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Descriptive epidemiology and seroprevalence
investigations of Crimean-Congo Hemorrhagic Fever
virus in domestic animals of northeast Afghanistan
2024 Volume 1, Article number: e007
https://doi.org/10.48130/animadv-0024-0007
Received: 8 October 2024
Revised: 29 October 2024
Accepted: 11 November 2024
Published online: 12 December 2024
Enayatullah Hamdard1, Ahmadullah Zahir2, Sayed Hussain Mosawi3,4,
Saeedullah Din Muhammad4, Babrak Karwand1 and Sebghatullah
Sayedpoor5*
1Veterinary Science Faculty, Kunduz University, Kunduz city, Kunduz Province, Afghanistan
2Faculty of Veterinary Sciences, Afghanistan National Agricultural Sciences and Technology University,
Kandahar, Afghanistan
3Medical Sciences Research Center, Ghalib University, Kabul, Afghanistan
4Central Veterinary Diagnostic and Research Laboratory, Ministry of Agriculture, Irrigation and
Livestock Kabul, Afghanistan
5Faculty of Agriculture, Takhar University, Taloqan, Afghanistan
* Corresponding author, E-mail: sebghat.sayedpoor@gmail.com
Abstract
This study investigates CCHF epidemiological cases at a national level from 2007 to 2024, focusing
on tick species identification, CCHFV molecular detection, intrinsic, and extrinsic factors associated
with the disease's distribution in domestic animals (cattle, sheep, goats, camels, and chickens) in
Kunduz and Takhar provinces of Afghanistan. Analyzing national surveillance data for CCHF
prevalence from 2007 to 2024, encompassing 1,200 samples (720 ticks and 480 blood) were analyzed.
Data concerning intrinsic and extrinsic factors were collected, and seroprevalence was determined
using RT-PCR and ELISA. The highest number of confirmed positive cases in humans were
reported in 2023 (n = 1,236), and 2022 (n = 389), indicating an annual increase in CCHF cases, with
a total case fatality rate of 463, the highest CFR recorded in 2023 (n = 114). Averaging 30.2% over
eight years, with a notable death increase until 2018. Among 4,672 collected tick species, Hyalomma
predominated, followed by Rhipicephalus, with Dermacentor least found. RT-PCR and ELISA
revealed 73 positive cases in Kunduz and 81 in Takhar, with higher seropositivity in the latter.
Rustaq (10%) and Dasht-e-Archi (8.2%) showed the highest CCHF prevalence. The present study
highlights that early detection plays a crucial role in CCHF mitigation, despite Afghanistan's limited
testing capacity and knowledge of CCHF from a one-health perspective.
Citation: Hamdard E, Zahir A, Mosawi SH, Din
Muhammad S, Karwand B, et al. 2024. Descriptive
epidemiology and seroprevalence investigations of
Crimean-Congo Hemorrhagic Fever virus in domestic
animals of northeast Afghanistan. Animal Advances 1: e007
https://doi.org/10.48130/animadv-0024-0007
Introduction
Crimean-Congo Hemorrhagic Fever (CCHF) is a tick-borne disease
prevalent in Afghanistan, with a Case Fatality Ratio (CFR) of 10% to 50%. Its
incidence is rising in northeast Afghanistan, with animals as the primary
source of infection. First identified in the 1940s in the Crimean Peninsula, it
is caused by an enveloped negative-sense single-stranded RNA virus
belonging to the Bunyaviridae family, Nairovirus genus. The main mode of
transmission is through ticks, especially the Hyalomma species[1].
Wild animals, such as rabbits, hedgehogs, and certain rat species,
serve as reservoirs for CCHF in different regions. Domestic animals
like cattle, sheep, goats, camels, horses, dogs, donkeys, and poultry also
act as reservoirs and amplifying hosts[1]. They can be asymptomati-
cally infected or harbor infected ticks, with cattle being particularly
important for CCHFV transmission[2]. Detecting CCHF viral RNA in
clinical samples is crucial during the acute phase, especially before
symptoms appear when antibody detection isn't feasible. Rapid and
reliable diagnostic methods are essential due to high fatality rates,
pathogenicity, and potential human-to-human transmission[3,4]. Early,
accurate detection and monitoring of viral load are crucial for manag-
ing cases and ensuring biosafety, given the absence of specific treat-
ment or approved vaccines[5]. CCHF is a major public health concern
in Eastern Europe, Africa, the Middle East, and Asia, where the
Hyalomma tick is common. People involved in animal husbandry and
slaughtering, especially in rural areas of Afghanistan, face significant
risk[6]. Transmission of CCHFV happens through tick bites, contact
with crushed infected ticks, animal secretions or blood on injured skin
or mucosa, and exposure to contaminated surgical instruments[1,7].
In Afghanistan, CCHF is mainly reported among livestock workers,
but cases have also been documented among healthcare personnel,
veterinarians, meat inspectors, butchers, livestock traders, hunters,
farmers, ranchers, and the general population[1]. Occupational expo-
sure to infected animals and humans increases the risk of contracting
CCHF. The first case was reported in 1998 in Takhar province, north-
east Afghanistan. The WHO noted a substantial rise in cases, with 30
reported in 2018 and 947 from all 34 provinces in 2023, leading to 100
fatalities. Afghanistan is an endemic area for CCHF, facilitated by the
Hyalomma tick's ecological range.
CCHF prevalence rises throughout the year, particularly during Eid-
Al-Adha, a religious holiday characterized by widespread animal sacri-
fices and unprofessional slaughtering in rural/urban areas[5]. Eid-ul-
Adha is an annual religious festival during which millions of farm
animals, including goats, cows, sheep, and camels, are slaughtered.
This period, typically falling between June and September, is consid-
ered the most susceptible time for disease contraction, particularly
Crimean-Congo Hemorrhagic Fever (CCHF). The preference for self-
slaughter due to the unavailability of butchers and the convenience of
house slaughtering by professional butchers contributes to animal-to-
human disease transmission. Notably, CCHF is primarily confined to
rural areas of Afghanistan[8,9].
RESEARCH ARTICLE Open Access
© The Author(s) Animal Advances | www.maxapress.com/animadv
In 2022, Afghanistan was among the countries with the highest
number of CCHF cases reported by the WHO. The number of
confirmed cases has been on the rise in Afghanistan recently, but the
capacity for laboratory testing and case management remains
limited[5,10]. Various lab tests diagnose CCHFV, such as ELISA, serum
neutralization, antigen detection, virus isolation, and RT-PCR. RT-
PCR is preferred for its simplicity, specificity, and sensitivity[4].
Therefore, this study aimed to investigate the CCHF virus in
Afghanistan, focusing on identifying its primary reservoirs and trans-
mission factors. We conducted molecular and seroprevalence analyses,
examined tick morphology, and reviewed national surveillance data
from 2007 to 2024. We assessed seroprevalence and molecular detec-
tion in blood and tick samples from domestic animals in Kunduz and
Takhar provinces. Our findings could guide future surveillance efforts
to address this public health threat.
Materials and methods
Study area
Kunduz province, strategically located at a border intersection with
Takhar, Baghlan, Balkh, and Tajikistan, is a pivotal crossing point.
Kunduz has a population of 1,308,389 residents, comprising both rural
and urban dwellers[11].
Takhar, situated in the Northeastern Region of Afghanistan, is one
of 34 provinces. The province has a population of 1,109,573 inhabi-
tants, including rural and urban populations. The main occupations in
these provinces encompass agriculture, animal husbandry, clothing
production, labor, carpet weaving, and business[11].
Study design
A cross-sectional study was conducted from January to March 2024 in
the Kunduz and Takhar provinces, Afghanistan. With an expected
prevalence of 50%, a sample size of 427 livestock per province was
calculated at a 95% confidence level and 5% precision.
Districts, farms, and villages were chosen based on WHO-identified
high outbreak areas. Animal species (cows, sheep, camels, goats, and
chickens) were randomly selected, regardless of age, sex, or breed,
without tagging animals on farms. A systematic sampling method
ensured each animal had an equal chance of selection, with owners
consenting before sampling.
Blood sample collection and processing
Four hundred and eighty blood samples were collected equally from four
districts each in Kunduz and Takhar provinces. Trained veterinarians
assisted in drawing 5 ml blood samples from cattle, sheep, camels, goats,
and chickens via the jugular vein using BD Vacutainer 10 ml Hematology
(K₃EDTA) tubes, regardless of age. Samples were promptly transported
on dry ice to the Central Veterinary Diagnostic and Research Laboratory
(CVDRL) to maintain cold chain integrity. Upon arrival, serum was
obtained through centrifugation, transferred to labeled 5 ml cryogenic
vials, and stored at −20°C until further serological and molecular testing.
Detection of CCHFV RNA in serum samples and
amplification
CCHF-suspected samples were meticulously investigated for CCHF RNA
presence. Total RNA extraction from serum samples utilized the Viral
Nucleic Acid Isolation Kit from BioPerfectus Technologies. Extracted
RNA was reverse transcribed to cDNA, and amplification was conducted
using the one-step RealStar® 1.0 RT-PCR kit from Altona Diagnostics
(Germany) on an AriaMx real-time PCR machine.
Tick sample collection and processing
Ticks were systematically collected from livestock farms, including cattle,
sheep, camels, goats, and chickens, with tick collectors wearing full-body
protective clothing. Animals underwent thorough examinations to locate
ticks in specific areas. Ticks were carefully removed using blunt forceps
and transferred into labeled safety-lock Eppendorf tubes®. Live ticks
were transported to the CVDRL in Kabul for morphological examina-
tions, then stored at −80 °C for mRNA extraction and further analysis.
Tick identification
Ticks were identified based on their geomorphological features under a
light stereomicroscope using a multiple electronic entomology key[12].
The ticks were identified up to the species level based on morphological
characteristics of the ticks for species identification and recorded
respectively.
Detection of antibodies directed against CCHFV and
RNA extraction
The sera were serologically tested as described by Schuster et al.[13]. All
samples were first tested in an adapted commercial species-specific
indirect CCHFV-IgG ELISA. In the adapted commercial species-specific
indirect CCHFV-IgG ELISA, the samples with an OD value > 0.7 were
considered positive. In a second step, samples with divergent results were
run in a commercial species-adapted indirect CCHFV-IgG immunofluo-
rescence assay (IFA) to obtain the result.
Samples collected from the field were transferred through a cold
chain system and stored in a −80 °C freezer until RNA extraction.
Total RNA for RT-PCR and real-time PCR was subsequently extracted
and purified from frozen tissues using the Viral Nucleic Acid Isolation
Kit (Silica-Based Spin Column) from Jiangsu Bioperfectus Technolo-
gies Co Ltd. (Jiangsu), following the manufacturer's protocols. This
process aimed to eliminate genomic (g) DNA.
Detection of CCHFV RNA in real-time in ticks and sera
Serum samples and ticks were individually washed twice with PBS and
crushed with a pestle in 200–300 µl of liquid nitrogen in 2 ml cryogenic
vials to detect CCHFV RNA. RNA extraction was performed using the
QIAamp Viral RNA Mini Kit according to the manufacturer's instruc-
tions, and total RNA was stored at −70 °C until use. Gel electrophoresis
assessed RNA quality, where the presence of two distinct bands indicated
high-quality RNA: the top band represented 28S ribosomal RNA (rRNA)
at 4.8 kb, and the lower band represented 18S rRNA at 2.0 kb. Addi-
tionally, an in-house molecular method was used alongside a commercial
kit for CCHF virus detection.
Questionnaire for data collection
A comprehensive questionnaire gathered socio-demographic data and
assessed CCHF risk factors. Before administering the structured
questionnaire, community engagement activities identified potential
additional risk factors for CCHF exposure. Data collected from livestock
owners included animal types and numbers, sample collection details,
location, weather conditions, and individual animal specifics. Intrinsic
factors (species, sex, age, and breed) and extrinsic factors (husbandry
practices, body condition score, and tick infestation count) were
recorded. Questions on CCHF awareness and public health aspects
included closed, multiple-choice, and open-ended questions. Moderated
interviews were conducted with farm owners in the local language.
Data analysis
All data underwent statistical analysis using SPSS Statistics 23.0.
Proportions were calculated for qualitative variables, while mean with
standard deviation (SD) and median with interquartile range (IQR) were
calculated for quantitative variables. The chi-square test of independence
and the Fisher exact test were utilized to determine associations among
various independent factors (species, sex, breed, housing, hygiene, tick
infestation, body condition score, and feeding systems) with CCHF
seropositivity rates in cattle, sheep, camels, goats, and chickens. Minitab®
18 software was employed, with statistical significance set at p < 0.05[14].
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
2Hamdard et al. Animal Advances 2024, 1: e007
Results
Prevalence of CCHF in Afghanistan during the years
2007-2024
Data extracted from Afghanistan's national surveillance system for
2007−2024 revealed 4,667 suspected cases, with 2651 laboratory-
confirmed positives and 463 reported deaths. Additional cases were
reported annually: 163 in 2016, 245 in 2017, 483 in 2018, 412 in 2022,
1,442 in 2023, and 113 as of March 2024, with the highest in 2023 (Fig. 1).
Notably, confirmed positive cases peaked in 2023 (1,236), followed by
2022 (389), 2018 (139), and 2017 (104). This indicates an annual increase
in CCHF cases, posing a significant public health threat, with a total case
fatality rate of 463, highest in 2023 (114) (Fig. 1).
From 2007 to 2024, the average case fatality ratio (CFR) of confirmed
CCHF cases in Afghanistan was 30.2%. The CFR varied annually: 36%
in 2016, 48% in 2017, 42.2% in 2018, 32% in 2019, 29% in 2020, 25% in
2021, 17% in 2022, 11% in 2023, and 2.1% as of March 2024. While
CCHF cases increased until 2018, deaths subsequently declined (Fig. 1).
Possible reasons for reduced CFR include improved public knowledge
leading to prompt action, rapid blood donation supply, and increased
preventive measures. Comparing January−March incidence from
2022−2024, no cases were reported in January−March 2022−2023, but
26 cases in January 2024, 47 in February, and 64 in March, indicating
an anticipated increase in 2024 prevalence. Occupationally, most
reported cases were in the 'others' category (23%), followed by unem-
ployed (17%), housewives (14.5%), health staff (12.8%), shepherds
(11%), butchers (7%), animal dealers and farmers (7.6%), and students
(6.7%) (Fig. 2).
Prevalence of CCHF in the northeast during the years
2007−2024
Data from the national surveillance system for northeast region provinces
(Kunduz, Takhar, Badakhshan, and Baghlan) showed higher CCHF
prevalence in Kunduz (29.6%), followed by Takhar (25.4%), Badakhshan
(24%), and Baghlan (20.8%) (Fig. 3). These findings suggest a higher
likelihood of future prevalence in Kunduz and Takhar provinces. Hence,
early mitigation is crucial, necessitating intensified biosecurity and tick
prevention measures on animal farms.
Ticks' identification
A total of 720 tick samples were collected, each containing an average of
27 ticks, totaling 4,672 ticks from Kunduz and Takhar provinces (Fig. 4).
Tick species were identified based on morphological characteristics,
CCHF Na�onal level Confirmed cases (2007–2024)
0
200
400
600
800
1,000
1,200
1,400
Years
2023 20212018 2020 2022 2019 2017 2016 2015 3/1/2024 2008 2014 2012 2009 2013 2011 2010 2007
1,442
613
483
434 412
369
245
163
113 113
66 57 40 36 36 22 19 4
1,236
189
139 178 167
104
50 34 15
114
49 59 52 15
63 50
2 2 6040 0 0
36 60
Suspected cases Lab Confirm Death CFR (%)
Fig. 1 Number of suspected and confirmed CCHF cases and death in Afghanistan, 2007–2024. The horizontal axis year (from 2007 to 2024) and vertical axis
shows the number of CCHF cases.
Occupat
ional Prevalence of CCHF (2007–2024)
0
100
200
300
400
500
600
Occupt
iaonal Infect
ion of CCHF
Others Unemployed Housewife Health staff Shepherd Butcher Student Farmer Animal delar
567
425
358
314
284 273
165
96 84
512
382
322 286 252
158 150
90 80
55
43
36
28
32
CCHF cases (n) Posit ive CCHF cases (%)
115
Fig. 2 Occupational prevalence due to CCHF for the period of 2007−2024. The blue color indicates number of recorded cases while the dark blue color
indicates the number of death cases respectively. The horizontal axis indicates the occupation of persons, and the vertical axis indicates the total number of
CCHF cases due to occupational incidences of CCHF for the period of 2007−2024.
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
Hamdard et al. Animal Advances 2024, 1: e007 3
revealing Hyalomma (H. asiaticum and H. marginatum), Rhipicephalus,
Argas, Ornithodorus, Dermacentor, and Linognathus ticks. Hyalomma
species were the most prevalent, followed by Rhipicephalus, while
Dermacentor was least found. This indicates a significant presence of
Hyalomma ticks, the primary vectors of CCHF, suggesting a high risk of
transmission from infected animals to humans in the region and
nationally (Fig. 4).
Laboratory investigations for CCHFV by RT-PCR and
ELISA
A total of 720 ticks and 480 blood samples were collected, covering eight
districts in two provinces equally. Among the samples tested by RT-PCR
and IgG ELISA, 73 ticks in Kunduz and 81 ticks in Takhar were
confirmed positive. In blood samples, 29 in Kunduz and 36 in Takhar
tested positive (Fig. 5). Seropositivity was higher in Takhar than in
Kunduz, with Rustaq in Takhar showing the highest prevalence. In
Kunduz, Dasht-e-Archi had the highest prevalence. Overall, 102 ticks
(17%) and 117 blood samples (19.5%) out of 720 and 480, respectively,
were presumed positive for CCHF (Fig. 5).
Evaluation of intrinsic and extrinsic factors
Intrinsic factors, notably animal species, demonstrated a significant
association with CCHF prevalence, with cattle showing the highest
prevalence, followed by sheep, goats, and camels. Seroprevalence was
notably higher in females than males (Table 1). Animals older than 2
years were more susceptible than younger ones, although differences
between indigenous and exotic breeds were non-significant, despite
higher prevalence in indigenous animals (Tables 2, 3). Extrinsic factors
such as housing system, feeding, hygiene practices, body condition score,
and tick infestation were also explored (Tables 4−8). Free-ranging
animals had a higher prevalence than tethered ones, with significant
CCHF annual Confirmed cases in North-east Region (2007–2024)
0
5
10
15
20
Years
2023 2021 2009 2019 2012 2013 2020 2022 2008 2010 2011 2017 2024 2007 2014 2015 2016 2018
21
7
4 4
3 3 3 3
2 2
111
0 0 0 0 0
14
2 2
11
1
2
7
17
1 1
0
4
1
22
0
1
0
5
0
2
3
2
1
2
0 0
1
0
4
11
21
0
2
4 4
1 1
0 0 0
8
0 0
Takhar Kunduz Baghlan Badakshan
Fig. 3 National surveillance data due to CCHF outbreak on an annual basis for the northeast region provinces (Kunduz, Takhar, Badakhshan, and Baghlan)
during the period of 2007−2024. The horizontal axis shows CCHF prevalence on year basis and vertical axis shows the number of CCHF confirmed cases by the
national surveillance system for the northeast region provinces.
Ticks species iden�fica�on in Kunduz and Takhar
2,430 (52.01%)
1,349 (28.87%)
289 (6.19%)
258 (5.52%)
234 (5.01%)
112 (2.4%)
Species of Ticks Hyalomma (H. asiacum, H. marginatum)Rhipecephalus
Linognathus(Lice) Ornithodorus Argas Dermacentor
Fig. 4 Different species of ticks presents in Kunduz and Takhar provinces
with their percentage. Each species of the ticks found are exhibited in the
figure with number and percentage.
Takhar 53.42%
Kunduz 46.58%
Province
Takhar
Kunduz
0 100 200 300 400
Province
Takhar
Kunduz
117
102
240
240
36
29
81
73
20
17
Provincial confirmed + Blood Blood confirmed + Tick Confirmed + Posi�ve (%)
Fig. 5 Prevalence of CCHF in Kunduz and Takhar provinces.
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
4Hamdard et al. Animal Advances 2024, 1: e007
associations observed between housing systems and seroprevalence
(Table 4). Pasture-grazing animals exhibited higher seroprevalence than
stall-fed ones, while animals receiving good hygienic practices had lower
prevalence compared to those with poor hygiene (Tables 5, 6). Obese
animals demonstrated a higher prevalence than emaciated and average-
weight animals, with significant differences based on body condition
Table 1. Association of sera-molecular prevalence of CCHF within animal species in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Cattle 60 15 30 0.1816 0.0609
Sheep 40 9 32.5
Goat 30 3 26.66666667
Camel 15 0 13.33333333
Chicken 5 0 0
Dasht-e-Archi Cattle 60 18 25 0.6031 0.088
Sheep 40 13 22.5
Goat 30 8 10
Camel 15 2 0
Chicken 5 0 0
Imam Sahib Cattle 60 9 15 0.5714 0.061
Sheep 40 11 27.5
Goat 30 5 16.66666667
Camel 15 2 13.33333333
Chicken 5 0 0
Char Dara Cattle 60 5 8.333333333 0.0742 0.045
Sheep 40 4 10
Goat 30 3 10
Camel 15 0 0
Chicken 5 0 0
Takhar Taloqan Cattle 60 14 23.33333333 0.4867 0.067
Sheep 40 11 27.5
Goat 30 5 16.66666667
Camel 15 1 6.666666667
Chicken 5 0 0
Rustaq Cattle 60 22 36.66666667 0.5683 0.109
Sheep 40 16 40
Goat 30 9 30
Camel 15 3 20
Chicken 5 0 0
Khwaja Bahawodeen Cattle 60 9 15 0.4477 0.053
Sheep 40 8 20
Goat 30 4 13.33333333
Camel 15 0 0
Chicken 5 0 0
Khwaja Ghar Cattle 60 3 5 0.4953 0.043
Sheep 40 5 12.5
Goat 30 2 6.666666667
Camel 15 0 0
Chicken 5 0 0
Table 2. Association of sera-molecular prevalence of CCHF within sex of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Male 77 12 15.58441558 0.5098 0.0361
Female 73 15 20.54794521
Dasht-e-Archi Male 77 11 14.28571429 0.0052 0.0302
Female 73 30 41.09589041
Imam Sahib Male 77 10 12.98701299 0.1713 0.0103
Female 73 17 23.28767123
Char Dara Male 77 4 5.194805195 0.2301 0.0016
Female 73 8 10.95890411
Takhar Taloqan Male 77 11 14.28571429 0.1079 0.0067
Female 73 20 27.39726027
Rustaq Male 77 19 24.67532468 8.125 0.015
Female 73 31 42.46575342
Khwaja Bahawodeen Male 77 7 9.090909091 0.1222 0.003
Female 73 14 19.17808219
Khwaja Ghar Male 77 3 3.896103896 0.1914 0.001
Female 73 7 9.589041096
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
Hamdard et al. Animal Advances 2024, 1: e007 5
scores (Table 7). Significant associations were found within districts and
between provinces (Kunduz and Takhar) regarding tick infestation, with
tick-infested animals showing higher seroprevalence (Tables 8, 9).
Discussion
Afghanistan is currently facing an intensified surge of Crimean-Congo
Hemorrhagic Fever (CCHF) nationwide. Domestic ruminants, including
cattle, sheep, goats, camels, and chickens, can act as reservoir hosts for
CCHFV, aiding virus transmission through tick bites or direct contact
with infected tissues. This situation raises substantial public health
concerns. From 2007 to 2024, Afghanistan has seen an annual rise in
confirmed CCHF cases and associated deaths. Public surveillance data
indicates 4,667 suspected cases during this period, with 2,651 confirmed
positive cases and 463 deaths. Specific numbers for certain years include:
163 cases in 2016, 245 in 2017, 483 in 2018, 412 in 2022, 1,442 in 2023,
and 113 as of March 2024. The highest confirmed cases were in 2023
(1,236), followed by 2022, 2018, and 2017. Despite a rise until 2018, there
has been a decline in deaths since then[5].
The present investigation compared CCHF incidences nationally
from January to March in 2022 to 2024. Surprisingly, no cases were
reported in January to March in 2022 and 2023. However, in January
Table 3. Association of sera-molecular prevalence of CCHF within age of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center < 6 months 20 3 15 1 0.0137
1 > Year 30 3 23.33333333
> 2 Year 40 7 25
2 > Year 60 14 35
Dasht-e-Archi < 6 months 20 3 15 1 0.027
1 > Year 30 7 10
> 2 Year 40 10 17.5
2 > Year 60 21 23.33333333
Imam Sahib < 6 months 20 2 10 1 0.012
1 > Year 30 5 16.66666667
> 2 Year 40 9 22.5
2 > Year 60 11 18.33333333
Char Dara < 6 months 20 1 5 1 0.007
1 > Year 30 3 10
> 2 Year 40 2 5
2 > Year 60 6 10
Takhar Taloqan < 6 months 20 2 10 1 0.016
1 > Year 30 5 16.66666667
> 2 Year 40 9 22.5
2 > Year 60 15 25
Rustaq < 6 months 20 5 25 1 0.035
1 > Year 30 10 33.33333333
> 2 Year 40 13 32.5
2 > Year 60 22 36.66666667
Khwaja Bahawodeen < 6 months 20 2 10 1 0.0103
1 > Year 30 3 10
> 2 Year 40 5 12.5
2 > Year 60 11 18.33333333
Khwaja Ghar < 6 months 20 1 5 1 0.006
1 > Year 30 2 6.666666667
> 2 Year 40 2 5
2 > Year 60 5 8.333333333
Table 4. Association of sera-molecular prevalence of CCHF within breed of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Indigenous 140 26 18.57142857 0.5571 0.45
Exotic 10 1 10
Dasht-e-Archi Indigenous 140 39 27.85714286 0.6757 0.504
Exotic 10 2 20
Imam Sahib Indigenous 140 26 18.57142857 0.5571 0.45
Exotic 10 1 10
Char Dara Indigenous 140 12 8.571428571 0.3558 0.401
Exotic 10 0 0
Takhar Taloqan Indigenous 140 30 21.42857143 0.4654 0.465
Exotic 10 1 10
Rustaq Indigenous 140 47 33.57142857 0.8684 0.541
Exotic 10 3 30
Khwaja Bahawodeen Indigenous 140 20 14.28571429 0.7389 0.429
Exotic 10 1 10
Khwaja Ghar Indigenous 140 10 7.142857143 0.399 0.395
Exotic 10 0 0
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
6Hamdard et al. Animal Advances 2024, 1: e007
2024, 26 cases were confirmed, followed by 47 in February and 64 in
March, totaling 137 cases with a CFR of 1%. These findings indicate a
higher tendency for increased CCHF cases in 2024 compared to previ-
ous years[15].
The present findings on occupational transmission of CCHF from
2007 to 2024 aligns with previous studies[16]. Most cases were from
individuals categorized as 'others' (23%), followed by the unemployed
(17%), housewives (14.5%), health staff (12.8%), shepherds (11%),
butchers (7%), animal dealers, and farmers (7.6%), and students
(6.7%). These patterns correspond with studies by Ahmad et al., Sahak,
and research in Pakistan, which reported CFR rates ranging from 10%
to 40%[5,17].
Table 5. Association of sera-molecular prevalence of CCHF with housing system of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Extensive 75 19 25.33333333 0.5086 0.007
Intensive 75 8 10.66666667
Dasht-e-Archi Extensive 75 29 38.66666667 0.0181 0.023
Intensive 75 12 16
Imam Sahib Extensive 75 22 29.33333333 0.0031 0.018
Intensive 75 5 6.666666667
Char Dara Extensive 75 10 13.33333333 0.026 0.003
Intensive 75 2 2.666666667
Takhar Taloqan Extensive 75 26 34.66666667 0.0005 0.029
Intensive 75 5 6.666666667
Rustaq Extensive 75 39 52 0.0005 0.07
Intensive 75 11 14.66666667
Khwaja Bahawodeen Extensive 75 17 22.66666667 0.0007 0.01
Intensive 75 4 5.333333333
Khwaja Ghar Extensive 75 9 12 0.0141 0.003
Intensive 75 1 1.333333333
Table 6. Association of sera-molecular prevalence of CCHF with feeding system of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Stall feeding 75 6 8 0.0076 0.0145
Pasture grazing 75 21 28
Dasht-e-Archi Stall feeding 75 6 8 4.8928 0.064
Pasture grazing 75 35 46.66666667
Imam Sahib Stall feeding 75 3 4 0.0001 0.027
Pasture grazing 75 24 32
Char Dara Stall feeding 75 1 1.333333333 0.0053 0.005
Pasture grazing 75 11 14.66666667
Takhar Taloqan Stall feeding 75 5 6.666666667 0.0004 0.029
Pasture grazing 75 26 34.66666667
Rustaq Stall feeding 75 9 12 0.002 0.088
Pasture grazing 75 41 54.66666667
Khwaja Bahawodeen Stall feeding 75 3 4 0.002 0.013
Pasture grazing 75 18 24
Khwaja Ghar Stall feeding 75 2 2.666666667 0.066 0.001
Pasture grazing 75 8 10.66666667
Table 7. Association of sera-molecular prevalence of CCHF with hygenenic measures for animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Good 75 5 6.666666667 0.0024 0.018
Poor 75 22 29.33333333
Dasht-e-Archi Good 75 7 9.333333333 0.0001 0.056
Poor 75 34 45.33333333
Imam Sahib Good 75 4 5.333333333 0.0007 0.023
Poor 75 23 30.66666667
Char Dara Good 75 2 2.666666667 0.026 0.003
Poor 75 10 13.33333333
Takhar Taloqan Good 75 7 9.333333333 0.0052 0.019
Poor 75 24 32
Rustaq Good 75 12 16 0.0013 0.061
Poor 75 38 50.66666667
Khwaja Bahawodeen Good 75 4 5.333333333 0.0077 0.01
Poor 75 17 22.66666667
Khwaja Ghar Good 75 3 4 0.2205 0.0008
Poor 75 7 9.333333333
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
Hamdard et al. Animal Advances 2024, 1: e007 7
Program experts suggest that the increase in CCHF cases may be
linked to environmental factors. Drought and a lack of fodder in the
West and North regions have led to dry pastures, prompting the
migration of livestock and people to areas with better grazing condi-
tions. This movement increases the potential for infected tick expo-
sure as migrating herds mix with others[2,4,10].
Data from the national surveillance system for the northeast region
provinces (Kunduz, Takhar, Badakhshan, and Baghlan) showed
Kunduz had the highest prevalence (29.6%), followed by Takhar
(25.4%), Badakhshan (24%), and Baghlan (20.8%)[18]. This suggests a
higher likelihood of prevalence in Kunduz and Takhar in the future.
Domestic ruminants like cattle, goats, and sheep can act as reservoir
hosts for CCHFV, making tick-borne diseases a significant concern
due to their veterinary and public health implications. Hyalomma
species are major vectors for CCHFV transmission to both animal and
human hosts through bites[18,19]. Across eight districts in the Kunduz
and Takhar provinces, a total of 720 ticks and 480 blood samples were
collected. Of the 360 ticks sampled in each province, 73 in Kunduz and
81 in Takhar tested positive for CCHFV using RT-PCR and IgG ELISA
(Fig. 5). Regarding blood samples, 29 out of 240 were positive in
Kunduz, while 36 out of 240 were positive in Takhar. Seropositivity
was higher in Takhar province than in Kunduz. In Takhar, Rustaq had
the highest prevalence, followed by Taloqan, Khwaja Bahawodeen, and
Khwaja Ghar, ranging from 10% to 2%. In Kunduz, Dasht-e-Archi had
the highest prevalence, followed by Kunduz Center, Imam Sahib, and
Char Dara, ranging from 8.2% to 2.4% (Fig. 5).
Remarkably, among the eight districts of both provinces, Rustaq
showed the highest prevalence of CCHF at 10%, followed by Dasht-e-
Archi at 8.2%. Across both provinces, 102 (17%) tick samples were
presumed positive and 117 (19.5%) blood samples out of 720 and 480,
respectively (Fig. 5).
These findings are in line with parallel studies conducted in various
countries. For instance, in Gambia[20], a higher prevalence was
reported in cattle compared to small ruminants (sheep and goats),
Table 8. Association of sera-molecular prevalence of CCHF with body condition score of animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Obese 50 15 44 5.9152 0.0002
Average 50 4 14
Emaciated 50 8 24
Dasht-e-Archi Obese 50 22 30 1.0036 0.001
Average 50 7 8
Emaciated 50 12 16
Imam Sahib Obese 50 16 32 1.3038 0.0004
Average 50 3 6
Emaciated 50 8 16
Char Dara Obese 50 7 14 7.6074 1.194
Average 50 1 2
Emaciated 50 4 8
Takhar Taloqan Obese 50 16 32 2.748 0.0003
Average 50 4 8
Emaciated 50 11 22
Rustaq Obese 50 17 34 2.386 0.0053
Average 50 6 12
Emaciated 50 27 54
Khwaja Bahawodeen Obese 50 11 22 2.4731 0.0001
Average 50 1 2
Emaciated 50 9 18
Khwaja Ghar Obese 50 4 8 0.0001 2.627
Average 50 1 2
Emaciated 50 5 10
Table 9. Association of sera-molecular prevalence of CCHF with tick infestation in animals in the Kunduz and Takhar provinces of Afghanistan.
Study province Study district Variables Examined Positive Seroprevalence (%) χ2 value p-value
Kunduz Kunduz-Center Indigenous 75 19 25.33333333 0.0508 0.007
Exotic 75 8 10.66666667
Dasht-e-Archi Indigenous 75 32 42.66666667 0.0013 0.041
Exotic 75 9 12
Imam Sahib Indigenous 75 18 24 0.1103 0.005
Exotic 75 9 12
Char Dara Indigenous 75 8 10.66666667 0.2663 0.0008
Exotic 75 4 5.333333333
Takhar Taloqan Indigenous 75 24 32 0.0052 0.019
Exotic 75 7 9.333333333
Rustaq Indigenous 75 39 52 0.0005 0.0702
Exotic 75 11 14.66666667
Khwaja Bahawodeen Indigenous 75 18 24 0.002 0.013
Exotic 75 3 4
Khwaja Ghar Indigenous 75 8 10.66666667 0.0666 0.0018
Exotic 75 2 2.666666667
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
8Hamdard et al. Animal Advances 2024, 1: e007
which aligns with the present results. Similarly, studies[18,21] in
different locations also revealed higher seropositivity of CCHFV in
cattle than in goats and sheep, consistent with the present findings.
Additionally, research in Pakistan reported the highest seroprevalence
of CCHFV antibodies in cattle, followed by sheep and goats. Studies in
Corsica, France[22] and Kosovo, Germany, also found higher seroposi-
tivity in cattle compared to sheep and goats[23].
The present findings reveal higher seroprevalence in cattle com-
pared to sheep, goats, and camels, suggesting they could serve as a
source of CCHFV transmission to these animals during grazing inter-
actions. This possibility is supported by previous research[24]. The
elevated seroprevalence in cattle may be attributed to Hyalomma ticks,
the primary carriers of CCHFV, which prefer feeding on larger
animals like cattle. Ticks readily attach to cattle for feeding, facilitating
efficient viral transfer between infected ticks and cattle. CCHFV repli-
cates to higher levels in cattle compared to sheep, goats, and camels,
leading to a higher viral load in the bloodstream. This increases
the likelihood of ticks acquiring CCHFV when feeding on infected
cattle.
In the present study, a significantly higher seroprevalence of CCHF
was found in female domestic animals compared to males (p > 0.05).
This aligns with previous research[18,20,25,26]. The elevated seropreva-
lence in female domestic animals could be attributed to factors such as
pregnancy stress, lactation stress, and limited access to balanced nutri-
tion, which may reduce immunity and decrease their resistance to tick
infestations.
The present study supports previous findings that local breeds
exhibit higher seropositivity compared to exotic breeds, as reported in
previous studies[18,25]. Similarly, previous research[18,25] indicates that
indigenous cattle breeds experience more tick infestations and exter-
nal parasites compared to exotic breeds, potentially leading to higher
seroprevalence. This similarity could be attributed to factors such as
poor hygiene, limited access to quality feed, and inferior husbandry
practices observed in Indigenous breeds compared to exotic breeds
found in the study areas. The current study highlights higher sero-
prevalence in animals raised extensively or on communal grazing
systems, while those in intensive housing systems exhibit lower sero-
prevalence. These findings align with previous research[18,24,27] . The
increased seroprevalence in extensively raised animals may be
attributed to their closer proximity to tick vectors, lack of acaricide
use, and poor hygiene management practices on the farm. Conversely,
the lower seroprevalence in animals kept in intensive housing systems
may result from effective tick control measures, such as regular acari-
cide application and good hygiene practices, which reduce tick popula-
tions[27].
Early studies support the present findings that higher seropreva-
lence in older and tick-infested cattle is age-dependent[28]. Seropreva-
lence in cattle increases with age and the presence of tick infestation, as
documented in previous research[29]. Studies conducted in Kenya,
northwestern Senegal, Afghanistan, and Uganda[30] also support this
association between seroprevalence and age in cattle. Additionally,
research suggests that the seroprevalence of CCHFV antibodies in
domestic ruminants is dependent on age, with older animals exhibit-
ing higher seroprevalence rates than younger ones[21]. This higher
seroprevalence with age may be attributed to increased production of
IgG antibodies in response to continuous exposure to CCHFV-
infected ticks in older animals in endemic areas, compared to younger
animals with maternal immunity.
The present investigations have identified a correlation between the
body condition of domestic animals and CCHFV antibody seropreva-
lence. Previous research[18] found a high seroprevalence in overweight
ruminants, correlating with weight. They observed that obese animals
were more susceptible to CCHF compared to emaciated animals due
to weakened immunity. The present study supports this, revealing that
obese domestic animals exhibited the highest seroprevalence, followed
by those of average weight, and then emaciated animals, respectively.
Furthermore, heavily infested ruminants play a crucial role in
CCHFV transmission and can become sources of infection for healthy
animals compared to tick-free animals, as reported previously[18,31].
Similarly, it was reported that tick-infested cattle have a higher sero-
prevalence compared to tick-free animals[28], which is fully consistent
with the current study.
Afghanistan, situated in the ecological range of the Hyalomma tick,
experiences an annual increase in CCHF incidence[10,32]. The variation
in seropositivity observed in the present study may be attributed to the
endemicity of CCHF in the region, the significant abundance of ticks,
and host behavior patterns influenced by climate changes and drought.
Additionally, differences in laboratory examinations for molecular and
serological detection of CCHFV antibodies, including specificity and
sensitivity could contribute to these variations. These insights call for
further investigation into the associated factors contributing to the
rising number of CCHF cases within the country.
Conclusions
The higher seroprevalence underscores a significant healthcare concern,
given the recent rise in CCHF cases and fatalities in Afghanistan. The
initial report highlights a notably elevated prevalence of CCHFV
nationally and regionally, urging urgent attention to mitigate further
spread, particularly in livestock. Extrinsic risk factors (husbandry
practices, animal condition, and tick infestation) and intrinsic factors
(species, sex, age, and breed) show significant associations with CCHFV
seroprevalence, detected through IgG antibodies and RT-PCR analysis.
Collaborating with Afghan molecular experts, an in-house molecular
method has been developed for CCHF virus detection in ticks and blood
samples, facilitating deeper genome studies. Early detection and
understanding of risk factors in animal hosts aid in mapping endemic
areas. Given CCHF's impact on human health, especially those in direct
animal contact, control strategies are imperative. Livestock plays a vital
role in rural Afghans' livelihoods and can transmit diseases. Raising local
awareness, collaborating with health and veterinary departments,
promoting animal health practices, and intensifying livestock husbandry
alongside establishing active disease surveillance are essential for
enhancing one-health approaches.
Ethical statement
All procedures were reviewed and approved by the Animal Care and
Research Committee of Ministry of Agriculture Irrigation and Livestock
(MAIL), identification number: (KBL-2023–MAIL-03), approval date:
2023-12-09, and implemented based on the standard of Experimental
Animal Care and Use Guidelines of Animals. The research followed the
"Replacement, Reduction, and Refinement" principles to minimize harm
to animals. This article provides details on the housing conditions, care,
and pain management for the animals, ensuring that the impact on the
animals is minimized during the experiment.
Author contributions
The authors confirm contribution to the paper as follows: writing – draft
manuscript preparation, investigation, conceptualization: Hamdard E;
formal analysis, data curation: Karwand B, Din Muhammad S; data
collection – review & editing, methodology: Zahir A, Din Muhammad S,
Mosavi SH. writing – final draft and editing: Sayedpoor S. All authors
reviewed the results and approved the final version of the manuscript.
Epidemiology and seroprevalance investigations of CCHF in northeast Afghanistan
Hamdard et al. Animal Advances 2024, 1: e007 9
Data availability
The original contributions presented in this study are included in the
article/supplementary material. Further inquiries can be directed to the
corresponding author.
Acknowledgement
We are thankful to the Central Veterinary Diagnostic and Research
Laboratory (CVDRL) for the provision of laboratory equipment. We also
acknowledge the support from the Directorate General of Health
Services, Government of Kunduz and Takhar provinces, for providing the
requested data. The contribution of Mr. Najeeb Zia in the graphical
presentation of the data is acknowledged.
Conflict of interest
The authors declare that they have no conflict of interest.
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