Seroprevalence of Crimean-Congo Hemorrhagic Fever in Domesticated Animals in Northwestern Senegal

Abstract

Crimean-Congo hemorrhagic fever (CCHF) is a tick-borne disease that can be contracted by direct contact with viremic animals or humans. In West Africa, recurrent CCHF outbreaks have been constantly observed in Mauritania and Senegal. Moreover, acquisition and epidemiology of the infection in humans are correlated with the occurrence and the seroprevalence of the virus in livestock. The main objective of this study is to provide updated information on the local spread of CCHF in animals in the northern region of Senegal. Out of a total of 283 animal sera collected, CCHF-specific antibodies were identified in 92 (32.5%; confidence interval [CI]_95% 27.1–38.3) sera by double antigen sandwich enzyme-linked immunosorbent assay (ELISA) test. The prevalence of CCHF virus (CCHFV) infection among horses, cattle, sheep, dogs, donkeys, and goats was 70.3% (45/64), 57.1% (8/14), 22.1% (30/136), 18.2% (2/11), 17.2% (5/29), and 6.9% (2/29), respectively. The antibody titers were found significantly affected by age (p < 0.0001) and gender (p < 0.05). High tick infestation by Rhipicephalus spp. and Hyalomma spp. was recorded on horses. The high seroprevalence to CCHFV among animals in the northern region of Senegal observed in this study indicates the permanent presence of the infection in the northern region of the country suggesting the need to strengthen surveillance plans for CCHF in Senegal.

Introduction

Crimean-Congo hemorrhagic fever (CCHF) is an infectious disease caused by Orthonairovirus of the Nairoviridae family. Human acquisition and infection are mediated by the bite of an infected tick, or by contact with an infected origin, including crashed ticks and viremic human or/and animals (Bente et al. 2013). Subclinical infection is observed in most human cases after exposure to the virus. In Mauritania, in an outbreak of seven patients, 36% of healthy people in their families were CCHF virus (CCHFV) positive (Gonzalez et al. 1990).

Animals develop an asymptomatic infection. Viremia and antibodies against CCHF have been observed in domestic and wild vertebrates, including cattle, goats, sheep, horses, pigs, camels, donkeys, mice, domestic dogs, hares, and ostriches.

Outbreaks of CCHF have been documented in Africa, Middle East, Eastern Europe, and Western Asia, where the tick of Hyalomma spp. is widespread. CCHF represents a major threat to human health and no satisfactory treatment has been developed. The disease is characterized in man by a feverish state, headaches, and myalgia. It can be aggravated by cutaneous and generalized hemorrhages that can be fatal. The fatality rate ranges from 10% to 40% (Bente et al. 2013).

In West Africa, several CCHF outbreaks have been observed in Mauritania and Senegal (Nabeth et al. 2004a, 2004b). As the presence of antibody against CCHF in livestock is possibly correlated with the occurrence of human cases, our objective was to provide updated information on the local spread of CCHFV in domestic animals in the northern region of Senegal. In this Sahelian zone, the role of wild ground-feeding birds in the ecology of the CCHFV has been highlighted (Zeller et al. 1994). This study uses a double antigen sandwich enzyme-linked immunosorbent assay (ELISA) that can detect IgG and IgM antibodies against CCHFV.

Materials and Methods

Animal samplings were collected by veterinarians with the agreement and in the presence of the owners according to Senegalese regulation. Survey was conducted during June 2014 in three Northern Senegalese areas near Keur Momar Sarr (15°55′0.0012″N; 15°58′0.0012″W): Gankette Balla, Loboudou, and Ndimb. Blood samples and ticks were collected from 136 sheep, 29 goats, 14 cattle, 64 horses, 29 donkeys, and 11 dogs.

Ticks morphological and molecular identification based on mitochondrial 12S rDNA has already been performed and reported (Dahmani et al. 2019).

Antibody against CCHF detection in animal sera was performed using ID Screen^® CCHF Double Antigen Multi-species (IDvet, Grabels, France) following the manufacturer's instruction (Sas et al. 2018).

Statistical analysis was performed on Epi info™ 5.01 using chi-squared/Fisher's exact test and analysis of variance. Statistical significance was defined as p ≤ 0.05.

Results

The seroprevalence observed among the tested animal sera was 32.5% (92/283, confidence interval [CI] 27.1–38.3). Overall results and prevalence of CCHFV infection according to respective species are shown in Table 1. No statistical seroprevalence difference was observed between the three villages (p ≥ 0.05). However, a significant difference was established between male and female (p = 0.05) and according to age (p < 0.0001). Positive animals are on average older (6.5-year ±4.8) than negative ones (3.5-year ±2.1). Finally, 204 ticks were collected from 48 animals. Fourteen on the 92 seropositive animals were found infested by ticks. The presence of ticks on the animal have no statistic influence on the seropositivity (odds ratio [OR] = 1.4, CI 0.6–2.9).

Table 1.

Serological Elisa Results of CCHF (Id Screen CCHF Double Antigen Multi-Species) in Domestic Animals from Three Localities in Northern Senegal

	Horses	Donkeys	Dogs	Cattle	Sheep	Goats	Total
Age (average)	7.5	5.3	3.1	2.9	3.4	3.1
Standard deviation	5.1	3	2.6	2.2	1.8	1.9
Ticks (total N)	139^a	6^b	2^c	9^d	48^e	NO	204
Out of N animals	26	2	2	3	15	NA	48
Localities
Gankette Balla	10/12	1/6	2/3	2/4	10/51	0/1	25/77
15°58′50.6″N, 15°55′42.6″W							32.5%
15°58′50.6″N, 15°55′42.6″W							CI 95% 22.2–44.1
Loboudou	18/30	0/2	0/5	3/7	1/12	1/16	23/72
15°57′10.98″N, 15°55′11.8668″W							31.9%
15°57′10.98″N, 15°55′11.8668″W							CI 95% 21.4–44.0
Ndimb	17/22	4/21	0/3	3/3	19/73	1/12	44/134
16°2′56.958″N, 16°0′10.5876″W							32.8%
16°2′56.958″N, 16°0′10.5876″W							CI 95% 25.0–41.5
Total	45/64	5/29	2/11	8/14	30/136	2/9
Average (%)	70.3	17.2	18.2	57.1	22.1	6.9
CI 95%	57.6–81.1	5.8–35.8	2.3–51.8	28.9–82.3	15.4–30.0	0.8–22.8

Rhipicephalus evertsi evertsi (113), Hyalomma impeltatum (10), Hy. rufipes (13) R. bursa (3).

R. e. evertsi (6).

R. muhsamae (2).

R.e. evertsi (5) and Hy. rufipes (4).

R. e. evertsi (48).

CCHF, Crimean-Congo hemorrhagic fever; CI, confidence interval; ELISA, enzyme-linked immunosorbent assay.

Discussion

Using an ELISA kit based on the identification of reactive antibody against a CCHFV recombinant protein (Sas et al. 2018), we report the circulation of CCHFV among animals in three northern regions of Senegal. The overall seroprevalence observed in our study is 32.5% (92/283). Reactive antibodies against CCHFV were detected among sera of animals belonging to different species. We report for the first time in Africa, the occurrence of CCHFV in horses and donkeys (Spengler et al. 2016). Furthermore, high seroprevalence was observed among horses (70.3%) and cattle (57.1%). This finding is probably due to the longevity of these animals and the persistence of antibodies. The lowest seroprevalence was observed among donkeys and dogs (17.2% and 6.9%, respectively).

Previous studies have observed one high seroprevalence (virus circulation sign) in farmed animals and the occurrence of the infection in humans more probably in rural area (Bente et al. 2013). In addition, it has been shown that seroprevalence in animals is five times higher than in humans in the same region (Nasirian et al. 2019). In endemic areas, mostly rural regions, living in proximity with infected animals increases the possibility of acquiring infection by contact or by exposition to tick bites that highly infest animals (such as horses and cattle) in the area (Bente et al. 2013). Although our results do not show any significant correlation between tick infestation of seropositivity (OR = 1.4, CI 0.6–2.9), we found that horses were the most infested animals with Rhipicephalus spp. and Hyalomma spp. Ticks of the genera Rhipicephalus are also capable of transmitting the disease (Zeller et al. 1997).

Meta-analysis of previously published results on the seroprevalence of CCHFV in animals shows an average prevalence of 24.6% with wide variation between countries. In cattle, the global seroprevalence comprises between 3.7% in Russia and 71% in Iran (the highest). However, in our study, cattle seroprevalence (57.1%) is higher than the average global seroprevalence (18.9%) (Nasirian et al. 2019). Compared with neighboring countries in Senegal, CCHFV seroprevalence was higher than in Mali 66% among 1074 cattle (Maiga et al. 2017) and lower among sheep (22.1%) than what had been reported in Mauritania (44%). In other areas of East and Central Africa, seroprevalences were found to be lower: in Sudan 19% among 282 tested cattle, whereas in Katanga (DRC) 1.6% of the 838 tested ruminants were found seropositive (Ibrahim et al. 2015, Sas et al. 2017).

Conclusions

Our results demonstrate the persistence and the circulation of CCHFV in the northern region of Senegal. Further studies are needed to investigate the correlation between the occurrence of the infection in this area and human infection. Our studies highlight the importance of horses and cattle as reservoirs and sentinels for the circulation of the infection in endemic area.

Footnotes

Author Disclosure Statement

One of the authors (L.C.) works at the IDvet company (310, rue Louis Pasteur, Grabels, France), which will commercialize this ELISA kit. However, this does not alter the authors' adherence to the principles of good scientific practice and to relevant policies on sharing data and materials. The authors declare no other competing interests.

Funding Information

This work was supported by the French Government under “Investments for the Future” programme managed by the National Agency for Research (ANR), Méditerranée Infection 10-IAHU-03, and was also supported by Région Provence-Alpes-Côte d'Azur. This work had received financial support from the Foundation Méditerranée Infection.

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