Differential Yellow Fever Susceptibility in New World Nonhuman Primates, Comparison with Humans, and Implications for Surveillance

Abstract

A major outbreak of yellow fever (YF) occurred in Brazil during 2016–2018. Epizootics in New World nonhuman primates are sentinel events for YF virus circulation. However, genus-specific susceptibilities and suitability for YF surveillance remain poorly understood. We obtained and compared epidemiologic, histopathologic, immunohistochemical, and molecular results from 93 human and 1,752 primate cases submitted during the recent YF outbreak in Brazil (2017), with the support of the Brazilian National YF Surveillance Program. We detected heterogeneous YF-associated profiles among the various genera of primates we analyzed. Alouatta primates were the most reliable sentinel; Sapajus and Callicebus primates had higher viral loads but lower proportional mortality rates. Callithrix primates were the least sensitive, showing lower viral loads, lower proportional mortality rates, and no demonstrable YF virus antigen or extensive lesions in liver, despite detectable viral RNA. These differences in susceptibility, viral load, and mortality rates should be considered in strategic surveillance of epizootics and control measures for YF.

Pathology and One Health implications of fatal Leptospira interrogans infection in an urbanized, free‐ranging, black‐tufted marmoset ( Callithrix penicillata ) in Brazil

“…Diseases causing hepatocellular damage and death are in the differential diagnosis for leptospirosis in marmosets in Midwestern Brazil. These include toxoplasmosis, yellow fever, and herpes simplex; however, histopathological features of these diseases are distinct from those observed in this marmoset (de Azevedo Fernandes et al, 2021;Mätz-Rensing et al, 2003;Paula et al, 2020).…”

Reemergence of Yellow Fever in Brazil: The Role of Distinct Landscape Fragmentation Thresholds

“…Among abundant species in fragmented landscapes are howler monkeys [ 44 ], hosts that can amplify lineages of YFV [ 11 , 12 ] and are frequently bitten by mosquito vector species in the forest [ 45 , 46 ]. Viral amplification in this transmission expansion scenario has been responsible for the occurrence of several human deaths and the local extinction of nonhuman primates [ 5 , 6 , 39 ].…”

“…e most affected nonhuman primate species are New World Monkeys of the genera Callithrix (marmosets) and Alouatta (howler monkeys) [10][11][12]. Higher male frequency (80%), average age of 50 years, and residence in rural areas are the main characteristic of human cases [13].…”

“…Thousands of cases and deaths are occurring, causing impacts on public health and on the biodiversity of neotropical primates [ 10 ]. The most affected nonhuman primate species are New World Monkeys of the genera Callithrix (marmosets) and Alouatta (howler monkeys) [ 10 – 12 ]. Higher male frequency (80%), average age of 50 years, and residence in rural areas are the main characteristic of human cases [ 13 ].…”

Yellow fever reemergence in Venezuela – Implications for international travelers and Latin American countries during the COVID-19 pandemic

“…In relation to New World non-human primates, one aspect to consider is the differential susceptibility to YF among different primates and how this influences viral load and overall mortality rates amongst these. Such information comes handy when designing strategic surveillance programs of epizootics and YF prevention and control measure [22].…”