito vectors, which were found
naturally infected or are experimentally assumed to play a role in transmission, include
Aedes calceatus (Edwards) [Stegomyia calceata], Ae. cordellieri (Huang) [Diceromyia
cordellieri], Ae. fulgens (Edwards) [Zavortinkius fulgens], Ae. luteocephalus (Newstead)
[Stegomyia luteocephala], Ae. opok (Corbet et van Someren) [Stegomyia opok], Ae. taylori
(Edwards) [Diceromyia taylori], Ae. vittatus (Bigot) [Fredwardsius vittatus], Coquillettidia
fuscopennata (Theobald), Culex quinquefasciatus, Mansonia africana (Theobald) and
Ma. uniformis (Rao, 1964; Jupp et al., 1981; Jupp, McIntosh, 1990; Diallo et al.,
1999, 2012; Woodall, 2001a; Silva et al., 2018). Chikungunya virus has been found in
Afghanistan, Djibouti, Iraq, Pakistan, Qatar, Saudi Arabia, Somalia, Sudan and Yemen, and
imported cases have been found in Oman and Turkey (Salim, Porterfield, 1973; Darwish
et al., 1983a; Arsen'eva, 1982; Oldfield et al., 1993; Watts et al., 1994; Wallace et al.,
2002; Farnon et al., 2010; Zayed et al., 2012; Andayi et al., 2014; Ciccozzi et al., 2014;
Malik et al., 2014; Rezza et al., 2014; Afzal et al., 2015; Al-Abri et al., 2015; Barakat
et al., 2016; Wahid et al., 2017; Yaqub et al., 2017; Humphrey et al., 2019; Ahmed et al.,
2020; Sawal et al., 2021). Cases of CHIKV imported from Pakistan were recently found
in Sistan and Baluchistan Province in southeastern Iran (Pouriayevali et al., 2019). More
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recently, Bakhshi et al. (2020
) detected the virus in Anopheles maculipennis Meigen
s. l. in Mazandaran Province and in A. maculipennis s. l., Culex tritaeniorhynchus and
Culisetta longiareolata (Macquart) in North Khorasan Province using primers designed
for CHIKV Asian genotype, however they failed to isolate the virus and whole genome
sequencing was not performed. Also, Tavakoli et al. (2020) detected CHIKV IgM
seropositivity in 16.07% of samples in eight southern provinces of Iran. Among known
vectors of Chikungunya virus, Aedes albopictus, Ae. vittatus and Mansonia uniformis occur
in Iran (Diallo et al., 1999, 2012; Silva et al., 2018; Azari-Hamidian et al., 2019, 2020),
however there is no information about the indigenous transmission of the virus in the
country.
Semliki forest virus
Semliki forest virus (SFV) (Togaviridae: Alphavirus) (synonym or subtype: Me Tri
virus) occurs mostly in Africa south of the Sahara, but the virus has been found in eastern
Russia and Vietnam and antibodies have been detected in Borneo, India, Indonesia,
Malaysia, the Philippines and Thailand. It seems that the main reservoirs are domesticated
mammals, such as cattle, horses and pigs. However, the virus has also been isolated
from monkeys, wild birds, rodents and insectivores. Among arthropods, the virus has
been isolated from species of the mosquito genera Aedes, Culex and Eretmapodites and
the hard tick Rhipicephalus guilhoni (Ha et al., 1995; Pfeffer, 2001; Tan et al., 2008;
Hubálek et al., 2014a). The virus was first isolated from Aedes abnormalis (Theobald)
[Aedimorphus abnormalis], but it seems the main vector in Africa is Ae. africanus. It has
been detected in Ae. vexans and Culex pipiens in eastern Russia and Cx. tritaeniorhynchus
in Vietnam, and has been found in many species in Africa, including Aedes aegypti,
Ae. argenteopunctatus (Theobald) [Catageiomyia argenteopunctata], Ae. fuscinervis
(Edwards) [Neomelaniconion fuscinerve], Ae. jamoti (Hamon et Rickenbach)
[Neomelaniconion jamoti], Ae. opok, Ae. palpalis (Newstead) [Neomelaniconion palpale],
Ae. punctocostalis (Theobald) [Neomelaniconion punctocostale], Ae. togoi (Theobald)
[Tanakaius togoi], Ae. vittatus, Eretmapodites chrysogaster Graham, Er. grahami Edwards,
Culex quinquefasciatus and Mansonia africana (Lee et al., 1974; Gaidamovich et al., 1975;
Ha et al., 1995; Pfeffer, 2001; Hubálek et al., 2014a). According to unpublished data in
Iran, antibodies for the virus were found in humans (3%) using the neutralization test
(the CDC Arthropod-Borne Virus Information Exchange, 1962, available at https://stacks.
cdc.gov). Among known vectors of the virus, Aedes vexans, Ae. vittatus, Culex pipiens,
Cx. quinquefasciatus and Cx. tritaeniorhynchus occur in Iran (Pfeffer, 2001; Hubálek et al.,
2014a; Azari-Hamidian et al., 2019). There is no recently verified and published information
about the occurrence of the virus in the country.
Sindbis fever
Sindbis fever, caused by Sindbis fever virus (SINV) (Togaviridae: Alphavirus) [synonyms
or subtypes: Babanki, Karelian, Kyzylagach (KYZV), Ockelbo, Pogosta and Whataroa],
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was reviewed by Azari-Hamidian et al. (2019). In addition to Iran, the virus has also been
found in Afghanistan (Arsenʼeva, 1982; Wallace et al., 2002), Armenia (Failloux et al.,
2017), Azerbaijan (Lvov, 1994; Lundström, Pfeffer, 2010; Storm et al., 2013; Alkhovsky
et al., 2014d), Iraq (Riddle et al., 2008; Barakat et al., 2016), Oman (Camp et al., 2019),
Pakistan (Darwish et al., 1983a), Saudi Arabia (Wills et al., 1985; Al-Khalifa et al., 2007;
Lundström, Pfeffer, 2010; Storm et al., 2013), Somalia (Oldfield et al., 1993), Sudan
(Hoogstraal, 1966; Farnon et al., 2010), Turkey (Hubálek et al., 2014a) and Turkmenistan
(Atkinson, Hewson, 2018). Recently, Hanafi-Bojd et al. (2021) detected Sindbis fever virus
in the pools of Culex pipiens and Cx. theileri in West Azerbaijan Province of Iran. Bakhshi
et al. (2022) reviewed the virus in Iran and adjacent countries. Principal vectors of the
virus in other countries that also occur in Iran include Cx. torrentium Martini and Culiseta
morsitans (Theobald) (Hubálek et al., 2014a; Azari-Hamidian et al., 2019).
Unclassified virus
Wanowrie virus
Wanowrie virus (WANV) (unclassified) was first isolated from Hyalomma marginatum
in India (Dandawate et al., 1970; Labuda, Nuttall, 2008). The virus was later found
in Hyalomma impeltatum Schulzae et Schlottke collected from camels in Egypt (Williams
et al., 1973) and identified in the brain of a human in Sri Lanka who died from an
infection (Pavri et al., 1976). Antibodies against WANV have been detected in sera of
domestic abunaks and humans in Pakistan (Darwish et al., 1983b). There is just one record
of Wanorie virus in Iran, isolated from Hyalomma asiaticum collected from goats in Razavi
Khorasan Province (Sureau, Klein, 1980; Sureau et al., 1980). Two other ticks from which
the virus has been isolated, H. impeltatum and H. marginatum, also occur in Iran (Hosseni-
Chegeni et al., 2019).
Other viruses in the countries neighboring Iran
There are other diseases and infections caused by arboviruses or viruses which may
be mechanically transmitted by arthropods in the countries neighboring Iran and in
the WHO Eastern Mediterranean Region that need to be considered. Although these viruses
have not been formally reported in Iran, their eventual occurrence in the country is very
possible, especially in view of tourism, immigration and the presence and/or importation
of possible vectors, hosts, reservoirs and migratory birds. The names of infections, viruses
and country records are as follow:
Flaviviridae
Banzi virus (BANV) (Flaviviridae: Flavivirus), transmitted by mosquitoes, known
in Somalia (Henderson et al., 1968; Cahill, 1971).
Barkedji virus (BJV) (Flaviviridae: Flavivirus), transmitted by mosquitoes, known
in Oman and the United Arab Emirates (Camp et al., 2019).
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Israel turkey meningoencephalitis virus (ITMV) [synonym or subtype: Bagaza virus
(BAGV)] (Flaviviridae: Flavivirus), transmitted by mosquitoes and possibly biting midges,
known in the United Arab Emirates (Hubálek et al., 2014a; Camp et al., 2019).
Kadam virus (KADV) (Flaviviridae: Flavivirus), transmitted by ticks, known in Saudi
Arabia (Wood et al., 1982; Al-Khalifa et al., 2007; Labuda, Nuttall, 2008).
Karshi virus (KSIV) (Flaviviridae: Flavivirus), transmitted by ticks, known
in Turkmenistan (Hoogstraal, 1985; Labuda, Nuttall, 2008; Atkinson, Hewson, 2018).
Kyasanur Forest disease virus (KFDV) (Flaviviridae: Flavivirus) [synonyms or subtypes:
Alkhurma virus, Aka Alkhumra virus or Alkhurma hemorrhagic fever virus (ALKV or
AHFV)], transmitted by ticks and possibly mosquitoes, known in Djibouti, Saudi Arabia
and Turkey (Hoogstraal, 1985; Zaki, 1997; Charrel et al., 2005, 2006a, 2007; Madani, 2005;
Labuda, Nuttall, 2008; Alzahrani et al., 2010; Carletti et al., 2010; Memish et al., 2010,
2011; Mahdi et al., 2011; Shibl et al., 2012; Ahmed, 2015; Horton et al., 2016; Atkinson,
Hewson, 2018; Hoffman et al., 2018; Shah et al., 2018).
Louping ill virus (LIV) (Flaviviridae: Flavivirus) (synonym: Negishi virus) (Hubálek
et al., 2014a), transmitted by ticks, known in Turkey [as LI-like virus or Turkish sheep
encephalomyelitis virus (TSEV)] (Hartley et al., 1969; Gao et al., 1997; Gould, 2001;
de la Fuente et al., 2008; Hubálek, Rudolf, 2012; Inci et al., 2016; Düzlü et al., 2020).
Royal farm virus (RFV) (Flaviviridae: Flavivirus), transmitted by ticks, known
in Afganistan and Pakistan (Williams et al., 1972; Darwish et al., 1983a; Hoogstraal, 1985;
Labuda, Nuttall, 2008).
Usutu virus (USUV) (Flaviviridae: Flavivirus), transmitted by mosquitoes, known
in Iraq (Barakat et al., 2016).
Yellow fever virus (YFV) (Flaviviridae: Flavivirus), transmitted by mosquitoes, known
in Somalia and Sudan (Henderson et al., 1968; Cahill, 1971; Salim, Porterfield, 1973;
Oldfield et al., 1993; Watts et al., 1994; Monath, 2001; World Health Organization, 2004;
Farnon et al., 2010; Gould et al., 2017; Braak et al., 2018; Ahmed et al., 2020).
Zika virus (ZIKAV) (Flaviviridae: Flavivirus), transmitted by mosquitoes, known
in Pakistan, Saudi Arabia, Somalia, Sudan and Turkey (Henderson et al., 1968; Cahill,
1971; Darwish et al., 1983a; Tomori, 2001; Evans et al., 2017; Kindhauser et al., 2016;
Benelli, Romano, 2017; Dehghani, Amiri, 2017; Epelboin et al., 2017; Gould et al., 2017;
Alayed et al., 2018; Sezen et al., 2018; Tavakoli et al., 2018; Noorbakhsh et al., 2019;
Ahmed et al., 2020; Nikookar et al., 2020; Kassiri et al., 2020a; Saleem et al., 2022).
Nairoviridae
Artashat virus (ARTSV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known
in Armenia and Azerbaijan (Hoogstraal, 1985; Lvov, 1994; Alkhovsky et al., 2014b, 2017).
Caspiy virus (CASV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known
in Azerbaijan and Turkmenistan (Hoogstraal, 1985; Lvov, 1994; Labuda, Nuttall, 2008;
Lvov et al., 2014a; Alkhovsky et al., 2017).
392
Dera Ghazi Khan virus (DGKV) (Nairoviridae: Orthonairovirus), transmitted by ticks,
known in Pakistan (Begum et al., 1970a, c; Hayes, Burney, 1981; Darwish et al., 1983b;
Labuda, Nuttall, 2008; Kuhn et al., 2016).
Geran virus (GERV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known
in Azerbaijan (Lvov et al., 2014c; Alkhovsky et al., 2017).
Hazara virus (HAZV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known
in Pakistan (Begum et al., 1970a, b; Hayes, Burney, 1981; Darwish et al., 1983b; Labuda,
Nuttall, 2008; Hartlaub et al., 2020).
Issyk-Kul virus (ISKV) (Nairoviridae: Orthonairovirus), transmitted by ticks and
mosquitoes, known in Azerbaijan and Turkmenistan (Lvov, 1994; Gavrilovskaya, 2001;
de la Fuente et al., 2008; Labuda, Nuttall, 2008; Atkinson et al., 2015; Atkinson, Hewson,
2018). Gavrilovskaya (2001) noted the possible occurrence of this virus in Iran, Afghanistan
and Pakistan.
Nairobi sheep disease virus (NSDV) (Nairoviridae: Orthonairovirus) [synonym or
Indian subtype: Ganjam virus (GANV)], transmitted by ticks, known in Africa (including
Somalia) and Asia (India and Sri Lanka) (Johnson et al., 1980; Davis, 1997; Peiris, 2001;
de la Fuente et al., 2008; Hubálek et al., 2014a). Hoogstraal and Valdez (1980) considered
the virus as “a prime candidate for investigation in Iran”.
Tamdy virus (TDYV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known
in Armenia, Azerbaijan, Turkey and Turkmenistan (Lvov, 1994; Labuda, Nuttall, 2008;
Lvov et al., 2014b; Failloux et al., 2017; Atkinson, Hewson, 2018).
Zirqa virus (ZIRV) (Nairoviridae: Orthonairovirus), transmitted by ticks, known on
Zirqa Island in the Persian Gulf (the United Arab Emirates) (Hoogstraal et al., 1970;
Varma et al., 1973; Labuda, Nuttall, 2008; Kuhn et al., 2016). The name of the virus was
misspelled as Zirga in the original paper (Varma et al., 1973).
Orthomyxoviridae
Batken virus (BKNV) (Orthomyxoviridae: Thogotovirus), transmitted by mosquitoes
and ticks, known in Azerbaijan (Lvov et al., 1974; Lvov, 1994; Hoogstraal, Valdez, 1980;
Frese et al., 1997; Labuda, Nuttall, 2008; Alkhovsky et al., 2014a). Hoogstraal and Valdez
(1980) considered this virus as “a candidate for investigation in Iranian sheep and goats”.
Dhori virus (DHOV) (Orthomyxoviridae: Thogotovirus), transmitted by ticks, known in
Armenia, Azerbaijan, Pakistan and Saudi Arabia (Williams et al., 1973; Semashko et al.,
1974; Hoogstraal, Valdez, 1980; Darwish et al., 1983b; Jones et al., 1989; Al-Khalifa
et al., 2007; Labuda, Nuttall, 2008; Hubálek, Rudolf, 2012; Failloux et al., 2017).
Peribunyaviridae
Aino virus (AINOV) (Peribunyaviridae: Orthobunyavirus) (synonyms: Kaikalur and
Samford viruses), transmitted by biting midges and mosquitoes, known in Turkey (Mellor,
2001b; Hubálek et al., 2014a; Contigiani et al., 2017).
393
Bakau virus (BAKV) (Peribunyaviridae: Orthobunyavirus), transmitted by mosquitoes
and ticks, known in Pakistan (Hayes, Burney, 1981; Darwish et al., 1983b; Hoogstraal,
1985).
Batai virus (BATV) (Peribunyaviridae: Orthobunyavirus) (synonyms: Calovo, Chitoor,
Olkya, Olyka and UgMP-6830), transmitted by mosquitoes, known in Armenia and Sudan
(Nashed et al., 1993; Failloux et al., 2017).
Ngari virus (NRIV) (Peribunyaviridae: Orthobunyavirus) (synonym: Garissa virus),
transmitted by mosquitoes, known in Somalia and Sudan (Bowen et al., 2001; Braak
et al., 2018).
Phenuiviridae
Arumowot virus (AMTV) (Phenuiviridae: Phlebovirus), transmitted by mosquitoes,
known in Somalia and Sudan (Tesh, 1988; Braak et al., 2018; Ahmed et al., 2020).
Gabek Forest virus (GFV) (Phenuiviridae: Phlebovirus), transmitted by sandflies, known
in Sudan (Tesh et al., 1976b; Tesh, 1988).
Grand Arbaud virus (GAV) (strain Art 363) (Phenuiviridae: Phlebovirus), transmitted
by ticks, known in Afghanistan (Hannoun, Rau, 1970; Williams et al., 1972; Hoogstraal,
1985; Hubálek, Rudolf, 2012; Palacios et al., 2013).
Manawa virus (MWAV) (Phenuiviridae: Phlebovirus), transmitted by ticks, known
in Pakistan (Hayes, Burney, 1981; Darwish et al., 1983b; Hoogstraal, 1985; Labuda, Nuttall,
2008).
Razdan virus (RAZV) (Phenuiviridae: Bandavirus), transmitted by ticks, known
in Armenia (Lvov, 1994; Labuda, Nuttall, 2008; Alkhovsky et al., 2013).
Uukuniemi virus (UUKV) (Phenuiviridae: Phlebovirus), transmitted by mosquitoes
and ticks, known in Azerbaijan (Gromashevsky, Nikimorov, 1973; Labuda, Nuttall, 2008;
Hubálek, Rudolf, 2012).
Reoviridae
Baku virus (BAKUV) (Reoviridae: Orbivirus), transmitted by ticks, known in Azerbaijan
and Turkmenistan (Lvov et al., 1971; Andreev et al., 1973; Gromashevsky, Nikimorov,
1973; Lvov, 1994; Labuda, Nuttall, 2008; Atkinson, Hewson, 2018).
Chenuda virus (CNUV) (Reoviridae: Orbivirus), transmitted by ticks, known
in Turkmenistan (Taylor et al., 1966b; Hoogstraal, 1985; Lvov, 1994; Belaganahalli et al.,
2015; Atkinson, Hewson, 2018).
Epizootic haemorrhagic disease virus (EHDV) (Reoviridae: Orbivirus), transmitted
by biting midges and possibly mosquitoes, known in Bahrain, Oman, Sudan and Turkey
(Al-Busaidy, Mellor, 1991a; Mellor et al., 2000; Mellor, 2001e; Temizel et al., 2009;
Wernery et al., 2013; Hubálek et al., 2014a).
Palyam virus (PALV) (Reoviridae: Orbivirus), transmitted by mosquitoes, known
in Sudan (Mohammad, Mellor, 1990; Mellor et al., 2000).
394
Rhabdoviridae
Barur virus (BARV) (Rhabdoviridae: Vesiculovirus), transmitted by ticks, known
in Somalia (Butenko et al., 1981; Labuda, Nuttall, 2008).
Malakal (MALV) (Rhabdoviridae: Ephemerovirus), transmitted by mosquitoes, known
in Sudan (Calisher et al., 1989; Blasdell et al., 2012b).
Obodhiang virus (OBOV) (Rhabdoviridae: Ephemerovirus), transmitted by mosquitoes,
known in Sudan (Calisher et al., 1989; Blasdell et al., 2012a).
Togaviridae
O'nyong-nyong virus (ONNV) (Togaviridae: Alphavirus), transmitted by mosquitoes,
known in Sudan (Salim, Porterfield, 1973; Woodall, 2001b; Ahmed et al., 2020).
Disscusion
The viruses which are associated with arthropods may be arranged in four ecological
groups: (1) Arthropod-borne viruses (arboviruses), (2) arthropod-transmitted animal viruses,
(3) arthropod viruses and (4) arthropod-transmitted plant viruses. The first two groups
include the viruses of medical and/or veterinary importance (Turell, 2019). Arboviruses
are the viruses which are biologically transmitted from one vertebrate host to another via
the bite of haematophagous arthropods, including biting midges, mosquitoes, sandflies or
ticks. These viruses replicate in both arthropod vectors and vertebrate hosts. Thus, the
viruses which are not transmitted by bite or merely mechanically transmitted by bite are
not among (true) arboviruses. The term “arbovirus” has no taxonomic importance, it is
a vernacular term that signifies a virus transmitted by an arthropod. Nearly all arboviral
infections are zoonotic (World Health Organization, 1967; Hart, 2001; Turell, 2019).
The World Health Organization (1967) provided nine criteria for considering a virus as
an arbovirus (five relating to the transmission cycle and four unrelated to the transmission
cycle). It seems that, based on the aforementioned definition of an arbovirus and the
nine criteria, different viruses may be grouped into four categories: (1) True arboviruses,
(2) probable arboviruses, (3) possible arboviruses and (4) most probably or definitely
not true arboviruses (World Health Organization, 1967; Hart, 2001). The World Health
Organization (1967) also mentioned four criteria for the recognition of a vector of an
arbovirus and classified them as suspected, probable and confirmed vectors based on those
criteria. Arboviruses are generally divided into two groups based on their pathogenicity
to humans: (1) Arthropod-borne viruses pathogenic to humans and (2) arboviruses not
pathogenic to humans (Hubálek, 2008).
Arthropod-transmitted animal viruses do not replicate in the arthropod vectors but do
so in vertebrate hosts and are mechanically transmitted (Turell, 2019). There are a few
important viral infections which arthropods mechanically play an important role in their
transmission and epidemiology, such as equine infectious anaemia, caused by the equine
infectious anaemia virus vectored by horseflies, stable flies and mosquitoes (Foil, Issel,
395
1991; Issel, Foil, 2015), lumpy skin disease, caused by the poxvirus lumpy skin disease
virus transmitted by stable flies, mosquitoes, ticks and Culicoides biting midges (Chihota
et al., 2003; Sprygin et al., 2019) and myxomatosis, caused by the Myxoma virus
(Poxviridae: Leporipoxvirus) transmitted by mosquitoes, fleas and horseflies (Jellison, 1959;
Krinsky, 1976; Fenner, 2001; Brugman et al., 2015).
Arthropod viruses replicate only in arthropods. They cannot cause disease
in vertebrates because they do not replicate in vertebrates, though they may be pathogenic
to the infected arthropod (Turell, 2019). These viruses are isolated only from arthropods,
including mosquito-only (mosquito-specific) flaviviruses (Cella et al., 2019) or those that
are pathogenic only to arthropods (Tinsley, 1979; Beckage et al., 1993). However, there
is no evidence for whether they are pathogenic to humans or domesticated animals and
biologically or mechanically transmitted to vertebrate hosts. Thus, they are not arboviruses
and are not of medical and veterinary significance, however they are important in view
of being a potential agent for biological control (Tinsley, 1979; Beckage et al., 1993)
or because of their impact on the biology of infected arthropods such as flight activity
or reproductivity, and their impact on the circulation of their related vector-borne pathogens
(Goenaga et al., 2015; Cella et al., 2019).
Finally, arthropod-transmitted plant viruses can be transmitted mechanically
or biologically to plants by some arthropods, including certain species of aphids,
leafhoppers, plant bugs and plant mites (Turell, 2019).
With the exception of one unclassified virus, the viruses treated in the present review are
members of 19 genera belonging to 14 families. The taxonomic placements of the viruses
are as follow. (1) Asfaviridae: Asfavirus - ASFV; (2) Flaviviridae: Flavivirus - BANV, BJV,
DENV, ITMV, JEV, KADV, KFDV, KSIV, LIV, RFV, TBEV, USUV, WNV, YFV, ZIKAV;
(3) Hantaviridae: Orthohantavirus - HTNV; (4) Herpesviridae: Varicellovirus - BHV; (5)
Nairoviridae: Orthonairovirus - AHV, ARTSV, CASV, CCHFV, DGKV, GERV, HAZV,
ISKV, NSDV, TDYN, ZIRV; (6) Orthomyxoviridae: Thogotovirus - BKNV, DHOV, QRFV,
THOV; (7) Paramyxoviridae: Morbillivirus - RPV; (8) Peribunyaviridae: Orthobunyavirus -
AINOV, AKAV, BAKV, BATV, NRIV, TAHV, SBV; (9) Phenuiviridae: Bandavirus - RAZV,
Phlebovirus - AMTV, BHAV, GAV, GFV, MWAV, RVFV, SFN-SV, UUKV; (10) Poxviridae:
Avipoxvirus - FPV, Capripoxvirus - LSDV, GPV, SPV; (11) Reoviridae: Orbivirus - AHSV,
BAKUV, BLUV, CNUV, EHDV, WMWV, PALV; (12) Retroviridae: Deltaretrovirus -
BLV, Lentivirus - EIAV; (13) Rhabdoviridae: Ephemerovirus - BEFV, MALV, OBOV,
Vesiculovirus - BARV, ISFV, Zamolirhabdovirus - ZARV; (14) Togaviridae: Alphavirus -
CHIKV, ONNV, SFV, SINV; unclassified virus: WANV.
In addition to various nonspecific signs and symptoms, such as fever, main clinical
syndromes associated with the arboviruses treated herein that are pathogenic to humans and
animals include: (1) Neurological maladies (meningitis, encephalitis, encephalomyelitis):
BHAV, JEV, SINV, TBEV, WNV (Hubálek et al., 2014a), (2) hemorrhagic disease: AHSV,
ASFV, CCHFV, DENV, RVFV (Hubálek et al., 2014a), (3) abortion and congenital disorders
396
such as arthrogryposis and hydranencephaly: AKAV, SBV (Hubálek et al., 2014a; Collins
et al., 2019; Asadolahizoj et al., 2021), (4) vesicular stomatitis: ISFV (Atkinson, Hewson,
2018) and (5) microcephaly: ZIKAV (Kassiri et al., 2020a).
The viral infections treated in the present review may be classified into four categories
based on their main vectors: (1) Biting midge-borne - AHSV, AKAV, BLUV, SBV, (2)
mosquito-borne - AMTV, BANV, BATV, BJV, CHIKV, DENV, JEV, MALV, NRIV, OBOV,
ONNV, PALV, RVFV, SFV, SINV, TAHV, USUV, WNV, YFV, ZIKAV, (3) sandfly-borne -
GFV, ISFV, SFS-NV and (4) tick-borne - AHV, ASFV, ARTSV, BAKUV, BARV, BHAV,
CCHFV, CASV, CNUV, DGKV, DHOV, GAV, GERV, HAZV, KADV, KSIV, LIV,
MWAV, NSDV, QRFV, RAZV, RFV, TDYV, THOV, TBEV, WMV, WANV, ZARV, ZIRV.
It is noteworthy that some other arthropods are involved or assumed to be involved in
the transmission of some viruses, including blackflies (Diptera: Simuliidae) - RVFV
(Bouloy, 2001), fleas - FPV, TBE (Federov et al., 1959; Sotnikova, Soldatov, 1964; Naumov,
Gutova, 1984; Della-Porta, 2001), horseflies - AHSV, BLV, EIAV, RPV, TBE (Krinsky,
1976; Foil, 1989), mites - FPV, HTNV, TBE (Naumov, Gutova, 1984; Della-Porta, 2001;
Houck et al., 2001; Xu, 2001; Sparagano et al., 2014), sheep head fly (Hydrotaea irritans)
- GPV, SPV (Kitching, Mellor, 1986), horn fly (Haematobia irritans) - LSDV (Kahana-
Sutin et al., 2017), face fly (Musca autumnalis) - BHV (Johnson et al., 1991) , house fly
(Musca domestica) - LSDV (Sprygin et al., 2018), sheep ked (Melophagus ovinus) - BLUV
(Gray, Bannister, 1961; Luedke et al., 1965), Musca (Biomyia) confiscata - LSDV (Weiss,
1968), stable fly (Stomoxys calcitrans) - ASFV, BHV, BLV, EIAV, FPV, LSDV, GPV, SPV
(Kitching, Mellor, 1986; Mellor et al., 1987; Della-Porta, 2001; Baldacchino et al., 2013)
and tropical bed bug (Cimex hemipterus) - CHIKV (Rao, 1964).
The role of arthropods in the transmission of different viruses and the epidemiology
of their infections is very disportionate and complicated, summarized as follows: (1) Some
arboviruses are mostly and biologically transmitted by certain arthropods. Other ways
of infection (generally defined as direct route or transmission) such as direct contact with
an infected person (or animal), contact with infected blood, body fluid and tissues, or via
the respiratory route and alimentary tract, do not have an important role in the epidemiology
of infection or their roles are uncertain. AHS is an example of these types of infections
(Mellor, 2001a). (2) While some arboviruses are mostly and biologically transmitted by
certain arthropods, other ways of direct transmission are also important in the epidemiology
of infection in animals or transmission to humans, such as CCHF (Saleem et al., 2020).
(3) There are a few arboviruses which are biologically transmitted by arthropods, but
it seems that the direct route of transmission is more significant in the epidemiology of the
disease, such as ASF (Beltrán-Alcrudo et al., 2017). (4) Exceptionally, some arthropods
mechanically have an important role in the transmission and epidemiology of a few viruses,
such as horseflies, mosquitoes and fleas in relation to myxomatosis (Krinsky, 1976; Bibikova,
1977), stable flies, mosquitoes, ticks and Culicoides biting midges in the case of lumpy
skin disease (Tuppurainen et al., 2015) and horseflies and the stable fly in EIAV infection
397
(Issel, 2001). (5) There are some viruses for which their major transmission route is direct.
Certain arthropods may be mechanically involved in transmission, although their role in
the epidemiology of disease is not important or uncertain such as horseflies in relation to
foot and mouth disease virus (Picornaviridae: Aphtovirus) and rinderpest virus (Krinsky,
1976). It is noteworthy that the late Professor M.P. Chumakov (1909-1993), a famous
Russian virologist, placed more emphasis on other possible ways of transmission (direct
route), even for well-defined and biologically transmitted viral infections (true arboviruses)
(World Health Organization, 1967), which shows the complex and complicated epidemiology
of viral (arboviral) infections. Moreover, the interrupted blood feeding of haematophagous
arthropods and their potential role in the mechanical transmission of infections should not
be neglected, even for the diseases caused by viruses for which biological transmission
is well and undoubtedly defined. That may explain some of the explosive outbreaks of
arboviral infections among vertebrate hosts that occur in just a few weeks (World Health
Organization, 1967). Finally, the role of each of the aforementioned factors (biological
or mechanical transmission via arthropods and/or direct route) associated with every disease
may be different in various foci; thus, the epidemiology of every infection and the role
of possible vectors should be extensively investigated in each focus. In view of the lack
of a specific vaccine or treatment for many viral infections, this basic knowledge will foster
better decisions about how and whether to control diseases by means of vector control
programs, sanitary procedures and/or health education.
Conclusion
The background, definitions and criteria presented herein clearly show that there is
not enough information about many viral (arboviral) infections in the region and available
information is very disportionate when considering countries or different epidemiological
aspects of infections. Even infections that are endemic and widespread in the region, for
which there is relatively more information, such as BEF, CCHF, SFN-S, SIN and WNF,
much more investigation is required, for example, there is little information about the
vectors of BEF in the region. On the other hand, there is little or no information about the
epidemiology of many viral infections and their vectors in the region, including BLU and
many RIDs and EIDs. Additionally, information on viruses in wildlife, which cause many
RIDs and EIDs, is very poor in comparison to information for humans and domesticated
animals. Last but not least, the records of many viral infections are based merely on
serological tests, which have their own limitations such as cross reactions; therefore,
isolation and genetic analysis of those viruses is necessary. The studies of the ecology
of vectors, as well as the epidemiology of related infections are necessary to provide
basic knowledge for vector control programs. This has been a very significant part of
integrated vector control in the One Health approach to decrease the burden of infections in
humans and domestic animals in concert with wildlife conservation. Moreover, expanding
interdisciplinary and international collaborations is necessary for fast detection, monitoring
398
and surveillance of viral infections and the vectors that cause them, in order to conduct
appropriate integrated vector and infection control programs.
Acknowledgements
The authors are grateful to Behzad Norouzi, Research Center of Health and Environment,
Guilan University of Medical Sciences, Rasht, for providing some literatures. Appreciation
is expressed to Professor Ahmad Ali Hanafi-Bojd, Department of Medical Entomology and
Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran,
for preparing the map of Iran. This research did not receive any specific grant from funding
agencies in the public, commercial or not-for-profit sectors. The authors declare that they
have no conflict of interest.
Data availability statement
Data sharing is not applicable to this article as no new data were created or analyzed
in this study.
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Вирусы,
прямо или косвенно передаваемые членистоногими,
в Иране и соседних странах
Ш. Азари-Хамидиан, Р. Е. Харбаш
Ключевые слова: арбовирусы, биологическая передача патогена, механическая
передача патогена, мобовирусы, очаги, переносчики, зоонозы
резюме
Членистоногие являются очень важной группой для медицины и ветеринарной
медицины из-за огромного количества переносимых ими патогенов. В данной работе
были проанализированы базы данных, включающие Web of Science, PubMed, Scopus,
Google Scholar, CABI, Scientific Information Database, IranMedex и Magiran, на период
конца декабря
2002 г. в отношении арбовирусных инфекций, выявленных в Иране.
В Иране были обнаружены тридцать три инфекции, прямо или косвенно переносимые
членистоногими. Для каждого заболевания приводятся данные об агентах (вирусах),
распространении (в 31 иранской провинции), хозяевах (людях и животных) и известных
переносчиках в Иране. В дополнение приведен список арбовирусов для соседних стран,
включающих Афганистан, Армению, Азербайджан, Бахрейн, Ирак, Кувейт, Оман, Пакистан,
Катар, Саудовская Аравия, Турция, Туркменистан и Объединенные Арабские Эмираты, а также
Джибути, Сомали, Судан, Сирию и Йемен, которые, хотя и не граничат с Ираном, но, подобно
Ирану, входят в Восточно-средиземноморский регион, выделенный Всемирной Организацией
Здравоохранения (ВОЗ). Список включает 40 вирусов, формально не зарегистрированных
в Иране. Эти вирусы относятся к 19 родам 14 семейств, из которых 3 вируса переносятся
москитами, четыре - мокрецами, 20 - комарами, и 29 - иксодовыми клещами.
440