Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters

Abstract

The human T-lymphotropic viruses (HTLVs) types 1 and 2 originated independently and are related to distinct lineages of simian T-lymphotropic viruses (STLV-1 and STLV-2, respectively). These facts, along with the finding that HTLV-1 diversity appears to have resulted from multiple cross-species transmissions of STLV-1, suggest that contact between humans and infected nonhuman primates (NHPs) may result in HTLV emergence. We investigated the diversity of HTLV among central Africans reporting contact with NHP blood and body fluids through hunting, butchering, and keeping primate pets. We show that this population is infected with a wide variety of HTLVs, including two previously unknown retroviruses: HTLV-4 is a member of a phylogenetic lineage that is distinct from all known HTLVs and STLVs; HTLV-3 falls within the phylogenetic diversity of STLV-3, a group not previously seen in humans. We also document human infection with multiple STLV-1-like viruses. These results demonstrate greater HTLV diversity than previously recognized and suggest that NHP exposure contributes to HTLV emergence. Our discovery of unique and divergent HTLVs has implications for HTLV diagnosis, blood screening, and potential disease development in infected persons. The findings also indicate that cross-species transmission is not the rate-limiting step in pandemic retrovirus emergence and suggest that it may be possible to predict and prevent disease emergence by surveillance of populations exposed to animal reservoirs and interventions to decrease risk factors, such as primate hunting.

Fig. 1.

Map of study sites shown in relation to distribution of lowland forest (green) in central Africa. Sites with evidence of PTLV infection are represented with colored circles, which correspond to the PTLV(s) found at the site.

Fig. 2.

HTLV WB serologic pattern of infected African hunters. HTLV classification based on phylogenetic analyses is provided above specimen codes. Asterisks indicate specimens with indeterminate WB results. Reactivity to HTLV-specific proteins is indicated on the left.

Fig. 3.

Phylogenetic relationships of PTLV polymerase (pol; 662 bp) (A), STLV-3 LTR (398 bp) (B), and PTLV-1 LTR (377 bp) (C) sequences by neighbor-joining analysis. Sequences generated in the current study are shown in boxes. NHP taxon codes are provided in Materials and Methods. Support for the branching order was determined by 1,000 bootstrap replicates; only values of 60% or more are shown. Branch lengths are proportional to the evolutionary distance (scale bar) between the taxa.