Abstract
South American Zika virus (ZIKV) recently emerged as a novel human pathogen, linked with neurological disorders. However, comparative ZIKV infectivity studies in New World primates are lacking. Two members of the Callitrichidae family, common marmosets (Callithrix jacchus) and red-bellied tamarins (Saguinus labiatus), were highly susceptible to sub-cutaneous challenge with the Puerto Rico-origin ZIKVPRVABC59 strain. Both exhibited rapid, high, acute viraemia with early neuroinvasion (3 days) in peripheral and central nervous tissue. ZIKV RNA levels in blood and tissues were significantly higher in New World hosts compared to Old World species (Macaca mulatta, Macaca fascicularis). Tamarins and rhesus macaques exhibited loss of zonal occludens-1 (ZO-1) staining, indicative of a compromised blood-brain barrier 3 days post-ZIKV exposure. Early, widespread dissemination across multiple anatomical sites distant to the inoculation site preceded extensive ZIKV persistence after 100 days in New and Old World lineages, especially lymphoid, neurological and reproductive sites. Prolonged persistence in brain tissue has implications for otherwise resolved human ZIKV infection. High susceptibility of distinct New World species underscores possible establishment of ZIKV sylvatic cycles in primates indigenous to ZIKV endemic regions. Tamarins and marmosets represent viable New World models for ZIKV pathogenesis and therapeutic intervention studies, including vaccines, with contemporary strains.
Highlights
Zika virus (ZIKV) is a single-stranded RNA virus, a member of the family Flaviviridae
Both New World monkey species were highly susceptible to sub-cutaneous ZIKVPRVABC59 inoculation, typified by rapid appearance 1–2 days post-infection and high virus load in blood associated with co-incident widespread virus dissemination in secondary lymphoid tissues
The role New World non-human primate (NHP) hosts may have played during this outbreak is poorly understood, susceptibility of different New World NHP species to contemporary ZIKV could have epidemiological consequences[33]
Summary
Zika virus (ZIKV) is a single-stranded RNA virus, a member of the family Flaviviridae. Red-bellied tamarins have been previously studied in our laboratory for acute hepacivirus infection, demonstrating susceptibility to flaviviruses[28] Data from these New World hosts were compared to Old World NHP models represented by two species, Indian rhesus macaque (Macaca mulatta, RM) and cynomolgus macaque (Macaca fascicularis, CM). As early as 3 dpi with ZIKV, evidence of a compromised blood brain barrier (BBB) was identified in both tamarins and RM preceding persisting infection in brain tissue sections up to 100 dpi Widespread persistence in both New and Old World hosts raises the possibility that a significant proportion of Zika-exposed individuals during the recent outbreak in South America may be harbouring Zika genome in multiple anatomical sites, including neurological tissue, with potential consequences on human health
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