Predictors of human-infective RNA virus discovery in the United States, China, and Africa, an ecological study

  1. Feifei Zhang  Is a corresponding author
  2. Margo Chase-Topping
  3. Chuan-Guo Guo
  4. Mark EJ Woolhouse
  1. Usher Institute, University of Edinburgh, United Kingdom
  2. Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, United Kingdom
  3. Department of Medicine, Li Ka Shing Faculty of Medicine, University of Hong Kong, China
28 figures, 4 tables and 1 additional file

Figures

Spatial distribution of human-infective RNA virus discovery in three regions, 1901–2019.

(A) United States. (B) China. (C) Africa. Red dots represent discovery points or centroids of polygons, with the size representing the cumulative virus species count.

Shared human-infective RNA virus species count in three regions.

Under/By the species count the ratios of vector-borne (V) to non-vector-borne (N) viruses and strictly zoonotic (Z) to human transmissible (T) viruses were shown.

Discovery curve of human-infective RNA virus species in three regions and the world.
Relative contribution of predictors to human-infective RNA virus discovery in three regions.

(A) United States. (B) China. (C) Africa. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate boosted regression tree models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Cumulative relative contribution of predictors to human-infective RNA virus discovery by group in each model of different regions.

The relative contributions of all explanatory factors sum to 100% in each model, and each colour represents the cumulative relative contribution of all explanatory factors within each group.

Predicted probability of human-infective RNA virus discovery in three regions in 2010–2019.

(A) United States. (B) China. (C) Africa. The triangles represented the actual discovery sites from 2010 to 2019, and the background colour represented the predicted discovery probability.

Appendix 3—figure 1
Relationship between published human-infective RNA virus count and total number of papers from the journals which published all human-infective RNA viruses in Web of Science.

(A) Total number of papers vs. published human virus count; (B) Total number of papers on viruses vs. published human virus count; (C) Total number of papers vs. total number of papers on viruses; (D) Percent of papers on viruses in each journal. Journal of Infectious Diseases (JID) is highlighted in blue.

Appendix 3—figure 2
Time lag of human-infective RNA virus discovery between the three regions and the world.

(A) United States. (B) China. (C) Africa. The blue dots represent the original discovery year of each virus in the world; the red dots represent the discovery year of each virus in three regions; and the segments between them represent the time lag.

Appendix 3—figure 3
Partial dependence plots showing the influence on human-infective RNA virus discovery for all predictors in the Unites States.

Partial dependence plots show the effect of an individual predictor over its range on the response after factoring out other predictors. Fitted lines represent the median (black) and 95% quantiles (coloured) based on 1000 replicated boosted regression tree models. Y axes are centred around the mean without scaling. X axes show the range of sampled values of predictors.

Appendix 3—figure 4
Partial dependence plots showing the influence on human-infective RNA virus discovery for predictors in China.

Partial dependence plots show the effect of an individual predictor over its range on the response after factoring out other predictors. Fitted lines represent the median (black) and 95% quantiles (coloured) based on 1000 replicated boosted regression tree models. Y axes are centred around the mean without scaling. X axes show the range of sampled values of predictors.

Appendix 3—figure 5
Partial dependence plots showing the influence on human-infective RNA virus discovery for all predictors in Africa.

Partial dependence plots show the effect of an individual predictor over its range on the response after factoring out other predictors. Fitted lines represent the median (black) and 95% quantiles (coloured) based on 1000 replicated boosted regression tree models. Y axes are centred around the mean without scaling. X axes show the range of sampled values of predictors.

Appendix 3—figure 6
Moran’s I across different spherical distances.

(A) United States; (B) China; (C) Africa. The solid line and dots represented the median Moran’s I value, and the grey area represented its 95% quantiles generated from 1000 samples (Blue: Raw virus data) or replicate boosted regression tree (BRT) models (Red: Model residuals). We used the fixed spherical distance as the neighbourhood weights—as there is no general consensus for selecting cut-off values, we chose spherical distances ranging from one time to fifteen times of distance of 1° grid cell at the equator, i.e. 110km to 1650km, considering the area of three regions. Our BRT models reduced Moran’s I value from a range of 0.19–0.50 for the raw virus data to 0.009–0.04 for the model residuals in the United States (A), 0.11–0.45 to –0.01–0.09 in China (B), 0.05–0.31 to –0.004–0.15 in Africa (C), suggesting that BRT models with 33 predictors have adequately accounted for spatial autocorrelations in the raw virus data in all three regions.

Appendix 3—figure 7
Relative contribution of predictors to human-infective RNA virus discovery in three regions.

Virus discovery data were matched to time-varying covariate data by year. (A) United States. (B) China. (C) Africa. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate boosted regression tree models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Appendix 3—figure 8
Relative contribution of predictors to human-infective RNA virus discovery in three regions.

Virus discovery data at year t were matched to time-varying covariate data at year t-1. (A) United States. (B) China. (C) Africa. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate boosted regression tree models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Appendix 3—figure 9
Distribution maps for 32 predictors in 2015 in the United States.

The values of these explanatory variables and latitude in each grid cell were used to predict the virus discovery in the corresponding grid cell in the Unites States in 2010–2019. Explanatory variables were log transformed where necessary to get better visualization, not meaning they entered the model by logged values.

Appendix 3—figure 10
Distribution maps for 32 predictors in 2015 in China.

The values of these explanatory variables and latitude in each grid cell were used to predict the virus discovery in the corresponding grid cell in China in 2010–2019. Explanatory variables were log transformed where necessary to get better visualization, not meaning they entered the model by logged values.

Appendix 3—figure 11
Distribution maps for 32 predictors in 2015 in Africa.

The values of these explanatory variables and latitude in each grid cell were used to predict the virus discovery in the corresponding grid cell in Africa in 2010–2019. Explanatory variables were log transformed where necessary to get better visualization, not meaning they entered the model by logged values.

Appendix 3—figure 12
Cumulative relative contribution of predictors to human-infective RNA virus discovery by group in each model of subgroups.

Subgroup 1 represents viruses firstly discovered from the region (United States or Africa); Subgroup 2 represents viruses firstly discovered elsewhere in the world. In the United States, virus count of Subgroup 1 and Subgroup 2 were 52 and 43, respectively. In Africa, virus count of Subgroup 1 and Subgroup 2 were 39 and 68, respectively. The relative contributions of all explanatory factors sum to 100% in each model, and each colour represents the cumulative relative contribution of all explanatory factors within each group.

Author response image 1
Relationship between published human-infective RNA virus count and total number of papers from the journals which published all human-infective RNA viruses in Web of Science.

A, total number of papers vs. published human virus count; B, total number of papers on viruses vs. published human virus count; C, total number of papers vs. total number of papers on viruses; D, Percent of papers on viruses in each journal. (J) Infect Dis (JID) is highlighted in blue.

Author response image 2
Relative contribution of predictors to human-infective RNA virus discovery in three regions.

Virus discovery data were matched to time-varying covariate data by year. (A) United States. (B) China. (C) Africa. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 3
Relative contribution of predictors to human-infective RNA virus discovery in three regions.

Virus discovery data at year t were matched to time-varying covariate data at year t-1. (A) United States. (B) China. (C) Africa. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 4
Correlation matrix for predictors.

Positive correlations are displayed in blue and negative correlations in red colour. Spearman’s rank correlation test was used. Colour intensity is proportional to the correlation coefficients.

Author response image 5
Relative contribution of predictors to human-infective RNA virus discovery in the United States by removing high-correlated predictors.

The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 6
Relative contribution of explanatory factors to human RNA virus discovery in the stratified model by transmissibility in Africa.

(A) Strictly zoonotic, (B) Transmissible in humans. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 7
Relative contribution of explanatory factors to human RNA virus discovery in the stratified model by transmission mode in Africa.

(A) Vector-borne, (B) Non-vector- borne. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 8
Relative contribution of explanatory factors to human RNA virus discovery in the stratified model by transmissibility in the United States.

(A) Strictly zoonotic, (B) Transmissible in humans. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers..

Author response image 9
Relative contribution of explanatory factors to human RNA virus discovery in the stratified model by transmission mode in the United States.

(A) Vector-borne, (B) Non-vector- borne. The boxplots show the median (black bar) and interquartile range (box) of the relative contribution across 1000 replicate models, with whiskers indicating minimum and maximum and black dots indicating outliers.

Author response image 10
Cumulative relative contribution of predictors to human-infective RNA virus discovery by group in each model of different regions.

The relative contributions of all explanatory factors sum to 100% in each model, and each colour represents the cumulative relative contribution of all explanatory factors within each group.

Tables

Appendix 1—table 1
Summary of the human-infective RNA virus data sets in the United States, Africa, and China.
SpeciesOriginal discovery yearUnited StatesChinaAfrica
Reported?Discovery yearlocationLatLonReported?Discovery yearlocationLatLonReported?Discovery yearlocationLatLon
Argentinian mammarenavirus1958NoNoNo
Brazilian mammarenavirus1994Yes Barry et al., 19951995New Haven, Connecticut41.31--72.93NoNo
Cali mammarenavirus1971Yes Buchmeier et al., 19741974Houston, Texas29.76--95.37NoNo
Chapare mammarenavirus2008NoNoNo
Guanarito mammarenavirus1991NoNoNo
Lassa mammarenavirus1970Yes Buckley and Casals, 19701970New Haven, Connecticut41.31--72.93NoYes Buckley and Casals, 19701970Lassa, Borno State, Nigeria10.6913.27
Lujo mammarenavirus2009NoNoYes Briese et al., 20092009Lusaka, Zambia--15.3928.32
Lymphocytic choriomeningitis mammarenavirus1934Yes Armstrong and Lillie, 19341934St. Louis county, Missouri38.61--90.41NoNo
Machupo mammarenavirus1964NoNoNo
Mobala mammarenavirus1985NoNoYes Georges et al., 19851985Bouboui and Gomoka village, Boali town, Central African Republic4.8918.14
Whitewater Arroyo mammarenavirus2000Yes Enserink, 20002000Alameda County, California37.60--121.72NoNo
Mamastrovirus 11975Yes Oshiro et al., 19811981Martin County, California40.22--123.10Yes Xu et al., 19811981Guangzhou, Guangdong23.13113.26Yes Dowling and Wynne, 19811981Lebowa, South Africa--23.529.5
Mamastrovirus 62008Yes Finkbeiner et al., 2009c2009St. Louis, Missouri38.63--90.20Yes Chu et al., 20102010Hong Kong22.40114.11Yes Kapoor et al., 20092009Maiduguri, Borno State, Nigeria11.8313.15
Mamastrovirus 82009Yes Finkbeiner et al., 2009a2009St. Louis, Missouri38.63--90.20Yes Wang et al., 20132013Nanjing, Jiangsu and Lanzhou, Gansu31.95118.78Yes Kapoor et al., 20092009Maiduguri, Borno State, Nigeria11.8313.15
Mamastrovirus 92009Yes Finkbeiner et al., 2009b2009Accomack and Northampton Counties, Virginia37.71--75.81Yes Tao et al., 20192019Jinan, Shandong36.68117.11Yes Kapoor et al., 20092009Maiduguri, Borno State, Nigeria11.8313.15
Mammalian 1 orthobornavirus1985Yes Rott et al., 19851985Philadelphia, Pennsylvania39.95--75.17Yes Chen et al., 19991999Taiwan23.70120.96Yes Bode et al., 19921992Rural area of East Africa--1.2834.53
Mammalian 2 orthobornavirus2015NoNoNo
Norwalk virus1972Yes Kapikian et al., 19721972Norwalk, Ohio41.24--82.62Yes Fang et al., 19951995Henan33.88113.48Yes Taylor et al., 19931993Pretoria, Gauteng province, South Africa--25.7528.23
Sapporo virus1980Yes Nakata et al., 19881988Houston, Texas29.76--95.37Yes Nakata et al., 19881988Shanghai31.23121.47Yes Wolfaardt et al., 19971997Pretoria, Gauteng province, South Africa--25.7528.23
Vesicular exanthema of swine virus1998Yes Smith et al., 19981998Corvallis, Oregon44.56--123.26NoNo
Alphacoronavirus 12007NoNoNo
Human coronavirus 229E1966Yes Hamre and Procknow, 19661966Chicago, Illinois41.88--87.63Yes Virus Research Group of Kun Number 323 Unit, The Chinese People’s Liberation Army, 19751975Kunming, Yunnan25.07102.68Yes Hays and Myint, 19981998Kumasi, Ghana6.70--1.62
Human coronavirus NL632004Yes Esper et al., 20052005New Haven, Connecticut41.31--72.93Yes Chan et al., 20052005Hong Kong22.40114.11Yes Smuts et al., 20082008Cape Town, Western Cape Province, South Africa--33.9018.57
Betacoronavirus 11967Yes McIntosh et al., 19671967Bethesda, Maryland38.98--77.09Yes Chan et al., 20052005Hong Kong22.40114.11Yes Venter et al., 20112011Pretoria, Gauteng province, South Africa--25.7528.23
Human coronavirus HKU12005Yes Esper et al., 20062006New Haven, Connecticut41.31--72.92Yes Woo et al., 20052005Hong Kong22.40114.11Yes Venter et al., 20112011Pretoria, Gauteng province, South Africa--25.7528.23
Middle East respiratory syndrome-related coronavirus2012Yes* Bialek et al., 20142014Lake county, Indiana41.45--87.37Yes* Gao and Song, 20152015Huizhou, Guangdong23.09114.40Yes* Abroug et al., 20142014Monastir, Tunisia35.7910.82
Severe acute respiratory syndrome-related coronavirus2003Yes* Charles M, 20032003Atlanta, Georgia33.75--84.39Yes Peiris et al., 2003a2003Hong Kong22.40114.11Yes Chiu et al., 20042004Pretoria, Gauteng province, South Africa--25.7528.23
Human torovirus (been abolished)1984NoNoNo
Bundibugyo ebolavirus2008NoNoYes Smuts et al., 20082008Bundibugyo and Kikyo town, Bundibugyo District, Western Uganda0.7130.06
Reston ebolavirus1991Yes Miranda et al., 19911991Reston, Fairfax County, Virginia38.96--77.35NoNo
Sudan ebolavirus1977NoNoYes Bowen et al., 19771977Maridi, South Sudan4.9129.45
Tai Forest ebolavirus1995NoNoYes Le Guenno et al., 19951995Abidjan, Cote-d’lvoire5.36--4.01
Zaire ebolavirus1977NoNoYes Johnson et al., 19771977Yambuku village, Democratic Republic of the Congo2.8322.22
Marburg marburgvirus1968Yes* Centers for Disease Control and Prevention, 20092009Denver county, Colorado39.55--105.78NoYes Gear et al., 19751975Johannesburg, South Africa--26.2027.90
Aroa virus1971NoNoNo
Bagaza virus2009NoNoNo
Banzi virus1959NoNoYes Smithburn et al., 19591959Maponde's Kraal(Usutu river), South Africa--26.5231.67
Cacipacore virus2011NoNoNo
Dengue virus1907Yes Lavinder and Francis, 19141914Savannah, Georgia32.02--81.12Yes Clarke et al., 19671967Southwest Taiwan23.06120.59Yes Edington, 19271927Durban, KwaZulu-Natal Province, South Africa--29.8631.02
Edge Hill virus1985NoNoNo
Gadgets Gully virus1991NoNoNo
Ilheus virus1947NoNoNo
Japanese encephalitis virus1933Yes* Perex-Pina and Merikangas, 19531953Waltham, Massachusetts42.38--71.24Yes Yen, 19411941Beijing40.01116.41Yes Simon-Loriere et al., 20172017Cunene, Angola--16.2815.28
Kokobera virus1964NoNoNo
Kyasanur forest disease virus1957NoYes Wang et al., 20092009Hengduanshan Mountain, Yunnan27.5099.00Yes Andayi et al., 20142014Djibouti, Republic of Djibouti11.5743.15
Langat virus1956NoNoNo
Louping ill virus1934Yes Rivers and Schwentker, 19341934New York40.71--74.01NoNo
Murray Valley encephalitis virus1952NoNoNo
Ntaya virus1952NoNoYes Smithburn, 19521952Bwamba county, Uganda0.7530.02
Omsk hemorrhagic fever virus1948NoNoNo
Powassan virus1959Yes Goldfield et al., 19731973Middlesex County, New Jersey40.54--74.37NoNo
Rio Bravo virus1962Yes Suklin et al., 19621962Dallas city, Texas32.78--96.80NoNo
Saint Louis encephalitis virus1933Yes Webster and Fite, 20091933St. Louis City, Missouri38.63--90.20NoNo
Tembusu virus1975NoYes Tang et al., 20132013Shandong36.40118.77No
Tick-borne encephalitis virus1938Yes* Cruse et al., 19791979Cleveland, Ohio41.51--81.69Yes Wang and Zhao, 19561956Bali village, Wuchang, Heilongjiang44.91127.16No
Uganda S virus1952NoNoYes Dick and Haddow, 19521952Bwamba county, Uganda0.7530.02
Usutu virus2009NoNoNo
Wesselsbron virus1957NoNoYes Smithburn et al., 19571957Lake Simbu region, Maputaland, KwaZulu-Natal, South Africa--27.3632.32
West Nile virus1940Yes Nash et al., 20012001New York40.71--74.01Yes Li et al., 20132013Jiashi County, Xinjiang39.5877.18Yes Smithburn et al., 19401940Omogo, West Nile district, Uganda0.4233.21
Yellow fever virus1901Yes Guiteras, 19041904Laredo, Texas27.51--99.51Yes* Chen and Lu, 20162016Beijing40.01116.41Yes Stokes et al., 19281928Larteh, Ghana5.94--0.07
Zika virus1952Yes* Foy et al., 20112011Northern Colorado39.55--105.78Yes* Sun et al., 20162016Gan County, Ganzhou city, Jiangxi25.86115.02Yes Dick, 19521952Zika, Uganda0.1232.53
Hepacivirus C1989Yes Choo et al., 19891989Emeryville, California37.83--122.29Yes Xu et al., 1990a1990Qidong county, Jiangsu31.88121.72Yes Kew et al., 19901990Johannesburg, South Africa--26.2027.90
Pegivirus C1995Yes Simons et al., 19951995Chapel Hill, North Carolina; Rochester, Minnesota; Dallas, Texas35.91--79.06Yes Wang et al., 19961996Beijing40.01116.41Yes Simons et al., 19951995Cairo, Egypt30.0431.24
Pegivirus H2015Yes Kapoor et al., 20152015New York city, New York40.71--74.01Yes Wang et al., 20182018Guangzhou, Guangdong23.13113.26Yes Rodgers et al., 20192019Ebolowa, Cameroon2.9211.15
Pestivirus A1988Yes Yolken et al., 19891989Whiteriver, Arizona33.83--109.97NoYes Giangaspero et al., 19881988Zambia--13.1327.85
Andes orthohantavirus1996NoNoNo
Bayou orthohantavirus1995Yes Morzunov et al., 19951995Louisiana30.98--91.96NoNo
Black creek canal orthohantavirus1995Yes Ravkov et al., 19951995Miami-Dade County, Florida25.76--80.34NoNo
Choclo orthohantavirus2000NoNoNo
Dobrava-Belgrade orthohantavirus1992NoNoNo
Hantaan orthohantavirus1978NoYes Lee et al., 19801980Zhejiang29.14119.79No
Laguna Negra orthohantavirus1997NoNoNo
Puumala orthohantavirus1980NoNoNo
Sangassou orthohantavirus2010NoNoYes Klempa et al., 20102010Sangassou village, Macenta district, Forest Guinea8.24--9.32
Seoul orthohantavirus1982Yes Forthal et al., 19871987Mississippi32.57--89.88Yes Song et al., 19821982Jiangsu33.14119.79Yes Tomori et al., 19861986Jos, Nigeria9.908.86
Sin Nombre orthohantavirus1993Yes Nichol et al., 19931993New Mexico34.52--105.87NoNo
Thailand orthohantavirus2006NoNoNo
Thottopalayam thottimvirus2007NoNoNo
Tula orthohantavirus1996NoNoNo
Orthohepevirus A1983Yes* De Cock et al., 19871987Los Angeles County, California34.05--118.24Yes Huang et al., 19891989Kashi county, Kashi city, Xinjiang39.4675.99Yes Belabbes et al., 19851985Medea town, Algeria36.262.75
Orthohepevirus C2018NoYes Sridhar et al., 20182018Hong Kong22.40114.11No
Crimean-Congo haemorrhagic fever orthonairovirus1967NoYes Yen et al., 19851985Bachu, southern Xinjiang39.7978.55Yes Simpson et al., 19671967Kisangani, Tshopo province, Democratic Republic of the Congo0.5325.19
Dugbe orthonairovirus1969NoNoYes Causey et al., 19691969Ibadan, Nigeria7.353.88
Nairobi sheep disease orthonairovirus1969NoNoYes Morrill et al., 19911991Mombasa; Malindi; and Kilifi, Coast Province, Kenya--3.3439.57
Thiafora orthonairovirus1989NoNoNo
Influenza A virus1933Yes Francis and Magill, 19351935Philadelphi, Pennsylvania39.95--75.17Yes Chang and Chiang, 19501950Beijing40.01116.41Yes Isaacs and Andrews, 19511951Johannesburg, South Africa and Cape Town, South Africa--26.2027.90
Influenza B virus1940Yes Francis, 19401940Irvington village, Greenburgh town, Westchester County, New York41.03--73.87Yes Wen and Chu, 19571957Beijing40.01116.41Yes Montefiore et al., 19701970Arusha, Arusha Region, Tanzania--3.3736.69
Influenza C virus1950Yes Francis et al., 19501950Ann Arbor city, Michigan42.28--83.74Yes Zhang, 19571957Beijing40.01116.41Yes Joosting et al., 19681968Johannesburg, South Africa--26.2027.90
Dhori thogotovirus1985NoNoNo
Thogoto thogotovirus1969NoNoYes Causey et al., 19691969Ibadan, Nigeria7.353.88
Avian orthoavulavirus 11943Yes Burnet, 19431943Washington, D. C.38.91--77.04NoNo
Hendra henipavirus1995NoNoNo
Nipah henipavirus1999NoNoNo
Canine morbillivirus1955Yes Karzon, 19551955Buffalo, New York42.89--78.88NoNo
Measles morbillivirus1911Yes Goldberger and Anderson, 19111911Washington, D. C.38.91--77.04Yes Tang et al., 19581958Beijing40.01116.41Yes Baylet et al., 19631963Dakar, Senegal14.72--17.47
Human respirovirus 11958Yes Chanock et al., 19581958Washington, D. C.38.91--77.04Yes Chen et al., 19641964Zhejiang29.14119.79Yes Taylor-Robinson and Tyrrell, 19631963Cape Town, Western Cape Province, South Africa--33.9018.57
Human respirovirus 31958Yes Chanock et al., 19581958Washington, D. C.38.91--77.04Yes Yu et al., 19871987Guangzhou, Guangdong23.13113.26Yes Taylor-Robinson and Tyrrell, 19631963Cape Town, Western Cape Province, South Africa--33.9018.57
Achimota pararubulavirus 22013NoNoYes Baker et al., 20132013Volta, Ghana6.050.37
Human orthorubulavirus 21956Yes Chanock, 19561956Cincinnati, Ohio39.10--84.51Yes Pathogen biology research group, Jiangsu new medical college, 19751975Nanjing, Jiangsu31.95118.78Yes Balestrieri et al., 19671967Accra, Ghana5.60--0.19
Human orthorubulavirus 41960Yes Johnson et al., 19601960Bethesda, Maryland38.98--77.09Yes Lau et al., 20052005Hong Kong22.40114.11Yes Niang et al., 20102010Ndiop village, Sine Saloum region, Senegal15.18--16.74
Mammalian orthorubulavirus 51959Yes Schultz and Habel, 19591959Stanford, California37.42--122.17NoNo
Menangle pararubulavirus1998NoNoNo
Mumps orthorubulavirus1934Yes Johnson and Goodpasture, 19341934Nashville, Tennessee36.16--86.78Yes Wang et al., 19581958Beijing40.01116.41Yes Bayer and Gear, 19551955Johannesburg, South Africa--26.2027.90
Simian orthorubulavirus1968NoNoNo
Sosuga pararubulavirus2014NoNoYes Albariño et al., 20142014ˉ3.7632.82
Tioman pararubulavirus2007NoNoNo
Bunyamwera orthobunyavirus1946Yes Work, 19641964Southern Florida26.92--81.21NoYes Smithburn et al., 19461946Bwamba County, Uganda0.7530.02
Bwamba orthobunyavirus1941NoNoYes Smithburn et al., 19411941Bwamba county, Western Province of Uganda0.7530.02
California encephalitis orthobunyavirus1952Yes Hammon and Reeves, 19521952Kern county, California35.49--118.86Yes Gu et al., 19841984Longhua, Shanghai31.22121.43Yes Bardos and Sefcovicova, 19611961Uganda1.3732.29
Caraparu orthobunyavirus1961NoNoNo
Catu orthobunyavirus1961NoNoNo
Guama orthobunyavirus1961NoNoNo
Guaroa orthobunyavirus1959NoNoNo
Kairi orthobunyavirus1967NoNoNo
Madrid orthobunyavirus1964NoNoNo
Marituba orthobunyavirus1961NoNoNo
Nyando orthobunyavirus1965NoNoYes Williams et al., 19651965Kisumu, Kenya--0.0934.77
Oriboca orthobunyavirus1961NoNoNo
Oropouche orthobunyavirus1961NoNoNo
Patois orthobunyavirus1972NoNoNo
Shuni orthobunyavirus1975NoNoYes Moore et al., 19751975Ibadan, Nigeria7.383.95
Tacaiuma orthobunyavirus1967NoNoNo
Wyeomyia orthobunyavirus1965NoNoNo
Candiru phlebovirus1983NoNoNo
Punta Toro phlebovirus1970NoNoNo
Rift Valley fever phlebovirus1931NoYes* Liu et al., 20162016Beijing40.01116.41Yes Daubney et al., 19311931Rift Valley of Kenya Colony--0.2836.07
Sandfly fever Naples phlebovirus1944NoNoYes Sabin, 19511951Cairo, Egypt30.0431.24
Heartland banyangvirus2012Yes McMullan et al., 20122012Andrew and Nodaway Counties, Missouri39.82--94.59NoNo
Huaiyangshan banyangvirus2011NoYes Zhang et al., 20112011Huaiyangshan31.37115.39No
Uukuniemi phlebovirus1970NoNoNo
Human picobirnavirus1988Yes Grohmann et al., 19931993Atlanta, Georgia33.75--84.39Yes Rosen et al., 20002000Lulong County, Hebei39.94116.94No
Equine rhinitis A virus1962NoNoNo
Foot-and-mouth disease virus1965NoYes Luo et al., 19991999Guangzhou23.13113.26Yes Donia and Youssef, 20022002Alexandria Governorate, Egypt30.7429.74
Cardiovirus A1947Yes Jonkers, 19611961New Orleans, Louisiana29.95--90.07Yes Feng et al., 20152015Changchun, Jilin43.87125.34Yes Dick and Best, 19481948Entebbe, Uganda0.0532.46
Cardiovirus B1963Yes Jones et al., 20072007San Diego, California32.72--117.16Yes Cheng et al., 2009a2009Lanzhou, Gansu36.06103.79Yes Zoll et al., 20092009Cameroon5.0312.40
Cosavirus A2008NoYes Dai et al., 20102010Shanghai31.23121.47Yes Kapusinszky et al., 20122012Maiduguri, Borno State, Nigeria11.8313.15
Cosavirus B2008NoYes Yang et al., 20162016Zhenjiang, Jiangsu32.19119.43No
Cosavirus D2008NoNoYes Kapusinszky et al., 20122012Maiduguri, Borno State, Nigeria11.8313.15
Cosavirus E2008NoNoYes Kapusinszky et al., 20122012Maiduguri, Borno State, Nigeria11.8313.15
Cosavirus F2012NoNoNo
Enterovirus A1949Yes Sickles and Dalldorf, 19491949New York43.30--74.22Yes Xiao et al., 19851985Tianjin39.34117.36Yes Bayer and Gear, 19551955Johannesburg, South Africa--26.2027.90
Enterovirus B1949Yes Sickles and Dalldorf, 19491949Wilmington39.74--75.54Yes Wu et al., 19601960Fuzhou, Fujian26.07119.30Yes Patz et al., 19531953Middelburg, Transvaal, South Africa--25.7729.46
Enterovirus C1909Yes Flexner and Lewis, 19091909New York city, New York40.71--74.01Yes Yen and Hsü, 19411941Bejing39.90116.41Yes Hudson and Lennette, 19331933Monrovia, Liberia6.29--10.76
Enterovirus D1967Yes Schieble et al., 19671967Berkeley, California37.87--122.27Yes Shanghai Eye and Skin Disease Prevention and Treatment Institute, 19791979Shanghai31.23121.47Yes Mirkovic et al., 19731973Morocco31.79--7.09
Enterovirus E1961Yes Moscovivci et al., 19611961Denver, Colorado39.74--104.99NoNo
Enterovirus H1965NoNoNo
Rhinovirus A1953Yes Price, 19561956Baltimore, Maryland39.29--76.61Yes Guangzhou Institute of Medicine and Health, 19751975Guangzhou, Guangdong23.13113.26Yes Taylor-Robinson, 19631963Cape Town, Western Cape Province, South Africa--33.9018.57
Rhinovirus B1960Yes Hamre and Procknow, 19611961Chicago, Illinois41.88--87.63Yes Xiang et al., 20082008Beijing40.01116.41Yes Briese et al., 20082008Pretoria, Gauteng province, South Africa--25.7528.23
Rhinovirus C2006Yes Lamson et al., 20062006New York city, New York40.71--74.01Yes Lau et al., 20072007Hong Kong22.40114.11Yes Briese et al., 20082008Pretoria, Gauteng province, South Africa--25.7528.23
Erbovirus A2005NoNoNo
Hepatovirus A1973Yes Feinstone et al., 19731973Bethesda, Maryland38.98--77.09Yes Microbiology Research Group of Shanghai First Medical College and Laboratory of Shanghai Sixth People’s Hospital, 19781978Shanghai31.23121.47Yes Szmuness et al., 19771977Dakar, Senegal14.72--17.47
Aichivirus A1991Yes Chhabra et al., 20132013Cincinnati, Ohio39.10--84.51Yes Yang et al., 20092009Shanghai31.23121.47Yes Sdiri-Loulizi et al., 20082008Monastir, Tunisia35.7710.82
Parechovirus A1958Yes Ramoz-alverz and Sabin, 19581958Cincinnati, Ohio39.10--84.51Yes Shan et al., 20092009Shanghai31.23121.47Yes Kapusinszky et al., 20122012Ouagadougou, Burkina Faso12.24--1.56
Parechovirus B2003NoNoNo
Salivirus A2009Yes Greninger et al., 20092009Northern California38.84--120.90Yes Shan et al., 20102010Shanghai31.23121.47Yes Li et al., 20092009Maiduguri, Borno State, Nigeria11.8313.15
Avian metapneumovirus2011Yes Kayali et al., 20112011Memphis, Tennessee35.15--90.05NoNo
Human metapneumovirus2001Yes Falsey et al., 20032003Rochester, New York43.16--77.61Yes Peiris et al., 2003b2003Hong Kong22.40114.11Yes Madhi et al., 20032003Johannesburg, South Africa--26.2027.90
Human orthopneumovirus1957Yes Chanock et al., 19571957Baltimore, Maryland39.29--76.61Yes Kun Number 323 Unit, the Chinese People’s Liberation Army, 19751975Kunming, Yunnan25.07102.68Yes Doggett, 19651965Cape Town, Western Cape Province, South Africa--33.9018.57
Colorado tick fever virus1946Yes Florio et al., 19461946Denver, Colorado39.74--104.99Yes Yang et al., 19961996Nanjing, Jiangsu31.95118.78No
Eyach virus1980NoNoNo
Corriparta virus1967NoNoNo
Great Island virus1963NoNoNo
Lebombo virus1975NoNoYes Moore et al., 19751975lbadan, Nigeria7.383.95
Orungo virus1976NoNoYes Tomori et al., 19761976Ibadan, Nigeria7.383.95
Mammalian orthoreovirus1954Yes Ramos-Alvarez and Sabin, 19541954Cincinnati, Ohio39.10--84.51Yes Zhao et al., 19951995Xuzhou, Jiangsu34.26117.19Yes Malherbe et al., 19631963Johannesburg, South Africa--26.2027.90
Nelson Bay orthoreovirus2007NoYes* Cheng et al., 2009b2009Hong Kong22.40114.11No
Rotavirus A1973Yes Kapikian et al., 19761976Washington, D. C.38.90--77.04Yes PaPa et al., 19791979Beijing40.01116.41Yes Tomori et al., 19761976Johannesburg, South Africa--26.2027.90
Rotavirus B1984Yes Eiden et al., 19851985Baltimore, Maryland39.29--76.61Yes Hung et al., 19841984Jinzhou, Liaoning41.10121.13Yes Nakata et al., 19871987Kenya--0.0237.91
Rotavirus C1986Yes Jiang et al., 19951995Providence, Rhode Island41.82--71.41Yes Qiao et al., 19991999Beijing40.01116.41Yes Sebata and Steele, 19991999Pretoria, Gauteng province, South Africa--25.7528.23
Rotavirus H1987NoYes Wang et al., 19871987Huaihua, Hunan Province27.55109.96No
Banna virus1990NoYes Xu et al., 1990b1990Xishuangbanna, Yunnan Province21.90100.80No
Primate T-lymphotropic virus 11980Yes Poiesz et al., 19801980Bethesda, Maryland38.98--77.09Yes Hung et al., 19841984Shenyang, Liaoing41.80123.38Yes Williams et al., 19841984Ibadan, Nigeria7.383.95
Primate T-lymphotropic virus 21982Yes Kalyanaraman et al., 19821982Seattle, Washington47.61--122.33Yes Ma et al., 20132013Henan and Hubei32.21112.96Yes Delaporte et al., 19911991Franceville, Gabon--1.6313.60
Primate T-lymphotropic virus 32005NoNoYes Calattini et al., 20052005Océan department, South Province, Cameroon2.5010.50
Human immunodeficiency virus 11983Yes Safai et al., 19841984Washington, D. C.38.90--77.04Yes Chang et al., 19861986Hong Kong22.40114.11Yes Brun-Vézinet et al., 19841984Kisangani, Tshopo province, Democratic Republic of the Congo0.5325.19
Human immunodeficiency virus 21986Yes* Centers for Disease Control, 19881988New Jersey40.06--74.41Yes* Yan et al., 20002000Fuzhou, Fujian26.07119.30Yes Kanki et al., 19861986Dakar, Senegal14.72--17.47
Simian immunodeficiency virus1992Yes Khabbaz et al., 19921992Atlanta, Georgia33.75--84.39NoYes Calattini et al., 20052005Cameroon7.3712.35
Central chimpanzee simian foamy virus2012NoNoYes Rua et al., 20122012Near Dja Nature Reserves, Southern Cameroon4.5013.50
Eastern chimpanzee simian foamy virus1971NoNoYes Achong et al., 19711971Kenya--0.0237.91
Grivet simian foamy virus1997NoNoNo
Guenon simian foamy virus2012NoNoYes Rua et al., 20122012Near lolodrof, Southern Cameroon3.2310.73
Taiwanese macaque simian foamy virus2002NoYes Huang et al., 20122012Yunnan25.18101.86No
Australian bat lyssavirus1998NoNoNo
Duvenhage lyssavirus1971NoNoYes Meredith et al., 19711971Pretoria, Gauteng province, South Africa--25.7528.23
European bat Yeslyssavirus1989NoNoNo
European bat 2 lyssavirus1986NoNoNo
Irkut lyssavirus2013NoYes Liu et al., 20132013Tonghua county, Jilin41.68125.76No
Mokola lyssavirus1972NoNoYes Familusi et al., 19721972Ibadan, Nigeria7.383.95
Rabies lyssavirus1903Yes Black and Powers, 19101910Southern California34.57--116.76Yes Wu, 19811981Beijing40.01116.41Yes Wilhelm and Alexis, 19331933Carolina, Mpumalanga, South Africa--26.0730.12
Bas-Congo tibrovirus2012NoNoYes Grard et al., 20122012Mangala village, Boma Bungu Health Zone, Democratic Republic of Congo (DRC)--4.0421.76
Ekpoma Yestibrovirus2015NoNoYes Stremlau et al., 20152015Irrua, Edo State, Nigeria6.746.22
Ekpoma 2 tibrovirus2015NoNoYes Stremlau et al., 20152015Irrua, Edo State, Nigeria6.746.22
Alagoas vesiculovirus1967NoNoNo
Chandipura vesiculovirus1967NoNoNo
Cocal vesiculovirus1964NoNoNo
Indiana vesiculovirus1958Yes Patterson et al., 19581958Beltsville, Prince George's County, Maryland39.05--76.90NoNo
Isfahan vesiculovirus1977NoNoNo
Maraba vesiculovirus1984NoNoNo
New Jersey vesiculovirus1950Yes Hanson et al., 19501950Madison, Wisconsin43.07--89.40NoNo
Piry vesiculovirus1974NoNoNo
Barmah Forest virus1986NoNoNo
Chikungunya virus1956Yes* Centers for Disease Control and Prevention, 20062006Minnesota46.44--93.36Yes Clarke et al., 19671967Southwest Taiwan23.06120.59Yes Ross, 19561956Newala district, Tanzania--10.6439.24
Eastern equine encephalitis virus1938Yes Howitt, 19381938Southwestern Massachusetts42.19--73.09NoNo
Everglades virus1970Yes Ehrenkranz et al., 19701970Homestead, Florida25.47--80.48NoNo
Getah virus1966NoYes Li et al., 19921992Baoting County, Hainan18.98109.83No
Highlands J virus2000Yes Meehan et al., 20002000Florida27.66--81.52NoNo
Madariaga virus1972NoNoNo
Mayaro virus1957Yes* Tesh et al., 19991999Ohio40.42--82.91NoNo
Mosso das Pedras virus2013NoNoNo
Mucambo virus1965NoNoNo
Ndumu virus1961NoNoYes Kokernot et al., 19611961Ndumu, Maputaland, KwaZulu-Natal, South Africa--26.9332.26
Onyong-nyong virus1961NoNoYes Williams and Woodall, 19611961Entebbe, Uganda0.0532.46
Pixuna virus1991NoNoNo
Rio Negro virus1993NoNoNo
Ross River virus1972NoYes Xu et al., 19991999Hainan19.16109.94No
Semliki Forest virus1979NoNoYes Mathiot et al., 19901990Bangui, Central Africa4.3618.58
Sindbis virus1955NoNoYes Taylor et al., 19551955Cairo, Egypt30.0431.24
Tonate virus1976NoNoNo
Una virus1963NoNoNo
Venezuelan equine encephalitis virus1943Yes Casals et al., 19431943New York40.71--74.01NoNo
Western equine encephalitis virus1938Yes Howitt, 19381938Fresno, California36.75--119.77NoNo
Whataroa virus1964NoNoNo
Rubella virus1942Yes Habel, 19421942Washington, D. C.38.91--77.04Yes He et al., 19791979Hangzhou, Zhejiang29.87119.33Yes Selzer, 19631963Cape Town, Western Cape Province, South Africa--33.9018.57
Hepatitis delta virus1977Yes Rizzetto et al., 19791979New Jersey40.06--74.41Yes Rizzetto et al., 19801980Taipei, Taiwan24.96121.51Yes Crocchiolo et al., 19841984Harare, Zimbabwe--17.8331.03
  1. Notes: Yes denotes the virus was ever discovered from the region; * denotes the virus was ever discovered from the region, but imported from other regions; No denotes the virus species has never been discovered from the region; The lat and long denote the coordidate of discovery points or centroids of polygons

Appendix 1—table 2
Resolution and covered grid cells for virus discovery data.
Polygon dataPoint dataTotal
Country levelState/Province levelCity/County level
United StatesVirus countsNA14 (14.7%)11 (11.6%)70 (73.7%)95
Gridded cell countsNA1891272*273
ChinaVirus countsNA22 (27.5%)47 (58.7%)11 (13.8%)80
Gridded cell countsNA1617012*243
Virus counts7 (6.5%)5 (4.7%)15 (14.0%)80 (74.8%)107
AfricaGridded cell counts307221780426
  1. *

    Grid cell counts here include viruses first detected in multiple points from the literature, NA, not applicable

Appendix 1—table 3
Model parameters.
ModelTree complexityLearning rateBag fractionNo. of trees
United States20.00200.51430
China20.00350.51473
Africa20.00300.51446
Appendix 1—table 4
Model validation statistics for analyses in three regions.
Model% of deviance explained (95% quantiles)ICC (95% quantiles)
United States50.5% (44.3%–56.8%)0.66 (0.60–0.70)
China42.0% (32.4%–50.8%)0.52 (0.41–0.60)
Africa42.4% (34.2%–50.0%)0.51 (0.44–0.62)
  1. ICC, intraclass correlation coefficient

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  1. Feifei Zhang
  2. Margo Chase-Topping
  3. Chuan-Guo Guo
  4. Mark EJ Woolhouse
(2022)
Predictors of human-infective RNA virus discovery in the United States, China, and Africa, an ecological study
eLife 11:e72123.
https://doi.org/10.7554/eLife.72123