1. Epidemiology and Global Health
  2. Microbiology and Infectious Disease
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Mapping the zoonotic niche of Ebola virus disease in Africa

  1. David M Pigott
  2. Nick Golding
  3. Adrian Mylne
  4. Zhi Huang
  5. Andrew J Henry
  6. Daniel J Weiss
  7. Oliver J Brady
  8. Moritz UG Kraemer
  9. David L Smith
  10. Catherine L Moyes
  11. Samir Bhatt
  12. Peter W Gething
  13. Peter W Horby
  14. Isaac I Bogoch
  15. John S Brownstein
  16. Sumiko R Mekaru
  17. Andrew J Tatem
  18. Kamran Khan
  19. Simon I Hay  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. Sanaria Institute for Global Health and Tropical Medicine, United States
  3. University of Toronto, Canada
  4. University Health Network, Toronto, Canada
  5. Harvard Medical School, United States
  6. Boston Children's Hospital, United States
  7. University of Southampton, United Kingdom
  8. National Institutes of Health, United States
  9. Flowminder Foundation, Sweden
  10. Li Ka Shing Knowledge Institute, St. Michael's Hospital, Canada
Research Article
Cite this article as: eLife 2014;3:e04395 doi: 10.7554/eLife.04395
8 figures and 2 tables

Figures

The epidemiology of Ebola virus transmission in Africa.

Of the suspected reservoir species, 1, 2 and 3 represent the three bat species from which Ebola virus has been isolated (Hypsignathus monstrosus, Myonycteris torquata and Epomops franqueti) and n represents unknown reservoirs of the disease yet to be discovered. Of the susceptible species, A represents Pan troglodytes, B Gorilla gorilla and m represents other organisms susceptible to the disease, such as duikers. H represents humans. Blue arrows indicate unknown transmission cycles or infection routes and red arrow routes have been confirmed or are suspected. Adapted from Groseth et al. (2007).

https://doi.org/10.7554/eLife.04395.003
The locations of Ebola virus disease outbreaks in humans in Africa.

(A) Illustrates the 23 reported outbreaks of Ebola virus disease through time, with the area of each circle and its position along the y-axis representing the number of cases. The onset year is represented by the colour as per (B). (B) Shows a map of the index cases for each of these outbreaks. (CH) Show these outbreaks over a series of time periods. Numbers refer to outbreaks as listed in Table 1. In (BH) the species of Ebola virus responsible for the outbreak is illustrated by the symbol shape, the number of resulting cases and onset date by symbol colour. The most recent outbreak (#23) is indicated in orange. Countries in which zoonotic transmission to humans has been reported or is assumed to have occurred are coloured in blue. In each map the Democratic Republic of Congo is outlined for reference.

https://doi.org/10.7554/eLife.04395.005
The locations of reported Ebola virus infection in animals in Africa.

(A) Shows the locations of reported Ebola virus infection in animals. (BD) Show these records in animals over three different time periods. Numbers refer to records as listed in Table 2. In all panels, the species in which infection was detected is given by symbol shape and the year recorded by symbol colour. Blue countries represent locations where zoonotic transmission to humans has been reported or is assumed to have occurred. In each map the Democratic Republic of Congo is outlined for reference.

https://doi.org/10.7554/eLife.04395.007
Predicted geographical distribution of the three species of Megachiroptera suspected to reservoir Ebola virus.

(A) Shows the distribution of the hammer-headed bat (Hypsignathus monstrosus), (B) The little collared fruit bat (Myonycteris torquata) and (C) Franquet's epauletted fruit bat (Epomops franqueti). In each map, the locations of reported observations of each species, extracted and curated from the Global Biodiversity Information Facility (GBIF, 2014) and used to train each model are given as grey points (H. monstrosus, n = 67; E. franqueti, n = 120 and M. torquata, n = 52). Expert opinion maps of the known range of each species, generated by the IUCN (Schipper et al., 2008), are outlined in grey. The colour legend represents a scale of the relative probability that the species occurs in that location from 0 (white, low) to 1 (green, high). Area under the curve statistics, calculated under a stringent ten-fold cross validation procedure, are 0.63 ± 0.04, 0.59 ± 0.04 and 0.58 ± 0.03 for H. monstrosus, M. torquata and E. franqueti respectively. (D) Is a composite distribution map giving the mean, relative probability of occurrence from (AC).

https://doi.org/10.7554/eLife.04395.008
Figure 5 with 3 supplements
Predicted geographical distribution of the zoonotic niche for Ebola virus.

(A) Shows the total populations living in areas of risk of zoonotic transmission for each at-risk country. The grey rectangle highlights countries in which index cases of Ebola virus disease have been reported (Set 1); the remainder are countries in which risk of zoonotic transmission is predicted, but in which index cases of Ebola have not been reported (Set 2). These countries are ranked by population at risk within each set. The population at risk Figure in 100,000 s is given above each bar. (B) Shows the predicted distribution of zoonotic Ebola virus. The scale reflects the relative probability that zoonotic transmission of Ebola virus could occur at these locations; areas closer to 1 (red) are more likely to harbour zoonotic transmission than those closer to 0 (blue). Countries with borders outlined are those which are predicted to contain at-risk areas for zoonotic transmission based on a thresholding approach (see ‘Materials and methods’). The area under the curve statistic, calculated under a stringent 10-fold cross-validation procedure is 0.85 ± 0.04. Solid lines represent Set 1 whilst dashed lines delimit Set 2. Areas covered by major lakes have been masked white.

https://doi.org/10.7554/eLife.04395.009
Figure 5—figure supplement 1
Covariates used in predicting zoonotic transmission niche of Ebola.

(A) Displays elevation across Africa measured in metres, relative to sea level. (B and C) Show enhanced vegetation index (EVI) values (mean and spatial range respectively) on a scale from 0 to 1. (DG) Display land surface temperature (LST) (mean and spatial range for day and night respectively) measured in degrees Celsius. (H) Shows potential evapotranspiration (PET) for Africa, in millimetres per month and (I) gives the composite, relative probability of occurrence of the three suspected reservoir bat species. For details of how each of these covariate layers was derived see ‘Materials and methods’.

https://doi.org/10.7554/eLife.04395.010
Figure 5—figure supplement 2
Marginal effect plots for each covariate used in the Ebola virus distribution model.

Each panel illustrates the marginal effect (averaging over the effects of other covariates) that changes in each of the covariates has on the predicted relative probability of occurrence of zoonotic Ebola virus transmission. Grey regions and solid lines give the 95% confidence region (a metric of uncertainty) and mean value calculated across all 500 submodels. The mean relative contribution of the covariate to the model (the proportion of iterations in which the covariate was selected by the model-fitting algorithm, indicating sensitivity to the covariates) is given as an inset number. The dependency plots are ordered by mean relative contribution of the covariate. EVI = enhanced vegetation index, LST = land surface temperature and PET = potential evapotranspiration.

https://doi.org/10.7554/eLife.04395.011
Figure 5—figure supplement 3
Comparison of predictions for zoonotic niche of Ebola virus excluding the Guinea outbreak.

(A) Shows the predicted zoonotic niche excluding the index case for the Guinea outbreak from the dataset used to train the model. (B) Shows the prediction when including the Guinea data in the model (the model presented in Figure 5). The circle depicts the location of the Guinean index case (#23 in Table 1). As per Figure 5, the scale reflects the relative probability that zoonotic transmission of Ebola virus could occur at these locations; areas closer to 1 (red) are more likely to harbour zoonotic transmission than those closer to 0 (blue).

https://doi.org/10.7554/eLife.04395.012
Changes in national population for countries predicted to contain areas at-risk of zoonotic Ebola virus transmission.

For each country the population (in millions) is presented for three time periods (1976, 2000 and 2014) as three bars. Each stacked bar gives the rural (green) and urban (blue) populations of the country. The grey rectangle highlights countries in which index cases of Ebola virus diseases have been reported (Set 1); the remainder are countries in which risk of zoonotic transmission is predicted, but where index cases have not been reported (Set 2). The fractional change in population between 1976 and 2014 is given above each set of bars.

https://doi.org/10.7554/eLife.04395.013
Changes in international flight capacity and traveller volumes for countries predicted to contain areas at-risk of zoonotic Ebola virus transmission.

The grey rectangle highlights countries in which index cases of EVD have been reported (Set 1). The remainder are countries in which risk of zoonotic transmission is predicted, but where index cases have not been reported (Set 2). (A) Shows changes in annual outbound international seat capacity (between 2000 in red and 2013 in blue). (B) Depicts changes in annual outbound international passenger volume by country (between 2005 in red and 2012 in blue). For each country, the fractional change in volume is given above each set of bars. Note that only one bar is presented for South Sudan as data for this region prior to formation of the country in 2011 were unavailable.

https://doi.org/10.7554/eLife.04395.014
Numbers of airline passengers arriving from at-risk countries to other countries stratified by major geographic regions and national income groups.

(A) Shows the locations of WHO regions (AFRO–African Region; AMRO–Region of the Americas; EMRO–Eastern Mediterranean Region; EURO–European Region; SEARO–South-East Asian Region; WPRO–Western Pacific Region). (B) Displays the numbers of passengers arriving in each of these regions from countries predicted to contain areas at risk of zoonotic Ebola virus transmission (Sets 1 and 2) in 2005 and 2012. (C) Shows the income tiers of all countries as defined by the World Bank. (D) Displays the total numbers of passengers arriving in countries in each of these income strata from at-risk countries in 2005 and 2012. The number above each pair of bars indicates the fractional change in these numbers of incoming passengers between 2005 and 2012.

https://doi.org/10.7554/eLife.04395.015

Tables

Table 1

Locations of outbreaks of Ebola virus disease in humans

https://doi.org/10.7554/eLife.04395.004
OutbreakCountriesDate rangeLocationSpeciesReference
1South SudanJun–Nov 1976NzaraSUDV(WHO International Study Team, 1978)
2DRCSep–Oct 1976YambukuEBOV(International Commission, 1978)
3DRCJun 1977BonduniEBOV(Heymann et al., 1980)
4South SudanJul–Oct 1979NzaraSUDV(Baron et al., 1983)
5Côte d’IvoireNov 1994Tai ForestTAFV(Le Guenno et al., 1995; Formenty et al., 1999)
6GabonNov 1994–Feb 1995Mekouka and Andock mining campsEBOV(Amblard et al., 1997; Georges et al., 1999; Milleliri et al., 2004)
7DRCJan–Jul 1995Mwembe ForestEBOV(Muyembe and Kipasa, 1995; Khan et al., 1999)
8GabonJan–Mar 1996Mayibout 2EBOV(Georges et al., 1999; Milleliri et al., 2004)
9GabonJul 1996–Jan 1997BooueEBOV(Georges et al., 1999; Milleliri et al., 2004)
10UgandaOct 2000–Feb 2001Rwot-ObilloSUDV(WHO, 2001; Okware et al., 2002; Lamunu et al., 2004)
11Gabon & ROCOct 2001–Mar 2002Memdemba Entsiami, Abolo and AmbomiEBOV(WHO, 2003; Milleliri et al., 2004; Nkoghe et al., 2005; Pourrut et al., 2005)
Ekata
Oloba
Etakangaye
Grand Etoumbi
12ROCDec 2002–Apr 2003YembelangoyeEBOV(WHO, 2003; Pourrut et al., 2005)
Nearby hunting camp
Mvoula
13ROCOct–Dec 2003MbandzaEBOV(Boumandouki et al., 2005)
14South SudanApr–Jun 2004Forests bordering YambioSUDV(WHO, 2005; Onyango et al., 2007)
15ROCApr–May 2005Odzala National ParkEBOV(Nkoghe et al., 2011)
16DRCMay–Nov 2007Mombo Mounene 2 marketEBOV(Leroy et al., 2009)
17UgandaAug–Dec 2007KabangoBDBV(Towner et al., 2008; MacNeil et al., 2010; Wamala et al., 2010)
18DRCNov 2008–Feb 2009LueboEBOV(Grard et al., 2011)
19UgandaMay 2011NakisamataSUDV(Shoemaker et al., 2012)
20DRCJuly–Nov 2012IsiroBDBV(CDC, 2014; WHO, 2012b)
21UgandaJuly–Oct 2012NyanswigaSUDV(CDC, 2014; WHO, 2012a)
22UgandaNov 2012–Jan 2013Luwero DistrictSUDV(WHO, 2012c; CDC, 2014)
23GuineaDec 2013 -MeliandouEBOV(Baize et al., 2014; Bausch and Schwarz, 2014)
  1. DRC = Democratic Republic of the Congo, ROC = Republic of Congo.

Table 2

Locations of reported infections with Ebola virus in animals

https://doi.org/10.7554/eLife.04395.006
SiteCountryDate rangeLocationSpeciesDiagnosisReference
1Côte d’IvoireOct–Nov 1994Tai ForestChimpanzeeSerology(Formenty et al., 1999)
2GabonJan 1996Mayiboth 2ChimpanzeePCR(Lahm et al., 2007)
3GabonJul 1996Near BooueChimpanzeeSerology(Georges-Courbot et al., 1997)
4GabonSept 1996Lope National ParkChimpanzeePCR(Lahm et al., 2007)
5Gabon & ROCAug 2001Mendemba/Lossi Animal SanctuaryChimpanzeePCR(Lahm et al., 2007)
6Gabon & ROCAug 2001Mendemba/Lossi Animal SanctuaryGorillaPCR(Lahm et al., 2007)
7Gabon & ROCAug 2001Mendemba/Lossi Animal SanctuaryCephalophus dorsalisPCR(Lahm et al., 2007)
8GabonNov 2001ZadieGorillaPCR(Rouquet et al., 2005)
9GabonNov 2001EkataGorillaPCR(Wittmann et al., 2007)
10GabonDec 2001Medemba and neighbouring villagesChimpanzee and GorillaPCR(Leroy et al., 2002)
11GabonFeb 2002ZadieGorillaPCR(Rouquet et al., 2005)
12GabonFeb 2002EkataVarious bat speciesSerology(Leroy et al., 2005)
13GabonMar 2002ZadieGorillaPCR(Rouquet et al., 2005)
14GabonMar 2002Grand EtoumbiGorillaPCR(Wittmann et al., 2007)
15GabonApr 2002EkataGorillaPCR(Wittmann et al., 2007)
16ROCMay 2002OlobaChimpanzeePCR(Lahm et al., 2007)
17ROCDec 2002Lossi Animal SanctuaryGorillaPCR(Rouquet et al., 2005)
18ROCDec 2002Lossi Animal SanctuaryGorillaPCR(Rouquet et al., 2005)
19ROCDec 2002Lossi Animal SanctuaryChimpanzeeSerology(Rouquet et al., 2005)
20ROCDec 2002Lossi Animal SanctuaryGorillaPCR(Rouquet et al., 2005)
21ROCDec 2002Lossi Animal SanctuaryGorillaPCR(Rouquet et al., 2005)
22ROCDec 2002Lossi Animal SanctuaryCephalophus spp.PCR(Rouquet et al., 2005)
23GabonFeb 2003MbomoVarious bat speciesPCR(Leroy et al., 2005)
24ROCFeb 2003Lossi Animal SanctuaryGorillaSerology(Rouquet et al., 2005)
25GabonFeb 2003Lossi Animal SanctuaryChimpanzeePCR(Wittmann et al., 2007)
26GabonJun 2003MbomoVarious bat speciesPCR and serology(Leroy et al., 2005)
27ROCJun 2003Near Mbomo and Ozala National ParkEpomops franquetiSerology(Pourrut et al., 2009)
28ROCJun 2003Near Mbomo and Ozala National ParkHypsignathus monstrosusSerology(Pourrut et al., 2009)
29ROCJun 2003Near Mbomo and Ozala National ParkMyonycteris torquataSerology(Pourrut et al., 2009)
30ROCJun 2003MbanzaGorillaPCR(Rouquet et al., 2005)
31ROCJan–Jun 2004LokouéGorillaReported(Caillaud et al., 2006)
32ROCMay 2004LokouéGorillaPCR(Wittmann et al., 2007)
33GabonFeb 2005Near FrancevilleEpomops franquetiSerology(Pourrut et al., 2009)
34GabonFeb 2005Near FrancevilleMyonycteris torquataSerology(Pourrut et al., 2009)
35GabonApr 2005Near LambareneEpomops franqueti and Hypsignathus monstrosusSerology(Pourrut et al., 2007)
36ROCMay 2005Near Mbomo and Ozala National ParkEpomops franquetiSerology(Pourrut et al., 2009)
37ROCMay 2005Near Mbomo and Ozala National ParkHypsignathus monstrosusSerology(Pourrut et al., 2009)
38ROCMay 2005Near Mbomo and Ozala National ParkMyonycteris torquataSerology(Pourrut et al., 2009)
39ROCJun 2005Odzala National ParkGorillaPCR(Wittmann et al., 2007)
40GabonFeb 2006Near TchibangaVarious bat speciesSerology(Pourrut et al., 2009)
41ROCMay 2006Near Mbomo and Ozala National ParkEpomops franquetiSerology(Pourrut et al., 2009)
42ROCMay 2006Near Mbomo and Ozala National ParkHypsignathus monstrosusSerology(Pourrut et al., 2009)
43ROCMay 2006Near Mbomo and Ozala National ParkMyonycteris torquataSerology(Pourrut et al., 2009)
44GabonOct 2006Near FrancevilleEpomops franquetiSerology(Pourrut et al., 2009)
45GhanaMay 2007SagyimaseEpomops franquetiSerology(Hayman et al., 2012)
46GhanaMay 2007SagyimaseHypsignathus monstrosusSerology(Hayman et al., 2012)
47GhanaMay 2007AdoagyirEpomophorus gambianusSerology(Hayman et al., 2012)
48GhanaMay 2007AdoagyirEpomops franquetiSerology(Hayman et al., 2012)
49GhanaJun 2007OyibiEpomophorus gambianusSerology(Hayman et al., 2012)
50GhanaJan 2008AccraEidolon helvumSerology(Hayman et al., 2010)
51GabonMar 2008Near FrancevilleEpomops franquetiSerology(Pourrut et al., 2009)
  1. ROC = Republic of Congo.

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