Detection of the mosquito-borne flaviviruses, West Nile, Dengue, Saint Louis Encephalitis, Ilheus, Bussuquara, and Yellow Fever in free-ranging black howlers (Alouatta caraya) of Northeastern Argentina

Abstract

Several medically important mosquito-borne flaviviruses have been detected in Argentina in recent years: Dengue (DENV), St. Louis encephalitis (SLEV), West Nile (WNV) and Yellow Fever (YFV) viruses. Evidence of Bussuquara virus (BSQV) and Ilheus virus (ILHV) activity were found, but they have not been associated with human disease. Non-human primates can act as important hosts in the natural cycle of flaviviruses and serological studies can lead to improved understanding of virus circulation dynamics and host susceptibility. From July–August 2010, we conducted serological and molecular surveys in free–ranging black howlers (Alouatta caraya) captured in northeastern Argentina. We used 90% plaque-reduction neutralization tests (PRNT90) to analyze 108 serum samples for antibodies to WNV, SLEV, YFV, DENV (serotypes 1and 3), ILHV, and BSQV. Virus genome detection was performed using generic reverse transcription (RT)-nested PCR to identify flaviviruses in 51 antibody-negative animals. Seventy animals had antibodies for one or more flaviviruses for a total antibody prevalence of 64.8% (70/108). Monotypic (13/70, 19%) and heterotypic (27/70, 39%) patterns were differentiated. Specific neutralizing antibodies against WNV, SLEV, DENV-1, DENV-3, ILHV, and BSQV were found. Unexpectedly, the highest flavivirus antibody prevalence detected was to WNV with 9 (8.33%) monotypic responses. All samples tested by (RT)-nested PCR were negative for viral genome. This is the first detection of WNV-specific antibodies in black howlers from Argentina and the first report in free-ranging non-human primates from Latin-American countries. Given that no animals had specific neutralizing antibodies to YFV, our results suggest that the study population remains susceptible to YFV. Monitoring of these agents should be strengthened to detect the establishment of sylvatic cycles of flaviviruses in America and evaluate risks to wildlife and human health.

Detection of antibodies against Icoaraci, Ilhéus, and Saint Louis Encephalitis arboviruses during yellow fever monitoring surveillance in non‐human primates (Alouatta caraya) in southern Brazil

“…For example, the lack of serological evidence of YFV‐neutralizing antibodies in all howler monkeys captured in an area with extensive YFV circulation during the 2008‐2009 epizootic, including previous positive results in area S1 , signals that the virus is not currently circulating after the regional epizootic. This lack of YFV immunity in most (or all) howler monkeys in the study populations is concerning because of the species’ high susceptibility to YF, making it potentially vulnerable in cases of YF re‐emergence . However, it is possible that the SLEV and ILHV contact detected in 8% of the howler monkeys will confer some degree of protection against future YFV re‐emergences …”

“…This lack of YFV immunity in most (or all) howler monkeys in the study populations is concerning because of the species’ high susceptibility to YF, making it potentially vulnerable in cases of YF re‐emergence . However, it is possible that the SLEV and ILHV contact detected in 8% of the howler monkeys will confer some degree of protection against future YFV re‐emergences …”

“…Otherwise, dead animal tissue is required . The low viral detection frequency by PCR and isolation in healthy free‐ranging animals is common in this type of study …”

“…Ilhéus virus‐neutralizing antibodies were detected in NHPs in Argentina . The virus, discovered in 1944 in mosquitoes in the city of Ilhéus, state of Bahia, Brazil, continues to circulate among golden‐headed lion tamarins ( Leontopithecus chrysomelas ) in that region .…”

“…For example, researchers have detected black howler monkeys ( Alouatta caraya ) infected with the Saint Louis Encephalitis virus (SLEV) in Argentina and red howler monkeys ( Alouatta macconnelli ), white‐faced sakis ( Pithecia pithecia ) and golden‐handed tamarins ( Saguinus midas ) with serological signs of YFV and Mayaro virus (MAYV) infection in French Guiana . In Argentina, recent serological findings for the West Nile virus (WNV) and dengue 1 and 3 viruses (DENV) yielded increased reports of arboviruses infecting NHPs …”