Iranian Journal of War and Public Health

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Motashar F, Rashid B, Sajem K, Akef I. Epidemiology of Crimean-Congo Hemorrhagic Fever in Iraq from 2021 to 2023. Iran J War Public Health 2024; 16 (2) :207-213
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1- Department of Community Health Techniques, College of Health and Medical Techniques, Middle Technical University, Baghdad, Iraq
2- Department of Community Health Nursing, Balad Technicqal Institute, Middle Technical University, Baghdad, Iraq
3- Communicable Disease Control Center, Baghdad, Iraq
* Corresponding Author Address: Medical City, Al-Amal National Hospital for Cancer Treatment, Iraq. Postal Code: 10001-10090 (eac0044@mtu.edu.iq)
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Introduction
According to the World Health Organization’s (WHO) Eastern Mediterranean Region (EMRO), Crimean Congo Hemorrhagic Fever (CCHF) is endemic, with occasional outbreaks and human cases in several countries in this region [1].
Acute tick-borne zoonotic sickness is caused by the Crimea-Congo virus [2], which belongs to the Nairoviridae family, and since 1979, there has been an endemic spread of the CCHF in Iraq [3]. Asymptomatic cases comprise 60-90% of cases of CCHF, and the proportion of asymptomatic or subclinical cases is higher in regions where the disease is particularly endemic. The residual 10-40% will initially have a fever, headaches, and exhaustion, followed by gastrointestinal symptoms. Severe cases may progress to bleeding, shock, and multiorgan failure [4].
CCHF is a serious public health concern due to its high mortality rate and potential to cause significant outbreaks. The virus is primarily transmitted to humans through the bites of infected Hyalomma ticks or contact with the blood or tissues of infected animals [5]. The transmission cycle of the virus is complex, involving various wild and domestic animals that serve as reservoirs, making control efforts difficult. Many infected animals show no clinical symptoms, allowing the virus to spread undetected within livestock populations. Clinically, CCHF presents a wide range of symptoms, which complicates early diagnosis as the initial signs often resemble those of other viral infections. Common symptoms include fever, severe headache, muscle pain, gastrointestinal issues like nausea and vomiting, and bleeding tendencies such as petechiae and ecchymosis. In severe cases, the disease can progress rapidly, leading to multi-organ failure and a sharp decline in the patient’s health [6, 7]. The case fatality rate varies from 10% to 40%, depending on factors such as patient demographics and access to healthcare. CCHF is endemic in regions across Africa, Europe, Asia, and the Middle East, with primary risk factors including occupational exposure among healthcare workers, veterinarians, and individuals working closely with livestock [6-8].
Surveillance and preventive measures are essential to manage outbreaks where the virus is prevalent. Preventive strategies primarily focus on reducing tick exposure through personal protective measures such as wearing long sleeves and insect repellents. Public health initiatives also aim to educate at-risk populations on safely handling animals and blood products [21]. Despite these efforts, no specific antiviral treatment exists for CCHF, leaving supportive care as the primary means of managing the disease [9]. In high-risk areas, a multifaceted approach is crucial for effective prevention [6-10].
Raising awareness about CCHF risks and preventive measures is vital for reducing transmission. Educational campaigns should focus on livestock handlers, healthcare professionals, and the general public, informing them about safe practices when handling animals or blood products [11]. In addition, robust surveillance systems are needed to monitor tick populations and detect potential outbreaks. Regular assessments can identify high-risk areas and enable timely interventions and control measures [12]. Maintaining livestock health through regular veterinary care and tick control measures can also reduce the risk of transmission from animals to humans. This includes treating animals with acaricides and isolating infected livestock to prevent further spread [11-13].
In healthcare settings within endemic regions, strict infection control measures are critical. Facilities should adopt isolation protocols for suspected cases and ensure that healthcare staff are trained in properly using personal protective equipment (PPE), as hospital-acquired infections have contributed to past outbreaks [14]. Continued research into antiviral therapies, vaccines, and more effective treatment protocols is necessary to improve outcomes for CCHF patients. While supportive care remains the cornerstone of treatment, exploring potential antiviral drugs like ribavirin or other new therapies could significantly enhance patient management [11-13]. By implementing these comprehensive strategies—from community engagement and surveillance to improved healthcare protocols and research—endemic regions can significantly reduce the risks associated with CCHF and protect public health.
Although it varies by region and even within epidemics, the case fatality rate (CFR) of disease outbreaks is typically as high as 40% [15].
Since Hyalomma ticks are the primary vector for CCHF, their geographic distribution coincides with that of the disease; Therefore, higher rates of CCHF disease are found in areas where Hyalomma tick densities are present [16]. In 2016, a sero-study was conducted in Iraq, Iran, and Turkey to investigate the disease's animal hosts. The results showed that 20-30% of the animals tested positive, with goats having the highest percentage (50%) of positive animals [17].
Since Al-Yarmouk Hospital saw the first cases of CCHF in 1979, the health authorities have documented occasional occurrences and epidemics. In 1979, 10 cases and seven deaths were documented, making it the most notable outbreak. There were several documented cases in Halabja City, in the Iraqi province of Sulaimani, in 1980. According to published studies, the number of yearly confirmed cases varied between 0 and 6 cases each year between 1980 and 2009. In 2010, 11 verified cases were recorded across three weeks, with a 36% case fatality rate [1]. During the 2018 epidemic, there were ten confirmed cases; Eight of these resulted in death [18]. However, in four years (2008, 2014, 2016, and 2017), no instances of CCHF have been reported. The number of cases began to rise in 2021, when 19 cases were verified by laboratories [19].
The spread of zoonotic diseases to humans is influenced by several factors, such as changing environmental conditions, rising levels of international trade, increased human mobility, and migration from rural to urban and suburban areas, along with the animals living there that are thought to be the disease's hosts [20].
Comprehensive cooperation and coordination among health, animal, and transport sectors must be achieved to control these disease hosts and vectors. This facilitates early diagnosis and detection to prevent the further spread of the disease [21, 22].
This study aimed to identify the seasonal trend of the disease over the study months and years, the demographic and environmental factors of the patients, the most prominent signs and symptoms, and the interval between their onset and hospital admission.

Instrument and Methods
This Cross-sectional epidemiological study collected retrospective data about the confirmed CCHF patients from the Communicable Diseases Control Center in Baghdad, Iraq. The study included 957 confirmed CCHF patients from Iraq (except for the Kurdistan region) for three years (2021, 2022, and 2023).
The demographic data (age, gender, living place, occupation, and …) were extracted from the patients' profiles. The consent of the Iraqi Ministry of Health, Department of Public Health, Communicable Diseases Control Center, Baghdad, Iraq, was obtained for collecting data, which was used for research purposes only while maintaining the privacy of the patient’s information.
Data was analyzed using descriptive statistical methods in SPSS 22 software.

Findings
In 2021, 19 confirmed CCHF cases were recorded between July and December, with a peak of 6 cases during September. In 2022, 374 cases were recorded from March to December, with a peak of 102 cases during May. Furthermore, the highest number of cases was recorded in 2023, with 564 cases during the twelve months of that year, with a peak of 140 cases in July, which follows Eid Al-Adha (Figure 1).


Figure 1. The seasonal trend of CCHF

The mean age of 957 patients was 35.8±15.3 (0-90 years). Male patients comprised 58.3% of the total, while female patients comprised the remaining 41.7%. Dhi Qar had the largest percentage of patients (33.3%), while Al Anbar had the lowest percentage (0.3%). Housewives had the largest percentage (35.7%) among the study population's occupations, while veterinarians had the lowest percentage (0.2%; Table 1).

Table 1. Distribution of the study population according to their demographic characteristics (n=957)


It was discovered that rural areas had the highest rate (45.6%), urban areas were second with 41.3%, sub-urban areas were 10.8%, and slum regions had the lowest rate (2.3%).
Fever was reported in 96.9% of the patients, but only 14.0% had nose bleeding. Furthermore, in 2023, conjunctival hyperemia was identified in 41 (7.3%) cases out of 564 patients, and it was introduced to the list of signs after updating the unified form for detecting CCHF disease (Table 2).

Table 2. Specific clinical features among the study population (the numbers in parentheses are percentages)


If confirmed, the duration between the beginning of symptoms and hospital admission for diagnosis and treatment varied from 0 to 15 days, with a mean of 3.9±2.5 days. Three days after the commencement of symptoms, most cases (17.9%) were admitted to the hospital (Table 3).

Table 3. The interval from symptoms onset to hospital admission


The majority of patients (58.7%) had contact with raw or undercooked meat, followed by those who had animals in their homes (52.0%) and those who had slaughtered an animal (45.9%). Those bitten by a tick had a lower epidemiological exposure (18.7%), while those who had direct contact with a similar CCHF case had (3.6%).
3379 samples were taken from animals within 50 meters of the patient's homes; Hyalomma anatolicum accounted for 92% of the samples, while Hyalomma marginatum comprised 8%. Most patients (82.8%) were cured, while 16.5% died (CFR) while at the hospital. However, 0.7% were discharged on their initiative.

Discussion
Except for patients from the Kurdistan Region, 957 positive RT-PCR Crimean-Congo Hemorrhagic Fever patients from throughout Iraq were included in this study for 2021, 2022, and 2023. Every year, more cases agree with Alhilfi et al. [19]. The COVID-19 pandemic restrictions and resource shortage in 2020 and the spring of 2021 prevented the veterinary department from carrying out their scheduled spraying and dipping campaigns, which in turn led to an increase in the tick population. The increased temperature and decreased humidity also made it easier for Hyalomma tick nymphs to molt into adults, which could be the reason for the sharp increase between 2021 and 2022. While the weather-related rationale indicated above may account for the increase from 2022 to 2023. Tick resistance to the applied insecticide is another likely explanation. Last but not least, the lack of water in water bodies caused a drought, which in turn caused people to migrate from rural to semi-urban or city centers. They brought animals that carried ticks, which changed the ticks' breeding grounds to areas where people were more likely to encounter them. As a result, the number of cases of CCHF rose. The cases are higher during May, June, and July, suggesting a seasonal trend inconsistent with Vesga et al. [23] and Ak et al. [24]. This is most likely because ticks can find more prospective hosts in the summer when more humans and animals typically spend time outside. Tick activity, particularly that of Hyalomma species, is increased by warmer temperatures, as is the potential host population. Summer is the optimal season for the growth and activity of Hyalomma ticks, which prefer warmer, drier weather. This leads to higher encounter rates with hosts, including people and animals. Islamic holidays, particularly Eid Al-Adha, may also be contributing factors to the increase in cases because of customs involving animal sacrifice. According to Baghdadi et al. [25] and Zia et al. [26], these animals may become infected.
This study participants' ages ranged from 1 day to 90 years. They also had a mean and standard deviation of 35.8±15.3 years, which was in line with the results of Owaysee Osquee et al. [27] with 32.86±13.67 and Nili et al. [28], who discovered that the mean age and SD were 31.90±13.59. According to Alhilfi et al. [19], the patients' ages ranged from 8 months to 99 years. Over half of the patients (58.3%) were men. The current study was supported by two other studies by Atim et al. [29] and Qaderi et al. [30] with 80% and 72.6% respectively. In contrast, two studies by Mourya et al. [31] and Çıtıl et al. [32] reported that the females comprised 52% and 54.9% of the study sample, respectively. These findings may have a scientific explanation. Whereas CCHF can strike anyone at any age from both sexes, it typically strikes those who are economically or occupationally engaged because of occupational exposure.
The distribution of CCHF cases indicates larger percentages in the country's southern governorates, supporting the findings of Alhilfi et al. [19] that the south had a higher case count. Furthermore, Dhi Qar governorate had the largest number of cases documented, 319 instances (33.3%), which is in line with findings from earlier research by Atwan et al. [33] with 120 cases and Al Salihi et al. [34] with 47 cases (48%). These results may be due to higher rural areas, environmental exposure, and animals in the country's south. CCHF has greater distribution (45.6%) in rural areas among urban, suburban, and slums, as reported by Karakecili et al. [35], who found that 94.2% of his sample lived in a rural location, and Mustafa et al. [18], who discovered that 90% of his study participants were from rural areas. The increased exposure to tick breeding grounds and the disease's animal host could be the cause.
Surprisingly, among other occupations, housewives reported the highest number of instances (35.7%). This is in agreement with Çıtıl et al. [32] of 47.9% of housewives, but not with Mustafa et al. [18], who claimed that animal owners had the highest percentage (40%). According to a different study, farmers or livestock owners comprised 77.2% of the sample [35]. The most plausible scientific explanation for the current study's findings is that the women handled raw or undercooked meat with their bare hands and without caution because they were either unaware of the proper handling procedures for uncooked meat to prevent illness or aware of them but chose not to follow them.
When compared to Mustafa et al. [18], who recorded the same clinical features (except for the bleeding from the nose) in Iraq for the 2018 epidemic in the percentages (100, 0, 10, 90, 20, and 60%), the present study recorded the most significant pre-hemorrhagic (fever and conjunctival hyperemia) and hemorrhagic (bleeding from injection sites, bleeding from gums, bleeding from nose, bleeding from body orifices, and ecchymosis). The lower percentages in the current study, as compared to the previous study, may indicate that people are likely becoming more aware of the illness and making more attempts to confirm the diagnosis and receive the necessary medical attention and management. According to the results, fever is the most common clinical feature that almost all patients experience. This finding is consistent with Owaysee Osquee et al. [27], who found that 99.4% of the patients in their study had fever. The time delay between the onset of sickness and hospital admission ranged from 0 to 15 days, with a mean and standard deviation of 3.9±2.5 days. Hasanoglu et al. [36] in Turkey reported 1-10 days with a mean of 3.7 days, while Qaderi et al. [30] in Afghanistan concurred with the current study by reporting the range of days as 1-13 days with a mean of 4.8 days.
The following percentages were found in the environmental risk factors; 52, 45.9, 18.7, 58.7, and 3.6%. Mustafa et al. [18] also looked at these environmental factors, reporting results of 50%, 0%, 30%, 50%, and 0%. The discrepancy in the number of cases (957 patients in the current study, compared to 10 patients in the other study) may cause the agreement with two elements and disagreement with three. According to the current study, the two types of tick vectors implicated in transmitting the CCHF virus in Iraq are H. anatolicum (92%) and H. marginatum (8%). These findings are consistent with those reported by Shahid et al. [37] and Salehi-Vaziri et al. [38], who reported that among other species in Pakistan and Iran, H. anatolicum accounted for 48% and 34.11%, and H. marginatum for 30.2% and 14.34%, respectively. However, H. anatolicum's dominance over H. marginatum might be attributable to the latter species' low tolerance for harsh climate conditions.
While only 16.5% of research participants died (CFR), the majority of CCHF patients (82.8%) who were included in the study survived. This is consistent with the findings of Cevik et al. [39], wherein 85.1% of study participants experienced a cure and 15.9% died. This suggests that patients receive appropriate medical care. Additionally, 7 (0.7%) patients of the present study participants were released on their initiative, having a vague fate.
There was a minor delay in data collection due to the large size of the study population from the whole country. Comprehensive campaigns are required, as well as the use of social media, to raise public awareness of the CCHF source of infection, method of transmission, and preventative and control measures for all individuals, but notably for those who are at risk, especially before the start of the season. Regular inspection of the facilities used for the slaughter of animals to stop haphazard or illegal slaughterhouses by substituting with standard typical facilities. For additional study and research about the potential ones in Iraq, the intended authorities must be aware of the potential resistance for the utilized insecticides because some affordable herbal acaricides and repellents do little to no environmental impact.

Conclusion
CCHF trend has significantly increased from 2021 to 2023. The disease also exhibits a seasonal trend, with an increase in cases during the summer and a decrease or even disappearance during the cooler months. Males of all occupations comprise the majority of the study population, although housewives are the largest category in terms of occupation. The majority of patients have contact with animals or animal products of slaughtering.

Acknowledgements: I want to thank my colleagues in the Ministry of Health, Public Health Department, and CDC staff for their cooperation and precious help, especially Senior M.T.C.H. Saad Hadi Saleh. Thanks to the Ministry of Agriculture, Veterinary Department, and Epidemiology section for their cooperation and advice.
Ethical Permissions: The consent of the Iraqi Ministry of Health, Department of Public Health, Communicable Diseases Control Center, Baghdad, Iraq, was obtained for collecting data used for research purposes only while maintaining the privacy of the patient’s information.
Conflicts of Interests: There were no conflicts.
Authors' Contribution: Motashar FM (First Author), Introduction Writer/Methodologist/Main Researcher/Discussion Writer/Statistical Analyst (25%); Rashid BA (Second Author), Introduction Writer/Methodologist/Main Researcher/Discussion Writer/Statistical Analyst (25%); Sajem KG (Third Author), Introduction Writer/Methodologist/Main Researcher/Discussion Writer/Statistical Analyst (25%); Akef IR (Fourth Author), Introduction Writer/Methodologist/Main Researcher/Discussion Writer/Statistical Analyst (25%)
Funding/Support: This study was not funded.
Keywords:

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