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Objective: Different studies have been performed on the prevalence of tick-borne pathogens in different areas of Iran; however, as far as our knowledge, there is no regional meta-analysis available for consideration and estimation of tick species infected with different pathogens in Iran. Methods: In this review, among different databases, a total of 95 publications were included, and the infection of different tick species to different tick-borne pathogens was determined; furthermore, presence of pathogens (with 95% confidence intervals) in tick vectors was calculated separately for each province, using Comprehensive Meta-Analysis version 2 (Biostat, USA). Results: Totally, among all 95 studies, 5 673 out of 33 521 investigated ticks were positive according to different detection methods. Overall estimated presence of pathogens in tick vectors in Iran was 8.6% (95% CI 7.0%-10.6%, P
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Tick-borne pathogens in Iran: A meta-analysis
Mehdi Khoobdel1, Amir Sajad Jafari2, Zakkyeh Telmadarraiy3, Mohammad Mehdi Sedaghat4, Hasan Bakhshi5
1Health Research Center, LifeStyle Institute, Baqiyatallah University of Medical Sciences, Tehran, Iran
2Department of Veterinary Medicine, Faculty of Veterinary Medicine, University of Zabol, Zabol, Iran
3Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran; Rahyan Novin
Danesh (RND) University, Sari, Mazandaran, Iran
4Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
5Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran
ABSTRACT
Objective: Different studies have been performed on the prevalence
of tick-borne pathogens in different areas of Iran; however, as far
as our knowledge, there is no regional meta-analysis available for
consideration and estimation of tick species infected with different
pathogens in Iran.
Methods: In this review, among different databases, a total of
95 publications were included, and the infection of different
tick species to different tick-borne pathogens was determined;
furthermore, presence of pathogens (with 95% confidence intervals)
in tick vectors was calculated separately for each province, using
Comprehensive Meta-Analysis version 2 (Biostat, USA).
Results: Totally, among all 95 studies, 5 673 out of 33 521
investigated ticks were positive according to different detection
methods. Overall estimated presence of pathogens in tick vectors in
Iran was 8.6% (95% CI 7.0%-10.6%, P<0.001). Of all 46 species
of ticks in 10 genera in Iran, 28 species in 9 genera, including
Alveonasus, Argas, Boophilus, Dermacentor, Haemaphysalis,
Hyalomma, Ixodes, Ornithodoros, and Rhipicephalus were infected
with at least 20 pathogens in 10 genera including Aegyptianella,
Anaplasma, Babesia, Borrelia, Brucella, Orthonairovirus [Crimean-
Congo hemorrhagic fever virus (CCHFV)], Coxiella, Ehrlichia,
Rickettsia and Theileria in 26 provinces of Iran. The presence of
pathogens in ticks collected in western Iran was more than other
regions. Hyalomma anatolicum (20.35%), Rhipicephalus sanguineus
(15.00%), and Rhipicephalus bursa (14.08%) were the most
prevalent infected ticks for different pathogens. In addition, most
literatures were related to CCHFV and Theileria/Babesia spp.
Conclusions: Public health and veterinary professionals should be
aware of diagnosing possible diseases or outbreaks in vertebrates.
KEYWORDS: Ticks; Tick-borne diseases; Vector-borne diseases;
Iran
1. Introduction
Ticks are external obligatory blood-sucking parasites of
vertebrates (phylum Arthropoda; class Arachnida) that fall into
three families including Ixodidae (hard ticks), Argasidae (soft
ticks), and Nuttalliellidae[1]. Ticks are the primary vectors and
reservoirs for different pathogens including viruses, bacteria,
and protozoa all over the world, which pose significant threats
to human and animal health[2,3]. Tick-borne pathogens cause
thousands of disease cases in human populations worldwide with
the animal cases seeming to be more than humans[4]. Different
species of ticks are able to transmit different diseases. And
Crimean-Congo hemorrhagic fever (CCHF), Colorado tick fever,
Q fever, borreliosis, relapsing fever, theileriosis, babesiosis,
anaplasmosis, ehrlichiosis and Rocky Mountain spotted fever are
Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
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How to cite this article: Khoobdel M, Jafari AS, Telmadarraiy Z, Sedaghat MM,
Bakhshi H. Tick-borne pathogens in Iran: A meta-analysis. Asian Pac J Trop Med
2021; 14(11): 486-504.
Meta-Analysis
To whom correspondence may be addressed. E-mail: hbakhshi89@gmail.com
Article history: Received 15 June 2021 Revision 21 October 2021
Accepted 22 November 2021 Available online 30 November 2021
10.4103/1995-7645.329009
Significance
Several studies have shown the presence of tick-borne pathogens
in ticks in Iran; however, as far as our knowledge, there is no
meta-analysis available for estimation of ticks infected with tick-
borne pathogens. Our analysis showed that the overall estimated
presence of pathogens in tick vectors in Iran was 8.6% (95%
CI 7.0%-10.6%, P<0.001). Furthermore, 28 tick species in 9
genera were found to be infected with at least 20 pathogens in 10
genera.
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Tick-borne diseases in Iran
among the most significant tick-borne diseases caused by these
pathogens[5]. The spectrum of tick-borne diseases of both medical
and veterinary importance has increased in recent years as a result
of advances in molecular biology. New microorganisms are being
detected in ticks collected in different countries, and the list of
potential tick-transmissible pathogens is updating[6]. Problems
caused by tick infestations are not limited only to transmission of
pathogens. Bite stress, production loss, physical damage, anemia
and poisoning are other aspects of tick bites[7]. Furthermore,
the importance of animal productions in the economy and food
industry around the world is undeniable[8]. Animal health can be
altered by the direct and indirect effects caused by the bites of
ticks and tick-borne diseases, leading to noteworthy production
decrement of meat, milk, eggs, and leathers. In some severe cases,
tick-borne pathogens lead to the death of humans and animals.
Indirect effects are related to the costs associated to the treatment
and control[8]. From past to present, ticks and tick-borne diseases
have been recognized as a threat for human and animal health.
Ticks are responsible for the majority of vector-borne diseases in
Asia, America and Europe[9].
Iran, covering an area of 1 648 195 km2, with a population of 83
million, is located in the Middle East. This country is located in
Palearctic and Oriental zoogeographic regions, with different types
of climate: mild and quite wet on the coast of the Caspian Sea,
continental and arid in the plateau, cold in high mountains, desert
and hot on the southern coast and in the southeast, resulting in
diversity of tick species[10,11]. Ecology of ticks, their interactions
with environment and risk of infection by tick-borne pathogens
are directly related to the spatial and temporal variations. As a
result, diversity of climate, as well as the vast geographical area,
increases the diversity of tick populations which leads to the risk
of transmission of different tick-borne pathogens[12]. To date, it
has been reported that 46 species of ticks (10 Argasidae and 36
Ixodidae) in 10 genera occur in the country[13].
Tick species can be considered as sentinels to track the circulation
of tick-borne pathogens before an outbreak breaks out in humans
and animals. Although many studies revealed data about prevalence
of different tick-borne pathogens in different areas of Iran, as far
as our knowledge, there is no comprehensive data available for
consideration and estimation of the damages caused by pathogens
transmitted by ticks, on the economy and public health in Iran.
For this reason, performing an updated regional review and meta-
analysis on the studies conducted on the prevalence of tick-borne
pathogens in different provinces of this country is highly necessary.
Considering the damages caused by tick-borne diseases on the
public health, animal husbandry, and Iran tourism industry, the
current study attempted to determine and highlight the presence of
pathogens in tick vectors and epidemiological aspects of tick-borne
diseases in Iran.
2. Materials and methods
2.1. Searching approach
The present meta-analysis was performed according to the
guidelines of preferred reporting items for systematic reviews
and meta-analyses statement. In this regional meta-analysis study,
nine English and Persian language databases including PubMed,
Google Scholar, Science Direct, Scopus, Web of Science, Magiran,
Civilica, Iranian Research Institute for Information Science and
Technology (IranDoc), and Scientific Information Database
(SID) were selected to explore the articles and data with no time
limitation (last updated: 7 March, 2021). Duplicate articles,
case series, animal-based studies, human-based studies and
studies carried out in other countries were excluded. All studies,
representing the prevalence of tick-borne pathogens in ticks as
hosts/reservoirs were concerned and all PRISMA criteria have
been met (Figure 1).
Totally, 95 articles and data fit into the criteria. Then, author(s)
names, year of publication, province of study, tick vectors,
pathogens, the number of examined ticks and the number of
positive ticks were extracted from the collected data. The search
was conducted using English and Persian language keywords with
different patterns (e.g.: Tick, Iran, Anaplasma, Babesia, Theileria,
Crimean-Congo hemorrhagic fever virus, CCHFV, Ehrlichia,
Agyptinella, Francisella, Brucella, Borrelia, Coxiella, and Rickettsia).
Advanced search options and Boolean operators 'AND' and 'OR'
were also used to find more relevant records.
2.2. Paper selection
PICO process or framework (Population, Intervention,
Comparator and Outcome) is a common method for formulating
a systematic review queries. However, this format is not suitable
for prevalence studies. Quality assessment for the included studies
of the present research were setup and developed according to
CoCoPop structure [Co (Condition) = infection by pathogens; Co
(Context) = provinces of Iran; Pop (Population) = ticks]. Studies and
the selected data were independently analyzed and the eligibility
was determined by HB and ASJ. Disagreements were resolved by
MK.
2.3. Meta-analysis
Initially, the prevalence of each genus of pathogen (with 95%
confidence intervals) was calculated separately for each province
(at least two studies were needed for calculation of each pathogen
in separate provinces). Then, an overall prevalence was calculated
for all pathogens in respect to each province. Furthermore, the total
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488 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
prevalence for each pathogen in Iran was estimated. Cochran Q test
(P<0.05 shows statistically significant heterogeneity) and I2 test
[25% (low), 50% (moderate), and 75% (high) heterogeneity] were
used to evaluate heterogeneity among studies. To compute overall
size effect (Q<0.05), random model was used; otherwise (Q>0.05),
fixed model was assessed. For determination of publication
bias, Egger’s and Begg's tests were applied (P>0.05 indicates
a reasonable publication bias). Also, a funnel plot was used to
visualize the publication bias. P<0.05 was considered statistically
significant for statistical analysis of prevalence. All statistical
analyses were performed using Comprehensive Meta-Analysis
version 2 (Biostat, USA).
3. Results
Among all databases screened, 3 328 records were identified
through database searching; then, a total of 95 publications were
selected and included in this review. Among these 95 publications,
33 521 ticks were surveyed and 5 673 were positive according
to different detection methods in all provinces of Iran. Of all 46
species of ticks (in 10 genera) which occur in Iran[13], 28 species
(in 9 genera) including Alveonasus (1 species: Al. canestrinii), Argas
(2 species: Ar. persicus, Ar. reflexus), Boophilus (Boophilus spp.),
Dermacentor (2 species: D. marginatus, D. niveus), Haemaphysalis
(4 species: Ha. concinna, Ha. inermis, Ha. punctata, Ha. sulcata),
Hyalomma (10 species: H. aegyptium, H. anatolicum, H. asiaticum,
H. detritum, H. dromedarii, H. excavatum, H. marginatum, H .
rufipes, H. schulzei, H. scupense, H. sp.), Ixodes (1 species: I. ricinus),
Ornithodoros (3 species: O. erraticus, O. lahorensis, O. tholozani), and
Rhipicephalus (5 species: R. annulatus, R. appendiculatus, R. bursa,
R. sanguineus, R. turanicus, R. spp.) were found to be infected with
at least 20 pathogens (in 10 genera) including Aegyptianella (1
species: Ae. pullorum), Anaplasma (4 species: An. ovis, An. bovis, An.
phagocytophilum, An. marginale, An. spp.), Babesia (3 species: Ba.
ovis, Ba. bigemina, Ba. occultans, Ba. spp.), Borrelia (3 species: Bo.
microti, Bo. anserina, Bo. persica, Bo. sp.), Brucella (Brucella sp.),
Orthonairovirus (1 virus: CCHFV), Coxiella (1 species: Cx. burnetii),
Ehrlichia (2 species: Eh. canis, Eh. ovina, Eh. spp.), Rickettsia (1
species: Ri. hoogstraalii, Ri. sp.), Theileria (4 species: Th. annulata,
Th. lestoquardi, Th. ovis, Th. equi, Th. spp.), as well as unspecified
An. centrale/An. bovis (Table 1). In this review, D. marginatus, D.
niveus, H. detritum and H. scupense were considered as separate
species.
Among the provinces where ticks were found to be infected with
different genera of pathogens (including CCHFV), Lorestan (7
genera), Ardabil (6 genera), Golestan (5 genera), and Sistan and
Baluchestan (5 genera) provinces had the most number of ticks
infected with different genera of pathogens (Table 2).
Among 31 provinces of Iran, 26 provinces were surveyed in
Figure 1. Fowchart of studies selection in terms of tick-borne pathogens in Iran.
Records identified through
database searching (n=3
328)
Additional records identified through
other sources e.g. experts in the field
of vector-borne diseases (n=1)
Records after dulpicates removed (n=2 749)
Records screened (n=580)
Full-text articles assessed
for eligibility (n=97)
Full-text articles excluded
due to no available data (n=2)
Studies included in
meta-analysis (n=95)
Records excluded due to not
meeting inclusion criteria (n=483)
-case series (n=5)
-animal-based studies (n=97)
-human-based studies (n=240)
-studies from other countries
(n=141)
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Table 1. Summary of tick-borne pathogens in tick species in different provinces of Iran.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Ardabil Ba. ovis 2017 200/10 2 8[14]
Ba. sp. 2016 289/0 [15]
Total 2 studies 489/10 2 8
Bo. sp. 2014 17/7 7[16]
Bo. sp.a,# 2002 1 421/NA [17]
Total 2 studies 17/7 7
CCHFV 2010 130/36 1 1 1 6 9 18 [18]
Total 1 study 130/36 1 1 1 6 9 18
Cx. burnetii 2020 280/40 24 8 8 [19]
Total 1 study 280/40 24 8 8
Eh. canis 2013 146/64 9 4 9 12 30 [20]
Total 1 study 146/64 9 4 9 12 30
Th. annulata 2016 289/69 47 13 9[15]
Total 1 study 289/69 47 13 9
Total 7 pathogens 7 studies 1 062/226 11 8 1 75 22 17 1 1 6 9 7 30 38
Azerbaijan,
East
An./Eh. sp.b,## 2021 168/37 2 216 5 4 5 3 [21]
An. ovis 2016 215/122 3 119 [22]
An./Ri. sp.b2021 30/10 10 [23]
Total 3 studies 413/169 12 219 5 4 119 5 3
Ba./Th. sp.c,## 2021 182/0 [21]
Ba./Th. sp.c2018 93/4 3 1 [24]
Total 2 studies 275/4 3 1
Br. sp.##,*** 2021 133/20 6 2 3 5 4 [21]
Total 1 study 133/20 6 2 3 5 4
CCHFV 2016 177/9 6 2 1[25]
Total 1 study 177/9 6 2 1
Total 5 pathogens 5 studies 998/202 27 419 8 11 1119 9 4
Azerbaijan,
west
Ba. bigemina 2017 530/52 22 18 12 [26]
Ba. ovis 2014 848/94 94 [27]
Ba. sp. 2013 211/9 1 8 [28]
Total 3 studies 1 589/155 22 113 20
Th. lestoquardi 2017 315/37 11 15 11 [29]
Total 1 study 315/37 11 15 11
Total 4 pathogens 4 studies 1 904/192 11 15 22 113 20 11
Fars Ba. ovis 2013 171/15 3 1 110 [30]
Total 1 study 171/15 3 1 110
Eh. ovina 2005 89/23 23 [31]
Total 1 study 89/23 23
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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490 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
Table 1. Continued.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
CCHFV 2016 200/9 3 2 4 [32]
Total 1 study 200/9 3 2 4
Th. lestoquardi 2013 171/5 2 1 2 [30]
Th. lestoquardi/Th.
sp.c2005 89/53 53 [31]
Th. ovis 2013 90/5 5 [33]
Total 3 studies 350/63 55 1 7
Total 5 pathogens 4 studies 550/110 84 3 1 4 117
Gilan An. marginale 2020 30/1 1[34]
An. ovis 2016 53/25 24 1 [22]
Total 2 studies 83/26 24 1 1
Bo. sp. 2020 507/2 1 1 [35]
Total 1 study 507/2 1 1
Br. spp.e2017 1/1 1[36]
Total 1 study 1/1 1
Total 4 pathogens 4 studies 591/29 124 1 1 1 1
Golestan An./ Eh. sp.b2017 48/12 2 1 2 2 5 [37]
Total 1 study 48/12 2 1 2 2 5
Ba. occultans 2017 48/1 1 [37]
Ba. ovis 2017 48/2 1 1 [37]
Total 1 study 48/3 1 1 1
Bo. sp. 2020 507/42 126 15 [35]
Total 1 study 507/42 126 15
CCHFV 2017 130/7 3 2 1 1 [38]
Total 1 study 130/7 3 2 1 1
Th. ovis 2017 48/14 1 2 1 3 1 2 1 3 [37]
Total 1 study 48/14 1 2 1 3 1 2 1 3
Total 6 pathogens 3 studies 685/78 7 4 1 5 1 5 1 3 36 15
Hamadan Bo. persica 2003 82/3 3[39]
Bo. persica 1998 1 157/0 [40]
Total 2 studies 1 239/3 3
CCHFV 2016 100/7 1 2 4 [41]
CCHFV 2010 328/63 2 2 48 11 [42]
CCHFV 2008 88/10 1 1 2 3 1 2 [43]
Total 3 studies 516/80 2 1 3 148 2 3 3 17
Total 2 pathogens 5 studies 1 755/83 2 1 3 148 2 3 3 3 17
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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Tick-borne diseases in Iran
Table 1. Continued.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Hormozgan An. sp. 2020 30/1 1[34]
Total 1 pathogen 1 study 30/1 1
Ilam CCHFVa2015 137/9 [44]
Total 1 pathogen 1 study 137/9
Isfahan CCHFV 2016 210/11 1 3 2 2 3 [45]
Total 1 pathogen 1 study 210/11 1 3 2 2 3
Kerman An. sp. 2020 96/23 2 111 9 [46]
Total 1 study 96/23 2 111 9
Ba. sp. 2016 211/0 [47]
Total 1 study 211/0
CCHFV 2020 258/0 [48]
CCHFV 2018 203/0 [49]
Total 2 studies 461/0
Cx. burnetii 2018 375/47 47 [50]
Cx. burnetii 2011 245/18 15 3 [51]
Total 2 studies 620/65 15 50
Eh. sp. 2016 408/25 25 [52]
Total 1 study 408/25 25
Total 5 pathogens 7 studies 1 796/113 17 111 84
Kermanshah CCHFV 2016 131/5 3 1 1 [53]
Total 1 study 131/5 3 1 1
Th. annulata 2019 420/20 20 [54]
Th. lestoquardi 2019 420/50 10 40 [54]
Th. ovis 2019 420/60 20 40 [54]
Total 1 study 420/130 30 20 80
Total 4 pathogens 2 studies 551/135 33 120 1 80
Khorasan,
North
Ba. caballi 2014 37/0 [55]
Ba. ovis 2014 44/2 1 1 [56]
Ba. motasi 2014 44/0 [56]
Total 2 studies 81/2 1 1
CCHFV 2019 62/5 3 2 [57]
CCHFV 2016 134/0 [58]
Total 2 studies 196/5 3 2
Th. equi 2014 37/3 2 1[55]
Th. lestoquardi 2012 220/5 5 [59]
Th. ovis 2012 220/10 5 5 [59]
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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492 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
Table 1. Continued.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Th. lestoquardi/
Th. ovisc2012 220/5 5 [59]
Total 2 studies 257/23 2 15 1 5
Total 7 pathogens 5 studies 497/30 5 16 1 2 6
Khorasan,
Razavi
Ba. sp. 2015 246/0 [60]
Ba. sp. 2013 429/0 [61]
Total 2 studies 675/0
Bo. persica 2016 996/52 52 [62]
Total 1 study 996/52 52
CCHFV 2020 100/6 6 [63]
CCHFV 2016 152/0 [58]
CCHFV 2015 105/4 1 1 1 1 [64]
Total 3 studies 357/10 1 7 1 1
Th. annulata 2002 510/231 1 230 [65]
Th. lestoquardi 2013 429/10 10 [61]
Th. lestoquardi 2013 169/5 5 [66]
Th. ovis 2013 429/25 25 [61]
Th. ovis 2013 169/10 10 [66]
Th.ovis/Th.
lestoquardic2013 429/0 [61]
Th. sp. 2015 246/1 1 [60]
Total 4 studies 1 354/282 1 230 1 50
Total 7 pathogens 8 studies 2 707/344 2 230 8 52 151
Khorasan,
South
An. ovis## 2020 100/20 20 [67]
An. ovis 2016 59/25 1 1 9 3 1 4 4 1 1 [22]
Total 2 studies 159/45 1 1 9 3 1 4 4 1 1 20
CCHF## 2020 100/7 3 3 1 [67]
CCHFV 2016 194/49 7 42 [58]
Total 2 studies 294/56 7 3 3 42 1
Cx. burnetii## 2020 100/0 [67]
Total 1 study 100/0
Total 3 pathogens 3 studies 553/101 1 1 16 6 4 46 4 1 2 20
Khuzestan Th. spp. 2018 655/67 54 10 2 1 [68]
Total 1 pathogen 1 study 655/67 54 10 2 1
Kohgiluyeh and
Boyer-Ahmad
CCHFV 2019 469/1 1 [69]
Total 1 pathogen 1 study 469/1 1
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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Table 1. Continued.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Kurdistan Ba. sp. 2018 3 107/1 303 13 221 18 25 31 283 385 327 [70]
Total 1 study 3 107/1 303 13 221 18 25 31 283 385 327
Bo. persica 2009 96/19 19 [71]
CCHFV 2012 90/5 1 1 3 [73]
Total 1 study 90/5 1 1 3
Th. sp. 2018 3 107/939 431 101 41 78 77 113 98 [70]
Total 1 study 3 107/939 431 101 41 78 77 113 98
Total 4 pathogens 4 studies 3 393/2269 13 653 119 66 1109 319 360 498 425
Lorestan Ae. pullorum 2018 20/5 5 [74]
Total 1 study 20/5 5
An. ovis 2020 70/14 11 3 [34]
Total 1 study 70/14 11 3
Bo. anserina 2017 212/140 140 [75]
Total 1 study 212/140 140
Cx. burnetii 2020 160/80 60 20 [76]
Total 1 study 160/80 60 20
CCHFV 2015 434/29 12 7 1 9 [77]
Total 1 study 434/29 12 7 1 9
Ri. hoogstraalii 2020 64/6 6 [78]
Total 1 study 64/6 6
Th. lestoquardi## 2015 54/5 5 [79]
Th. lestoquardi 2015 171/1 1 [30]
Th. lestoquardi## 2013 54/5 5 [80]
Total 3 studies 279/11 10 1
Th. ovis## 2014 152/37 37 [79]
Th. ovis## 2015 152/37 37 [80]
Total 2 studies 304/74 74
Total 8 pathogens 9 studies 1 543/359 60 171 22 18 1 1 86
Mazandaran An. bovis 2013 618/364 422 6105 5 119 8 95 [81]
An. bovis/ An.
centraleb2014 101/50 1 14 1 34 [82]
An.
phagocytophilum 2004 98/5 5 [83]
Total 3 studies 817/419 422 6106 24 1 119 42 95
Bo. sp. 2020 507/27 16 1 7 3 [35]
Total 1 study 507/27 16 1 7 3
Cx. burnetii 2005 605/0 [84]
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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494 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
Table 1. Continued.
Provinces Pathogens screened*Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Total 1 study 605/0
CCHFV 2017 130/7 3 2 1 1 [38]
CCHFV 2016 58/1 1 [85]
Total 2 studies 188/8 3 2 1 2
Th. ovis 2012 20/1 1 [86]
Th. /Ba. sp.c2012 20/10 10 [86]
Total 1 study 20/11 11
Total 7 pathogens 8 studies 2 137/465 422 6106 3 2 1 40 1120 62 98
Qazvin Bo. microti## 2007 24/12 12 [87]
Bo. persica 2010 344/16 16 [88]
Bo. Persica## 2007 231/20 20 [87]
Bo. sp. 2010 344/3 3[88]
Total 2 studies 599/51 3 36
Total 3 pathogens 2 studies 599/51 12 3 36
Qom CCHFV 2012 88/6 6 [89]
Total 1 Pathogen 1 study 88/6 6
Semnan Bo. persica 1999 5 938/243 243 [90]
Total 1 study 5 938/243 243
CCHFV 2018 93/4 1 2 1 [91]
Total 1 study 93/4 1 2 1
Total 2 pathogens 2 studies 6 031/247 1 2 243 1
Sistan and
Baluchestan
An. / Eh. sp.b,** 2019 256/175 79 24 232 36 2[92]
An. marginale 2021 248/12 12 [93]
An. ovis## 2020 100/20 20 [94]
An. ovis / Eh. sp.b2014 53/14 8 3 1 2 [95]
Total 4 studies 657/221 107 27 232 36 2 1 2 12
Cx. burnetii## 2020 100/0 [94]
Cx. burnetii 2017 583/18 7 6 5 [96]
Cx. burnetiia2016 1 305/105 [97]
Total 3 studies 1 988/123 7 6 5
Eh. sp. 2017 50/5 5 [98]
Total 1 study 50/5 5
CCHFV## 2020 100/0 [94]
CCHFV 2017 49/3 1 1 1[99]
CCHFV 2013 140/6 1 5 [100]
Total 3 studies 289/9 1 1 5 1 1
Th. sp. 2019 110/18 9 4 5 [101]
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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Tick-borne diseases in Iran
Table 1. Continued.
Provinces Pathogens screened* Year of
study
Total tested/
positive tick
specimens
Tick vectors
Ref.
Th. sp. 2003 346/36 30 6 [102]
Th. / Ba. sp.b2018 93/12 2 10 [24]
Total 3 studies 549/66 2 30 9 20 5
Total 7 pathogens 12 studies 3 533/424 2 1 144 36 2 32 6 37 2 6 33 1 17
Tehran CCHFV 2017 89/0 [103]
Total 1 study 89/0
Th. annulata 2020 27/18 18 [104]
Total 1 study 27/18 18
Total 2 pathogens 2 studies 116/18 18
Yazd CCHFV 2011 140/8 1 1 2 3 1 [105]
Total 1 study 140/8 1 1 2 3 1
Th. annulata 2015 250/15 15 [106]
Th. lestoquardi 2015 250/0 [106]
Total 1 study 250/15 15
Total 3 pathogens 2 studies 390/23 16 1 2 3 1
Unspecified
Locationsf
Ba. sp. 2013 211/9 1 8 [28]
Ba. sp. 2007 269/34 20 6 8 [107]
Ri. sp. 2020 61/36 20 1 5 10 [108]
Total 2 pathogens 3 studies 541/79 20 1 5 10 21 14 8
Total 22 pathogensg95 studies 33 521 /5 673h60 192 2 1 79 922 8120 10 11 155 238 125 94 363 146 13515 43 12 132 360 384 1799 851 23 303 NA
Totally, 95 studies were included; of 31 provinces, the infection of different ticks by different pathogens were recorded in 26 provinces; at least 20 pathogens (in 10 genera) were detected in 28 species of tick vectors (in 9 genera);
Abbreviations: Ba: Babesia; Bo: Borrelia; Cx: Coxiella; Eh: Ehrlichia; Ri: Rickettsia; Th: Theileria; An: Anaplasma; Ae: Aegyptianella; Br: Brucella, Brucellaceae; Al: Alveonasus; Ar: Argas; D: Dermacentor; Ha: Haemaphysalis; H:
Hyalomma; I: Ixodes; O: Ornithodoros; R: Rhipicephalus; NA: not applicable.
*: In this table, all unidentified species of pathogens (e.g.: Ba. sp.) have been considered as separate pathogens in the meta-analysis; in Ilam province, the species of CCHFV vector(s) have not been mentioned in the source.
**: In this review, total positive ticks have been reported as 175 in its source; however, the addition of individual positive ticks is reported as 174. For this reason, we changed the positive number of H. anatolicum from 78 to 79.
***: Abdoli et al., have reported Brucellaceae in this research. We considered this finding as Brucella in our analysis.
#: In this study, the total number of positive (infected to pathogen) ticks as well as their species has not been reported. As a result, the number related to this research has not been concluded in our table.
##: In these studies, the total number of tested ticks has been reported in terms of each specific pathogen. As a result, total sample size of the study may be different from each pathogen’s sample size.
a: In these investigations, only the exact number of positive ticks were reported and the number of positive species were not specified
b: In these investigations, further to insufficient data regarding genus of pathogen, we considered the pathogen of these studies as Anaplasma sp. in the meta-analysis.
c: In these investigations, further to insufficient data regarding genus of pathogen, we considered the pathogen of these studies as Theileria sp. in the meta-analysis.
d: In this study, due to insufficient data regarding the number of positive ticks, the percentage of infection was used as the number of positive samples.
e: This study was not included in the meta-analysis due to sample size less than 2.
f: In some investigations, the province of the infected tick(s) was not specified. We have grouped these studies as “unspecified location”.
g: Of 22 pathogens investigated, the infection of ticks to Ba. caballi and Ba. ovis was not confirmed; ticks were found to be infected with 20 pathogens.
h: In some investigations, the species or genera of positive ticks have not been stated. In such cases, we have included the studies as well. So, the sum of the total positive ticks differs with the total number of the ticks
morphologically identified at the genus/species level.
Al. canestrinii
Ar. persicus
Ar. reflexus
Boophilus spp.
D. marginatus
D. niveus
Ha. concinna
Ha. inermis
Ha. punctata
Ha. sulcata
H. aegyptium
H. anatolicum
H. asiaticum
H. detritum
H. dromedarii
H. excavatum
H. marginatum
H. rufipes
H. schulzei
H. scupense
H. sp.
I. ricinus
O. erraticus
O. lahorensis
O. tholozani
R. annulatus
R. appendiculatus
R. bursa
R. sanguineus
R. sp.
R. turanicus
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496 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
Table 2. Different genera of pathogens (as well as CCHFV) detected in tick vectors in different provinces of Iran.
Province Total tested/positive tick(s) Positive tick vector(s) Pathogen(s)
Ardabil 1 062/226
D. marginatus; D. niveus; H. aegyptium; H. anatolicum; H.
asiaticum; H. excavatum; H. marginatum; H. schulzei; H. sp.; O.
lahorensis; O. tholozani; R. bursa; R. sanguineus
Babesia; Borrelia; CCHFV;
Coxiella; Ehrlichia; Theileria
Azerbaijan, East 998/202 D. marginatus; Ha. sulcata; H. anatolicum; H. asiaticum; H.
marginatum; I. ricinus; O. lahorensis; R. bursa; R. sanguineus
Anaplasma; Babesia; Brucella;
CCHFV
Azerbaijan, West 1 904/192 D. marginatus; H. marginatum; R. annulatus; R. bursa; R.
sanguineus; R. turanicus Babesia; Theileria
Fars 550/110 H. anatolicum; H. marginatum; H. sp.; R. sanguineus; R. sp.; R.
turanicus
Babesia; Ehrlichia; CCHFV;
Theileria
Gilan 591/29 Boophilus spp.; D. marginatus; I. ricinus; R. annulatus; R.
sanguineus; R. sp. Anaplasma; Borrelia; Brucella
Golestan 685/78
H. anatolicum; H. dromedarii; H. excavatum; H. marginatum;
H. rufipes; H. scupense; I. ricinus; R. bursa; R. sanguineus; R.
turanicus
Anaplasma; Babesia; Borrelia;
CCHFV; Theileria
Hamadan 1 755/83
Ar. reflexus; Ha. punctata; H. anatolicum; H. asiaticum; H.
detritum; H. dromedarii; H. marginatum; O. tholozani; R.
bursa; R. sanguineus
Borrelia; CCHFV
Hormozgan 30/1 H. dromedarii Anaplasma
Ilam 137/9 NA CCHFV
Isfahan 210/11 Ha. sulcata; H. anatolicum; H. asiaticum; H. sp.; R. sanguineus CCHFV
Kerman 1 796/113 H. anatolicum; H. asiaticum; H. marginatum; R. sanguineus Anaplasma; Coxiella; Ehrlichia
Kermanshah 551/135 H. anatolicum; H. asiaticum; H. marginatum; R. sanguineus; R.
turanicus CCHFV; Theileria
Khorasan, North 497/30 H. anatolicum; H. marginatum; R. bursa; R. sanguineus; R.
turanicus Babesia; CCHFV; Theileria
Khorasan, Razavi 2 707/344 H. asiaticum; H. excavatum; H. marginatum; O. tholozani; R.
appendiculatus; R. turanicus Borrelia; CCHFV; Theileria
Khorasan, South 553/101
Ar. persicus; D. niveus; H. anatolicum; H. asiaticum; H.
detritum; H. dromedarii; H. marginatum; O. lahorensis; R.
sanguineus; R. sp.
Anaplasma; CCHFV
Khuzestan 655/67 H. anatolicum; H. asiaticum; H. detritum; H. dromedarii Theileria
Kohgiluye and Boyer-
Ahmad 469/1 R. bursa CCHFV
Kurdistan 3 393/2 269
Ha. punctata; H. anatolicum; H. asiaticum; H. detritum; H.
dromedarii; H. excavatum; H. marginatum; O. tholozani; R.
annulatus; R. bursa; R. sanguineus
Babesia; Borrelia; CCHFV;
Theileria
Lorestan 1 543/359 Al. canestrinii; Ar. persicus; H. anatolicum; H. asiaticum; H.
detritum; H. marginatum; R. sanguineus
Aegyptianella; Anaplasma;
Borrelia; Coxiella; CCHFV;
Rickettsia; Theileria
Mazandaran 2 137/465
D. marginatus; Ha. concinna; Ha. inermis; Ha. punctata; H.
anatolicum; H. dromedarii; H. marginatum; I. ricinus; R.
annulatus; R. bursa; R. sanguineus; R. turanicus
Anaplasma; Borrelia; CCHFV;
Theileria
Qazvin 599/51 O. erraticus; O. lahorensis; O. tholozani Borrelia
Qom 88/6 H. marginatum CCHFV
Semnan 6 031/247 H. anatolicum; H. dromedarii; O. tholozani; R. sanguineus Borrelia; CCHFV
Sistan and Baluchestan 3 533/424
D. marginatus; Ha. inermis; H. anatolicum; H. asiaticum; H.
detritum; H. dromedarii; H. excavatum; H. marginatum; H.
schulzei; H. sp.; R. sanguineus; R. sp.; R. turanicus
Anaplasma; Coxiella;
Ehrlichia; CCHFV; Theileria
Tehran 116/18 R. sanguineus Theileria
Yazd 390/23 H. anatolicum; H. asiaticum; H. detritum; H. dromedarii; H.
marginatum CCHFV; Theileria
Babesia (7 provinces), Borrelia (10 provinces), CCHFV (19 provinces), Coxiella (4 provinces), Ehrlichia (4 provinces), Theileria (14 provinces), Anaplasma
(9 provinces), Brucella (2 provinces), Aegyptianella (1 province), Rickettsia (1 province); Positive tick species in different provinces are as follows: Al.
canestrinii (1 province), Ar. persicus (2 provinces), Ar. reflexus (1 province), D. marginatus (6 provinces), D. niveus (2 provinces), H. aegyptium (1 province), H.
anatolicum (17 provinces), H. asiaticum (13 provinces), H. detritum (7 provinces), H. dromedarii (10 provinces), H. excavatum (5 provinces), H. marginatum
(17 provinces), H. rufipes (1 province), H. schulzei (2 provinces), H. scupense (1 province), Ha. concinna (1 province), Ha. inermis (2 provinces), Ha. punctata
(3 provinces), Ha. sulcata (2 provinces), I. ricinus (4 provinces), O. erraticus (1 province), O. lahorensis (4 provinces), O. tholozani (6 provinces), R. annulatus
(4 provinces), R. appendiculatus (1 province), R. bursa (9 provinces), R. sanguineus (18 provinces), R. turanicus (8 provinces), Boophilus spp. (1 province),
Hyalomma spp. (4 provinces), Rhipicephalus sp. (4 provinces), NA (1 province).
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Tick-borne diseases in Iran
terms of detection of infection of different pathogens in ticks;
meanwhile, the status of tick infection with different pathogens
remained unclear in Alborz, Bushehr, Chaharmahal and Bakhtiari,
Markazi, and Zanjan provinces. The provinces in which the
most studies have been carried out are Sistan and Baluchestan
(12 studies), Lorestan (9 studies), Razavi Khorasan (8 studies),
Mazandaran (8 studies), Kerman (7 studies), and Ardabil (7
studies). On the other hand, Hormozgan, Ilam, Isfahan, Khuzestan,
Kohgiluyeh and Boyer-Ahmad, and Qom were among the least
studied provinces (only one study in each province). More than
60 literatures were related to CCHFV and Theileria/Babesia spp.,
while Aegyptianella, Brucella and Rickettsia were limited to less
than 10 publications (Table 1). According to a random effect
model, the total prevalence of tick-borne pathogens in Iran was
calculated as 8.6% (95% CI 7.0%-10.6%, P<0.001). The highest
and lowest prevalence rate occurred in Kurdistan (20.5%; 95%
CI 14.0%-29.1%, P<0.001), and Khorasan, Razavi (2.4%; 95%
CI 0.8%-6.7%, P=0.008), respectively. In addition, Anaplasma
sp. was the pathogen with the highest statistically significant
prevalence (23.5%; 95% CI 15.1%-34.7%, P<0.001), while the
lowest infection rate belonged to Babesia sp. (4.0%; 95% CI 1.9%-
8.1%, P<0.001) (Table 3).
Statistical analysis revealed that the highest prevalence of
Anaplasma sp., Babesia sp., Borrelia sp., CCHFV, Coxiella sp., and
Theileria sp. occurred in East-Azerbaijan (36.5%; 95% CI 15%-
63.9%, P=0.335), West-Azerbaijan (8.8%; 95% CI 6.1%-12.5%,
P<0.001), Kurdistan (8.5%; 95% CI 1.2%-41.6%, P=0.022),
South-Khorasan (14.3%; 95% CI 3.7%-42.0%, P=0.017), Kerman
(9.9%; 95% CI 5.8%-16.4%, P<0.001), and Mazandaran (21.0%;
95% CI 1.5%-82.4%, P=0.009), respectively. Brucella sp., Ehrlichia
sp., Rickettsia sp., and Aegyptianella sp. did not meet the criteria for
entering province-specific meta-analysis (less than 2 publications
in each province). A forest plot was used to show the prevalence of
tick-borne pathogens across the country (Supplementary Figure 1).
In addition, funnel plot revealed an asymmetry in the funnel which
might indicate that some studies were missed on the right side of
the plot (Figure 2). In line with funnel plot, the results of Egger’s
test (P<0.001) showed a publication bias among studies. Based on
the funnel plot, most of the studies with low prevalence of tick-
borne pathogens were included in this meta-analysis (Figure 2).
Standard error
0.0
0.5
1.0
1.5
2.0
-8 -7 -6 -5 -4 -3 -2 -1 0 1 2 3 4 5 6 7 8
Logit event rate
Figure 2. Funnel plot of standard error by logit event rate.
4. Discussion
As far as we know, the present meta-analysis is the first large-
scale study that examined the prevalence of tick-borne pathogens
in tick vectors in Iran. Overall estimated prevalence of tick-borne
pathogens in Iran was 8.6% (95% CI 7.0%-10.6%, P<0.001).
The greatest infection rates among tick vectors were dedicated
to Rickettsia sp. (P>0.05), and Anaplasma sp., respectively.
Anaplasma species are Gram-negative obligate intraerythrocytic
bacteria (Rickettsiales; Anaplasmataceae) which are of great
veterinary concern. An. marginale, the most probable causative
agent of bovine anaplasmosis, has been reported worldwide. This
pathogen mainly affects ruminants resulting in mild to severe
febrile hemolytic anemia that leads to significant economic
losses[109]. Other species are as follows An. ovis and An. mesaeterum
(in sheep and goat), An. phagocytophilum (in horse, dogs and cats),
An. platys (in dogs) and An. centrale in cattle[110,111]. Although
medically important pathogens such as Borrelia sp., Coxiella sp.,
and CCHFV were less prevalent in ticks according to the pooled
results of literature review, it should be noted that to determine
the epidemiological status of a pathogen, all factors affecting
pathogen’s life cycle must be taken into consideration. For
example, CCHF is endemic in Iran and its neighboring countries
and a significant number of human cases are reported each year.
In a recent review on distribution of ticks and their infection
to CCHFV, the main vectors of CCHF, H. marginatum and H.
anatolicum, have been reported in more than 38.7% of provinces
of Iran[112]. In our review, among all pathogens, CCHFV positive
ticks were reported in 19 provinces. The point may be that in Iran,
the main way of CCHFV transmission is not tick bite. CCHFV
infection in human mostly occurs due to direct contact with
infected livestock (blood, tissues, secretions), which have been
infected by ticks[113,114].
Q fever is a zoonosis caused by the bacterium Cx. burnetii. Human
infection mainly occurs through inhalation of contaminated animal
products, direct contact with infected animals and consumption
of unpasteurized milk or other dairy products contaminated
with this pathogen. Ticks play a key role in transmitting bacteria
between animals, and are considered as reservoirs of Cx.
burnetii bacteria and guarantee the long-term presence of this
microorganism in nature[84]. Borrelia spp. is the causative agent
of Lyme disease and relapsing fever which are zoonotic vector-
borne diseases transmitted primarily by ticks[115]. In a descriptive
and retrospective study during 1997-2006, Masoumi et al. reported
that the disease is detected in humans in 18 provinces of the 31
provinces in Iran[116]. Other reports also revealed that Borrelia
spp. is present in ticks and other vertebrates[35,117]. According
to reports of Cx. burnetii and Borrelia spp. in ticks, humans, and
animals in Iran, Q-fever, Lyme disease and relapsing fever can be
considered as emerging diseases in the country[118-120].
The most infected provinces in terms of tick-borne pathogens
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498 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
Table 3. Meta-analysis result of different genera of pathogens (including CCHFV), detected in each province as well as in the country.
Provinces Pathogens No. of
studies Sample size
Prevalence
(pooled
effect size)
95% CI Heterogeneity
P values of
prevalence
Publication bias
Lower Upper I2(%) Q test
Begg’s test
(2 tailed P
value)
Egger’s test
(2 tailed P
value)
Ardabil Babesia sp. 2 489 0.012 0.000 0.255 81.938 5.537 0.009 NA NA
Tick borne
pathogens 7 1 351 0.186 0.104 0.310 93.410 91.046 <0.001 0.763 0.357
Azerbaijan, East Anaplasma sp. 3 413 0.365 0.158 0.639 95.564 45.088 0.335 1.000 0.678
Theileria sp. 2 275 0.032 0.013 0.077 71.037 3.45 <0.001 NA NA
Tick borne
pathogens 7 998 0.133 0.051 0.305 96.091 153.502 <0.001 0.367 0.051
Azerbaijan, West Babesia sp. 3 1 589 0.088 0.061 0.125 75.961 8.320 <0.001 0.296 0.032
Tick borne
pathogens 4 1 904 0.097 0.074 0.125 67.142 9.130 <0.001 0.308 0.176
Fars Theileria sp. 3 350 0.123 0.009 0.682 97.645 84.928 0.158 1.000 0.081
Tick borne
pathogens 6 810 0.115 0.035 0.316 96.359 137.321 <0.001 0.259 0.045
Gilan Anaplasma sp. 2 83 0.169 0.008 0.830 89.515 9.537 0.326 NA NA
Tick borne
pathogens 3 590 0.049 0.001 0.699 96.472 56.697 0.127 1.000 0.334
Golestan Babesia sp. 2 96 0.033 0.011 0.097 0.000 0.331 <0.001 NA NA
Tick borne
pathogens 6 829 0.066 0.030 0.139 87.992 41.639 <0.001 0.707 0.683
Hamedan Borrelia sp. 2 1 239 0.005 0.000 0.278 88.288 8.538 0.017 NA NA
CCHFV 3 516 0.124 0.066 0.221 78.850 9.456 <0.001 0.296 0.126
Tick borne
pathogens 5 1 755 0.060 0.023 0.149 88.583 35.034 <0.001 0.027 0.001
Hormozgan NA
Ilam NA
Isfahan NA
Kerman Coxiella sp. 2 620 0.099 0.058 0.164 75.927 4.154 <0.001 NA NA
CCHFV 2 461 0.002 0.000 0.015 0.000 0.014 <0.001 NA NA
Tick borne
pathogens 7 1 796 0.060 0.029 0.119 88.637 88.637 <0.001 0.763 0.110
Kermanshah Theileria sp. 3 1 260 0.096 0.055 0.164 90.249 20.511 <0.001 0.296 0.042
Tick borne
pathogens 4 1 391 0.082 0.047 0.139 88.747 26.659 <0.001 0.308 0.164
Khorasan, North Babesia sp. 3 125 0.029 0.009 0.087 0.000 1.209 <0.001 1.000 0.050
CCHFV 2 196 0.023 0.001 0.319 77.002 4.348 0.014 NA NA
Theileria sp. 4 697 0.036 0.024 0.054 37.422 4.794 <0.001 1.000 0.938
Tick borne
pathogens 9 1 018 0.038 0.027 0.054 31.263 11.639 <0.001 0.676 0.219
Khorasan, Razavi Babesia sp. 2 675 0.002 0.000 0.014 0.000 0.000 <0.001 NA NA
CCHFV 3 357 0.044 0.024 0.078 52.013 4.168 <0.001 0.269 0.102
Theileria sp. 7 2 381 0.033 0.007 0.139 98.126 327.182 <0.001 0.367 0.014
Tick borne
pathogens 13 4 409 0.024 0.008 0.067 97.677 516/536 <0.001 0.076 0.008
Khorasan, South Anaplasma sp. 2 159 0.299 0.129 0.552 88.666 8.823 0.115 NA NA
CCHFV 2 294 0.143 0.037 0.420 12.466 91.978 0.017 NA NA
Tick borne
pathogens 5 553 0.176 0.089 0.317 87.984 33.288 <0.001 0.426 0.243
Khuzestan NA
Kohgiluyeh and
Boyer-Ahmad NA
Kurdistan Borrelia sp. 2 196 0.085 0.012 0.416 90.511 10.538 0.022 NA NA
Tick borne
pathogens 5 6 500 0.205 0.140 0.291 97.348 150.833 <0.001 0.462 0.240
Lorestan Theileria sp. 5 583 0.125 0.064 0.228 83.837 24.748 <0.001 0.086 0.000
Tick borne
pathogens 11 1 543 0.172 0.087 0.314 96.425 279.715 <0.001 0.061 0.064
Mazandaran Anaplasma sp. 3 817 0.323 0.131 0.601 96.098 51.254 0.207 0.296 0.231
CCHFV 2 188 0.047 0.023 0.090 15.618 1.185 <0.001 NA NA
Theileria sp. 2 40 0.210 0.015 0.824 85.552 6.921 0.009 NA NA
Tick borne
pathogens 9 2 157 0.100 0.031 0.277 97.765 357.961 0.001 0.754 0.049
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Tick-borne diseases in Iran
were Kurdistan (20.5%), Ardabil (18.6%), South Khorasan
(17.6%), Lorestan (17.2%), East Azerbaijan (13.3%) and Fars
(11.5%), respectively. Geographically, these provinces (except
South Khorasan) are located in the western parts of Iran. Therefore,
it can be concluded that although tick-borne pathogens have been
reported from different regions of Iran, the western part of the
country is more infected than other regions. This high prevalence
can be justified due to high livestock population, common border
with neighboring countries and traditional livestock holding
methods with low hygiene.
In this analysis, 26 out of 31 provinces were surveyed regarding
tick-borne pathogen detection in ticks; meanwhile, the status of
infection of ticks to different pathogens remained unclear in five
provinces: Alborz, Bushehr, Chaharmahal and Bakhtiari, Markazi,
and Zanjan. Due to the importance of ticks and their impact on
human and animal health, it is highly advisable to conduct studies
concerning tick-borne diseases to clarify the status of these
provinces. Vector surveillance seems to be vital for observing the
presence or occurrence of emerging and reemerging tick borne
diseases in Iran and provides a preliminary warning for predicting
probable epidemics.
In our analysis, H. anatolicum (20.35%), R. sanguineus (15.00%),
and R. bursa (14.08%), were the most prevalent infected ticks in
Iran. Genera of Hyalomma species have received much attention
due to the role in the transmission of Theileria spp., Babesia
spp., Rickettsia spp., and CCHFV. R. sanguineus (brown dog tick,
kennel tick) is found worldwide with an interest toward warmer
climates (tropics and sub-tropics)[121]. Dogs are specific host for
R. sanguineus, however, it can be found on domestic ruminants
and other vertebrates. Several pathogens such as Ba. canis, Cx.
burnetii, Eh. canis, Ri. conorii, Ri. rickettsii, Theileria sp., Anaplasma
sp., and CCHFV have been isolated from R. sanguineus[122-124].
R. bursa is common among livestock transmitting the protozoans
Ba. bigemina, Ba. caballi, Th. equi and Ba. bovis[125]. Following
these highly infected vectors, much lower prevalence levels were
detected in R. appendiculatus, H. schulzei, H. rufipes, H. aegyptium
Table 3. Continued.
Provinces Pathogens No. of
studies Sample size
Prevalence
(pooled
effect size)
95% CI Heterogeneity
P values of
prevalence
Publication bias
Lower Upper I2(%) Q test
Begg’s test
(2 tailed P
value)
Egger’s test
(2 tailed P
value)
Qazvin Borrelia sp.
= Tick borne
pathogens
4 943 0.077 0.020 0.253 94.702 56.624 0.001 0.734 0.993
Qom NA
Semnan Tick borne
pathogens 2 6 031 0.041 0.036 0.046 0.000 0.010 <0.001 NA NA
Sistan and
Baluchestan
Anaplasma sp. 4 657 0.241 0.054 0.641 98.232 169.554 0.193 0.734 0.083
Coxiella sp. 3 1 988 0.041 0.015 0.103 89.324 18.734 <0.001 1.000 0.374
CCHFV 3 289 0.040 0.018 0.090 28.217 2.786 <0.001 1.000 0.430
Theileria sp. 3 549 0.122 0.097 0.152 29.684 2.844 <0.001 1.000 0.471
Tick borne
pathogens 14 3 533 0.093 0.043 0.188 97.420 503.959 <0.001 1.000 0.392
Tehran Tick borne
pathogens 2 116 0.110 0.000 0.975 93.702 15.878 0.477 NA NA
Yazd Theileria sp. 2 500 0.015 0.001 0.299 82.719 5.787 0.014 NA NA
Tick borne
pathogens 3 640 0.055 0.037 0.081 65.569 5.809 <0.001 0.296 0.142
Unspecified
location
Babesia sp. 2 480 0.077 0.026 0.208 89.207 9.265 <0.001 NA NA
Tick borne
pathogens 3 541 0.175 0.033 0.565 97.476 79.225 0.093 1.000 0.982
Iran (all collected
data)
Anaplasma sp. 18 2 373 0.235 0.151 0.347 96.596 498.733 <0.001 0.080 0.000
Babesia sp. 17 6 943 0.040 0.019 0.081 97.737 706.904 <0.001 0.010 0.000
Borrelia sp. 15 5 124 0.068 0.029 0.150 97.567 534.363 <0.001 1.000 0.289
Brucella sp. NA
CCHFV 31 4 819 0.056 0.039 0.081 86.951 199.253 0.001 0.091 0.000
Coxiella sp. 9 3 753 0.065 0.030 0. 138 96.738 245.246 <0.001 1.000 0.450
Ehrlichia sp. 4 693 0.177 0.056 0.437 96.744 92.137 0.019 0.734 0.594
Rickettsia sp. 2 125 0.283 0.029 0.839 96.370 27.552 0.480 NA NA
Theileria sp. 36 11 076 0.093 0.067 0.129 96.157 910.777 <0.001 0.827 0.000
Tick borne
pathogens 135 35 184 0.086 0.070 0.106 97.429 5211.303 <0.001 0.933 0.000
Note: In this analysis, each row of Table 1 was considered as an individual data. Furthermore, the sample size of each row of Table 1 was considered a
separate sample size, and all pathogens were included. Provinces with less than two data were not included in meta-analysis. However, the pathogens
detected in these provinces were calculated in Iran’s total prevalence of pathogens section.
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500 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
and Boophilus sp. These vectors should not be underestimated, as
future investigations may reveal a high tendency of these species to
transmit pathogens.
Controlling strategies against ticks and tick-borne diseases for
prevention of significant losses due to both economic and public
health problems are also seem to be important and helpful. Many
attempts have been carried out for the control of ticks and tick-
borne diseases[126]. Some other additional methods have been
suggested: (1) livestock sheds should be checked regularly
in terms of tick infestation; (2) different species of livestock
should be held separately to avoid interspecies tick infection; (3)
quarantine of newly purchased animals decreases the chance of
tick transmission to existing animals; (4) periodic application of
acaricide and chemotherapy according to regional and national
guidelines is sometimes suggested; (5) clearance of vegetation
cut off the connection between different stages of tick’s life and
disrupts their life cycle is also suggested; (6) some novel methods
including application of vaccines against tick-borne pathogens,
biological control, and genetically resistant livestock breeds are in
the spotlight[127].
This investigation had some limitations: In the old classification
of Iran provinces, some provinces are currently divided in two or
more provinces, resulting in the less accuracy of the old literature,
as they cover a larger area. In addition, access to the full text of
some dissertations required a visit to the relevant center, which
was very difficult due to the COVID-19 pandemic. In such cases,
we missed some dissertations. Furthermore, the scientific name
of some of tick species had changed since the publication of the
associated papers, so we had to search with the old names as well.
In conclusion, the occurrence of at least 20 different pathogens
(in 10 genera) in 28 species (in 9 genera) of ticks in 26 provinces
of Iran, sheds light on the current status of the country in terms
of tick-borne pathogens. Rate of infection to different pathogens
in different regions, especially western parts of Iran, is a warning
for public and animal health. Further investigations and persistent
surveillance of vectors as well as vertebrate hosts will expand
the chance of controlling tick-borne pathogens. In most parts of
the meta-analysis concerning total pathogens of Iran, the results
showed high heterogeneity (I2 > 75%). Similarly, meta-analysis
of separate provinces revealed high heterogeneity. This is not
unexpected due to the variations associated with the different
detection methods, sample size, geographical traits, location, time
of the study, and population of interest. While the significance
of a meta-analysis in regarding to the prevalence of tick-borne
pathogens is undeniable, it is suggested that meta-analysis should
not be an adequate alternative for large-scaled epidemiological
studies due to heterogeneous approaches, regions and times of
different studies.
Conflict of interest statement
The authors declare that there is no conflict of interest.
Authors contributions
HB, MK, and ASJ planned for the study. HB, ASJ, MK, and
MMS performed the literature search and data extraction. MK and
ZT critically evaluated the manuscript. ASJ performed the meta-
analysis. The final manuscript approved by all the authors.
References
[1] Salman MD, Tarrés-Call J. Ticks and tick-borne diseases: Geographical
distribution and control strategies in the Euro-Asia region. CABI:
Wallingford; 2013.
[2] Brites-Neto J, Duarte KMR, Martins TF. Tick-borne infections in human
and animal population worldwide. Vet world 2015; 8(3): 301.
[3] Nicholson WL, Sonenshine DE, Noden BH, Brown RN. Chapter
27-Ticks (Ixodidae). In: Mullen GR, Durden LA. Medical and veterinary
entomology. 3rd ed. New York: Academic Press; 2019, p. 603-672.
[4] de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE.
Overview: Ticks as vectors of pathogens that cause disease in humans and
animals. Front Biosci 2008; 13(13): 6938-6946.
[5] Abubakar M, Perera PK, Iqbal A, Manzoor S. Introductory chapter: Ticks
and tick-borne pathogens. In: Ticks and tick-borne pathogens. London:
IntechOpen; 2018.
[6] Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: A
One Health perspective. Trends Parasitol 2012; 28(10): 437-446.
[7] Mashebe P, Lyaku JR, Mausse F. Occurrence of ticks and tick-borne
diseases of livestock in Zambezi region: A review. J Agric Sci 2014; 6(2):
142.
[8] Hurtado OJB, Giraldo-Ríos C. Economic and health impact of the ticks
in production animals. In: Ticks and tick-borne pathogens. London:
IntechOpen; 2018.
[9] Rochlin I, Toledo A. Emerging tick-borne pathogens of public health
importance: A mini-review. J Med Microbiol 2020; 69(6): 781.
[10] Estrada-Peña A, Ayllón N, De La Fuente J. Impact of climate trends on
tick-borne pathogen transmission. Front Physiol 2012; 3: 64.
[11] Kiyani Haftlang K. The book of Iran: A survey of the geography of Iran.
Tehran: Alhoda UK; 2003.
[12] Randolph SE. Tick ecology: Processes and patterns behind the
epidemiological risk posed by ixodid ticks as vectors. Parasitology 2004;
129(S1): S37.
[13] Hosseini-Chegeni A, Tavakoli M, Telmadarraiy Z. The updated list of
ticks (Acari: Ixodidae & Argasidae) occurring in Iran with a key to the
[Downloaded free from http://www.apjtm.org on Wednesday, December 1, 2021, IP: 10.232.74.23]
501
Tick-borne diseases in Iran
identification of species. Syst Appl Acarol 2019; 24(11): 2133-2166.
[14] Gholamreza S, Somaieh M, Roya S, Alireza B, Ghazale A, Yasin B. First
detection of Babesia ovis in Dermacentor spp. in Ardabil area, northwest
of Iran. J Vector Borne Dis 2017; 54(3): 277.
[15] Arjmand Yamchi J, Tavassoli M. Survey on infection rate, vectors and
molecular identification of Theileria annulata in cattle from North West,
Iran. J Parasit Dis 2016; 40(3): 1071-1076.
[16] Aghaei A, Ghazinezhad B, Naddaf SR. Detection of Borrelia DNA in
Ornithodoros tholozani ticks and their eggs. J Med Microbiol Infect Dis
2014; 2(3): 118-120.
[17] Arshi SH, Majidpour A, Sadeghi H, Emdadi D, Asmar M, Derakhshan
MH. Relapsing fever in Ardabil, a northwestern province of Iran. Arch
Iran Med 2002; 5(3): 141-145.
[18] Telmadarraiy Z, Ghiasi SM, Moradi M, Vatandoost H, Eshraghian MR,
Faghihi F, et al. A survey of Crimean-Congo haemorrhagic fever in
livestock and ticks in Ardabil Province, Iran during 2004-2005. Scand J
Infect Dis 2010; 42(2): 137-141.
[19] Esmaeilnejad B, Gharekhani J, Rezaei ASH. Molecular detection of
Coxiella burnetii in ticks isolated from goats of Meshkin-Shahr County,
Ardabil Province, Iran. Nov Biol Reper 2020; 7(3): 315-321.
[20] Khazeni A, Telmadarraiy Z, Oshaghi MA, Mohebali M, Zarei Z, Abtahi
SM. Molecular detection of Ehrlichia canis in ticks population collected
on dogs in Meshkin-Shahr, Ardebil Province, Iran. J Biomed Sci Eng
2013; 6: 1-5.
[21] Abdoli R, Bakhshi H, Kheirandish S, Faghihi F, Hosseini-Chegeni A,
Oshaghi MA, et al. Circulation of Brucellaceae, Anaplasma and Ehrlichia
spp. in borderline of Iran, Azerbaijan, and Armenia. Asian Pac J Trop
Med 2021; 14: 223-230.
[22] Tajedin L, Bakhshi H, Faghihi F, Telmadarraiy Z. High infection of
Anaplasma and Ehrlichia spp. among tick species collected from different
geographical locations of Iran. Asian Pacific J Trop Dis 2016; 6(10): 787-
792.
[23] Nadim A, Khanjani M, Hosseini-Chegeni A, Telmadarraiy Z. Identity
and microbial agents related to Dermacentor marginatus Sulzer (Acari:
Ixodidae) with a new record of Rickettsia slovaca (Rickettsiales:
Rickettsiaceae) in Iran. Syst Appl Acarol 2021; 26(2): 367-378.
[24] Jafarbekloo A, Ramzgouyan MR, Shirian S, Tajedin L, Bakhshi H,
Faghihi F, et al. Molecular characterization and phylogenetic analysis of
Theileria spp. and Babesia spp. isolated from various ticks in southeastern
and northwestern regions of Iran. Vector-Borne Zoonotic Dis 2018;
18(11): 595-600.
[25] Shafei E, Dayer MS, Telmadarraiy Z. Molecular epidemiology of
Crimean-Congo hemorrhagic fever virus in ticks in northwest of Iran. J
Entomol Zool Stud 2016; 4(5): 150-154.
[26] Rajabi S, Esmaeilnejad B, Tavassoli M. A molecular study on Babesia
spp. in cattle and ticks in West-Azerbaijan province, Iran. Vet Res Forum
2017; 8(4): 299-306.
[27] Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani
K, Jalilzadeh-Amin G, et al. PCR-based detection of Babesia ovis in
Rhipicephalus bursa and small ruminants. J Parasitol Res 2014; 2014: 1-6.
doi: 10.1155/2014/294704.
[28] Tavassoli M, Tabatabaei M, Mohammadi M, Esmaeilnejad B,
Mohamadpour H. PCR-based detection of Babesia spp. infection in
collected ticks from cattle in west and north-west of Iran. J Arthropod
Borne Dis 2013; 7(2): 132.
[29] Mohammadi SM, Esmaeilnejad B, Jalilzadeh-Amin G. Molecular
detection, infection rate and vectors of Theileria lestoquardi in goats from
West Azerbaijan province, Iran. Vet Res Forum 2017; 8(2): 139-144.
[30] Abdigoudarzi M. Detection of naturally infected vector ticks (Acari:
Ixodidae) by different species of Babesia and Theileria agents from three
different enzootic parts of Iran. J Arthropod Borne Dis 2013; 7(2): 164-
172.
[31] Spitalska E, Namavari MM, Hosseini MH, Shad-Del F, Amrabadi OR,
Sparagano OAE. Molecular surveillance of tick-borne diseases in Iranian
small ruminants. Small Rumin Res 2005; 57(2-3): 245-248.
[32] Farhadpour F, Telmadarraiy Z, Chinikar S, Akbarzadeh K,
Moemenbellah-Fard MD, Faghihi F, et al. Molecular detection of
Crimean-Congo haemorrhagic fever virus in ticks collected from infested
livestock populations in a New Endemic Area, South of Iran. Trop Med
Int Heal 2016; 21(3): 340-347.
[33] Yaghfoori S, Razmi G, Heidarpour M. Molecular detection of Theileria
spp. in sheep and vector ticks in Fasa and Kazeroun areas, Fars Province,
Iran. Arch Razi Institute 2013; 68(2): 159-164.
[34] Hosseini-Chegeni A, Tavakoli M, Goudarzi GH, Telmadarraiy Z,
Sharifdini M, Faghihi F, et al. Molecular detection of Anaplasma
marginale and Anaplasma ovis (Rickettsiales: Anaplasmataceae) in ixodid
tick species in Iran. Arch Razi Inst 2020; 75(1): 39-46.
[35] Naddaf SR, Mahmoudi A, Ghasemi A, Rohani M, Mohammadi A,
Ziapour SP, et al. Infection of hard ticks in the Caspian Sea littoral of Iran
with Lyme borreliosis and relapsing fever borreliae. Ticks Tick Borne Dis
2020; 11(6): 101500.
[36] Hosseini-Chegeni A, Tavakoli M, Telmadarraiy Z, Sedaghat MM,
Faghihi F. Detection of a Brucella-like (Alphaproteobacteria) bacterium
in Boophilus spp. (Acari: Ixodidae) from Iran. J Med Microbiol Infect Dis
2017; 5(3): 66-68.
[37] Bekloo AJ, Bakhshi H, Soufizadeh A, Sedaghat MM, Bekloo RJ,
Ramzgouyan MR, et al. Ticks circulate Anaplasma, Ehrlichia, Babesia
and Theileria parasites in North of Iran. Vet Parasitol 2017; 248: 21-24.
[38] Sedaghat MM, Sarani M, Chinikar S, Telmadarraiy Z, Moghaddam
AS, Azam K, et al. Vector prevalence and detection of Crimean-Congo
haemorrhagic fever virus in Golestan Province, Iran. J Vector Borne Dis
2017; 54(4): 353.
[39] Vatandoost H, Ghaderi A, Javadian E, Nia AHZ, Rassi Y, Piazak N, et al.
Distribution of soft ticks and their infection with Borrelia in Hamadan
province, Iran. Iran J Public Health 2003; 32(1): 22-24.
[40] Shahraki G, Asmar M. Study on distribution of Arasid-ticks and their
infection to Borrelia persica in indoor resting places of Hamadan.
[Online]. Available from: http://sjh.umsha.ac.ir/article-1-1065-en.html.
[Accessed on 8 November 2021].
[41] Taher M, Dayer M, Jalali T, Khakifirouz S, Telmadarraiy Z, Salehi-Vaziri
M. Molecular epidemiology of Crimean-Congo hemorrhagic fever virus
in ticks collected from western Iran. Asian Biomed 2016; 10(6): 603-607.
[Downloaded free from http://www.apjtm.org on Wednesday, December 1, 2021, IP: 10.232.74.23]
502 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
[42] Tahmasebi F, Ghiasi SM, Mostafavi E, Moradi M, Piazak N, Mozafari
A, et al. Molecular epidemiology of Crimean-Congo hemorrhagic fever
virus genome isolated from ticks of Hamadan province of Iran. J Vector
Borne Dis 2010; 47(4): 211-216.
[43] Telmadarraiy Z, Moradi AR, Vatandoost H, Mostafavi E, Oshaghi
MA, Zahirnia AH, et al. Crimean-Congo hemorrhagic fever: A
seroepidemiological and molecular survey in Bahar, Hamadan province
of Iran. Asian J Anim Vet Adv 2008; 3(5): 321-327.
[44] Sharifinia N, Rafinejad J, Hanafi-Bojd AA, Chinikar S, Piazak N,
Baniardalani M, et al. Hard ticks (Ixodidae) and Crimean-Congo
hemorrhagic fever virus in south west of Iran. Acta Med Iran 2015; 53(3):
177-181.
[45] Biglari P, Chinikar S, Belqeiszadeh H, Telmadarraiy Z, Mostafavi E,
Ghaffari M, et al. Phylogeny of tick-derived Crimean-Congo hemorrhagic
fever virus strains in Iran. Ticks Tick Borne Dis 2016; 7(6): 1216-1221.
[46] Ranjbar R, Anjomruz M, Enayati AA, Khoobdel M, Rafinejad A,
Rafinejad J. Anaplasma infection in ticks in southeastern region of Iran. J
Arthropod Borne Dis 2020; 14(2): 126-133.
[47] Akhtardanesh B, Saberi M, Nurollahifard SR, Aghazamani M. Molecular
detection of Babesia spp. in tick-infested dogs in Southeastern Iran. J Dis
Glob Heal 2016; 8(2): 72-77.
[48] Salehi-Vaziri M, Vatandoost H, Sanei-Dehkordi A, Fazlalipour M,
Pouriayevali MH, Jalali T, et al. Molecular assay on detection of Crimean
Congo hemorrhagic fever (CCHF) virus in ixodid ticks collected from
livestock in slaughterhouse from South of Iran. J Arthropod Borne Dis
2020; 14(3): 286-292.
[49] Khakifirouz S, Mowla SJ, Baniasadi V, Fazlalipour M, Jalali T, Mirghiasi
SM, et al. No detection of Crimean Congo hemorrhagic fever (CCHF)
virus in ticks from Kerman Province of Iran. J Med Microbiol Infect Dis
2018; 6(4): 108-111.
[50] Khalili M, Rezaei M, Akhtardanesh B, Abiri Z, Shahheidaripour S.
Detection of Coxiella burnetii (Gammaproteobacteria: Coxiellaceae) in
ticks collected from infested dogs in Kerman, Southeast of Iran. Persian
J Acarol 2018; 7(1): 93-110. doi: 10.22073/pja.v7i1.30699.
[51] Fard SN, Khalili M. PCR-detection of Coxiella burnetii in ticks collected
from sheep and goats in Southeast Iran. Iran J Arthropod Borne Dis 2011;
5(1): 1-6.
[52] Motaghipisheh S, Akhtardanesh B, Ghanbarpour R, Aflatoonian MR,
Khalili M, Nourollahifard SR, et al. Ehrlichiosis in household dogs and
parasitized ticks in Kerman-Iran: Preliminary zoonotic risk assessment. J
Arthropod Borne Dis 2016; 10(2): 245-251.
[53] Mohammadian M, Chinikar S, Telmadarraiy Z, Vatandoost H, Oshaghi
MA, Hanafi-Bojd AA, et al. Molecular assay on Crimean Congo
hemorrhagic fever virus in ticks (Ixodidae) collected from Kermanshah
Province, Western Iran. J Arthropod Borne Dis 2016; 10(3): 381-391.
[54] Rahmani-Varmale M, Tavassoli M, Esmaeilnejad B. Molecular detection
and differentiation of Theileria lestoquardi, Th. ovis and Th. annulata in
blood of goats and ticks in Kermanshah Province, Iran. J Arthropod Borne
Dis 2019; 13(3): 297-309.
[55] Abedi V, Razmi G, Seifi H, Naghibi A. Molecular and serological
detection of Theileria equi and Babesia caballi infection in horses and
ixodid ticks in Iran. Ticks Tick Borne Dis 2014; 5(3): 239-244.
[56] Seidabadi M, Razmi G, Naghibi A. Molecular detection of Babesia spp.
in sheep and vector ticks in North Khorasan province, Iran. Iran J Vet
Med 2014; 8(1): 35-39.
[57] Saghafipour A, Mousazadeh-Mojarrad A, Arzamani N, Telmadarraiy Z,
Rajabzadeh R, Arzamani K. Molecular and seroepidemiological survey
on Crimean-Congo hemorrhagic fever virus in Northeast of Iran. Med J
Islam Repub Iran 2019; 33: 41. doi: 10.34171/mjiri.33.41.
[58] Champour M, Chinikar S, Mohammadi G, Razmi G, Mostafavi E, Shah-
Hosseini N, et al. Crimean-Congo hemorrhagic fever in the one-humped
camel (Camelus dromedarius) in East and Northeast of Iran. J Arthropod
Borne Dis 2016; 10(2): 168-177.
[59] Rashidi A, Razmi G. Molecular detection of Theileria spp. in sheep and
vector ticks in the North Khorasan Province, Iran. Trop Anim Health Prod
2012; 45(1): 299-303.
[60] Khodaverdi Azghandi M, Razmi G. Identification of Babesia and
Theileria species in goats and ticks with smear observation and molecular
examination in Mashhad, Khorasan Razavi province, Iran. J Vet Res
2015; 70(1): 1-5.
[61] Razmi G, Pourhosseini M, Yaghfouri S, Rashidi A, Seidabadi M.
Molecular detection of Theileria spp. and Babesia spp. in sheep and
ixodid ticks from the northeast of Iran. J Parasitol 2013; 99(1): 77-81.
[62] Shayeghi M, Piazak N, Gollampuor A, Nasirian H, Abolhassani M. Tick-
borne relapsing fever in Sabzevar (Khorasan Razavy Province), North-
Eastern Iran. Bangladesh J Med Sci 2016; 15(4): 551-555.
[63] Maghsood H, Nabian S, Shayan P, Jalali T, Darbandi MS, Ranjbar MM.
Molecular epidemiology and phylogeny of Crimean-Congo haemorrhagic
fever (CCHF) virus of ixodid ticks in Khorasan Razavi Province of Iran.
J Arthropod Borne Dis 2021; 14(4): 400-407.
[64] Fakoorziba MR, Naddaf-Sani AA, Moemenbellah-Fard MD, Azizi K,
Ahmadnia S, Chinikar S. First phylogenetic analysis of a Crimean-Congo
hemorrhagic fever virus genome in naturally infected Rhipicephalus
appendiculatus ticks (Acari: Ixodidae). Arch Virol 2015; 160(5): 1197-
1209.
[65] Razmi GR, Ebrahimzadeh E, Aslani MR. A study about tick vectors of
bovine theileriosis in an endemic region of Iran. J Vet Med Ser B 2003;
50(6): 309-310.
[66] Razmi G, Yaghfoori S. Molecular surveillance of Theileria ovis, Theileria
lestoquardi and Theileria annulata infection in sheep and ixodid ticks
in Iran. Onderstepoort J Vet Res 2013; 80(1): 635. doi: 10.4102/ojvr.
v80i1.635.
[67] Jafari A. Epidemiology and molecular detection of Crimean-Congo
hemorrhagic fever (CCHF), Coxiella burnetii and Anaplasma spp. in hard
ticks (Ixodidae) in the South Khorasan regions. DVM. Thesis. Zabol, Iran:
University of Zabol; 2020.
[68] Asadollahi Z, Jalali MHR, Alborzi A, Hamidinejat H. Detection of
Theileria-like organisms in Hyalomma ticks (Acarina: Ixodidae) in
Khuzestan, Iran. Sci Parasitol 2018; 19(1-2): 34-39.
[69] Hosseini Z, Salehi Vaziri M, Ahmadnia S, Fakoorziba MR, Jalali T,
Telmadarraiy Z, et al. Hard ticks infesting domestic ruminants, species
composition and infection with Crimean-Congo hemorrhagic fever virus
[Downloaded free from http://www.apjtm.org on Wednesday, December 1, 2021, IP: 10.232.74.23]
503
Tick-borne diseases in Iran
in a highland province, SW Iran. J Heal Sci Surveill Syst 2019; 7(2): 52-
59.
[70] Hasheminasab SS, Moradi P, Wright I. A four year epidemiological and
chemotherapy survey of babesiosis and theileriosis, and tick vectors in
sheep, cattle and goats in Dehgolan, Iran. Ann Parasitol 2018; 64(1): 43-
48. doi:10.17420/ap6401.131.
[71] Moemenbellah-Fard MD, Benafshi O, Rafinejad J, Ashraf H. Tick-borne
relapsing fever in a new highland endemic focus of western Iran. Ann
Trop Med Parasitol 2009; 103(6): 529-537.
[72] Banafshi O, Rafinejed J, Esmaeelnasab N. Study of the spread of
soft ticks (Argasidae) in indoor areas and the study of infection of
Ornithodoros tolozani with Borrelia persica in Bijar city of Kurdistan
province. Sci J Kurdistan Univ Med Sci 2004; 8(31): 50-58.
[73] Fakoorziba MR, Golmohammadi P, Moradzadeh R, Moemenbellah-Fard
MD, Azizi K, Davari B, et al. Reverse transcription PCR-based detection
of Crimean-Congo hemorrhagic fever virus isolated from ticks of
domestic ruminants in Kurdistan Province of Iran. Vector Borne Zoonotic
Dis 2012; 12(9): 794-799.
[74] Chegeni AH, Tavakoli M. Aegyptianella pullorum (Rickettsiales:
Anaplasmataceae) in tick Argas persicus (Acari: Argasidae) from Iran:
A preliminary assessment. Persian J Acarol 2018; 7(3): 307-311.
doi:10.22073/pja.v7i3.37407.
[75] Chegeni AH, Telmadarraiy Z, Tavakoli M, Faghihi F. Molecular detection
of Borrelia anserina in Argas persicus (Acari: Argasidae) ticks collected
from Lorestan province, west of Iran. Persian J Acarol 2017; 6(4): 287-
297. doi:10.22073/pja.v6i4.28372.
[76] Hosseini-Chegeni A, Kayedi MH. Molecular detection of Coxiella
(Gammaproteobacteria: Coxiellaceae) in Argas persicus and Alveonasus
canestrinii (Acari: Argasidae) from Iran. Microb Pathog 2020; 139:
103902.
[77] Kayedi MH, Chinikar S, Mostafavi E, Khakifirouz S, Jalali T, Hosseini-
Chegeni A, et al. Crimean-Congo hemorrhagic fever virus clade (Asia
1) in ticks of Western Iran. J Med Entomol 2015; 52(5): 1144-1149.
[78] Kooshki H, Goudarzi G, Faghihi F, Telmadarraiy Z, Edalat H, Hosseini-
chegeni A. The first record of Rickettsia hoogstraalii (Rickettsiales:
Rickettsiaceae) from Argas persicus (Acari: Argasidae) in Iran. Syst Appl
Acarol 2020; 25(9): 1611-1617.
[79] Nasser H-R, Saeed H, Mohammad A. Molecular detection of Theileria
ovis and Th. lestoquardi in vector ticks in Lorestan province, Iran. Int J
Biosci 2014; 4(12): 78-83.
[80] Hashemi S, Estaki Oregani K. Molecular identification of Theileria
ovis and Th. lestoquardi in vector ticks of Ixodidae family in Lorestan
province. Iran Vet J 2015; 11(3): 97-104.
[81] Pazhoom F, Ebrahimzade E, Shayan P, Nabian S. Anaplasma spp.
identification in hard ticks of Iran: First report of Anaplasma bovis in
Haemaphysalis inermis. Acarologia 2016; 56(4): 497-504.
[82] Hosseini-Vasoukolaei N, Oshaghi MA, Shayan P, Vatandoost H,
Babamahmoudi F, Yaghoobi-Ershadi MR, et al. Anaplasma infection in
ticks, livestock and human in Ghaemshahr, Mazandaran Province, Iran. J
Arthropod Borne Dis 2014; 8(2): 204-211.
[83] Bashiribod H. First molecular detection of Anaplasma phagocytophilum
in Ixodes ricinus ticks in Iran. J Med Sci 2004; 4(4): 282-286.
[84] Bashiribod H, Rahbarian N, Eslami G, Kazemi B, Jannatsharif E,
Mahmoudirad M, et al. Prevalence of Coxiella burnetii in human, animal
hosts and hard ticks in West Mazandaran Province Iran, 2003-2004.
Pajouhesh Dar Pezeshki 2008; 32(3): 253-257.
[85] Hosseini-Vasoukolaei N, Chinikar S, Telmadarraiy Z, Faghihi F,
Hosseini-Vasoukolaei M. Serological and molecular epidemiology
of Crimean-Congo hemorrhagic fever in Ghaemshahr county in
Mazandaran province, Iran. Trop Biomed 2016; 33(4): 807-813.
[86] Zakkyeh T, Mohammad Ali O, Nasibeh HV, Mohammad Reza YE,
Farhang B, Fatemeh M. First molecular detection of Theileria ovis in
Rhipicephalus sanguineus tick in Iran. Asian Pac J Trop Med 2012; 5(1):
29-32. doi: 10.1016/S1995-7645(11)60240-X.
[87] Aghighi Z, Assmar M, Piazak N, Javadian E, Seyedi RMA, Kia EB, et
al. Distribution of soft ticks and their natural infection with Borrelia in a
focus of relapsing fever in Iran. J Arthropod Borne Dis 2007; 1(2): 14-18.
[88] Barmaki A, Rafinejad J, Vatandoost H, Telmadarraiy Z, Mohtarami F,
Leghaei SH, et al. Study on presence of Borrelia persica in soft ticks in
Western Iran. Iran J Arthropod Borne Dis 2010; 4(2): 19-25.
[89] Telmadarraiy Z, Saghafipour A, Farzinnia B, Chinikar S. Molecular
detection of Crimean-Congo hemorrhagic fever virus in ticks in Qom
Province, Iran, 2011-2012. Iran J Virol 2012; 6(3): 13-18.
[90] Nekooyi H, Asmar M, Amirkhani A, Piyazak N. Geographical
distribution of ticks in Semnan province and the rate of infection of soft
ticks with Borrelia. Iran J Heal 1999; 4(1): 103-110.
[91] Faghihi F, Telmadarraiy Z, Chinikar S, Nowotny N, Fooks AR,
Shahhosseini N. Spatial and phylodynamic survey on Crimean-Congo
hemorrhagic fever virus strains in northeast of Iran. Jundishapur J
Microbiol 2018; 11(3): e59412. doi: 10.5812/jjm.59412.
[92] Choubdar N, Karimian F, Koosha M, Nejati J, Oshaghi MA. Hyalomma
spp. ticks and associated Anaplasma spp. and Ehrlichia spp. on the Iran-
Pakistan border. Parasit Vectors 2021; 14: 469.
[93] Khodadadi N, Nabavi R, Sarani A, Saadati D, Ganjali M, Mihalca AD,
et al. Identification of Anaplasma marginale in long-eared hedgehogs
(Hemiechinus auritus) and their Rhipicephalus turanicus ticks in Iran. Ticks
Tick Borne Dis 2021; 12(2): 101641.
[94] Asadollahi S. Epidemiology & molecular detection of Crimean-Congo
hemorrhagic fever (CCHF), Coxiella burnetii and Anaplasma spp. in
hard ticks (Ixodidae) in the Sistan regions. DVM. Thesis. Zabol, Iran:
University of Zabol; 2020.
[95] Jafarbekloo A, Bakhshi H, Faghihi F, Telmadarraiy Z, Khazeni A,
Oshaghi MA, et al. Molecular detection of Anaplasma and Ehrlichia
infection in ticks in borderline of Iran-Afghanistan. J Biomed Sci Eng
2014; 7(11): 919-926. doi: 10.4236/jbise.2014.711089.
[96] Ghashghaei O, Fard SRN, Khalili M, Sharifi H. A survey of ixodid ticks
feeding on cattle and molecular detection of Coxiella burnetii from ticks
in Southeast Iran. Turkish J Vet Anim Sci 2017; 41(1): 46-50.
[97] Fard SRN, Ghashghaei OO, Khalili M, Sharifi H. Tick diversity and
detection of Coxiella burnetii in tick of small ruminants using nested
Trans PCR in southeast Iran. Trop Biomed 2016; 33(3): 506-511.
[98] Hormozzayi H. Molecular study of Ehrlichia infection in Rhipicephalus
[Downloaded free from http://www.apjtm.org on Wednesday, December 1, 2021, IP: 10.232.74.23]
504 Mehdi Khoobdel et al./ Asian Pacific Journal of Tropical Medicine 2021; 14(11): 486-504
sanguineus ticks isolated from dogs in Zabol city. DVM. Thesis. Kerman,
Iran: University of Kerman; 2017.
[99] Shahhosseini N, Jafarbekloo A, Telmadarraiy Z, Chinikar S, Haeri A,
Nowotny N, et al. Co-circulation of Crimean-Congo hemorrhagic fever
virus strains Asia 1 and 2 between the border of Iran and Pakistan.
Heliyon 2017; 3(11): e00439.
[100] Mehravaran A, Moradi M, Telmadarraiy Z, Mostafavi E, Moradi
AR, Khakifirouz S, et al. Molecular detection of Crimean-Congo
haemorrhagic fever (CCHF) virus in ticks from southeastern Iran. Ticks
Tick Borne Dis 2013; 4(1-2): 35-38.
[101] Zarei F, Ganjali M, Nabavi R. Identification of Theileria species in
sheep and vector ticks using PCR method in Zabol, Eastern Iran. J
Arthropod Borne Dis 2019; 13(1): 76-82.
[102] Razmi GR, Hosseini M, Aslani MR. Identification of tick vectors of
ovine theileriosis in an endemic region of Iran. Vet Parasitol 2003;
116(1): 1-6.
[103] Talaie P, Sedaghat MM, Mostafavi E, Telmadarraiy Z, Rouhani M,
Salehi-Vaziri M. A Survey of Crimean-Congo hemorrhagic fever virus
in ticks of Shahr-e Ray, Iran, 2016-2017. J Med Microbiol Infect Dis
2020; 8(2): 56-59.
[104] Habibi G, Imani A, Afshari A, Bozorgi S. Detection and molecular
characterization of Babesia canis vogeli and Theileria annulata in free-
ranging dogs and ticks from Shahriar County, Tehran Province, Iran.
Iran J Parasitol 2020; 15(3): 321-331. doi: 10.18502/ijpa.v15i3.4196.
[105] Yaser SA, Sadegh C, Zakkyeh T, Hassan V, Maryam M, Ali OM, et al.
Crimean-Congo hemorrhagic fever: A molecular survey on hard ticks
(Ixodidae) in Yazd Province, Iran. Asian Pac J Trop Med 2011; 4(1): 61-
63.
[106] Khodabandeh S, Razmi G. Molecular detection of Theileria species
and its vectors in cattle of Yazd by Semi-nested PCR method. J Vet Res
2015; 70(3): 249-253.
[107] Shayan P, Hooshmand E, Rahbari S, Nabian S. Determination of
Rhipicephalus spp. as vectors for Babesia ovis in Iran. Parasitol Res 2007;
101(4): 1029-1033.
[108] Hosseini-Chegeni A, Telmadarraiy Z, Faghihi F. Molecular detection of
spotted fever group Rickettsia (Rickettsiales: Rickettsiaceae) in ticks of
Iran. Razi Vaccine Serum Res Inst 2019; 75(3): 317-325.
[109] Ybañez AP, Inokuma H. Anaplasma species of veterinary importance
in Japan. Vet World 2016; 9(11): 1190-1196. doi: 10.14202/
vetworld.2016.1190-1196.
[110] Yang J, Liu Z, Niu Q, Liu J, Han R, Liu G, et al. Molecular survey
and characterization of a novel Anaplasma species closely related to
Anaplasma capra in ticks, northwestern China. Parasit Vectors 2016;
9(1): 1-5.
[111] Rymaszewska A, Grenda S. Bacteria of the genus Anaplasma-
characteristics of Anaplasma and their vectors: A review. Vet Med 2008;
53(11): 573-584.
[112] Hanafi-Bojd AA, Jafari S, Telmadarraiy Z, Abbasi-Ghahramanloo A,
Moradi-Asl E. Spatial distribution of ticks (Arachniada: Argasidae and
Ixodidae) and their infection rate to Crimean-Congo hemorrhagic fever
Virus in Iran. J Arthropod Borne Dis 2021; 15(1): 41-59.
[113] Salehi-Vaziri M, Baniasadi V, Jalali T, Mirghiasi SM, Azad-Manjiri S,
Zarandi R, et al. The first fatal case of Crimean-Congo hemorrhagic
fever caused by the AP92-like strain of the Crimean-Congo hemorrhagic
fever virus. Jpn J Infect Dis 2016; 69(4): 344-346.
[114] Mostafavi E, Haghdoost A, Khakifirouz S, Chinikar S. Spatial analysis
of Crimean Congo hemorrhagic fever in Iran. Am J Trop Med Hyg 2013;
89(6): 1135-1141.
[115] Cutler SJ, Ruzic-Sabljic E, Potkonjak A. Emerging borreliae-expanding
beyond Lyme borreliosis. Mol Cell Probes 2017; 31: 22-27.
[116] Asl HM, Goya MM, Vatandoost H, Zahraei SM, Mafi M, Asmar M, et
al. The epidemiology of tick-borne relapsing fever in Iran during 1997-
2006. Travel Med Infect Dis 2009; 7(3): 160-164.
[117] Rezaei A, Gharibi D, Pourmahdi Borujeni M, Mosallanejad B.
Seroprevalence of Lyme disease and Q fever in referred dogs to
veterinary hospital of Ahvaz. Iran Vet J 2016; 11(4): 34-41.
[118] Esmaeili S, Golzar F, Ayubi E, Naghili B, Mostafavi E. Acute Q fever in
febrile patients in northwestern of Iran. PLoS Negl Trop Dis 2017; 11(4):
e0005535.
[119] Mobarez AM, Amiri FB, Esmaeili S. Seroprevalence of Q fever among
human and animal in Iran; A systematic review and meta-analysis. PLoS
Negl Trop Dis 2017; 11(4): e0005521.
[120] Rezaei M, Khalili M, Akhtardanesh B, Shahheidaripour S. Q fever in
dogs: An emerging infectious disease in Iran. J Med Bacteriol 2016; 5(1-
2): 1-6.
[121] Kumar B, Manjunathachar HV, Ghosh S. A review on Hyalomma
species infestations on human and animals and progress on management
strategies. Heliyon 2020; 6(12): e05675.
[122] René-Martellet M, Minard G, Massot R, Moro CV, Chabanne L,
Mavingui P. Bacterial microbiota associated with Rhipicephalus
sanguineus (sl) ticks from France, Senegal and Arizona. Parasit Vectors
2017; 10(1): 1-10.
[123] Dantas-Torres F. The brown dog tick, Rhipicephalus sanguineus
(Latreille, 1806)(Acari: Ixodidae): From taxonomy to control. Vet
Parasitol 2008; 152(3-4): 173-185.
[124] Dantas-Torres F. Biology and ecology of the brown dog tick,
Rhipicephalus sanguineus. Parasit Vectors 2010; 3(1): 26. doi:
10.1186/1756-3305-3-26.
[125] Vatansever Z. Rhipicephalus bursa Canestrini and Fanzago, 1878
(Figs. 117-119). In: Ticks of Europe and North Africa. Cham: Springer
International Publishing; 2017, p. 299-303.
[126] Vatandoost H, Moradi Asl E, Telmadarreiy Z, Mohebali M, Masoumi
Asl H, Abai MR, et al. Field efficacy of flumethrin pour-on against
livestock ticks in Iran. Int J Acarol 2012; 38(6): 457-464.
[127] Muhammad G, Naureen A, Firyal S, Saqib M. Tick control strategies in
dairy production medicine. Pak Vet J 2008; 28(1): 43-50.
[Downloaded free from http://www.apjtm.org on Wednesday, December 1, 2021, IP: 10.232.74.23]
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