Clinical Presentation and Serologic Response during a Rabies Epizootic in Captive Common Vampire Bats (Desmodus rotundus)

Abstract

We report mortality events in a group of 123 common vampire bats (Desmodus rotundus) captured in México and housed for a rabies vaccine efficacy study in Madison, Wisconsin. Bat mortalities occurred in México and Wisconsin, but rabies cases reported herein are only those that occurred after arrival in Madison (n = 15). Bats were confirmed positive for rabies virus (RABV) by the direct fluorescent antibody test. In accordance with previous reports, we observed long incubation periods (more than 100 days), variability in clinical signs prior to death, excretion of virus in saliva, and changes in rabies neutralizing antibody (rVNA) titers post-infection. We observed that the furious form of rabies (aggression, hyper-salivation, and hyper-excitability) manifested in three bats, which has not been reported in vampire bat studies since 1936. RABV was detected in saliva of 5/9 bats, 2-5 days prior to death, but was not detected in four of those bats that had been vaccinated shortly after exposure. Bats from different capture sites were involved in two separate outbreaks, and phylogenetic analysis revealed differences in the glycoprotein gene sequences of RABV isolated from each event, indicating that two different lineages were circulating separately during capture at each site.

Keywords: clinical signs; neutralizing antibody; outbreak; rabies virus; vampire bat.

Figure 1

Location of seven capture sites in the State of San Luis Potosí in relation to areas recognized as free (green) or under control (orange) for rabies in livestock species according to the Mexican National Service for Agrifood Health, Safety and Quality (SENASICA) in 2018.

Figure 2

Timeline of vampire bat observations and mortalities recorded in Madison, Wisconsin, from September 2018 to January 2019. All bats were captured in México in August and transported to Madison on September 4–6. Bats from Groups 1 (A) and 2 (B) were never in contact since capture and presented two distinct RABV lineages based on phylogenetic analysis of N and G gene sequences. Bats in Group 1 with “(f)” are females and were never in contact with males from the same site. Sites of capture are color coded: Loma (blue), Catedral (gray), Guadalcázar (green), and Milagro (orange). Group 2 bats moved to Cage 4 after the first rabies mortality in that group (#576) are indicated with a circle and those moved to Cage 5 with a triangle. Bold/underline lettering indicates bats that were vaccinated. “V+” indicates RABV shedding detected in oral swabs prior to mortality.

Figure 3

Phylogenetic analysis of glycoprotein (A) and nucleoprotein (B) nucleotide sequences. Phylogenetic trees were estimated by Maximum Likelihood in Mega7. Newly generated sequences from Mexican Desmodus rotundus (magenta, Group 1 and blue, Group 2) clustered with isolates of RABV circulating in Desmodus rotundus in Mexico (A, left). The yellow box highlighted on the glycoprotein gene tree is enlarged on the right to show more detail. Numbers at branch points indicate bootstrap value (out of 1000 replicates). Scale bars indicate number of changes per site. Reference sequences from RABV strains circulating in vampire bats in México, Guatemala, Brazil, and French Guiana were included; references from RABV isolated from a Mexican free-tailed bat (Tadarida brasiliensis) and a dog (historical) were included as outgroups. Reference sequences are labeled with accession number, country, and year of isolation.