Rift Valley fever virus-infected mosquito ova and associated pathology: possible implications for endemic maintenance

William S Romoser¹, Marco Neira Oviedo¹, Kriangkrai Lerdthusnee², Lisa A Patrican³, Michael J Turell⁴, David J Dohm⁴, Kenneth J Linthicum⁵, Charles L Bailey⁶
1Department of Biomedical Sciences, College of Osteopathic Medicine, Tropical Disease Institute, Ohio University, Athens, Ohio, USA; 2Department of Entomology, Faculty of Agriculture, Kasetsart University, Bangkok, Thailand; 3Infectious Disease Division, National Center for Medical Intelligence, Fort Detrick, Frederick, Maryland, USA; 4Department of Vector Assessment, Virology Division, United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, Maryland, USA; 5Center for Medical, Agricultural, and Veterinary Entomology, United States Department of Agriculture – Agricultural Research Service, Gainesville, Florida, USA; 6National Center for Biodefense and Infectious Disease, School of Systems Biology, College of Science, George Mason University, Manassas, Virginia, USA

Background: Endemic/enzootic maintenance mechanisms like vertical transmission (pathogen passage from infected adults to their offspring) are central in the epidemiology of zoonotic pathogens. In Kenya, Rift Valley fever virus (RVFV) may be maintained by vertical transmission in ground-pool mosquitoes such as Aedes mcintoshi. RVFV can cause serious morbidity and mortality in humans and livestock. Past epidemics/epizootics have occurred in sub-Saharan Africa but, since the late 1970s, RVFV has also appeared in North Africa and the Middle East. Preliminary results revealed RVFV-infected eggs in Ae. mcintoshi after virus injection into the hemocoel after the first of two blood meals, justifying further study.
Methods: Mosquitoes were collected from an artificially flooded water-catching depression along a stream in Kenya, shipped live to the USA, and studied using an immunocytochemical method for RVFV-antigen localization in mosquito sections.
Results and conclusion: After virus injection into the hemocoel, RVFV-infected reproductive tissues were found, particularly follicular epithelia and oocyte/nurse cells. Ovarian infection from the hemocoel is a crucial step in establishing a vertically transmitting mosquito line. Ovarian follicles originate from germarial cells, primordia located distally in each ovariole, and infection of these cells is expected to be requisite for long-term vertical transmission. However, no germarial cell infection was found, so establishing a new line of vertically transmitting mosquitoes may require two generations. The findings support the hypothesis that Ae. mcintoshi is involved in the endemic maintenance of RVFV by vertical transmission. Detection of distinct pathology in infected eggs raises the possibility of virus-laden eggs being deposited among healthy eggs, thereby providing an exogenous source of infection via ingestion by mosquito larvae and other organisms. This has potentially significant epidemiological implications. Possible modes of entry of virus from the hemocoel into the ovaries and routes by which larvae might become infected by ingesting virus are discussed.

Keywords: hemocoel, ovary, vertical transmission, Aedes mcintoshi, arbovirus, antigen positive