Rift Valley Fever, Sudan, 2007 and 2010

Imadeldin E. Aradaib, Bobbie R. Erickson, Rehab M. Elageb, Marina L. Khristova, Serena A. Carroll, Isam M. Elkhidir, Mubarak E. Karsany, AbdelRahim E. Karrar, Mustafa I. Elbashir, and Stuart T. Nichol

Author affiliations: Author affiliations: University of Khartoum, Khartoum, Republic of the Sudan (I.E. Aradaib, I.M. Elkhidir, A.E. Karrar, M.I. Elbashir); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (B.R. Erickson, M.L. Khristova, S.A. Carroll, S.T. Nichol); Federal Ministry of Health, Khartoum (R.M. Elageb, M.E. Karsany)

Abstract

To elucidate whether Rift Valley fever virus (RVFV) diversity in Sudan resulted from multiple introductions or from acquired changes over time from 1 introduction event, we generated complete genome sequences from RVFV strains detected during the 2007 and 2010 outbreaks. Phylogenetic analyses of small, medium, and large RNA segment sequences indicated several genetic RVFV variants were circulating in Sudan, which all grouped into Kenya-1 or Kenya-2 sublineages from the 2006–2008 eastern Africa epizootic. Bayesian analysis of sequence differences estimated that diversity among the 2007 and 2010 Sudan RVFV variants shared a most recent common ancestor circa 1996. The data suggest multiple introductions of RVFV into Sudan as part of sweeping epizootics from eastern Africa. The sequences indicate recent movement of RVFV and support the need for surveillance to recognize when and where RVFV circulates between epidemics, which can make data from prediction tools easier to interpret and preventive measures easier to direct toward high-risk areas.

Rift Valley fever (RVF) is a mosquito-borne viral disease that typically occurs in various areas of sub-Saharan Africa, where virus activity varies from a low-level enzootic cycle to explosive outbreaks covering large areas. Periodically, Rift Valley fever virus (RVFV) spreads to other areas, including northward into Egypt in 1977 and eastward across the Red Sea into Saudi Arabia and Yemen in 2000 (1–7). How RVFV travels is unclear but probably involves movement of infected livestock or mosquitoes.
Flooding and filling of shallow depressions (damboes) during unusual weather events create ideal conditions for emergence of RVFV-infected mosquitoes. The primary vector is Aedes spp. floodwater mosquitoes, which transmit the virus transovarially, so infected mosquito eggs lay dormant, ready to hatch when surface water levels rise. The infected mosquitoes feed on livestock, causing high viremia, and provide a way for RVFV to 1) infect secondary vector mosquito species (e.g., Culex spp. mosquitoes), which can further transmit the virus to other animals and humans, and 2) infect humans who contact infected animal tissues and blood (8,9).
RVF in livestock can devastate agricultural communities; it causes almost 100% mortality rates among young animals and high abortion rates among livestock. Most RVF in humans is asymptomatic or a mild febrile illness; only 1%–2% of cases progress to more severe disease, such as acute hepatitis, encephalitis, retinitis, and/or a hemorrhagic syndrome; case-fatality rates among hospitalized patients reach 10%–20% (10–12). When outbreaks cover a wide geographic area, hundreds of thousands of livestock are affected, leading to tens of thousands of human infections and hundreds of hospitalizations.
The first reported outbreak of RVF in Sudan occurred in 1973 in sheep and cattle in White Nile State; shortly thereafter, RVFV was isolated from a herd of cattle in northern Khartoum (2,3,13). Serologic surveys have detected RVFV antibodies in domestic livestock (14,15) and in humans from different Sudanese states, including Nile, Khartoum, Kassala, El Gezira, Sennar, and White Nile (16–18). A recent seroepidemiologic survey reported a high prevalence of RVFV IgG among febrile patients admitted to New Halfa Hospital in Kassala State (19). New Halfa is an extensively irrigated agricultural area ≈500 km east of Khartoum. Although the presence of IgG does not indicate recent infection, it does suggest considerable circulation of RVFV in the area at some time in the past.
In late fall and early winter 2007, a large outbreak of RVF, characterized by abortion storms among domestic livestock and febrile hemorrhagic illness in humans, was reported in several Sudanese states (20). Estimates suggested ≈75,000 human infections, similar to the number estimated to have occurred in Kenya around this time (21). The clinical descriptions of severe RVF cases from the 2007 outbreak are similar to those reported from earlier outbreaks (22–24). Several human RVF cases also were reported in 2010 from the El Gezira State after an increase in abortions among ewes and does; however, the outbreak appears to have been limited geographically, and little information is available about the outbreak (I.E. Aradaib, pers. comm.).
The large, well-documented RVF outbreak in Kenya and Tanzania in 2006–2007, with subsequent spread to Madagascar by 2008 (1,8,25–30), was characterized as a steady expansion of many circulating strains of RVFV from 2 sublineages (Kenya-1 and Kenya-2) rather than the introduction and spread of a single strain (5,25,26,31). However, to our knowledge, no information is available about the genetic lineages of RVFV strains circulating in Sudan during this time and in subsequent years. The purpose of this study, therefore, was to generate whole-genome sequences of RVFV associated with the 2007 and 2010 RVFV outbreaks in Sudan. Comparison of these sequences with those derived from known strains from eastern Africa and Egypt may provide insight into the origins of Sudan RVFV strains and whether recent outbreaks in Sudan resulted from single or multiple virus introductions.