Emerging zoonotic and anthroponotic potential for yellow fever transmission

Models based on primates and disease vectors indicate a risk of zoonotic and anthroponotic yellow fever expansion in South America and Africa.

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The yellow fever is a mosquito-borne disease caused by a flavivirus found in Africa and South America1. Since the late 20th century, there has been a resurgence of yellow fever in Africa and in South America2. The globalization of transports, and the expansion of vectors that are themselves evolving, help new virus lineages spread and increase the risk of transmission to humans3,4. Areas at risk of yellow fever transmission should be delineated according to geographic and environmental factors related to yellow fever, in order to prevent and respond efficiently to the occurrence of new outbreaks2,5. Previous studies have analysed the influence of non-human primates on the yellow fever infection rates in humans. Further studies were needed in order to understand the potential extent and geography of the risk of yellow fever transmission to humans favoured by the presence of non-human primates and sylvatic mosquitoes. This is the most relevant contribution of our results.

In South America, the potential for zoonotic yellow fever transmission involves regions within the western, eastern and central Amazon basin, and also great part of the Atlantic forests of Brazil (i.e., the “Mata Atlantica”) (Fig. 1). In Africa, this potential could affect some open and forested savannas to the north and south of the Central African rainforests. Nevertheless, our estimation of the geographic relevance of the yellow fever zoonotic cycle is conservative, as it was made on the basis of the pure effect of non-human primate distributions (Fig. 1.), excluding areas where their contribution could be correlated with that of other environmental factors.

Fig 1. Areas where the non-human primates could favour the occurrence of yellow fever regardless of correlations with other factors during the early 21st century.

The involvement of primates in the virus transmission to humans, for example in the Mata Atlantica, and the high rate of evolution recently shown by this pathogen, could lead to new variants finally reaching human populations, considering that zoonotic cycles in south-eastern Brazil are closely related to urban areas. Forest fragmentation could also amplify the risk of disease transmission by increasing the proximity of human populations to wildlife. Should yellow fever surveillance in non-human primates were addressed, we propose to focus on the list of species belonging to chorotypes significantly related to the distribution of disease cases (see the supplementary information linked to the paper). These chorotypes represent the diversity of primates suspected of being infected with yellow fever virus and geographically linked to the distribution of cases in humans. Yellow fever virus has been detected in 13 non-human primate genera in South America, and in 11 genera in Africa.

Our analyses can also help to identify new areas that could be prioritised for vaccination, for which we propose to consider three yellow-fever-transmission geographic scenarios into account. The first scenario involves areas with very favourable conditions (F>0,5) for both the presence of the virus and mosquito vectors (Fig. 2). This is the case of some areas in West and Central Africa and of southern Brazil. Our model supports the vaccination programme planned by the Brazilian Health Ministry in 2019 in many states in eastern Brazil6, although this zone is not yet considered by WHO6 and CDC7 as a priority. The second scenario describes areas with low but not negligible risk of yellow-fever transmission (0,2 ≤ F ≤ 0,5), such as northern Namibia, western Zambia, eastern Ethiopia and some regions of Somalia. These areas are not considered for vaccination by the WHO8 and CDC7. Finally, the third scenario involves areas environmentally favourable to the presence of mosquito vectors but not as much to the virus occurrence. This situation occurs, for example, in North America, southern Europe, Asia and Oceania, which are outside the yellow fever endemic area. In this situation, the prevention of virus introduction through international travelling is the appropriate policy. There are countries that do not require the yellow fever vaccination certificate for travellers, although these countries coincide with high-risk zones according to our models and with areas where vaccination is recommended by the WHO9. Vaccination of third country citizens in countries with high or medium risk of yellow fever transmission could be required without exceptions. In areas with a stable presence of yellow fever vectors that are close to endemic areas, vaccination should be an option to consider. The WHO vaccination programme in the northern provinces of Argentina are positive examples6.

Fig 2. Enhanced global transmission-risk model for the early 21st century. Mosquitoes drawn by Gabriela Aliaga-Samanez. Humans clip art source: http://www.freepik.com.

References

  1. CDC. Global Health - Newsroom - Yellow Fever. (2018). Available at: https://www.cdc.gov/globalhealth/newsroom/topics/yellowfever/index.html. (Accessed: 11th January 2021)
  2. Shearer, F. M. et al. Existing and potential infection risk zones of yellow fever worldwide: a modelling analysis. Lancet Glob. Heal. 6, e270–e278 (2018).
  3. Tatem, A. J., Hay, S. I. & Rogers, D. J. Global traffic and disease vector dispersal. Proc. Natl. Acad. Sci. U. S. A. 103, 6242–6247 (2006).
  4. Kraemer, M. U. G. et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. Albopictus. Elife 4, 1–18 (2015).
  5. Hamrick, P. N. et al. Geographic patterns and environmental factors associated with human yellow fever presence in the Americas. PLoS Negl. Trop. Dis. 11, 1–27 (2017).
  6. World Health Organization. Yellow Fever Vaccination Recommendations in the Americas, 2013-2020. (2019). Available at: https://who.maps.arcgis.com/apps/webappviewer/index.html?id=7f2ecf3d51c244ba8694c3bf725a7601. (Accessed: 19th April 2021)
  7. CDC. Yellow Fever Maps. (2018). Available at: https://www.cdc.gov/yellowfever/maps/index.html. (Accessed: 19th April 2021)
  8. World Health Organization. Yellow Fever Vaccination Recommendations in Africa, 2015. (2015). Available at: http://gamapserver.who.int/mapLibrary/Files/Maps/ITH_YF_vaccination_africa.png?ua=1. (Accessed: 19th April 2021)
  9. World Health Organization. International Travel and Health - Country List. 1, 1–46 (2021).

 

Alisa Aliaga-Samanez

PhD student, University of Malaga