Hepatitis E virus (HEV) is an icosahedral and single-stranded positive sense polarity RNA virus. The virions are shed naked in feces and bile, and they circulate quasi-enveloped (cloaked in a lipid envelope) in blood (1).

Hepatitis E virus belongs to the Hepeviridae family and to the genus Orthohepevirus. This last is divided into four species, named Orthohepevirus A to D. Orthohepevirus A encompasses eight distinct genotypes (HEV-1 to HEV-8) and several sub-genotypes (2). Hepatitis E virus-1 and HEV-2 infect only humans, HEV-3 and HEV-4 humans and several mammal species (mainly suidae and less frequently red deer and roe deer), HEV-5 and HEV-6 wild boars, HEV-7 dromedary camels and humans, and HEV-8 Bactrian camels and long-tailed macaques (3–6).

Hepatitis E virus is one of the five known hepatotropic viruses in humans (7). According to Li et al. (8), it is responsible of an acute self-limiting hepatitis, and it infects about 939 million individuals all around the world. Every year, 20 million new HEV infections, with 3.3 million acute clinical cases and over than 44.000 related deaths are reported worldwide (9). Hepatitis E virus-1 and HEV-2 are epidemic and endemic in developing countries in Asia and Africa, while HEV-3 and HEV-4 are sporadic in developed countries in Europe, North America and Japan (10–13), causing a variety of hepatic and extrahepatic manifestations (14). Hepatitis E virus-3, 4 and 7 infections are zoonotic (15) transmitted between animals and humans by consumption of raw or undercooked meat (HEV3 and 4) and milk (HEV-7) or contact with infected animals (16).

All over the world, the seroprevalence of HEV infection in dromedary camels range from 8.3 to 62.9% (17, 18). In Algeria, there are about 416.500 camels (Camelus dromedarius) raised following three breeding systems (sedentary, nomadic, and transhumant) in 9 Steppic and 8 Saharan provinces (19), where they occupy a crucial place in sustaining the livelihood of local and nomadic populations by participating to their food security, facilitating their displacements, and providing household incomes. In addition, they play other cultural and social functions such as utilization in some religious feasts and traditional celebrations, racing, gaming, exhibitions and some recreational activities. This close contact with people will increase the likelihood of transmitting many zoonotic infectious agents (including HEV) through all possible routes.

Review of the literature revealed scarce information regarding HEV infection in camels all over the world and none in Algeria. Thus, we have undertaken this preliminary study to elucidate the seroprevalence of this infection and some of its associated risk factors in the camelid population of this country.

An overall apparent anti-HEV seroprevalence of 35.1% was found, corresponding to a true prevalence of 34.8%. As shown in Table 1, the univariate analysis revealed that the factors province of origin, sex and age strata have a significant association with HEV seropositivity in camels (p = 0.034, p = 0.042, and p = 0.026, respectively). In fact, 50.7% of positive animals were females and 49.3% were males; however, 43.3% of sampled males were positive against 29.6% of sampled females. The infection was significantly more frequent in camels from Adrar province (53.3%) followed by Ouargla (50.0%) and Ain Saleh (43.3%) than the other provinces. As well, camels of the Targui breed yielded more seropositivity (38.5%) as compared to those of the Sahraoui one (30.8%), but not significantly. Concerning animals’ age, young camels of 1–6 years old were significantly the most seropositive (47.8%).

When subjected to the logistic regression analysis, only age strata still having a negative impact on the seropositivity (Table 2).

Finally, all the attempts to detect viral RNA in pools of HEV-positive sera were unsuccessful.

To the best of our knowledge, this is the first survey to assess HEV seroprevalence in one-humped camels and its associated risk factors in Algeria.

The study revealed that 35.1% of camels tested positive for HEV antibodies. This value is higher than the 22.4 and 23.1% seroprevalences detected in Ethiopia and Saudi Arabia, respectively (28, 29). It is almost of the same level as the rates reported in this animal species in Nigeria (30.7%) (30), Kenya (31.4%), United Arab Emirates (37.1%), Somalia (40.0%), and Sudan (42.9%) (18). However, it is lower than the ones found in Israel (68.6%) by Bassal et al. (31) and in Egypt (62.9%) by Rasche et al. (18). Until now, no data are available for this infection in camels of the surrounding countries, apart from the work of Ouoba et al. (17) in the Sahelian zone of West Africa, where the seroprevalence was very low (8.3%) when compared to ours. This region includes, besides Burkina Faso, two other countries (Mali and Niger) that border Algeria from the southwest and the southeast. Differences in HEV prevalence between countries may result from many associations of factors that commonly affect several infectious diseases in camels (32, 33) and by factors associated to HEV epidemiology (34, 35). These latter factors are related to geographic and climatic disparities, camels’ husbandry and breeding systems, herds’ health management strategies (particularly biosecurity measures and sanitation), animals’ traits (sex, age, and health status), feed, and grazing management. In addition to other factors, specifically related to HEV, that should be investigated and identified in further studies. For instance, farming practices, such as extensive farming, absence of sanitary ford and quarantine period, and contact with domestic species have been identified as risk factors for HEV occurrence in pigs (34, 35).

In perfect accordance with the outcomes of our work, the impact of camels’ sex on HEV seropositivity has been well established in favor of males by El-Kafrawy et al. (28) and Sarani et al. (36). Conversely, in the studies by Li et al. (29) and Ouoba et al. (17), no statistically significant relationship between HEV seropositivity in camels and their sex was notified. The role of sexual dimorphism in the epidemiology of HEV in dromedary camels is not well established. Some physiological and molecular mechanisms could make males more predisposed to the infection than females. This risk factor deserves to be investigated further.

The fact that camels imported from Sudan and Djibouti were slightly less seropositive than Saudi Arabia’s domestic camels (28) and those imported from Afghanistan and Pakistan were more infected than Iranian local camels (36), implies a geographic (country) influence on the HEV distribution. This effect could not be ascertained by Ouoba et al. (17), who observed a random distribution of HEV-positive camels among the three countries of their study. We confirmed in our work an impact of province (county) of origin on the spread of this infection; however, similar surveys are unavailable to examine it, except the paper published by Sarani et al. (36) in Iran. Remarkably, geographic differences in HEV seroprevalence rates of cattle within different localities or provinces of the same country have already been demonstrated in Egypt and China (37, 38).

It is noteworthy that unrestrained camels’ displacements with nomadic families may contribute to the spread of this infection. These movements are very frequent across the Algerian borders (of about 6.500 km long), especially in the Southern provinces. Camels and other animals’ herds/flocks move through different countries for grazing lands and watering points where they mix and get contact with other domestic and wild animals that may contribute to the dissemination of this virus. Furthermore, within these regions, animals are sold in traditional marketplaces, where no biosecurity measures are applied, and several livestock coming from different herds and regions, congregate together with very close contact allowing contagion and spread of several infectious agents. As well, the possibility that humans may transfer the infection to camels cannot be excluded in these regions, since both animals and humans share the same HEV genotype (HEV-7) (5). Because of the non-enveloped nature of HEV outside its host, it resists and stays potentially infectious in water, soil, and grass for long periods (39).

El-Kafrawy et al. (28) and Ouoba et al. (17) could not find any effect of age on HEV seroprevalence in their sampled camels, in contrast to Bassal et al. (31) who recoded a prevalence of 88.9% in camels aged 10 years and more, 56.0% in those of 7 years old and 67.4% in younger ones (3 years old). In addition, Li et al. (29) and Sarani et al. (36) reported young camels of 2 and 3 years old and those less than 2 years old as the most frequently positive (40.0, 36.4, and 100%, respectively). These last results corroborate well with ours, as we have recorded a significant high prevalence among camels aged of 1–6 years old (47.8%). The high prevalence within this age stratum could be related to the sex of animals (males) and their origin. Indeed, this age section (1–6 years old) is largely composed of males, which are significantly more seropositive than females. Furthermore, it also contains the largest proportion of males of the whole study as compared to the other age strata. As well, it is composed of animals belonging to provinces where the prevalence rates are significantly higher as compared to the others (Adrar, Ouargla vs. El Oued, Tindouf, and Touggourt). According to Yugo et al. (40), absence of association between age and HEV seropositivity in calves and adult cows may be due to transient seroconversion. Corman et al. (41) reported that camels get HEV-7 infection in the first 6 months of life and clear the virus after 2 months approximately, making young animals more seropositive than elder ones, just like in our study.

As far as it could be found out, no information is accessible on the impact of camels’ breeds on the anti-HEV prevalence. According to Al Ramadan et al. (42), there is no evidence of particular resistance or susceptibility of certain camel breeds to some infections (may be hepatitis E is one of them).

Positive slaughtered animals yield contaminated meat and offal that can transfer the virus through direct contact to slaughterhouse workers, veterinarians, butchers, and consumers (43). Slot et al. (44), and Obaidat and Roess (45) described meat consumption as a major risk for HEV infection. In order to neutralize this risk and completely inactivate HEV, Barnaud et al. (46) recommend heating food to an internal temperature of at least 71°C for not less than 20 min.

Our study also agrees with Bassal et al. (31) and Li et al. (29) who failed to detect HEV RNA in all anti-HEV positive serum samples, which indicates absence of active infection with this virus in their sampled animals. HEV RNA is more likely to be present in young camels’ sera (1–3 years old) than in those of elder animals that have acquired HEV infection at younger age then cleared it by aging (28). Interestingly, Corman et al. (41) described camel meat as less risky in HEV transmission, since the infection in this species occurs in a very young age with a short viremia, while these animals are usually slaughtered at higher ages.

Finally, our study has some limitations that should be taken into consideration. First, the small sample size for a vast zone with big dromedary camels’ population. Second: the absence of recent infection in sampled camels led to the non-detection of any virus RNA in plasma/sera. Thus, further studies must include other samples’ types such as feces and tissues (mainly liver) to increase the sensitivity of HEV RNA detection in camels as well as other animal species that are in close contact with them.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

The animal studies were approved by Scientific and Ethics Committee for Animal Experimentation of the Institute of veterinary sciences, University Frères Mentouri of Constantine 1. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent was not obtained from the owners for the participation of their animals in this study because Ethical review and approval was waived for this work, as blood samples were collected before slaughtering. No animals were sacrificed specifically for the purpose of this study.

AA: Conceptualization, Investigation, Writing – original draft, Writing – review & editing. MB: Resources, Writing – original draft. IB: Resources, Writing – original draft. LD: Investigation, Writing – original draft. SH: Data curation, Writing – original draft. GI: Writing – original draft. MM: Writing – original draft. ID: Conceptualization, Writing – original draft, Writing – review & editing.

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was financially co-supported by the Algerian Ministry of Higher Education and Scientific Research (PADESCA Research Laboratory, Institute of Veterinary Sciences, University Frères Mentouri of Constantine 1) and the Italian Istituto Superiore di Sanità (Department of Food Safety, Nutrition and Veterinary Public Health).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.