Emerging Pattern of Rabies Deaths and Increased Viral Infectivity

Sharon L. Messenger, Jean S. Smith, Lillian A. Orciari, Pamela A. Yager, Charles E. Rupprecht

Disclosures

Emerging Infectious Diseases. 2003;9(2) 

In This Article

Results and Discussion

Phylogenetic analysis (Figure 1) links 20 of 27 bat-associated human cases (24/32 cases, including formalin-fixed samples not shown in Figure 1) with L. noctivagans and P. subflavus variants. In contrast to the patterns seen in humans (Figures 1 and 2A), a wide variety of bat rabies variants are implicated in the terrestrial mammal cases across a broad geographic area and largely correspond to the most common bat rabies virus variants in that geographic region (Figures 1 and 2B). Two notable exceptions to this general geographic pattern occur in the northwestern and the southeastern United States (Figure 2B). In these two regions, L. noctivagans and P. subflavus variants account for a substantially larger percentage of transmission events to terrestrial mammals than expected, given the rarity of the host bat species and L. noctivagans and P. subflavus variants in those geographic areas (Figure 2C) (because spillover of these variants to other bat species is rare, we used the prevalence of rabid Silver-haired Bats and Eastern Pipistrelles as a surrogate for the prevalence of L. noctivagans and P. subflavus variants). These two geographic regions also match very closely the geographic distribution of human rabies deaths in the United States associated with these variants (Figure 2A). In the northwest region, delimited by the human cases associated with Silver-haired Bats (clade 1), the L. noctivagans rabies virus variant accounted for 57% of bat-associated cases in terrestrial mammals and 80% of bat-associated cases in humans, despite the fact that rabies-positive Silver-haired Bats account for only 5% of all bats submitted for testing. Similarly, in the southeast region, delimited by human cases associated with Eastern Pipistrelles (clade 2), where neither Eastern Pipistrelles nor Silver-haired Bats exceed an average of 2% of all rabies-positive bats submitted, the P. subflavus variant accounted for 63% of bat-associated cases in terrestrial mammals and 89% of bat-associated cases in humans. The high prevalence of L. noctivagans and P. subflavus variants among terrestrial mammals in the same regions where human cases have occurred suggests that a similar mechanism, such as increased infectivity of these rabies virus variants, is responsible for both epidemiologic patterns.

Phylogenetic tree of bat-associated rabies cases. Taxa represent 203 rabies virus variants from 27 human rabies cases.

Geographic distribution of (A) human (including 5 formalin-fixed samples not shown in Figure 1) and (B) terrestrial mammal cases identified by rabies virus variant isolated.

Our study included 13 terrestrial mammal species, both domesticated and wild, suggesting that exposure to bat species likely occurred in a variety of habitats, including more remote forest habitats. Our data set was comprised mostly of foxes and cats (two species likely to capture and feed upon bats), but we had no reason to suspect that their behavior would create a disproportionate opportunity for infection by L. noctivagans and P. subflavus variants compared with other bat variants.

While our data do not invalidate the small vector hypothesis, the terrestrial mammal data show that even when vector size does not play a role in determining whether bat bites are recognized, L. noctivagans and P. subflavus variants are still the most prevalent rabies virus variants among bat-associated terrestrial mammal deaths in the northwestern and southeastern United States. For human rabies cases, small vector size may still play a role in the probability of detecting a bat bite, while the increased infectivity of L. noctivagans and P. subflavus variants enhances the likelihood of a successful infection following a superficial bite. Additional experimental data (e.g., site-directed mutagenesis) will be necessary to show definitively whether L. noctivagans and P. subflavus variants have evolved genetic changes associated with increased infectivity. Nonetheless, comparisons of phylogenetic patterns between independent datasets in which one data set can be used to control for one or more potentially relevant parameters offers a valid method of hypothesis testing. Additionally, through phylogenetic analyses such as these, we can target those taxa and genomic regions that warrant further investigation.

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