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Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.

1, 63-74 1
Afghanistan Journal of Infectious Diseases
AJID
https://ajid.ghalib.edu.af/index.php/ajid

Vol. 2, No.1, January 2024, pp. 63-74

Epidemiology and Outcomes of Crimean-Congo Hemorrhagic Fever in


Afghanistan: A Review of 2010–2019
Kubra Rahmani1, Raihana Behrad2, Ali Rahimi3,4 , Sharareh Shayan4, Gökçe Uğurlu5, Nasar Ahmad Shayan6

1. Roshana Eye Hospital, Herat, Afghanistan


2. General Department, Faculty of Medicine, Ghalib University, Herat, Afghanistan
3. Scientific Research Center, Jami University, Herat, Afghanistan
4. Department of Para-clinic, Faculty of Medicine, Jami University, Herat, Afghanistan
5. Department of Public Health, Faculty of Medicine, Hacettepe University, Ankara, Turkey
6. Department of Epidemiology and Biostatistics, Faculty of Medicine, Western University, London, ON, Canada
A R ART I C L E I N F O
ABSTRACT
Type: Review Article
Received: 2023/04/17 Background: The study investigates the recent surge in Crimean-Congo
Accepted: 2023/06/13 Hemorrhagic Fever (CCHF) cases in Afghanistan, a high-risk viral disease
transmitted through tick bites and livestock, and aims to identify patterns
of the increase and offer prevention strategies.

Methods: A systematic review of all scholarly articles published on CCHF


*Corresponding Author: in Afghanistan between 2010 and 2019 was conducted using a
Ali Rahimi comprehensive and rigorous search strategy using the PubMed database.
Address: Scientific Research The quality of the included studies was assessed using the Newcastle-
Center, Jami University, Herat,
Afghanistan Ottawa Scale and the Cochrane Risk of Bias Tool.

[email protected] Results: During the study period, 1537 suspected cases of CCHF were
Iran reported in Afghanistan, with the highest number and deaths in the western
region. The majority of cases were male, aged 16-84, and involved in
animal husbandry, agriculture, and healthcare workers, with a 2:1 male-to-
female ratio. The majority of cases were aged 16-84.

Conclusion: This study highlights the need for effective measures to


prevent CCHF transmission in Afghanistan, such as education, improved
animal management, and infection control in hospitals and laboratories, to
reduce outbreak risks and enhance public health.

DOI: Kewwors: Crimean-Congo Hemorrhagic fever, CCHF, Afghanistan,


https://doi.org/10.60141/AJID/V.2.I.1.8
systematic review, public health.
To cite this article: Rahmani K, Behrad R, Rahimi A, Shayan S, Uğurlu G, Shayan NA. Epidemiology and Outcomes of Crimean-Congo
Hemorrhagic Fever in Afghanistan: A Review of 2010–2019. Afghanistan Journal of Infectious Diseases. 2024;2(1):63-74.
https://doi.org/10.60141/AJID/V.2.I.1.8

Copyright © 2023 Afghanistan Journal of infectious Diseases, and Ghalib University. All rights reserved.
This work is licensed under a Creative Commons Attribution-Noncommercial 4.0 International License
64 Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74

1. Introduction
and contact with infected animals, occupational
Crimean-Congo hemorrhagic fever (CCHF) is a exposure is also a concern for those working in the
viral disease transmitted to humans through the bite livestock and agricultural sectors in Afghanistan
of infected ticks (1, 2). The disease was first (22). The first humanitarian incident was reported
identified in the Crimea region of the former Soviet in 1998 in Takhar Province (19 cases and 12
Union in 1944 and later in the Congo region in deaths). In 2000, CCHF occurred in the Golran
1969, leading to the renaming of the disease as district of Herat Province, with 25 cases and 15
Crimean-Congo Hemorrhagic Fever (3, 4). The deaths. No positive CCHF events were reported in
virus responsible for CCHF, called Crimean- Afghanistan until 2007 (1). Between 2007 and
Congo Hemorrhagic Fever Virus (CCHFV), was 2009, 1,562 cases were reported in Afghanistan
first identified in 1956 (5,6) and is a member of the (23).
Nairoviridae family, with ixodid ticks being the
main carriers of the virus (7–10). Humans can It is important to implement effective control
become infected through the bite of an infected measures to prevent the transmission of CCHF in
tick, contact with the skin or blood of infected Afghanistan, including education about the
animals, or contact with the blood or bodily fluids prevention and awareness of the danger of the
of infected patients. Risk factors for transmission disease, as well as improved management of
include working with CCHFV samples in infected animals and the implementation of proper
laboratories, working in hospitals where patients infection control measures in hospitals and
with CCHF are being treated, and not following laboratories. This study aimed to determine the
proper infection prevention guidelines (10–17). cause of the recent increase in the number of CCHF
cases in Afghanistan and provide academic
Risk factors for transmission include working with suggestions and approaches for disease prevention.
CCHFV samples in laboratories, working in By better understanding the factors contributing to
hospitals where patients with CCHF are being the spread of CCHF in Afghanistan, we can take
treated, and not following proper infection steps to reduce the risk of outbreaks and improve
prevention guidelines (3). The incubation period is public health in the region.
1–5 days, with a maximum of 9 days in the case of
contact with infected blood or tissues (18). The pre- 2. Materials and Methods
hemorrhagic phase lasts for three days and is
characterized by fever (39–41 °C), lethargy, This study is a systematic review of all scholarly
headache, muscle and chest pain, and facial articles published on CCHF in Afghanistan
bleeding. The hemorrhagic phase usually begins 3- between 2010 and 2019. The review was
5 days after disease onset and lasts for 2-3 days, conducted using a comprehensive and rigorous
with a mucocutaneous petechial rash being a search strategy in the PubMed database, which
common manifestation. The convalescent phase included the keywords "CCHF" and
begins 10–20 days after the beginning of the "Afghanistan." The initial search yielded 31
infection and may last for up to a year. There is no articles, of which 27 were published between 2010
specific treatment or vaccine for CCHF, and death and 2019.
rates can be high, particularly in severe cases (19–
21). Following the selection process that involved the
assessment of full-text articles, 25 articles were
CCHF is a public health concern in Afghanistan, deemed relevant to the current review. Of these, 11
where it is transmitted through ticks and livestock, articles met the inclusion criteria and were included
leading to past outbreaks (22). This disease is in the final analysis. In addition to these 11 articles,
particularly prevalent in regions where agricultural three reports on CCHF cases in Afghanistan from
activities and animal husbandry are common. In 2019 to 2021 were reviewed and included in the
addition to the risk of infection through tick bites study (Figure 1). The authors of the current study
Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74 65

followed a standardized protocol for the selection, The majority of affected individuals were male,
assessment, and synthesis of the included studies. with the highest male-to-female ratio of 2:1. The
The process involved the assessment of the age range of the affected individuals varied, with
authors, study area, research plan, work method, the majority falling between 16 and 44 years old.
key findings, and the final results of each study. All The occupations of the affected individuals were
the authors of the review participated in the process diverse, with housewives, health staff, shepherds,
of selecting, reading, and evaluating the included butchers, students, animal dealers, and farmers
studies to ensure a high level of rigor and being the most affected. It is worth noting that the
consistency. The data extraction process was studies and reports reviewed in this table had
carried out independently by two authors, and different sample sizes and study designs, which
discrepancies were resolved by consensus. The may affect the generalizability of the findings.
quality of the included studies was assessed using Furthermore, the table also shows that CCHF cases
the Newcastle-Ottawa Scale (NOS) for were continuously reported in Afghanistan in 2019,
observational studies and the Cochrane Risk of according to the WHO EMRO and the Ministry of
Bias Tool for randomized controlled trials. The Public Health.
results of the studies were synthesized narratively,
with a focus on the occurrence and characteristics 3-1. The 2019 Report of the Ministry of Public
of CCHF in Afghanistan. This study is a systematic Health on CCHF
review of all scholarly articles published on CCHF
in Afghanistan between 2010 and 2019. It was The Ministry of Public Health's 2019 report
based on a comprehensive and rigorous search (currently only available offline) provides
strategy, and the inclusion of relevant articles was information on the number of COVID-19 cases and
determined through a standardized selection mortality rates in various provinces in Afghanistan
process. The quality of the included studies was (Figure 2). The provinces with the highest number
assessed, and the results were synthesized of cases were Herat and Kabul, with 138 and 137
narratively to gain a more comprehensive cases, respectively. However, the mortality rate
understanding of the occurrence and characteristics was the highest in Kunduz, with 6 out of 16 deaths.
of CCHF in Afghanistan. The province with the lowest number of cases was
Parwan, with only 12 cases and two deaths. The
3. Results provinces included 51 cases and five deaths. The
total number of cases in all provinces was 440, with
This study aimed to investigate the a mortality rate of 50 deaths. Notably, the mortality
epidemiological status of Crimean-Congo rate varies greatly among provinces (24).
hemorrhagic fever (CCHF) in Afghanistan
between 2010 and 2019 (except for one report from 3-2. The 2019 Eastern Mediterranean Region
2021) by systematically reviewing 14 studies and Report on CCF in Afghanistan
reports. The summary table includes information
on the title of the study, authors, year of According to the WHO Eastern Mediterranean
publication, type of study, sample size, number of Regional Office (EMRO) report, in 2019, 359
confirmed cases by ELISA, percentage of males suspected cases of CCHF were reported in
affected, the age range of affected individuals, and Afghanistan, of which 46 were confirmed to be
occupation of affected individuals (Table 1). The fatal. Compared to previous years, the number of
studies and reports reviewed in this table indicate suspected cases in 2019 was lower than that in
that CCHF is a significant public health concern in 2017 and 2018, which saw a peak of 483 and 245
Afghanistan. According to a national surveillance suspected cases, respectively. However, the
study, 239 of the 1284 cases reported from 2016 to number of confirmed deaths in 2019 was higher
2018 were confirmed by ELISA. than that in 2014 and 2015, which saw 2 and 20
confirmed deaths, respectively (23, 25). Overall,
based on WHO reports, there were a total of 1537
66 Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74

Studies included terms


"CCHF" and "Afghanistan"
n=31

Studies after 2010


n=27

Full text studies


n=11

Reports
n=3

Total=14

Fig. 1. Search and selection process for CCHF articles included in this study.

suspected cases reported, 491 confirmed cases, and 25). Figure 3 compares the annual suspected,
205 deaths recorded between 2010 and 2019 (23, confirmed, and death cases of CCHF since 2010.

Table 1: Summary of the studies reviewed in this paper, including information such as study design, sample size, and
main findings.

1. Descriptive
epidemiology of
housewives (15%),
Crimean-Congo
Surveillance health staff (13%),
Hemorrhagic Fever
Mohammad study/ shepherds (11%),
(CCHF) in 16-
Nadir Sahak 2019 Descriptive 1284 239 68.5 butchers (6%),
Afghanistan: 44
et al epidemiology students (6%),
Reported cases to
study animal dealers and
National
farmers (both 2%)
Surveillance
System, 2016-2018
2. CCHF virus
Studies

variants in
Adnan Descriptive
Pakistan and 18-
Khurshid et 2015 epidemiology 49 10 - -
Afghanistan: 56
al study
Emerging diversity
and epidemiology
3. Complete
sequence and
phylogenetic Molecular
Stephan
characterization of epidemiology
Olschlager et 2011 - - - - -
Crimean–Congo /virology
al
hemorrhagic fever study
virus from
Afghanistan
Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74 67

4. Prevalence of
Zoonotic and
Vector-Borne
Catherine S. Prevalence 18-
Infections Among 2016 809 33 - -
Todd et al study 36
Afghan National
Army Recruits in
Afghanistan
5. Investigation of
Crimean-Congo
hemorrhagic Fever
descriptive
in Patients Hossein 10-
2019 study/case- 120 29 2:1 -
Admitted to Antani Hatami et al 85
control study
Hospital, Kabul,
Afghanistan

Housewife (36.5)
Farmer (22.2)
Butcher (11.1)
Laborer (9.5)
6. Crimean-Congo
Shepherd (4.8)
Hemorrhagic
Aziz-ur- descriptive 9- Unemployed (4.8)
Fever, Herat
Rahman 2019 case series 63 32 60.3 90 Waiter (3.2)
Province,
Niazi et al study Engineer (1.6)
Afghanistan, 2017
Student (1.6)
Driver (1.6)
The security guard
(1.6)
Shopkeeper (1.6)
96 total:
7. Crimean-Congo 58 were farmers,
hemorrhagic fever Yavuz Ince et Surveillance 21 were HCWs, 12
2014 3426 61 67 -
infections reported al study were butchers, and
by ProMED 5 were leather
business workers
8. Crimean-Congo
Hemorrhagic Fever A descriptive
(CCHF) in Shohra and analytic 20-
2021 231 51 37 butchers
Afghanistan: A Qaderi retrospective 50
retrospective study
single-center study
9. Consensus
report: Preventive
measures for Haken
Crimean-Congo Leblebicioglu 2015 - - - - - -
Hemorrhagic Fever et al
during Eid-al-Adha
festival.
10. Crimean-
Congo
hemorrhagic fever
virus strains Hoti
and Afghanistan Robert W.
2020 - - - - - -
cause viremia and Cross
mild clinical
disease in
cynomolgus
monkeys
11. Genome
John
Sequence of Ex-
Chamberlain 2013 - 1 1 - 38 -
Afghanistan
et al
Crimean-Congo
68 Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74

Hemorrhagic Fever
Virus SCT Strain,
from an Imported
United Kingdom
Case in October
2012
Housewife
(32.9%), Farmer
(25.0%), Shepherd
(6.7%), Butcher
12. Crimean-
(6.7%), Self-
Congo
Aziz-ur- Descriptive employed (4.8%),
hemorrhagic fever
Rahman 2021 case series 252 - 63.5 - Worker (2.0%),
in Herat province
Niazi et al Report Student (1.6%),
of Afghanistan,
Security guard
2007-2021
(0.4%), Collegian
Reports

(0.4%), Jobless
(0.8%), Other
(18.7%)
13. CCHF cases
continuously Descriptive
reported in WHO EMRO 2019 case series 359 120 - - -
Afghanistan, in Report
2019
14. Ministry of
Descriptive
Public Health Ministry of
2019 case series 440 - - - -
Report on CCHF Public Health
Report
in 2019

Fig. 2. Geographic distribution of CCHF cases in Afghanistan in 2019 (24).


Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74 69

suspected confirmed death

600
500
400
300
200
100
0
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
YEAR

Fig. 3. Number of Suspected, Confirmed, and CCHF Deaths between 2010-2019.

18
16
14
12
10
8
6
4
2
0
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
YEAR

18
16
14
12
10
8
6
4
2
0
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
YEAR

Figure 4. Case fatality rates of CCHF cases between 2010-2019.

4. Discussion continuously in the country from 2010 to 2019. The


total number of reported cases in the surveillance
This review summarizes the findings of 14 studies studies ranges from 3426 to 1284, with a confirmed
and reports on the occurrence and characteristics of case percentage of ELISA ranging from 2% to
CCHF in Afghanistan from 2010 to 2019 (Table 1). 61%. The majority of the studies reported that the
The studies included surveillance, descriptive and majority of cases were male (ranging from 60.3%
analytic epidemiology, molecular epidemiology to 68.5%) and that the age range of cases was
and virology, and prevalence studies. Overall, between 9 and 85 years. It is important to note that
these studies indicate that CCHF is present in the studies had different sample sizes and years of
Afghanistan and that it has been reported data collection, which may affect the comparability
70 Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74

of the findings. Additionally, some studies did not In Afghanistan, unemployed people (19%) had the
provide information on some of the variables, such highest statistics, while animal sellers (1.7%) had
as occupation, which limits the interpretation of the the lowest (25). Therefore, further research is
results. needed to investigate the reasons for this age
distribution and to develop targeted prevention and
The results of this study indicated that the majority control strategies for CCHF in Afghanistan.
of reported cases of CCHF in Afghanistan from
2010 to 2019 were male (Table 1). The percentage The studies also provided information on the
of male patients ranged from 60.3% to 68.5% occupations of the participants. The most common
across the 14 studies and the reports included in the occupation among the cases was that of a
review. This suggests that there may be certain housewife, followed by health staff, shepherds,
factors that make men more susceptible to butchers, and farmers. Other common occupations
contracting CCHF in Afghanistan or that men may included those of students, animal dealers, and
be more likely to seek medical attention and be laborers. In Iran, butchers and soldiers have the
diagnosed with the disease. Further research is highest and lowest statistics, respectively (27). A
needed to investigate the reasons for this sex study conducted in Turkey found that the high-risk
disparity and to develop targeted prevention and groups for CCHF were men and women working
control strategies for CCHF in the country. These in agriculture and animal husbandry, as well as
findings are consistent with other CCHF studies those working in healthcare settings (29).
conducted in Turkey (26) and Iran (27). Some Additionally, it has been reported that
studies have concluded that the higher occurrence slaughterhouse workers, butchers, and livestock
of CCHF in males is due to the more frequent handlers are at high risk of contracting CCHF (30,
exposure of men to CCHF risk factors, such as 31). These findings suggest that individuals who
farming and animal handling (13, 14). are more likely to come into contact with infected
The results of this study indicate that the majority ticks or animals are at greater risk of contracting
of reported cases of CCHF in Afghanistan from CCHF.
2010 to 2019 were reported in the age range of 9–
85 years old, with a specific emphasis on the age When comparing the occurrence of CCHF in
group of 16–30 years old (Table 1). This is Afghanistan to other regions, it is important to note
probably because this age group is the working age that the disease is endemic to many countries in the
in Afghanistan, and more people were exposed to Middle East, Central Asia, and Africa. The World
CCHF risk factors in these age groups than in the Health Organization (WHO) estimates that the
younger or older categories (22). The studies disease causes an annual incidence of up to
reviewed showed that 45% of reported cases were 150,000 cases globally, with a case fatality rate of
from this age group, with the lowest number of up to 30%. In comparison, Afghanistan has a
reported cases being from the age group of 60 years relatively low case-fatality rate for CCHF (0–
and older at 5%. These findings are consistent with 16.74%) compared to other countries in the region.
a study conducted by Mohammad Nader Sohak et For example, Pakistan reported a case-fatality rate
al. between 2016 and 2018, which also found that of 10–40% in 2018 (32). Additionally, most CCHF
the highest number of reported cases were from the cases reported in Afghanistan are in rural areas,
age group between 16 and 30 years (25). In where the main sources of infection are believed to
Pakistan, the highest statistics belong to the age be ticks and livestock. This is in contrast to other
group over 65 years (5.0%) and the lowest to the countries in the region, where the majority of cases
age group of 15–24 years (1.6%) (28). In Iran, the are reported in urban areas and the main sources of
findings show that the highest number of infection are believed to be mosquitoes and
respondents relates to the 10–29 year age group domestic animals.
(52.4%), and the lowest was for the 1–9 year age
The province of Herat in Afghanistan shares a
group (4.8%) (27). Farmers accounted for the
border with Iran, which has a high incidence of
highest number of reported Iranian cases (28.5%).
CCHF. In 2017, 33 cases of CCHF were reported
Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74 71

in Iran, particularly in governorates situated near the paucity of studies in certain regions of
Herat (33). Additionally, there has been an increase Afghanistan and the lack of long-term follow-up
in reported cases of CCHF in the Eastern data on CCHF cases may have limited the
Mediterranean Region (34). However, it is worth generalizability of the findings to the entire
noting that even though more cases have been country. Therefore, further research, including
reported in Pakistan, the provinces bordering larger and more comprehensive studies, is needed
Pakistan have had fewer reported cases of CCHF. to obtain a more comprehensive understanding of
Studies have also shown that the majority of CCHF the occurrence and characteristics of CCHF in
cases in Afghanistan, Iran, and Pakistan belong to Afghanistan.
the same Asia 1 genogroup (35).
7. Conclusion
5. Recommendations
In conclusion, this study is a systematic review of
The findings of this study suggest the need to scholarly articles published on CCHF in
develop targeted prevention and control strategies Afghanistan between 2010 and 2019. This study
for CCHF in Afghanistan. Further research should found that CCHF is a public health concern in
be conducted to investigate the reasons for gender Afghanistan, with a significant increase in reported
and age disparities in the occurrence of the disease cases in recent years. The main risk factors for
and to develop targeted prevention and control transmission include tick bites and contact with
strategies for these groups. Healthcare workers and infected animals, as well as occupational exposure
individuals in high-risk occupations, such as for those working in the livestock and agricultural
agriculture, animal husbandry, and sectors. To prevent the spread of CCHF in
slaughterhouses, should be educated about risk Afghanistan, effective control measures, such as
factors and the importance of taking preventive education on prevention, improved management of
measures. Additionally, public awareness infected animals, and proper infection control
campaigns should be conducted to educate the measures in hospitals and laboratories, need to be
general population regarding the risk factors and implemented. This study provides academic
symptoms of the disease. The government should suggestions and approaches for disease prevention
also take measures to improve the surveillance by better understanding the factors contributing to
system for CCHF and strengthen the capacity of the spread of CCHF in Afghanistan to reduce the
the healthcare system to diagnose and manage risk of outbreaks and improve public health in the
cases effectively. Finally, international cooperation region.
and coordination are essential to address the
transboundary nature of the disease and prevent its Acknowledgment
spread to other countries in the region.
We would like to extend our sincere gratitude to all
6. Limitations those who supported us in completing this study.
Special thanks go to Professor Hilal Özcebe for her
This review had several limitations that should be
cooperation, critical reading of the text, and
considered when interpreting the results. Most of
invaluable constructive comments. We would also
the included studies were observational, which
like to acknowledge the authors of the reviewed
may have introduced biases and limitations in the
studies for their significant contributions to the
analysis and interpretation of the results.
field of CCHF in Afghanistan. This research would
Moreover, the lack of standardized methods for
not have been possible without their invaluable
data collection and reporting may have affected the
contributions, and we are deeply grateful for their
comparability of the results. Additionally, reliance
support and guidance throughout the process.
on reported data could have been affected by
under- and over-reporting, potentially influencing
Conflict of interest statement
the overall results and conclusions. Furthermore,
72 Rahmani K, eat. al. / Afghanistanjournal of infectious diseases (2024), Vol. 2, No.1, 63-74

The authors declare that they have no conflicts of Ahmadabad, India, 2010-2011. PLoS Negl Trop
interest. Dis. 2012;6(5):e1653.
13. Greiner AL, Mamuchishvili N, Kakutia N,
Stauffer K, Geleishvili M, Chitadze N, et al.
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