Le Infezioni in Medicina, n. 1, 83-89, 2024

doi: 10.53854/liim-3201-11

ORIGINAL ARTICLES

Seroprevalence of Crimean-Congo hemorrhagic fever virus in the population of Turkestan region

Gulzhan Narkenovna Abuova1, Farida Abdullayevna Berdaliyeva1, Tatyana Vasiliyevna Polukchi1, Daulet Sabyrovich Aliyev1, Gulamzhan Sattarkulovich Raymkulov1, Maksim Vladimirovich Kulemin2, Ratbek Saylaubekuly2

1Department of Infectious Diseases and Dermatovenerology, South Kazakhstan Medical Academy,
Shymkent, Republic of Kazakhstan; 2Anti-Plague Station, Shymkent, Republic of Kazakhstan

Received 1 November 2023, accepted 9 February

Corresponding author

Tatyana Vasiliyevna Polukchi

E-mail: tatyana_polukchi@mail.ru

SummaRY

Purpose: To determine the level of seroprevalence to the virus of Crimean-Congo Hemorrhagic Fever (CCHF) in population of rural area of the particular districts of Turkestan region, Kazakhstan and its connection with epidemiological alerts.

Materials and methods: For determining the real Crimean-Congo hemorrhagic fever virus (CCHFV) circulation in Turkestan region, Kazakhstan, massive sero-epidemiologic studies were conducted. Healthy residents of Turkestan Region aged from 10 to 75 years were examined without having been previously registered with CCHF. After receiving an informed consent, 5 ml of venous blood was collected for ELISA assay using the following test kits: VectoCrimea-CHF-IgG and VectoCrimea-CHF-IgM by the Vector-Best JSC. Findings on CCHF morbidity rate along with prevalence of ticks were received from the reports of the Committee of Sanitary and Epidemiological Control of the Ministry of Healthcare of the Republic of Kazakhstan.

Results: Blood serum samples were collected prospectively from 4259 residents in all 16 districts of rural areas of Turkestan region. CCHF seroprevalence was detected in 2.39% of cases. Anamnesis of a tick-bite along with livestock contact in 18-30 years and 41-50 years age groups were considered as risk factors. The highest rate of CCHF seroprevalence was determined in the following recognized endemic regions and districts, namely Sozak District (4.04%), Turkestan Region (3.85%), Jetisu Region (3.6%). Reactivity probes were detected in residents of all 16 districts of Turkestan Region. The research statistics displayed that CHHF pathogen considerably increased its circulation in the endemic regions and the disease communicated into a number of new districts.

Conclusion: IgG ELISA was performed to screen CCHFV in 4259 village inhabitants of Turkestan Region and revealed the presence of antibodies in 2.39% of its population. Weak linear correlation relationship was established between CCHFV seroprevalence rate and CCHFV morbidity rate in the particular districts of Turkestan Region. As people grow older, CCHFV IgG detection rate increases. Living on CHHF endemic territories is a serious risk factor to become CHHF positive which is characterized by manifestation of the subclinical forms of this disease.

Keywords: Congo-Crimean hemorrhagic fever, seroprevalence, immunoglobulin G, morbidity, Turkestan region.

INTRODUCTION

According to the research statistics of the World Health Organization’s systematic review in detecting the spread of Crimean-Congo hemorrhagic fever virus (CCHFV) in European Region based on the serologic prevalence of IgG antibodies, it has been detected that the highest CCHFV prevalence rate can be observed in the countries of Central and Eastern Europe, whereas the countries of South and West Europe such as Greece and Spain have a lower endemicity rate [1]. The authors of another scientific work have carried out a meta-analysis aiming to identify the characteristics of CCHF seroprevalence on a global scale [2]. Generally, CCHF seroprevalence total ratio made up 4.7% for humans and 24.6% for animals. As for camels, the coefficient made up 17.1%. It constituted 18.9% for cattle and 24.3% for sheep. As for goats and livestock it made up 29.3% and 27.1%, respectively [3]. World-wide, CCHF seroprevalence has been 7.5 times higher in individuals, who have been occupationally exposed to infected animals and their blood, compared to those ones who have not. Furthermore, it has been reported that CCHF seroprevalence in animals (camels; cattle, goats, sheep and livestock) was 5 times higher than in healthy individuals. Animal contact, cattle breeding, farming along with tick biting and its salivary secretion effect were the most frequently registered risk factors in CCHF seropositivity [1].

The risk factors of zoonoses along with their prevalence in Zhambyl Region of Kazakhstan have been estimated in the research carried out by Kazakhstani scientists. Weighted prevalence of CCHFV among everyone involved in the study constituted 1.2% having an increase up to 3.4% in the villages where the cases of CCHF have been registered. Evidence of CCHFV circulation in prior non-endemic regions has been detected. The authors stated that human activities are also a risk factor of seropositivity, which faces people to a high risk of tick-borne diseases [4].

Another study, which was conducted by Turkish scientists, aimed at CCHF prevalence detection: blood samples were collected from healthy residents of Van Province and its surrounding villages according to the results of which seroprevalence made up 14.4% [1, 5].

The potential CCHF virus circulation was rated by running a serosurvey in asymptomatic adults being blood donors in the west of Spain in accordance with the data of the first research carried out there and showing CCHF circulation in healthy individuals [6]. CCHF prevalence in Castile and Leon, Spain was from 0.58% up to 1.16%.

National seroepedimiologic studies have been conducted to determine the real CCHFV circulation in Bulgaria [7]. Blood serum samples were collected prospectively from 1500 inhabitants of all 28 districts of Bulgaria. CCHF seroprevalence was detected in 3.7% of cases. Tick bite anamnesis, livestock contact and the age over 40 were stated as risk factors. The highest seroprevalence rate was observed in the recognized endemic districts in the southeast of Bulgaria: Haskovo (28%) and Yambol (12%) [7]. In comparison to the previous studies the reported data indicated that CCHF pathogen considerably increased its circulation in the endemic regions and invaded into the new ones.

The research on the serologic CCHF prevalence detection and determination of risk factors for healthcare workers was carried out by the Turkish scientists among the hospital staff from one of the provinces located in Central Anatolia [8]. The authors consider that the issues about the transmission routes of hospital-associated infections are still remaining unanswered. As a result, it is necessary to define HAI risk factors in order to reinforce HAI prevention [8].

Occupational exposure to CCHF has been registered for stock-breeders, vets and healthcare professionals according to the research statistics received in India [9]. Males, family members and neighbors have been defined as a high-risk group for being CCHF positive.

CCHFV circulation in Almaty region which is not yet considered endemic was described by Kazakhstani researchers for the first time [4]. Moreover, it was revealed that CCHFV antibodies and CCHFV RNA detected in blood serum pointed at mild and even asymptomatic infection forms of CCHF. It was recommended by the authors of this publication that doctors, who treat their patients for pyrexia of unknown origin, should know about CCHF’s mild forms [9, 10]. The purpose of the study was to determine the seroprevalence to the virus of Crimean-Congo Hemorrhagic Fever (CCHF) in the population of the particular districts of Turkestan region, Kazakhstan and its connection with epidemiological alerts.

MATERIALS AND METHODS

Healthy residents of Turkestan Region aged from 10 to 75 years were examined without being previously registered with CCHF. After receiving an informed consent, 5 ml of venous blood was collected for ELISA assay using the following test kits: VectoCrimea-CHF-IgG and VectoCrimea-CHF-­IgM by Vector-Best JSC. The analyses collected from 2019 to 2020 were carried out in the laboratory of particularly dangerous infections of the Shymkent Anti-Plague station, Kazakhstan. Findings on CCHF morbidity rate along with prevalence of ticks were received from the reports of the Committee of Sanitary and Epidemiological Control of the Ministry of Healthcare of the Republic of Kazakhstan. Correlations between CCHF seroprevalence and CCHF morbidity rate in the population across Turkestan region were assessed using Spearman’s rank correlation. The prognostic model, which characterizes dependence of the quantity variable on factors, was developed by means of linear regression method.

RESULTS

Hundred-two (2.39%) individuals out of 4259 healthy residents of Turkestan region were seropositive to CCHF where the coefficient made up 21 subjects (20.59%) for males and 81 subjects for females (79.41%) respectively. The age range was from 14 up to 90 years. Thus, the majority of seropositive patients were respondents from the age group from 41 up to 50 years (30 subjects). The age group from18 up to 30 years accounted for 27 respondents, whereas the number of subjects in the age group from 51 up to 60 years made up 25 individuals. Out of the total number of the respondents, 5 of them came in contact with a CCHF positive individual, 2 respondents reported to come in contact with febrile people, 24 of them had a contact with the blood of a tick, 59 of them informed to have been tick-bitten, 9 of them had body temperature rise, 13 respondents stated that they had a tick removed in medical preventive institutions. 4259 people have lived on the CCHF endemic territory (Table 1).

Table 1 - Analysis of seropositive CCHF findings received in districts across Turkestan Region.

We also studied CCHFV seroprevalence and morbidity rate in the districts of Turkestan region. As a result, the highest rates were detected in the following districts: Sozak District - 4.04%; Turkestan - 3.85%; Jetisu Region - 3.60%; Kazygurt - 3.00% (Table 2, Figure 1).

Table 2 - Distribution of CCHF seroprevalence and morbidity rate findings across the districts of Turkestan Region.

Figure 1 - Seroprevalence of CCHFV in the population of Turkestan Region 2019-2020.

CCHFV prevalence in ticks in the administrative districts of Turkestan Region within the years from 2016 to 2019 is depicted in Figure 2; therefore the highest rates were registered in Saryagash, Keles and Jetisu Regions, where the percent of CCHFV infected ticks is more than10.

Figure 2 - Seroprevalence of CCHFV in the tick population across the administrative districts of Turkestan region 2016-2019.

When comparing the analysis of seropositive CCHF data, no statistically significant differences were obtained depending on gender (p=0.425). The chances of obtaining seropositive CCHF data increased 1.22-fold in females (95% CI: 0.74-1.98). There was a weak relationship between the compared signs (V=0.723).

It is evident from the analysis while comparing seropositive CCHF findings that there were not revealed any statistically significant differences in contacting with CCHF positive individuals, febrile patients or in a medical history of removing a tick in medical preventive institutions. Statistically significant differences were obtained from the analysis while comparing seropositive CCHF findings on having exposure to the blood of a tick (p=0.05). The possibility of CCHF seroprevalence in patients being exposed to the blood of a tick was 3.7 times higher (95% C.I.: (0.87-16.2) than in those ones who were not. One can notice a strong relationship between the compared values (V=0.706).

Statistically remarkable differences were received from the analysis while comparing seropositive CCHF findings on having fever (p=0, 018). The possibility of CCHF seroprevalence in febrile patients was 11.86 times higher (95% C.I.: (2.43-57.79) than in those ones who did not have fever. There was a strong relationship between the compared values (V=0.603) (Table 3).

Table 3 - Analysis of seropositive CCHF findings obtained in the districts across Turkestan Region.

Statistically essential differences were delivered from the analysis while comparing seropositive CCHF findings in different age groups (p=0.025). There was moderate relationship between the compared values (V=0.432).

We carried out the correlation analysis on interrelation between the CCHF seroprevalence in the population of Turkestan Region and its morbidity rate, so the indicator was p=0.302, which indicates that there is no connection between the studied parameters. Weak linear correlation was revealed while estimating the interrelation of the morbidity rate and seroprevalence.

The observable dependence of the morbidity rate on the CCHF seroprevalence in the population of Turkestan Region is described by the paired linear regression equation:

Incidence = 0.023 = X seroprevalence + 0.472

Thus, the morbidity rate rise by 0.023 is observed as a result of 1% seroprevalence increase. The obtained model explains 0.1% of the observable dispersion in the morbidity rate (Figure 3).

Figure 3 - Correlation analysis findings on interrelation between CCHF seroprevalence and CCHF morbidity rate in the population across Turkestan region.

DISCUSSION

In our study, which included 4,259 healthy residents of the Turkestan region, seropositivity for CCHF was 2.39%, of whom the majority were women who accounted for 79,81% (81 people). The main risk factors were: contact with a CCHF patient, contact with tick blood, contact with feverish patients, living in a territory endemic to CCHF. Our data are similar to those reported in the study conducted by the authors from Turkey. In their work, the seroprevalence index was 2.3%, and the above factors were also included [11]. Similar indicators were also identified by scientists from Sudan. In their study in one of the regions of Sudan, the seroprevalence index was 2.6%, but in the other two regions it was significantly higher, where the maximum indicator was 7.4% [12]. The authors from Pakistan report that the serological prevalence of CCHF is high and amounts to 1.78%, especially in groups of people living in endemic areas [13]. A study conducted in Bulgaria showed that antibodies against CCHFV were detected in 3.2% of the sera studied and the results show that the proportion of positive results increases with age. In addition, significant risk factors for CCHFV infection, as in our study, are tick bites, livestock breeding and living in rural areas [14]. In another study conducted by authors from Greece, seroprevalence rates ranged from 3.4% to 3.8% with a significant difference in indicators between the eastern and western parts of the country. In addition to the risk factors described in previous studies (age, gender, tick bite, agro-pastoral activity), altitude, vegetation type and transitional wooded/shrubby terrain per person, as well as livestock per person, and in particular, the number of goats, sheep and cattle per person, were shown to significantly affect the serological prevalence [15, 16]. In another study involving 2,319 participants, the majority, as in our study, were female, although the seropositivity of IgG to CCHFV was 5.6% [17]. According to the authors, the rate of seropositivity among the participants was lower, with an indicator of 2.0%, which may be due to a smaller sample of respondents [18]. In another similar study conducted by researchers from Spain, the sero-presponsiveness of CCHFV ranged from 0.58% to 1.16% [19]. In another study conducted by authors from Kazakhstan, the seroprevalence index varies from 1.2% to 12.7%, which is similar to our data, demonstrating that animal husbandry was largely associated with seropositivity of CCHFV [3, 20].

CONCLUSIONS

Stability and high risk population of H. scupense and H. anatolicum ticks being highly infected contribute to CCHFV circulation in Southern Kazakhstan. There is a high probability to come down with Crimean-Congo Hemorrhagic Fever in CCHF hot spots, and namely for those individuals who are employed in cattle breeding and households. IgG ELISA was performed to screen CHHFV in 4259 village inhabitants across Turkestan Region and revealed the presence of antibodies in 2.39% of them. Weak linear correlation relationship was established between the variables of CCHF seroprevalence and its morbidity rate in the particular areas of Turkestan Region. As people grow older, CHHFV IgG detection rate increases. Living on an endemic CCHF territory is a serious contamination risk-factor and is displayed by subclinical forms of the disease.

Conflict of interest

None to declare.

Funding source

None to declare.

Ethical approval statement

The study was conducted in accordance with the ethical principles approved by the Experiments Ethics Committee of South Kazakhstan Medical Academy (Protocol N. 6 of 30.05.2021). All participants gave written informed consent before study entry.

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