Rift Valley Fever, an Emerging Viral Zoonosis Worthy of Increased Attention

Rift Valley Fever (RVF) is an emerging zoonotic disease transmitted by mosquitoes. Though North America is considered free of RVF, surveillance and monitoring of high-risk groups would be important for early detection of potential introduction of the disease. Rift Valley Fever Virus (RVFV) is an RNA virus that primarily affects livestock but can also infect humans with varying severity of infection. Though the disease is mainly prevalent in African countries, the vectors involved in the transmission of RVF are present in many regions in the American and European continents. So, the potential for emergence of this disease in new geographical locations is imminent. There is an unmet need for development of improved research and diagnostic tools to further investigate and manage RVF and to better understand its significance from a One Health perspective.

Rift Valley Fever (RVF) is an important emerging mosquito-borne zoonotic viral disease that is primarily present in most of the African continent but may present a potential threat globally with changes in climate and vector distribution. The disease is caused by the Rift Valley Fever Virus (RVFV), a Phlebovirus in the Phenuviridae family, within the order Bunyavirales. Disease outbreaks and epidemics can be devastating to both human and animal health. An abortion storm may present in animal herds, while humans may exhibit ocular pathology and even hemorrhagic disease, with mortalities being experienced in both groups. Transmission of the virus is based upon the mosquito vectors, especially the Aedes genus, which are critical for inter-epidemic maintenance and viral transmission, with other mosquito species contributing to epidemic (epizootic) outbreaks [1]. Considering this, and the fact that the virus is largely enzootic in developing regions, that may often be faced with food scarcity and a myriad of other public health threats, RVF presents a significant global One-Health concern.

The RVFV is an enveloped negative-sense RNA virus with a spherical or pleomorphic virion structure, measuring approximately 100 nm in diameter. The genome is tripartite, with a Small (S), Medium (M) and Large (L) segments, with these segments being encapsulated by the Nucleocapsid (N) protein, as part of the Ribonucleoprotein (RNP) complex [2]. Furthermore, the S segment encodes the N proteins and Nonstructural (NS) proteins which are known to be primary virulence factors for RVF infection [3,4]. The S-segment is interesting in that it carries ambi-sense polarity, where the N gene is negative-sense, and the NS gene is positive-sense RNA. While the M segment incorporates five distinct sites for translation initiation, included in this, is the site that encodes a Glycoprotein Precursor (GPC) [2]. This GPC is then cleaved to produce two structural glycoproteins Gn and Gc, which have functions in host-cell entry, specifically at virus entry and fusion [5,6]. The L segment encodes the viral RNA dependent RNA polymerase (RdRp), and as such along with the other structural proteins (N, Gn and Gc), it is required for viral replication [4].

The virus is mosquito-borne, and as such, there is a strong connection with outbreaks of the disease and periods with high-rainfall conditions. This is primarily due to increased rainfall causing the filling, and flooding, of pans and other water bodies which are breeding grounds for the mosquitoes [1,5,7]. Of these, mosquitoes of the genus Aedes have been identified as the primary reservoir and vector of the virus, while Culex, Anopheles and Mansonia spp. are considered secondary or amplifying vectors [1]. In Aedine mosquitoes, vertical transmission (transovarial) of RVFV occurs, and it is believed that the extended period of survival through dry conditions in these mosquito eggs is critical for the interepidemic survival of the virus [1,5]. These eggs carrying the virus can survive prolonged periods of desiccation, and then hatch following periods of excessive rain to yield infected Aedine mosquitoes that transmit RVFV to their vertebrate hosts. Thereafter, the virus can be spread between mammal hosts and then the secondary vectors may further transmit and amplify this disease outbreak (particularly where ruminant livestock are present), potentially leading to an epizootic or epidemic event [1,5,7]. Thus, within this model, the Aedine mosquito eggs are essential to the enzootic cycle of the disease (which may be based on associations with wildlife), that may precede the epizootic cycle which usually follows a period of high rainfall and flooding. The epizootic cycle then includes multiple mosquito species as well as livestock that become infected, and this can cause a spillover into humans leading to a potential epidemic.

Studies using hemagglutinin inhibition and other serological tests have indicated that RVFV is able to infect a wide range of mammals (particularly, wild animal populations) [1,8,9]. However, the most severe infection occurs in domestic ruminants, mainly sheep, goats, and cattle, with the severity of pathogenicity being greatest in sheep and lowest in cattle [1,2,5]. Infection occurs in animals of all ages, but disease severity is worst in young animals where the mortality rate in lambs is 90% [1,5]. Infection of pregnant animals at any stage will almost cause abortion and death of the fetus, and as such, in a flock/herd setup, abortion storms are possible [1,2,5]. Within these animals, the disease is largely characterized by hepatic lesions, including hemorrhage and necrosis, which may result in icterus. In addition, similar lesions may be seen in the spleen, as well as hemorrhage within the gastrointestinal tract resulting in hemorrhagic diarrhea, and young animals may show pulmonary congestion. Beyond the obvious effects on production, the virus may produce mortality rates of 10 to 50% in adult ruminants. Therefore, in the face of an outbreak the virus may have devastating consequences on a flock or herd. However, given that direct transmission between vertebrates does not occur, this may help to reduce the spread of the disease slightly given the dependence on mosquito transmission [1].

Humans are susceptible to RVFV and may become infected from mosquitoes, usually Culex or Mansonia species, but more commonly through contact with infected animals and their tissues [1,5]. Exposure to respiratory droplets or contact with mucous membranes through infected animal carcasses is the most cited route of infection, and therefore vocational exposure to livestock animals is a significant risk factor for human infection [1,10]. Disease in humans can be variable in severity and the degree of effects that might be seen, although similar to animals, the main organ affected is the liver. The main clinical sign seen is fever, which might be biphasic, and flu-like symptoms which do not progress further. However, ocular disease of varying severity (including blindness), is a serious and not-infrequent complication of infection [11]. Other potential severe forms of infection are hepatotropic, hemorrhagic and neurological diseases, although all of these severe disease forms are usually rare [1,5,10]. The RVF is a serious infection in humans, and while the effect on pregnancy is not as severe as in animals, the virus can result in mortalities in all age groups where outbreaks take place [1].

The first outbreak of RVF is believed to have surfaced in 1930 within the Rift Valley region in Kenya [5] (Table 1). Since then, there have been a number of outbreaks with both human and animal cases over the decades, often with long gaps between outbreaks within a region. It is challenging to provide precise data on how many cases occur from RVFV, as routine surveillance and investigation of cases is limited in the most severely affected regions. However, some of the biggest outbreaks over the last nine decades have occurred in Kenya, South Africa, Egypt, Mauritania, East Africa, Saudi Arabia, and Tanzania, amongst others [5,12] (Table 1). Seroprevalence studies that demonstrate viral presence in at least 31 countries have been performed, and as mentioned, the virus is mainly within Africa with multiple outbreaks in the Arabian Peninsula, with humans, cattle, goats, camels and wildlife all showing exposure [13]. A systematic review of some of the serological studies performed in Africa reported a median seroprevalence of 12.9% in sheep, 12.6% in cattle, 11.3% in wildlife and 5.9% in humans, with the range varying dramatically, especially when comparing studies during outbreaks to seroprevalence investigations [13]. Additionally, there have been multiple RVFV seropositive cases within Turkey and Tunisia to indicate presence of the virus in these areas, as well as other serological findings within Algeria, Western Sahara, Libya, Iraq and Iran which might warrant further surveillance for RVFV in these regions [14-21]. A number of other studies have been conducted in Sub-Saharan Africa to investigate potential risk factors and the seroprevalence of the virus in these regions [22-25]. Beyond this, other studies have been conducted to try to illicit the mechanisms behind the enzootic circulation of the virus that supports its survival and spread between epizootics (epidemics) and how outbreaks occur in previously-free regions [7,26-29]. The potential role of livestock and wildlife reservoirs in maintaining a low-level of infection and transmission as part of the enzootic cycle is worth considering, especially in areas with wildlife-livestock interface. The role of the expanding range of mosquito hosts in previous outbreaks is of interest as it is now seen that the mosquito vectors have an expanded range which now includes Europe and the Americas [1]. An additional potential consideration is the transport of subclinically-infected hosts (similar to that seen with a human case from Mali) or vectors which could be the source of a potential disease-spillover when livestock are involved [30]. Insightful reviews of the epidemiological data of RVFV in humans and animals in Africa was published by Clark MHA, et al. [13], Ebogo-Belobo JT, et al. [21] and Gerken KN, et al. [31], and these can be consulted for further information on prevalence and epidemiological data.

Diagnosis of RVFV infection is primarily based upon RT-qPCR as well as ELISA assays, which are laboratory-based tests [5] (Table 2). The ELISA test as well as other serological tests such as the Viral Neutralization Test (VNT), are based on the presence of host antibodies as seen through IgM and IgG levels. Although there is still a lag IgM ELISA can be used for acute infections from approximately day 4, while IgG ELISAs will have an even longer lag-phase for results are thus the best option for historical evaluations ([1,5,32]). The VNT is the gold standard for detecting previous RVFV exposure, but historically could only be carried out in biosafety level 3 laboratories given the use of the virus to run the assay. However, Schreur and colleagues presented a VNT assay based upon an avirulent RVFV with an enhanced Green Fluorescent Protein (eGFP) that is apparently safe and thus bypasses the need for biosafety containment procedures [33]. The RT-qPCR, that is based upon direct identification of specific viral nucleic acids, and the VNT, offer the highest sensitivity and specificity levels for the identification of the pathogen, and the detection of antibodies, respectively. Alongside PCRs as nucleic acid based assays, RT-LAMP (RT-loop-mediated amplification)is currently widely used and offers a very high sensitivity of 10 copies/reaction, and another developed RPA (recombinase polymerase amplification) provided a limit of detection of 19 RNA molecules/reaction [32]. In addition, researchers are investigating and developing potential multiplex nucleic acid-based diagnostic assays which would be well-suited to cases presenting with non-specific clinical signs such as fever of unknown origin where these tropical diseases are known to occur. An assay using a rapid microfluidic chip alongside RT-LAMP was developed for detection of eight vector-borne viruses, including RVFV, with promising results [34]. Furthermore, a multiplex real-time PCR assay was developed to detect 17 hemorrhagic fever syndrome viruses, which also performed well and seems well suited to public health applications [35]. Lapa and colleagues (2024) provide an insight review on the diagnostics of Rift Valley Fever Virus [32].

The RVFV presents a challenge to both human and animal health, given the potential severity of the disease experienced, coupled with the fact that treatment options are mostly limited. In the absence of widespread vector control, which may not be feasible given the wide distribution of mosquitoes, vaccination may be the best mitigation strategy. There has been active research in investigating potential vaccines for human and animal use, with the main focus being an effective vaccine that prevents the severe forms of disease while avoiding negative side effects [4,36,37]. It is also important that the vaccine should be stable and ideally should tolerate being stored and used in resource-limited regions where environmental factors may vary. Additionally, a vaccine candidate that assists serological surveillance efforts by easily allowing Differentiating Infected from Vaccinated Animals (DIVA) would be advantageous. This will facilitate detection of RVFV through serological surveillance in areas declared free from RVFV, while also allowing vaccination of naïve populations to provide protection. Commercial vaccines have been available for many decades for animal use, such as the Smithburn strain vaccine which was first produced in 1949 still produced by Onderstepoort Biological Products in South Africa [36,38,39]. Many such vaccines are effective but some vaccines (such as the Smithburn strain) present significant risk in pregnant animals (abortions and teratogenicity), poor DIVA capability, and a risk of virulence and disease outbreaks [1,36]. Kitandwe PK, et al. [36] provided an excellent review of some of the different vaccines in development and options that might be available. Unfortunately, at this time there are no widely available human vaccines and thus control measures should ideally prevent spread of infection to humans. It would be of additional value to develop antiviral compounds that could help to limit RVFV infection and prevent development of serious sequelae such as blindness and neurological disease in humans. Studies have demonstrated promising activity in vitro and in animal models, and hopefully this translates to an effective therapeutic being made available soon [40].

As has been discussed, RVF presents a considerable threat to health and to livestock production. It has been demonstrated that this threat is expanding as the virus has been identified in more regions within Africa and the Middle East than ever before. In addition to that, it has been shown that mosquito vectors have expanded their range to include Europe and the Americas. Hardcastle AN, et al. [41] further demonstrated that there is a potential large range that can support the virus and mosquito vectors should these be introduced. Therefore, it is rational to believe that RVFV should be elevated from an emerging tropical disease, which might associate a limited impact, to a disease of global significance that warrants the associated research and diagnostics with a One Health approach.

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