Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates

Abstract

The recognition that AIDS originated as a zoonosis heightens public health concerns associated with human infection by simian retroviruses endemic in nonhuman primates (NHPs). These retroviruses include simian immunodeficiency virus (SIV), simian T-cell lymphotropic virus (STLV), simian type D retrovirus (SRV), and simian foamy virus (SFV). Although occasional infection with SIV, SRV, or SFV in persons occupationally exposed to NHPs has been reported, the characteristics and significance of these zoonotic infections are not fully defined. Surveillance for simian retroviruses at three research centers and two zoos identified no SIV, SRV, or STLV infection in 187 participants. However, 10 of 187 persons (5.3%) tested positive for SFV antibodies by Western blot (WB) analysis. Eight of the 10 were males, and 3 of the 10 worked at zoos. SFV integrase gene (int) and gag sequences were PCR amplified from the peripheral blood lymphocytes available from 9 of the 10 persons. Phylogenetic analysis showed SFV infection originating from chimpanzees (n = 8) and baboons (n = 1). SFV seropositivity for periods of 8 to 26 years (median, 22 years) was documented for six workers for whom archived serum samples were available, demonstrating long-standing SFV infection. All 10 persons reported general good health, and secondary transmission of SFV was not observed in three wives available for WB and PCR testing. Additional phylogenetic analysis of int and gag sequences provided the first direct evidence identifying the source chimpanzees of the SFV infection in two workers. This study documents more frequent infection with SFV than with other simian retroviruses in persons working with NHPs and provides important information on the natural history and species origin of these infections. Our data highlight the importance of studies to better define the public health implications of zoonotic SFV infections.

FIG. 1.

Detection of antibodies to SFV in infected workers by using the CA-WB assay. Neg, negative control sera. Seroreactivity to the diagnostic monkey or ape SFV Gag doublet proteins (p68/72 or p70/74, respectively) was observed in all SFV-infected specimens.

FIG. 2.

Phylogenetic relationship of integrase sequences of SFV-infected workers and NHPs. The tree was derived by NJ analysis using 2 Kimura distances. The 13 cases of SFV infection are boxed. Samples were not available from subject 11. The subspecies origins for all 14 chimpanzee SFV sequences (B1, 1040, 1436, 1016, 1058, Cpz2, Cpz4, C941, A101, A055, C1138, A182, C679, and A136) are indicated. Virus origins: SFV6cpz and SFV7cpz, common chimpanzees (subspecies unknown); SFV1a, SFV1b, SFV2, and SFV_MAC, macaques; SFV3_AGM and SFV3lk, African green monkeys; SFV_HUM, SFV_AGM-infected human; SFV_CAT, sooty mangabey (C. atys). Values on branch nodes represent the percentages of 1,000 bootstrap replicates, and only values greater than 60% are shown. The scale bar represents an evolutionary distance of 0.05 nucleotide per site. Trees were rooted by using the New World spider monkey (SFV8_SPM) sequence.

FIG. 3.

Phylogenetic relationship of gag sequences of selected SFV_CPZ-infected workers and NHPs. The tree was derived by NJ analysis using 2 Kimura distances. The eight cases of SFV_CPZ infection are shown in boxes. The subspecies origin for 11 chimpanzee SFV sequences (B1, 1040, 1016, 1058, Cpz4, C941, A101, A055, A182, C679, and A136) is indicated. SFV1, macaque. Values on branch nodes represent the percentages of 1,000 bootstrap replicates, and only values greater than 60% are shown. The scale bar represents an evolutionary distance of 0.05 nucleotide per site.