Ecological processes underlying the emergence of novel enzootic cycles: Arboviruses in the neotropics as a case study

Abstract

Pathogens originating from wildlife (zoonoses) pose a significant public health burden, comprising the majority of emerging infectious diseases. Efforts to control and prevent zoonotic disease have traditionally focused on animal-to-human transmission, or "spillover." However, in the modern era, increasing international mobility and commerce facilitate the spread of infected humans, nonhuman animals (hereafter animals), and their products worldwide, thereby increasing the risk that zoonoses will be introduced to new geographic areas. Imported zoonoses can potentially "spill back" to infect local wildlife-a danger magnified by urbanization and other anthropogenic pressures that increase contacts between human and wildlife populations. In this way, humans can function as vectors, dispersing zoonoses from their ancestral enzootic systems to establish reservoirs elsewhere in novel animal host populations. Once established, these enzootic cycles are largely unassailable by standard control measures and have the potential to feed human epidemics. Understanding when and why translocated zoonoses establish novel enzootic cycles requires disentangling ecologically complex and stochastic interactions between the zoonosis, the human population, and the natural ecosystem. In this Review, we address this challenge by delineating potential ecological mechanisms affecting each stage of enzootic establishment-wildlife exposure, enzootic infection, and persistence-applying existing ecological concepts from epidemiology, invasion biology, and population ecology. We ground our discussion in the neotropics, where four arthropod-borne viruses (arboviruses) of zoonotic origin-yellow fever, dengue, chikungunya, and Zika viruses-have separately been introduced into the human population. This paper is a step towards developing a framework for predicting and preventing novel enzootic cycles in the face of zoonotic translocations.

Detection and Phylogenetic Analysis of a Novel Tick-Borne Virus in Yunnan and Guizhou Provinces, Southwestern China

“…In recent years, more and more novel arboviruses have been identified from various vector hosts [ 10 , 11 ]. Additionally, a growing number of novel TBVs were also discovered throughout the world, for instance, BRBV in USA [ 4 ], ALSV in China [ 5 ], Hunter island group virus (HIGV) in Australia [ 12 ], Muko virus (MUV), and Tarumizu tick virus (TarTV) in Japan [ 13 , 14 ], etc.…”

Flavivirus Persistence in Wildlife Populations

“…There is potential enzootic transmission, but regular dengue virus spillback cannot be excluded. Except for bats, acute dengue infection among animals is still limited in evidence [ 34 , 35 ]. Similar to WNV, the newly emerging mosquito-borne Usutu virus (USUV) is also transmitted between mosquito arthropods and avian species [ 36 ].…”

Lack of Evidence of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Spillover in Free-Living Neotropical Non-Human Primates, Brazil

“…Given the evolutionary lability of CoVs, there has been considerable concern about spillover of SARS-CoV-2 from humans into additional species since the inception of the pandemic [8], and indeed surveillance has revealed SARS-CoV-2 infection of individuals of a wide variety of animal species in domestic, farm, and zoological park environments [9][10][11]. Alarmingly, significant virus transmission within some of these species has been documented, particularly farmed mink [12].…”

“…Together, these findings on natural and experimental infection ring a warning bell about potential spillover of SARS-CoV-2 to free-living neotropical monkeys living in close proximity to humans. If such spillover led to sustained transmission within these monkeys, this new transmission cycle would greatly complicate efforts to control SARS-CoV-2 in humans and could represent a catastrophe for conservation of neotropical non-human primates [8,25]. Thus, the current study investigated evidence for SARS-CoV-2 spillover into NHPs in two regions of Brazil, namely, Manaus and São José do Rio Preto, that have experienced prolonged, high-intensity transmission of SARS-CoV-2.…”