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Original Article
Crimean-Congo Hemorrhagic Fever in the One-Humped Camel (Camelus

dromedarius) in East and Northeast of Iran

Mohsen Champour 1, Sadegh Chinikar 2, *Gholamreza Mohammadi 1, Gholamreza Razmi 1,
Ehsan Mostafavi 2, Nariman Shah-Hosseini 2, Sahar Khakifirouz 2, Tahmineh Jalali 2

1Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
2Arboviruses and Viral Hemorrhagic Fever Laboratory (National Reference Lab) Pasteur Institute of

Tehran, Iran

(Received 3 Aug 2013; accepted 22 Feb 2015)

Abstract
Background: This comprehensive study was conducted on multi-purpose one-humped camel (Camelus
dromedarius) sera and ticks to assess the epidemiological aspects of the Crimean-Congo hemorrhagic fever virus
(CCHFV) in northeast Iran.
Methods: From May 2012 to January 2013, eleven cities were randomly selected in the Khorasan Provinces of Iran
as “clusters,” and at least 14 one-humped camels were sampled from each area. Reverse transcriptase polymerase
chain reaction was used for the detection of the CCHFV genome in ticks. Sera were analyzed using specific enzyme-
linked immunosorbent assay tests.
Results: Four hundred and eighty ixodid ticks were collected, and the genome of the CCHFV was detected in 49
(10.2%) out of 480 ticks. The CCHFV genome was detected in two out of four tick species, and in tick samples from
three cities in Khorassan-e-Jonoobi. All three provinces, and six out of eleven cities, were CCHFV-specific IgG-
positive. In total, nine (5.3%) out of 170 one-humped camels were IgG-positive. The highest rate of IgG-positive
samples was found in Nehbandan (16.67%).
Conclusion: Continued surveillance and strictly enforced importation and quarantine practices should be imple-
mented to prevent human exposure and the on-going dispersal of infected ticks and livestock in these regions. It is
recommended that acaricides be used to prevent CCHF transmission to humans, and to reduce the tick population. In
addition, care should be taken by abattoirs workers and people who work with one-humped camels.

Keywords: Epidemiology, Survey, CCHFV, ELISA, RT-PCR, Iran

Introduction

“Crimean-Congo hemorrhagic fever virus
belongs to the genus Nairovirus in the
Bunyaviridae family, and is a human patho-
gen that can cause a severe, and often fatal,
hemorrhagic fever.” (Ergonul 2006). CCHF
virus is the most geographically widespread
tick-borne virus of medical importance
(Ergonul 2006). The disease is endemic in
large areas of sub-Saharan Africa and the
Middle and Far East, as well as in Eastern
Europe. A significant increase of cases in
countries such as Kosovo, Albania, Turkey,
Iran, and Greece has recently been observed

(Alavi-Naini et al. 2006). The CCHFV ge-
nome has been isolated from at least 31 dif-
ferent tick species in the Ixodidae (hard
ticks) and Argasidae (soft ticks).

Hyalomma spp ticks are considered the
most important in the epidemiology of
CCHFV; however, the virus has also been
isolated from ticks of other genera (i.e.,
Rhipicephalus, Boophilus, Dermacentor,
Haemaphysalis, and Ixodes spp, (Saijo et al.
2002, Tahmasebi et al. 2010). Infected ani-
mals are, however, asymptomatic (Papa et
al. 2009). Humans in high-risk occupations

*Corresponding author: Dr Gholamreza Mohammadi,
E-mail: gmohamad@um.ac.ir



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(e.g., slaughterhouse workers, shepherds, health
care workers, and veterinarians) are prone to
CCHF infection (Garcia et al. 2006).

This study was performed to ascertain the
prevalence of CCHFV in ticks present on the
one-humped camel (Camelus dromedarius),
and to estimate the prevalence of CCHFV
IgG in the one-humped camel's sera in three
provinces: Khorassan-e-Shomali, Khorassan-
e-Razavi, and Khorassan-e-Jonoobi of Iran.

Materials and Methods

Study area
The study was conducted in three prov-

inces: Khorassan-e-Shomali, Khorassan-e-
Razavi, and Khorassan-e-Jonoobi located at
55°17′, 61°15′E and 30°24′, 38°17′N in
northeastern and east of Iran (Fig. 1).
Khorassan-e-Shomali is a mountainous region,
with temperate, cold weather. Khorassan-e-
Razavi is a semi-desert region that has mild
weather. Khorassan-e-Jonoobi is a semi-
desert region that experiences arid condi-
tions. The average annual rainfall is approxi-
mately 300–400 mm in the northern areas
(Khorassan-e-Shomali) and 150 mm in the
central and southern areas (Khorassan-e-
Razavi and Khorassan-e-Jonoobi). There are
approximately 25 million camels in the world,
and nearly 150,000 one-humped camels are
in Iran, this is 0.6% of the world camel pop-
ulation, and 3.8% of the Asian camel pop-
ulation (FAO 2011). The majority of Iran's
camels are dromedaries, and they are scat-
tered across the country’s provinces. In the
Khorassan Provinces the camel population is
37,400 (Ministry of Agriculture Jihad, 2002),
but in the authors’ experience at present the
actual number is several times greater, the
majority of these are in Khorassan-e-Shomali
and Khorassan-e-Jonoobi.

Sampling
From May 2012 to January 2013, eleven

cities and towns were randomly selected from

three provinces: Khorassan-e-Shomali,
Khorassan-e-Razavi and Khorassan-e-Jonoobi
as “clusters,” and at least 14 one-humped
camels were sampled from each cluster.
From each animal, two or three ticks were
collected and placed in separate sterile tubes;
the tubes were labeled with the date of
collection, animal number, sex, age, and
area. Collected ticks were sent to the labor-
atory and identified under a stereo micro-
scope using general identification keys
(Hoogstraal 1979, Apanaskevich and Filippova
2007). The samples were then pooled ac-
cording to the area, sex and species of tick
(each pool routinely contained 1–8 ticks, but
occasionally the number was greater) and
immediately sent to the Arboviruses and Viral
Hemorrhagic Fevers Laboratory (National
Reference Laboratory), Pasteur Institute of
Iran, and stored at −70 °C until analysis. For
the serum assay, 20 mL of blood collected
from the jugular vein of each camel then the
sample was labeled with the date of col-
lection, animal number, sex, age, and area.
The samples were immediately sent to a
laboratory and centrifuged at 5000 rpm for
10 min. The sera were then separated and
transferred into holding tubes and sent to the
Arboviruses and Viral Hemorrhagic Fevers
Laboratory and stored at −70 °C until
analysis.

Tick sample size calculation
According to previous studies in animals,

tick infectious was 10% and with assump-
tion 5% accuracy, 95% confidence interval
and design effect equal 1.5 we need at least
207 ticks.

Serum sample size calculation
With assumption 20% seropositivity in

the studied animals, 8% accuracy, 95% de-
gree of confidence, and design effect equal
1.5, the sample size will be 144, each cluster
has at least 14 sera.



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Molecular detection
Reverse transcriptase polymerase chain

reaction: Ticks were individually washed
twice by PBS (PBS, pH 7.4) and crushed
with a mortar and pestle in 200-300μl of
PBS. Total RNA was extracted using an
RNeasy mini kit (QIAgen, Cat No. 2215716)
according to the manufacturer's instructions.
The extracted viral RNA was stored at −70
°C until analysis. For the RT-PCR, a master
mix was prepared as follows: 28 μl of RNase
free water, 10 μl of buffer (5 x conc), 2 μl of
dNTP mixture, 2μl of enzyme mixture con-
taining reverse transcriptase and Taq DNA
polymerase enzymes, 1μl of primer F2 (5'-
TGGACACCTTCACAAACTC-3'), 1μl of
Primer R3 (5'-GACAATTCCCTACACC-
3'), 1μl of RNase inhibitor and 5μl of ex-
tracted viral RNA as template. The F2 and
R3 primers amplify a 536 bp fragment inside
the S-segment of the CCHFV genome, 536
bp fragment is RT-PCR target. The thermal
cycling program for the RT-PCR, included
30 min at 50 °C for reverse transcription re-
action (cDNA synthesis), 15 min at 95 °C
for activation of Hot Star Taq DNA poly-
merase and inactivation of reverse tran-
scriptase, followed by 35 cycles of 95 °C for
30 sec, 50 °C for 30 sec, 72 °C for 45 sec,
and a final extension at 72 °C for 5 min. For
gel-based RT-PCR product analysis, 5μl of
the PCR product was mixed with 1μl loading
buffer (6 x conc). Then, the mixture was
load in agarose gel 1.5%, and visualized
with ethidium bromide (Chinikar et al. 2004,
Chinikar et al. 2010).

IgG-sandwich ELISA
For IgG antibody detection, the ELISA

plates were coated overnight at 4 °C with
mouse hyperimmune ascitic fluid diluted at
1:1000 in 0.05% Tween 20-PBS containing
5% skim milk as a saturating reagent. This
solution was used to dilute antigen and sera.
The native or the recombinant antigen (pro-
duced in our laboratory) diluted in PBSTM

(PBS containing 0.05% Tween and 3% skim
milk) was added to the plates and the plates
were incubated for 1h at 37 °C and exten-
sively washed. Serum samples diluted in
PBSTM were added, and the plates were in-
cubated for 1h at 37 °C. After washing, the
peroxidase-labeled anti-human or animal im-
munoglobulin diluted in PBSTM was added
to each weel and the plates were incubated
for 1 h at 37 °C. The plates were then
washed 3 times with PBS containing 0.5%
Tween (PBST). Finally, hydrogen peroxide
and tetramethylbenzidine (TMB) were added
and the plates were incubated for 15 min at
room temperature. The enzymatic reaction
was stopped by the addition of sulphuric
acid (4N) and the plates read by ELISA
reader (Anathos 2020) at 450 and 620 nm.
Taken together, an IgG-positive serum was
considered as positive control and a negative
serum taken as negative control in the IgG
ELISA (Garcia et al. 2006, Duh et al. 2008,
Chinikar et al. 2010).

Statistical analysis
Data were analyzed using IBM/ SPSS

version 20.0 statistics package. Descriptive
statistics (i.e. prevalence and percentages)
were used to summarize the quantitative
variables. Location of noted research is
shown on the map (Fig. 1).

Results

A total of 200 one-humped multi-purpose
camels (rearing for milk, meat, riding and
offspring) were examined. Tick infestation
was observed in 170 of them, and 480 ixodid
ticks (133 females and 347 males) were col-
lected from different regions in the
Khorassan-e-Shomali, Khorassan-e-Razavi and
Khorassan-e-Jonoobi (Table 1).

In the current study, only four species of
Hyalomma genus were observed. Population
frequency of H. dromedarii (90.7%) was



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higher than others and H. asiaticum had
the lowest frequency (0.4%). Hyalomma
marginatum comprised about 2.9% and H.
anatolicum accounted for 6% of total col-
lected species. H. dromedarii is the most
dominant tick species of camel in the
Khorassan region and a one humped camel
is a suitable host. The life cycle of this tick
includes one, two, or three hosts. Immature
ticks feed on small or large mammals, de-
pending on their life cycle. Hyalomma
dromedarii, H. anatolicum and H. marginatum
were collected from all three provinces but
in contrast, H. asiaticum only was collected
from Khorassan-e-Razavi's one-humped camels
(Table 2).

The CCHFV genome was found in 49
(10.2%) of 480 ticks, and three (6%) of 50
pools. Therefore, the tick prevalence was
10.2%. All of the CCHF-positive ticks were
male. The CCHFV genome was detected in
two out of four tick species, and of these, 42
(85.7%) belonged to H. dromedarii and 7

(14.3%) belonged to H. anatolicum (Table
2). The viral genome was detected in tick
samples from three cities in Khorassan-e-
Jonoobi. The positivity rates were as follows:
Boshroyeh, 25 out of 480 (51%), Birjand, 17
out of 480 (34.7%), and Nehbandan, 7 out of
480 (14.3%, Table 1).

Sera from 170 one-humped camels were
collected. All three provinces, and six out of
eleven cities and towns, were IgG-positive
for CCHFV. Nine (5.3%) out of 170 camels
were IgG-positive, this means that the IgG
prevalence was 5.3%. The positivity rates for
the provinces varied, and were as follows:
Boshroyeh, 12.5%, Kanimani, 7.14 %, Birjand,
8%, Nehbandan, 16.67%, Chehl dokhtaran,
7.14%, and Sabzevar, 6.66%. The highest
rate of IgG-positive samples was found in
Nehbandan (16.67%, two out of 12 sera),
Khorassan-e-Jonoobi. Eight out of the nine
positive samples were collected from female
camels (Table 3).

Fig. 1. Study area in Khorassan-e-Shomali, Khorassan-e-Razavi and Khorassan-e-Jonoobi are shown with asterisks



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Table 1. Positivity rates, number, and sex of ticks collected from one-humped camels from Khorassan-e-Shomali,
Khorassan-e-Razavi and Khorassan-e-Jonoobi in East and Northeast Iran

Area No Males No Females Total RT- PCR Positive
Nehbandan 27 9 36 7
Sarayan 28 23 51 0
Birjand 41 7 48 17
Kanimani 26 24 50 0
Boshroyeh 52 7 59 25
Robatsang 32 0 32 0
Quchan 28 13 41 0
Sabzevar 18 13 31 0
Mashhad 31 17 48 0
Chehl dokhtaran 28 6 34 0
Mangale 36 14 50 0
Total 347 133 480 49

Table 2. The sex, species and CCHF-positive rate of ticks infesting one-humped camels

Tick spp Male Female Total CCHF Positive
H. dromedarii 307 128 435 42

H .marginatum 10 4 14 0

H. anatolicum 29 0 29 7

H. asiaticum 1 1 2 0

Total 347 133 480 49

Table 3. IgG antibody-positive sera collected from one-humped camels from Khorassan-e-Shomali, Khorassan-e-
Razavi and Khorassan-e-Jonoobi

Area No. sera No. IgG Positive Local Positivity
Nehbandan 12 2 16.67

Sarayan 13 0 0

Birjand 25 2 8

Kanimani 14 1 7.14

Boshroyeh 16 2 12.5

Robatsang 16 0 0

Quchan 14 0 0

Sabzevar 15 1 6.66

Mashhad 16 0 0

Chehl dokhtaran 14 1 7.14

Mangale 15 0 0



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Fig. 2. Amplification of the S segment of the
CCHFV genome using RT-PCR, in tick samples from

the Khorasan province. (PC: Positive Control, NC:
Negative Control, S1-10: Samples, S1, S2, S3, S4,

S5, S6, S7 and S9 are negative, S8 and S10 are
positive)

Discussion

In this study, H. dromedarii was the most
dominant species of tick on one-humped
camels, and this is in agreement with the re-
sults obtained by Salimabadi (2010) in Iran
and Lawal et al. (2007) in Nigeria. Crimean-
Congo hemorrhagic fever infection was de-
tected in 49 (10.2%) of 480 tick samples and
this is a higher percentage than that previ-
ously reported by Salim-Abadi (3.79%) in
the Yazd Provinces of Iran (2011).

All the positive samples were obtained
from Hyalomma spp. Hyalomma ticks are
the primary vectors for the transmission of
CCHFV throughout Europe, Asia, the Mid-
dle East, and Africa (Ergonul 2006). Alt-
hough Hyalomma ticks are considered the
most important vector and reservoir for the
CCHFV, the virus has also been reported in
other tick genera (Tahmasebi et al. 2010).
The CCHFV genome was detected in two
out of the four tick species that were col-
lected (H. dromedarii, 85.7% and H.
anatolicum, 14.3%). This result is similar to
that found by Salim-Abadi et al. (2011),
therefore, these results suggest that H.
dromedarii and H. anatolicum act as vectors
for CCHFV in one-humped camels.

Hyalomma dromedarii is distributed
throughout the world wherever camels are
present, and H. anatolicum is widely distrib-
uted throughout Iran. Hyalomma anatolicum
transmits at least five Arboviruses, and is a
significant vector of CCHFV to humans
(Nabian and Rahbari 2008).

Telmadarraiy et al. (2010) detected the
CCHFV genome in Rhipicephalus bursa (in
one of the three ticks that were sampled), but
we failed to discover R. bursa in our study.
In the present study, we only found the
CCHFV genome in one-humped camel ticks
in Khorassan-e-Jonoobi (Birjand, Boshroyeh,
and Nehbandan). This province has an un-
usual geographical location, as it borders
Afghanistan to the east, the Sistan-va-Ba-
luchistan Province of Iran in the south, and
the Khorassan-e-Razavi Province of Iran in
the north. Since 2000, the disease has in-
fected 23 out of 31 provinces in Iran: Sistan-
va-Baluchistan (283 confirmed human cases),
Isfahan (44 confirmed cases), Fars (26 con-
firmed cases), Tehran (17 confirmed cases),
and Khorasan (12 confirmed cases) (Chinikar
et al. 2012). Notably, Sistan-va-Baluchistan
Province (south of Khorassan-e-Jonoobi) has
not just had the highest number of CCHFV
cases, but CCHF infections have been
observed in this area since 2000 (Chinikar et
al. 2012), as it shares a border with two
CCHF-endemic countries: Pakistan and Af-
ghanistan (Chinikar et al. 2010). The unu-
sual location of Khorassan-e-Jonoobi, which
is connected in the north, south, and east to
heavily infected or endemic areas of CCHF,
may explain why it was the only CCHFV-
positive area found in the study. We could
not ascertain why all the reverse transcrip-
tase polymerase chain reaction-positive ticks
were male, but this may have been due to the
presence of more males than females on the
animals, and also in our samples (347 males
vs 133 females).

During the last decade, an increasing
number of human CCHFV infections have



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been reported in various regions of Iran
(Chinikar et al. 2008). IgG-positive serum
samples collected from sheep, goats, cows,
and humans have been frequently reported in
different parts of the country (Saidi et al.
1975, Chinikar et al. 2005, Moradi et al.
2008). We found CCHFV IgG antibodies in
one-humped camel sera in all three prov-
inces studied, and these results, as well as
those from a previous study by Chinikar et
al. (2012), may indicate that CCHF is en-
demic to these regions, or that it has spread
from neighboring countries. In total, nine
(5.3%) out of 170 camels were IgG positive.
This finding is not in accordance with the
results obtained by Saidi et al. (1975), who
found that CCHF samples were negative in
all 157 camels that they had studied, from
south and southeast Iran. However, Williams
et al. (2000) found that 17 (16%) out of 109
camels sampled in Oman were tested posi-
tive for the CCHF IgG antibody.

Sistan-va-Baluchistan has been the most
CCHFV-infected province in Iran since
2000, because, as mentioned previously, it
shares a border with two CCHF-endemic
countries, Pakistan and Afghanistan (Izadi et
al. 2006, Chinikar et al. 2012). Khorasan,
which is connected to heavily infected or
endemic areas of CCHF, shares a large bor-
der area with neighboring countries, shares
common pasture with herds from CCHF-en-
demic areas, and experiences the illegal im-
portation of animals across the border, which
may explain why it is a CCHF-positive area.

Another important issue is the presence of
disease reservoirs and vectors, such as
Hyalomma spp., in this area. The CCHFV
genome has been isolated from at least 31
different tick species in Ixodidae (hard ticks)
and Argasidae (soft ticks) (Saijo et al. 2002,
Tahmasebi et al. 2010). As Champour (2013)
noted, the main tick species that affect one-
humped camels in this region are H.
dromedarii, H. anatolicum, H. marginatum,
and H. asiaticum. Hyalomma spp ticks are

considered the most important species in the
epidemiology of CCHFV in camels in this
area (Hoogstraal 1979). Six out of the eleven
cities and towns studied yielded one-humped
camel serum that was IgG-positive for
CCHF, and it has been shown that CCHF is
distributed across these three provinces.

We could not ascertain why almost all of
the positive-IgG sera samples were collected
from female camels (8/9), but this may have
been due to the presence of more females
than males in the samples (136 females vs 34
males), possibly because female camels re-
mained in herds longer than did males at the
time of sampling.

Our results reveal a lower prevalence of
seropositivity in one-humped camels (5.3%)
than in other domestic animals (30%) in Iran
(Chinikar et al. 2009). However, due to the
fact that camels remain in herds for longer
than do other animals (Champour et al. 2013),
and because camel pasture is very widely
geographically distributed, this small per-
centage has a significant effect on the
epidemiology of CCHF. The importance of
camels in the epidemiology of CCHF in
Russia and Astrakhan Oblast has been pre-
viously reported by Kurbanov, Berezin, and
Chumakov (Steele 1994).

Conclusion

Because CCHF is a serious threat to Iran,
imported animals, particularly one-humped
camels that carry a large number of ticks,
should be inspected and treated carefully.
Continued surveillance and strictly enforced
importation and quarantine practices will be
required to prevent human exposure and the
on-going dispersal of infected ticks and live-
stock in these regions. The use of commer-
cially available insect repellent, and the use
of clothing impregnated with permethrin,
can give some protection against tick bites
(Telmadarraiy et al. 2010, Salim-Abadi et al.



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2011). Further surveys of human and animal
populations, particularly of those animals
imported from neighboring countries to
these regions, are recommended, in order to
provide a better understanding of the distri-
bution and epidemiology of the virus in
these provinces.

Acknowledgements

The project was funded by Arboviruses
and Viral Hemorrhagic Fever Laboratory,
(National Reference Lab) Pasteur Institute
Tehran-Iran and Ferdowsi University of
Mashhad, bearing registration code 3/230667.
Thanks to staff members of Veterinary De-
partment of Khorassan-e-Shomali, particu-
larly Dr Razavi, Dr Ramezani, Dr Mohammad
Mehdi Ahmadi, Dr Hassan Safaei, Dr
Hossein Janati and Dr Shahin Ahmadi for
their collaboration in sampling. The authors
declare that there is no conflict of interests.

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