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Table of Contents
RESEARCH ARTICLE
Year : 2021  |  Volume : 58  |  Issue : 1  |  Page : 70-73

Serosurvey of Crimean-Congo hemorrhagic fever virus in livestock, Kohgiluyeh and Boyer-Ahmad, Iran, 2017


1 Department of Veterinary, Behbahan Branch, Islamic Azad University Behbahan, Iran
2 Department of Arboviruses and Viral Hemorrhagic Fevers (National Reference Laboratory), Pasteur Institute of Iran, Tehran, Iran
3 Agriculture and Natural Research Center, Kohgiluyeh and Boyer-Ahmad Province, Iran
4 Department of Medical Virology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
5 Research Centre for Emerging and Reemerging Infectious Disease; Department of Arboviruses and Viral Hemorrhagic Fevers (National Reference Laboratory), Pasteur Institute of Iran, Tehran, Iran

Date of Submission15-Jan-2019
Date of Acceptance30-Apr-2020
Date of Web Publication18-Nov-2021

Correspondence Address:
Mostafa Salehi-Vaziri
Department of Arboviruses and Viral Hemorrhagic Fevers (National Ref Lab), Pasteur Institute of Iran, Postcode: 1316943551, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.313958

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  Abstract 

Background & objectives: Crimean-Congo hemorrhagic fever (CCHF) is a tick-borne viral zoonosis with up to 50% mortality rate in humans. In addition to the role of animals in the transmission of the virus and spread of infected ticks through livestock trade, they can be employed as sentinel hosts for monitoring the infection. Iran is one of the endemic counties for CCHF and the disease has been documented in all provinces. However, in some provinces such as Kohgiluyeh and Boyer-Ahmad, the rate of the disease has been dramatically low. Therefore, this serosurvey was designed to investigate CCHF virus (CCHFV) seroprevalence among livestock in different parts of Kohgiluyeh and Boyer-Ahmad Province.
Methods: This study was conducted in 2017, in which, blood samples were collected from 501 sheep and goats from eight different cities of Kohgiluyeh and Boyer-Ahmad Province. CCHFV IgG antibodies were detected in livestock serum samples by specific ELISA assays for detection of ovine and caprine antibodies.
Results: In total, four sheep serum of out of 501 (0.8%) livestock samples (3 from Gachsaran and 1 from Dena) had CCHFV IgG antibodies. No significant association was found between CCHFV seropositivity and sex or age of animals (P>0.05).
Interpretation & conclusion: Our findings suggest a minor CCHFV circulation in Kohgiluyeh and Boyer-Ahmad Province, Iran. However, due to the notion that outbreaks of tick-borne infections is hard to predict; steady and comprehensive monitoring programs especially in ticks and animals would be critical for understanding the circulation on the pathogen in a region.

Keywords: Crimean-Congo hemorrhagic fever virus, livestock, Kohgiluyeh and Boyer-Ahmad, Iran


How to cite this article:
Ghasemian SO, Fazlalipour M, Hosseini G, Pouryaievali MH, Azad-Manjiri S, Khakifirouz S, Vasmehjani AA, Salehi-Vaziri M. Serosurvey of Crimean-Congo hemorrhagic fever virus in livestock, Kohgiluyeh and Boyer-Ahmad, Iran, 2017. J Vector Borne Dis 2021;58:70-3

How to cite this URL:
Ghasemian SO, Fazlalipour M, Hosseini G, Pouryaievali MH, Azad-Manjiri S, Khakifirouz S, Vasmehjani AA, Salehi-Vaziri M. Serosurvey of Crimean-Congo hemorrhagic fever virus in livestock, Kohgiluyeh and Boyer-Ahmad, Iran, 2017. J Vector Borne Dis [serial online] 2021 [cited 2021 Nov 27];58:70-3. Available from: https://www.jvbd.org/text.asp?2021/58/1/70/313958


  Introduction Top


Crimean-Congo hemorrhagic fever virus (CCHFV), a member of Nairoviridae family and genus Orthonairovirus, is one of the reemerging tick-borne pathogens posing a serious threat to public health. CCHF is endemic in many countries in Africa, Southeast Europe, Asia, and the Middle East including Iran[1],[2]. Although the majority of human infections with CCHFV result in a mild febrile illness, infected people may experience a life-threatening hemorrhagic fever syndrome, with fatality rates ranging from 5% to 50%[3].

Ixodidae ticks play a major role in the survival of CCHFV in nature, as they are reservoirs and vectors of the virus. Infected ticks transmit the virus to a wide range of mammals, including livestock[4]. Despite being viremic for up to two weeks, animals do not demonstrate any clinical symptoms of the disease. On the other hand, individuals with direct contact with blood or tissues of viremic (but asymptomatic) livestock are at a great risk of CCHF[5]. Additionally, animals, especially livestock, can be used as sentinel hosts for monitoring the circulation of CCHFV in a region[6].

The first evidence of CCHF infection in the livestock of Iran was reported by Chumakov and Smirnova in 1970[7], 29 years before identification of the disease in a clinical case[8]. CCHFV antibodies were identified in cattle, camels, and sheep (9% of cattle, 19% of camels, and 45% of sheep[9]. So far, human cases of CCHF have been recorded in all 31 provinces of Iran, including Kohgiluyeh and Boyer-Ahmad Province[10]. However, in comparison with hyper-endemic regions, such as Eastern provinces, the number of human cases in Kohgiluyeh and Boyer-Ahmad is very limited (only one case out of more than 1300 confirmed cases during 2000–2018). Moreover, little data is available with regard to CCHFV infection in animals in this province. Therefore, this study was designed to investigate the seroprevalence of CCHFV in livestock in Kohgiluyeh and Boyer-Ahmad Province, southwest of Iran.


  Material & Methods Top


Study area and sampling

This survey was carried out in Kohgiluyeh and Boyer-Ahmad Province (30.67°N 51.60°E) in southwest of Iran. This province has a geographical area of approximately 16,249 km2 and is located in the frontal middle part of Zagros Mountains, with neighboring provinces of Fars, Khuzestan, Bushehr, Isfahan, and Chaharmahal-va-Bakhtiari. This province has two tropical and mountainous climates, with maximum temperature of 36°C in summer and minimum temperature of -7°C in winter. Kohgiluyeh and Boyer-Ahmad Province has eight major cities, including Bahmai, Basht, Boyer-Ahmad, Choram, Dena, Gachsaran, Kohgiluyeh, and Landeh. Boyer-Ahmad and Dena are located in cold regions, while the remaining six regions are tropical. Kohgiluyeh and Boyer-Ahmad is one of the main provinces in south of Iran for livestock breeding. In fact, agriculture and animal husbandry are very common in the rural areas of this province (Iranian Veterinary Organization, unpublished data).

Between May and November 2017, blood samples (10 mL) were collected from a total of 501 locally born and bred domestic animals, including 191 sheep and 310 goats from eight counties of Kohgiluyeh and Boyer-Ahmad Province (Bahmei, 37; Basht, 48; Boyer-Ahmad,138; Choram, 40; Dena, 21; Gachsaran,78; Kohgiluyeh, 118; and Landeh, 21) [Figure 1]. Sample size was calculated using Cochran’s sample size formula, and sample collection was performed according to random sampling technique. Following serum separation, serum samples were sent to the department of Arboviruses and Viral Hemorrhagic Fevers of Pasteur Institute of Iran (National Reference Laboratory) for CCHFV IgG detection. Demographic characteristics of the livestock (i.e., gender, age, and sampling region) are presented in [Table 1].
Figure 1: Location of Kohgiluyeh and Boyer-Ahmad Province in Iran. Cities with CCHFV seropositive livestock are represented in grey.

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Table 1: Demographic features of livestock included in this study.

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Ethical statement

The ethical approval for this study was obtained from the Agricultural and Natural Recourses Committee, Kohgiluyeh and Boyer Province.

Enzyme-linked immunosorbent assay (ELISA)

CCHFV IgG antibodies were detected using ELISA assay. For this purpose, Nunc MaxiSorp™ ELISA plates (Thermo Fisher Scientific, USA) were coated with diluted mouse hyperimmune ascetic fluid (1:1000) in phosphate-buffered saline (PBS 1X) and incubated overnight at 4°C. After washing, CCHFV antigen in PBS (1:500 dilution), containing 0.5% Tween (Merck, Germany) (PBST) and 3% skimmed milk (Merck, Germany) (PBSTM) was added and then incubated for three hours at 37°C. After adding the diluted sera in PBSTM (1:100) and incubation for one hour at 37°C, peroxidase-labeled anti-ovine/caprineIgG (ICN Biomedicals Inc., USA; 1:700 dilution in PBSTM) was added and incubated again for one hour at 37°C. After the washing step (three times), hydrogen peroxide (H2O2) (MP Biomedical, France) and 3,3’, 5,5’-tetramethylbenzidine (TMB; MP Biomedical, France) were added and incubated for 15 minutes at room temperature. Finally, the reaction was terminated using H2SO4 (Sigma, USA), and the plates were read at 450 nm.

Statistical analysis

Data were analyzed using SPSS version 16. Chisquare test was used to evaluate the association between CCHF infection and categorical variables. P-values<0.05 were considered statistically significant.


  Results Top


In this study, a total of 501animals, including 191 sheep (171 females, 20 males) and 310 goats (292 females, 18 males) were investigated for CCHF IgG antibodies. All animals were categorized in four age groups, including 13–24 months (n=120; 24%), 25-36 months (n=261; 52.1%), 37–48 months (n=101; 20.2%) and >48 months (n=19; 3.8%). A total of 294 samples were collected from plain areas, while the rest (n=207) were collected from mountainous areas.

Overall, four out of 501 (0.8%) specimens were tested positive for CCHFV IgG antibodies, three of which were from Gachsaran (from plain areas) and one from Dena (from a mountainous area). All positive animals were sheep (one male, three females), which was statistically significant (P=0.011). Regarding age, one positive case belonged to the age group of 13–24 months, one case to the age group of 25–36 months, and two cases to the age group of 37–48 months. There was no significant association between seropositivity for CCHFV and area of sampling or livestock sex and age (P>0.05).


  Discussion Top


Considering the role of domestic animals in the maintenance of CCHFV and virus transmission to humans, surveillance of livestock is an essential strategy for monitoring infections and estimating the human exposure risk[11]. To the best of our knowledge, the present study is the first serosurvey of CCHFV in Kohgiluyeh and Boyer-Ahmad Province in southwest of Iran. The findings of the present study indicated the low prevalence of CCHFV infection in the livestock (0.8%), suggesting low risk of CCHFV exposure in this region. The limited number of human CCHF cases from this province supports this claim. However, the low frequency of health problems does not mean that not having a chance to report any human cases. Similar to other tick-borne infections, CCHFV can also easily spread to other regions. It has been well documented that CCHFV reservoir ticks can be transferred to other areas via livestock trade or migratory birds. Recent emergence of CCHF in Spain is supposedly associated with the transfer of infected ticks from Africa to Spain by migratory birds[12],[13],[14]. Therefore, the possibility of CCHF outbreaks should be taken into account in any region where reservoir ticks exist.

In a study conducted between 2010 and 2011, Mostafavi et al. reported the low seroprevalence of CCHFV in sheep from Mazandaran Province, northern Iran, where no human cases of the disease had been recorded[15]. They concluded that CCHF disease is not a considerable health challenge in Mazandaran, as the infection rate was low among sheep in this province, and there were no reports of human infection in this region. However, in 2012 the first human case of CCHF was reported in Mazandaran, and until now more than 30 human cases have been reported in this area. Therefore, in endemic regions, regardless of the low rate of CCHF infection among animals, there is a potential risk of disease outbreak in human populations. Consequently, regular surveillance of CCHF in ticks and livestock is critical for the prediction of future outbreaks.

Although several livestock species, including cattle, sheep, goats, and ostriches, play a role in CCHFV circulation, sheep has been considered the most suitable amplifying host for the virus[15]. In the present study, we only detected CCHF infection in sheep (P=0.011). However, the seropositivity rate was significantly lower than that reported in other similar studies from Iran. For instance, in the first study of CCHF infection in sheep, Saidi et al. detected a CCHF seroprevalence of 38% in 728 sheep[16]. In 2004 and 2007, two studies from Isfahan Province showed infection rates of 54.2% in 107 sheep and 76.6% in 286 sheep, respectively[17],[18]. Another study from Ardabil Province demonstrated that 41.9% of the sheep (n=43) had a history of CCHF infection[19]. Additionally, Mostafavi et al. reported that 3.7% of sheep (n=270) from Mazandaran Province had CCHF IgG antibodies[15]. Finally, a study from Fars Province found infection rates of 12.7% and 20.3% in 63 sheep and 148 goats, respectively[20].

The low prevalence of CCHFV in our study could be attributed to the sampling method. It should be noted that previous studies were mainly carried out in provinces with a high number of human cases, such as Isfahan[17],[18], Fars[20], and Mazandaran[15], or regions with high tick infection rates (28%), such as Ardabil[19]. Nevertheless, during 2000–2018, only one human case of CCHF has been documented in Kohgiluyeh and Boyer-Ahmad Province. The geographical features of this region might have also affected our findings, as areas of high altitude, such as Kohgiluyeh and Boyer-Ahmad, are categorized as low-CCHF prevalence areas[21].


  Conclusion Top


The findings of the present study indicated low prevalence of CCHF infection in the livestock of Kohgiluyeh and Boyer-Ahmad Province in Iran. However, further studies need to be conducted not only on livestock, but also on ticks, wild animals, and humans to shed more light on the epidemiology of CCHF in this province.

Conflict of interest: None

 
  References Top

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Papa A, Markatou F, Maltezou HC, Papadopoulou E, Terzi E, Ventouri S, et al. Crimean-Congo haemorrhagic fever in a Greek worker returning from Bulgaria, August 2018. Eurosurveillance. 2018; 23(35): 1800432.  Back to cited text no. 1
    
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Maltezou HC, Papa A. Crimean-Congo hemorrhagic fever: epidemiological trends and controversies in treatment. BMC medicine 2011; 9(1): 131.  Back to cited text no. 3
    
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Chumakov M, Smirnova S, Tkachenko E. Antigenic relationships between the Soviet strains of Crimean hemorrhagic fever virus and the Afro-Asian Congo virus strains. Mater 1969; 16: 152–4.  Back to cited text no. 7
    
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Mardani M. Nosocomial Crimean-Congo hemorrhagic fever in Iran, 1999–2000. Clin Microbiol Infec 2001; 7(1): 213.  Back to cited text no. 8
    
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Chumakov M. Detection of antibodies to CHF virus in wild and domestic animal blood sera from Iran and Africa. 1972.  Back to cited text no. 9
    
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Spengler JR, Bergeron E, Rollin PE. Seroepidemiological studies of Crimean-Congo hemorrhagic fever virus in domestic and wild animals. PLoS neglected tropical diseases 2016; 10(1): e0004210.  Back to cited text no. 11
    
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Cajimat MN, Rodriguez SE, Schuster IU, Swetnam DM, Ksiazek TG, Habela MA, et al. Genomic characterization of Crimean–Congo hemorrhagic fever virus in Hyalomma tick from Spain, 2014. Vector-Borne and Zoonotic Diseases 2017; 17(10): 714–9.  Back to cited text no. 12
    
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Estrada-Peña A, Palomar AM, Santibáñez P, Sánchez N, Habela MA, Portillo A, et al. Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010. Emerging infectious diseases. 2012; 18(1): 179.  Back to cited text no. 14
    
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Mostafavi E, Chinikar S, Esmaeili S, Amiri FB, Tabrizi AMA, KhakiFirouz S. Seroepidemiological survey of Crimean-Congo hemorrhagic fever among sheep in Mazandaran province, northern Iran. Vector-Borne and Zoonotic Diseases 2012; 12(9): 739–42.  Back to cited text no. 15
    
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Saidi S, Casals J, Faghih M. Crimean hemorrhagic fever-Congo (CHF-C) virus antibodies in man, and in domestic and small mammals, in Iran. The American journal of tropical medicine and hygiene 1975; 24(2): 353–7.  Back to cited text no. 16
    
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Izadihassan M, Salehi H, Chinikar S, mostafavizadeh K, Darvishi M, Jonaidi N, et al. A Geographical Distribution Survey on CCHF Positive Antibody Ovine›s of Isfahan Province in 1383-1384. Journal of Military Medicine 2007; 9(2): 97–102.  Back to cited text no. 17
    
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Ataei B, Touluei HR, Chinikar S, Darvishi M, Jalali N, Izadi M, et al. Seroepidemiology of Crimean-Congo hemorrhagic fever in the local and imported sheep in Isfahan province, Iran, 2002. Iran J Clin Infect Dis 2006; 1(1): 19–23.  Back to cited text no. 18
    
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Shabani M, Shakeri H, Salehi-Vaziri M, Sadeghi K, Azadani HN, Hosseini Y, et al. Seroepidemiological Survey of Crimean-Congo Hemorrhagic Fever Among Livestock in Southern Iran, Jahrom, 2015-2016. Journal of Research in Medical and Dental Science 2018; 6(4): 41–5.  Back to cited text no. 20
    
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