Rabbit hemorrhagic disease (RHD) is a devastating non-zoonotic disease of rabbits caused by the rabbit hemorrhagic disease virus (RHDV), a Lagovirus of the Caliciviridae family, which is a positive-sense single-stranded RNA virus. The first clinical report of rabbit hemorrhagic disease was in the 1980s in China where the disease killed 14 million European Angora rabbits in 9 months (1). In less than a year, RHD killed 140 million domestic rabbits in China and spread over an area of 50,000 km² (2). Confirmed rabbit hemorrhagic disease virus-2 [RHDV-2 (a variant strain)] outbreak has been reported in domestic rabbits from Benin Republic (3), Egypt (4), Saudi Arabia (5), United Kingdom (6), Portugal (7), and several other countries. However, before 2020, there have been no confirmed cases in Nigeria making it difficult to trace the source of the outbreak, the spatial and temporal spread as well as the socio-economic impact on rabbit farmers. The disease is transmitted by direct contact with infected animals, body fluid, carcasses, fomites, or vectors like flies, fleas, and mosquitoes (8, 9).

The RHDV-2 has 100% morbidity and 60–90% mortality rates (10). Currently, three strains of RHDV have been identified: RHDV, RHDVa, and RHDV-2. Similarly, three clinical forms of the RHD have been identified: the per-acute, acute and sub-acute forms with the incubation period ranging from 3 to 5 days (11). In the per-acute form, infected animals show no signs and die suddenly (10, 12). In acute infections, the rabbits are observed to be inactive, reluctant to move, with bloody discharge from all orifices as well as blood in feces or urine and may develop a fever with temperature up to 42°C (10). Rabbits with the acute form die within 12–36 h from the onset of fever (12). The sub-acute forms present in the same way but with milder symptoms and most rabbits survive. The clinical signs include lethargy, anorexia, weight loss, and jaundice. Death occurs within 1–2 weeks after the onset of symptoms due to liver failure (10). Rabbits infected with RHDV2 are more likely to show sub-acute or chronic signs than those infected with RHDVa (13). Postmortem signs seen in rabbits with RHD are extensive hepatic necrosis, jaundice, multifocal hemorrhages, splenomegaly, bronchopneumonia, pulmonary hemorrhage or edema, and myocardial necrosis (10, 14).

The first laboratory-confirmed RHDV outbreak that was reported to the Office International des Epizooties (OIE) from Nigeria was recorded on the 13th of October 2020 (15). The source of the outbreak is still unknown. The index case of the virus was in Kwara State, Nigeria, where over 300 rabbits were affected on the farm. Subsequently, confirmed outbreaks have been reported in Oyo and Ogun states (15). A national response was instituted by the federal government to stop the further spread of the disease and to enlighten farmers on biosecurity measures which they should adopt on their farms. As of November 30th, 2020, a total of 1,639 self-reported rabbit deaths have been recorded from 2,053 susceptible or infected cases in Nigeria (16). Hence, this study conducted an outbreak investigation and assessed the Spatio-temporal distribution of the RHD among 28 infected farms in Kwara State. Furthermore, the study identified the risk factors and assessed the economic impact of the outbreak in Kwara State.

The outbreak of transboundary animal diseases (TADs) such as RHD has a serious socio-economic impact on the livelihood of small-scale farmers. Although several un-investigated reports have described the occurrence of an acute hemorrhagic disease of rabbit that was imported from Benin Republic into Nigeria (17), it was never investigated, diagnosed, monitored, and reported to the OIE. This study shows that RHD is a devastating disease that spreads very fast from farm to farm, possibly as a result of mechanical transmission through the common practice of animal sharing for mating purposes as well as other fomites.

The disease has a very high morbidity (100%) and mortality (79.8%) rates occurring in clusters within affected areas and the effect tends to be less in farms that have considerable distance from other farms signifying the role of fomites in its transmission. Similar to outbreaks in Ghana (18), we observed a seasonal peak of RHD infections in July, which may be attributed to the mating season in wild hares which brings into close contact hares from different areas as observed in the outbreak in Portugal. Similar results were observed in which some rabbit farmers introduced bucks to other farms for mating. The poor veterinary expert-seeking behavior of the farmers could be responsible for the increased incidence of the disease after the initial outbreak as most farmers resulted to self-medication using antibiotics; this may portend a danger of antimicrobial residues in humans who consume such animals.

Kwara state has an international border with Benin Republic. Hence, TADs such as RHD could spread easily into susceptible rabbit populations in Nigeria. Several factors favor the introduction of TADs into Nigeria. These factors include the poor animal disease surveillance system and the lack of animal movement control across the land borders.

Our findings showed that several factors were common among RHD-infected farms. These include: 1. The introduction of a new rabbit(s) into farms was the single most important risk factor for the introduction of the RHDV-2 into susceptible rabbits. 2. There was no difference in sex distribution of affected rabbits as morbidity and mortality cut across both male and female rabbits. 3. Some of these farms had stagnant water, hence the possibility of transmission via vectors such as insects and houseflies. 4. Farmers within clusters (i.e., close proximity) had unrestricted meetings, hence could serve as mechanical fomites. 5. Younger rabbits <2 months old were less affected than older rabbits. In affected farms, rabbits were culled, the environment fumigated, and reported to the veterinarian only in a few cases.

The most common clinical presentation seen among these rabbits and the CFR were similar to reports of OIE (14), and Happi et al. (19).

Although rabbits were kept in cages, domestic and migratory birds could have access to rabbit cages which could serve as sources of infection for rabbits. The training that most of the farmers reported to have received in rabbit production, coupled with their high level of education could be responsible for some of the biosecurity practices noticed in most farms visited. The use of antibiotics by the farmers is similar to an earlier study of Chah et al. (20) who reported high unprescribed use of antibiotics in rabbits in Enugu State. Similarly, Chah et al. (20) also reported that rabbits were mostly affected by sniffles, mange, and diarrhea. The un-prescribed use of antibiotics could result in the emergence of drug-resistant micro-organisms, some of which could pose a public health threat (21).

Although, the official government policy is “no vaccination against RHD,” some of the rabbit farmers have restocked their farms and vaccinated their rabbits using foreign vaccines. This is highly discouraged as the efficacy of such foreign vaccines on local rabbit populations has not been ascertained and might lead to the introduction of novel strains into Nigeria. In addition, the vaccine only confers immunity for 12 months (22) to 14months (23) and it is believed that vaccination could make RHD endemic (24, 25). Hence, several countries including Nigeria discourage the use of vaccines until a comprehensive epidemiology is carried out to determine causative serotypes in order to adequately provide guidance.

Moreover, it may be more helpful to develop in-country vaccines based on circulating strains. Our findings Figure 1 showed the increasing spread of the virus over time in the state from the index case. Hence, it is essential to carry out statewide active surveillance of RHD to know the true prevalence and incidence of the disease. The RHDV-2 outbreak has devastated farmers with economic losses running into millions of Naira. Hence, the affected farmers should be adequately compensated by the government.

The main strength of the study was its novelty as the first confirmed RHD outbreak in Nigeria and the major limitation was the small sample size.

This study investigated the first RHD outbreak in Kwara State, Nigeria. The disease has spread to other parts of Nigeria. Hence, a nationwide active surveillance of RHD should be conducted. Nigeria must immediately evaluate the efficacy and immunogenicity of the available RHD vaccines and advise farmers accordingly to prevent the huge economic impact of TADs such as RHD.

The raw data supporting the conclusions of this article will be made available by the authors without undue reservation.

Ethical clearance was obtained from the ethical review board of the Kwara State Ministry of Agriculture and Rural Development (MoARD), Ilorin-Nigeria (reference number: VKW/ERB/OM/02/77). Informed consent was sought from the respondents and participants could opt-out at any time.

AA-M and LA were involved in planning the study and data collection. AA-M and MO drafted the initial manuscript. All authors did the overall review of the manuscript, read, and approved the final manuscript.

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.

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