Yellow fever surveillance suggests zoonotic and anthroponotic emergent potential

Abstract

Yellow fever is transmitted by mosquitoes among human and non-human primates. In the last decades, infections are occurring in areas that had been free from yellow fever for decades, probably as a consequence of the rapid spread of mosquito vectors, and of the virus evolutionary dynamic in which non-human primates are involved. This research is a pathogeographic assessment of where enzootic cycles, based on primate assemblages, could be amplifying the risk of yellow fever infections, in the context of spatial changes shown by the disease since the late 20^th century. In South America, the most relevant spread of disease cases affects parts of the Amazon basin and a wide area of southern Brazil, where forest fragmentation could be activating enzootic cycles next to urban areas. In Africa, yellow fever transmission is apparently spreading from the west of the continent, and primates could be contributing to this in savannas around rainforests. Our results are useful for identifying new areas that should be prioritised for vaccination, and suggest the need of deep yellow fever surveillance in primates of South America and Africa.

Fig. 1. Methodological steps of the approach used for yellow fever transmission risk modelling.

a Vector models result from combining, through the fuzzy union (∪), favourable areas for the presence of urban (Ae. aegypti and Ae. albopictus) and sylvatic vectors. b Baseline disease models describe the areas favourable to the occurrence of yellow fever cases. c Transmission risk models quantify the level of yellow fever transmission risk, according to the fuzzy inteserccion (∩) between vector and baseline disease models. d Model fit assessment and validation of model predictive capacity. Methodological details are given in Supplementary Methods, which includes very detailed methodological explanations for all elements with a code in parentheses: A, B, C, D1, D2, D3, D4.1, D4.2, E, E.1, E.2, F, F.1, F.2.

Fig. 2. Contribution of the zoogeographic factor.

a Model of favourability for the occurrence of yellow fever cases according to the presence of non-human primate chorotypes (i.e., zoogeographic model) [the scale for favourability values is: high (F > 0.8); high-intermediate (0.5 ≤ F ≤ 0.8); low-intermediate (0.2 ≤ F < 0.5)]. b Partial contribution of primates on the presence of yellow fever cases in humans [the numbers are percentages of contribution to the distribution of favourability in the disease models (Z: zoogeographic factor, S/E: spatial/environmental factor)]. The maps in a represent the areas where the primate presence could favour the occurrence of disease cases in humans, although correlations with other factors influencing the primate biogeography (such as climate, topography or land cover) might be involved in this relation. Instead, the maps in b highlight the areas where the presence of primates could favour the occurrence of yellow fever regardless of correlations with other factors.

Fig. 3. Global baseline disease, vector and transmission-risk model.

a maps for the late 20th century. b maps for the early 21st century. The risk of transmission is estimated as the fuzzy intersection (∩) between favourable conditions for the occurrence of yellow fever cases, and favourable conditions for the presence of vector species. The Favourability values were considered on the following scale: High (F > 0.8); High-Intermediate (0.5 ≤ F ≤ 0.8); Low-Intermediate (0.2 ≤ F < 0.5); and Low (F < 0.2). The spatial resolution is based on 7,774-km² hexagons. Recorded occurrences of yellow fever cases and of vector presences are also mapped (see “Yellow fever datasets” and “Vector dataset” in the Methods section for details). Mosquito and humans clip art source: http://www.freepik.com.

Fig. 4. Enhanced global baseline disease, vector and transmission-risk models for the early 21^st century.

The risk of transmission is estimated as the fuzzy intersection (∩) between favourable conditions for the occurrence of yellow fever cases, and favourable conditions for the presence of vector species. Compared to the models in Fig. 3, additional predictor variables only available for the 21^st century were considered. Recorded occurrences of yellow fever cases and of vector presences are also mapped. The Favourability values were considered on the following scale: High (F > 0.8); high-intermediate (0.5 ≤ F ≤ 0.8); Low-Intermediate (0.2 ≤ F < 0.5); and Low (F < 0.2). The spatial resolution is based on 7774- km² hexagons. Recorded occurrences of yellow fever cases and of vector presences are also mapped (see “Yellow fever datasets” and “Vector dataset” in the Methods section for details). Mosquito and humans clip art source: http://www.freepik.com.