Mosquito-transmitted arboviruses constitute a large proportion of emerging infectious diseases that are both a public health problem and a threat to animal populations. Many such viruses were identified in East Africa, a region where they remain important and from where new arboviruses may emerge. We set out to describe and review the relevant mosquito-borne viruses that have been identified specifically in Uganda. We focused on the discovery, burden, mode of transmission, animal hosts and clinical manifestation of those previously involved in disease outbreaks. A search for mosquito-borne arboviruses detected in Uganda was conducted using search terms ‘Arboviruses in Uganda’ and ‘Mosquitoes and Viruses in Uganda’ in PubMed and Google Scholar in 2020. Twenty-four mosquito-borne viruses from different animal hosts, humans and mosquitoes were documented. The majority of these were from family Peribunyaviridae, followed by Flaviviridae, Togaviridae, Phenuiviridae and only one each from family Rhabdoviridae and Reoviridae. Sixteen (66.7 %) of the viruses were associated with febrile illnesses. Ten (41.7 %) of them were first described locally in Uganda. Six of these are a public threat as they have been previously associated with disease outbreaks either within or outside Uganda. Historically, there is a high burden and endemicity of arboviruses in Uganda. Given the many diverse mosquito species known in the country, there is also a likelihood of many undescribed mosquito-borne viruses. New generation diagnostic platforms have great potential to identify new viruses. Indeed, four novel viruses, two of which were from humans (Ntwetwe and Nyangole viruses) and two from mosquitoes (Kibale and Mburo viruses) including the 2010 yellow fever virus (YFV) outbreak were identified in the last decade using next generation sequencing. Given the unbiased approach of detection of viruses by this technology, its use will undoubtedly be critically important in the characterization of mosquito viromes which in turn will inform other diagnostic efforts.
Hrnjaković CvjetkovićIB,
CvjetkovićD,
PatićA,
NikolićN,
Stefan MikićS et al. Chikungunya - a serious threat for public health. Med Pregl2015; 68:122–125 [View Article] [PubMed]
TheilerM,
DownsWG.
The arthropod-borne viruses of vertebrates. In An Account of the Rockefeller Foundation Virus Program, 1951-1970. the Arthropod-Borne Viruses of Vertebrates an Account of the Rockefeller Foundation Virus Program, 1951-19701973
AbudurexitiA,
AdkinsS,
AliotoD,
AlkhovskySV,
Avšič-ŽupancT et al. Taxonomy of the order Bunyavirales: update 2019. Arch Virol2019; 164:1949–1965 [View Article] [PubMed]
KarabatsosN.
International Catalogue of Arboviruses, Including Certain Other Viruses of Vertebrates, American Society of Tropical Medicine and Hygiene San Antonio, TX: 1985
KiryaBG.
A yellow fever epizootic in Zika forest, Uganda, during 1972: Part 1: Virus isolation and sentinel monkeys. Trans R Soc Trop Med Hyg1977; 71:254–260 [View Article] [PubMed]
KokernotR,
SmithburnK,
De MeillonB,
PatersonH.
Isolation of Bunyamwera Virus from a naturally infected human being and further isolations from Aedes (Banksinelld) circumluteolus Theo. Am J Trop Med Hyg1958; 7:579–584 [View Article]
DickGW,
HaddowAJ.
Uganda S virus; a hitherto unrecorded virus isolated from mosquitoes in Uganda. I. Isolation and pathogenicity. Trans R Soc Trop Med Hyg1952; 46:600–618 [View Article] [PubMed]
DickG.
Epidemiological Notes on Some Viruses isolated in Uganda (Yellow Fever, Rift Valley Fever, Bwamba Fever, West Nile, Mengo, Semliki Forast, Bunyamwera, Ntaya, Uganda S and Zika Viruses. Trans R Soc Trop Med Hyg1953; 47:13–43 [View Article] [PubMed]
CarringtonLB,
WillsB.
Lessons from history: viral surveillance in 1940s East Africa: Epidemiological notes on some viruses isolated in Uganda, GWA Dick. Trans R Soc Trop Med Hyg1953; 47:13–48
CrabtreeMB,
KadingRC,
MutebiJP,
LutwamaJJ,
MillerBR.
Identification of host blood from engorged mosquitoes collected in western Uganda using cytochrome oxidase I gene sequences. J Wildl Dis2013; 49:611–626 [View Article] [PubMed]
EdridgeAW,
DeijsM,
NamazziR,
CristellaC,
JebbinkMF et al. Novel orthobunyavirus identified in the cerebrospinal fluid of a Ugandan child with severe encephalopathy. Clin Infect Dis2019; 68:139–142 [View Article] [PubMed]
McMullanLK,
FraceM,
SammonsSA,
ShoemakerT,
BalinandiS et al. Using next generation sequencing to identify yellow fever virus in Uganda. Virology2012; 422:1–5 [View Article] [PubMed]
WilliamsM,
WoodallJ.
O’nyong-nyong fever: an epidemic virus disease in East Africa. II. Isolation and some properties of the virus. Trans R Soc Trop Med Hyg1961; 55:135–141 [View Article] [PubMed]
HaddowAJ,
WilliamsMC,
WoodallJP,
SimpsonDI,
GomaLK.
Twelve Isolations of Zika Virus from Aedes (Stegomyia) Africanus (Theobald) Taken in and above a Uganda Forest. Bull World Health Organ1964; 31:57–69 [PubMed]
LanciottiRS,
LudwigML,
RwagumaEB,
LutwamaJJ,
KramTM et al. Emergence of epidemic O’nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology1998; 252:258–268 [View Article] [PubMed]
LutwamaJJ,
RwagumaEB,
NawangaPL,
MukuyeA.
Isolations of Bwamba virus from south central Uganda and north eastern Tanzania. Afr Health Sci2002; 2:24–28 [PubMed]
ShoemakerTR,
NyakarahukaL,
BalinandiS,
OjwangJ,
TumusiimeA et al. First laboratory-confirmed outbreak of human and animal rift valley fever virus in Uganda in 48 years. Am J Trop Med Hyg2019; 100:659–671 [View Article] [PubMed]
McCraeAW,
HendersonBE,
KiryaBG,
SempalaSD.
Chikungunya virus in the Entebbe area of Uganda: isolations and epidemiology. Trans R Soc Trop Med Hyg1971; 65:152–168 [View Article] [PubMed]
SimpsonDI,
HaddowAJ,
WilliamsMC,
WoodallJP.
Yellow fever in central Uganda, 1964. Iv. Investigations on blood-sucking diptera and monkeys. Trans R Soc Trop Med Hyg1965; 59:449–458 [View Article] [PubMed]
WeinbrenMP,
HaddowAJ,
WilliamsMC.
The occurrence of Chikungunya virus in Uganda. I. Isolation from mosquitoes. Trans R Soc Trop Med Hyg1958; 52:253–257 [View Article] [PubMed]
WamalaJF,
MalimboM,
OkotCL,
Atai-OmorutoAD,
TenywaE et al. Epidemiological and laboratory characterization of a yellow fever outbreak in northern Uganda, October 2010–January 2011. Int J Infect Dis2012; 16: e536–e542 [View Article] [PubMed]
GonzalesJ,
GeorgesA.
Bunyaviral fevers: Bunyamwera, Ilesha, Germiston, Bwamba, and Tataguine. In The arboviruses: Epidemiology and ecology Vol 21988 pp 87–98
SmithburnK.
Neutralizing antibodies against certain recently isolated viruses in the sera of human beings residing in East Africa. J Immunol1952; 69:223–234 [PubMed]
WorkTH,
HurlbutHS,
TaylorR.
Indigenous wild birds of the Nile Delta as potential West Nile virus circulating reservoirs. Am J Trop Med Hyg1955; 4:872–888 [View Article] [PubMed]
WoodallJP,
GillettJD,
CorbetPS,
WeinbrenMP,
WilliamsMC.
The isolation of West Nile virus from the bird-biting mosquito Mansonia metallica in Uganda. Ann Trop Med Parasitol1961; 55:398–402 [View Article] [PubMed]
WilliamsMC,
SimpsonDI,
HaddowAJ,
KnightEM.
The isolation of West Nile virus from man and of Usutu virus from the bird-biting mosquito Mansonia aurites (Theobald) in the Entebbe area of Uganda. Ann Trop Med Parasitol1964; 58:367–374 [View Article] [PubMed]
HaddowA,
SmithburnK,
MahaffyA,
BugherJ.
Monkeys in relation to yellow fever in Bwamba County, Uganda. Trans R Soc Trop Med Hyg1947; 40:677–700 [View Article]
KotsakioziP,
EvansBR,
Gloria‐SoriaA,
KamgangB,
MayanjaM et al. Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa. Ecol Evol2018; 8:7835–7848 [View Article]
SmithburnKC,
HaddowAJ,
LumsdenWH.
An outbreak of sylvan yellow fever in Uganda with Aedes (Stegomyia) Africanus Theobald as principal vector and insect host of the virus. Ann Trop Med Parasitol1949; 43:74–89 [View Article] [PubMed]
LumsdenW,
BuxtonA.
A study of the epidemiology of yellow fever in West Nile District, Uganda. Trans R Soc Trop Med Hyg1951; 45:53–78 [View Article] [PubMed]
TullochJ,
PatelK.
Yellow fever in central Uganda, 1964. Part II. Report of a fatal case. Trans R Soc Trop Med Hyg1965; 59:441–443 [View Article] [PubMed]
HendersonBE,
CheshirePP,
KiryaGB,
LuleM.
Immunologic studies with yellow fever and selected African group B arboviruses in rhesus and vervet monkeys. Am J Trop Med Hyg1970; 19:110–118 [View Article] [PubMed]
HaddowA,
DickG,
LumsdenW,
SmithburnK.
Monkeys in relation to the epidemiology of yellow fever in Uganda. Trans R Soc Trop Med Hyg1951; 45:189–224 [View Article] [PubMed]
KiryaB,
OkiaN.
A yellow fever epizootic in Zika Forest, Uganda, during 1972: Part 2: Monkey serology. Trans R Soc Trop Med Hyg1977; 71:300–303 [View Article] [PubMed]
KwagonzaL,
MasiiraB,
Kyobe-BosaH,
KadoberaD,
AtuheireEB et al. Outbreak of yellow fever in central and southwestern Uganda, February-may 2016. BMC Infect Dis2018; 18:548 [View Article] [PubMed]
GillettJ.
Further studies on the biting behaviour of Aëdes (Stegomyia) simpsoni Theobald in Uganda. Ann Trop Med Parasitol1955; 49:154–157 [View Article]
MukwayaLG.
Host preference in Aedes simpsoni (Theo.) (Diptera, Culicidae) with special reference to the anthropophilic and non-anthropophilic forms in Uganda. Bull Entomol Res2009; 64:129–139 [View Article]
BoyerS,
CalvezE,
Chouin-CarneiroT,
DialloD,
FaillouxA-. B.
An overview of mosquito vectors of Zika virus. Microbes Infect2018; 20:646–660 [View Article] [PubMed]
WeinbrenM,
WilliamsM.
Zika virus: further isolations in the Zika area, and some studies on the strains isolated. Trans R Soc Trop Med Hyg1958; 52:263–268 [View Article] [PubMed]
HaddowA,
WilliamsM,
WoodallJ,
SimpsonD,
GomaL.
Twelve isolations of Zika virus from AEDES (Stegomyia) Africanus (Theobald) taken in and above a Uganda forest. Bull World Health Organ1964; 31:57–69 [PubMed]
KayiwaJT,
NankyaAM,
AtalibaIJ,
MosselEC,
CrabtreeMB et al. Confirmation of Zika virus infection through hospital-based sentinel surveillance of acute febrile illness in Uganda, 2014-2017. J Gen Virol2018; 99:1248–1252 [View Article] [PubMed]
LaavanyaVP,
JayasuryaR,
KavithaN,
PrabakaranG,
JayakumariS.
A review on microcephaly associated with zika fever in new born babies. Res J Pharm Technol2017; 10:337 [View Article]
KrauerF,
RiesenM,
ReveizL,
OladapoOT,
Martínez-VegaR et al. Zika virus infection as a cause of congenital brain abnormalities and Guillain–Barré syndrome: systematic review. PLoS Med2017; 14:e1002203 [View Article] [PubMed]
DaubneyR,
HudsonJR,
GarnhamPC.
Enzootic hepatitis or rift valley fever. An undescribed virus disease of sheep cattle and man from East Africa. J Pathol1931; 34:545–579 [View Article]
Van den BerghC.
Rift Valley Fever Virus Circulation in Livestock and Wildlife, and Population Dynamics of Potential Vectors, in Northern Kwazulu-Natal South Africa: University of Pretoria; 2019
MohamedM,
MoshaF,
MghambaJ,
ZakiSR,
ShiehWJ et al. Epidemiologic and clinical aspects of a Rift Valley fever outbreak in humans in Tanzania, 2007. Am J Trop Med Hyg2010; 83:22–27 [View Article] [PubMed]
PowersAM,
BraultAC,
TeshRB,
WeaverSC.
Re-emergence of Chikungunya and O’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol2000; 81:471–479 [View Article]
RodhainF,
GonzalezJP,
MercierE,
HelynckB,
LarouzeB et al. Arbovirus infections and viral haemorrhagic fevers in Uganda: a serological survey in Karamoja district, 1984. Trans R Soc Trop Med Hyg1989; 83:851–854 [View Article] [PubMed]
ClementsTL,
RossiCA,
IrishAK,
KibuukaH,
EllerLA et al. Chikungunya and O’nyong-nyong Viruses in Uganda: Implications for Diagnostics. In Open Forum Infectious Diseases Vol 6 Oxford University Press US; 2019 p ofz001 [View Article] [PubMed]
KalundaM,
Lwanga-SsoziC,
LuleM,
MukuyeA.
Isolation of Chikungunya and Pongola viruses from patients in Uganda. Trans R Soc Trop Med Hyg1985; 79:567567 [View Article] [PubMed]
ZellerH,
Van BortelW,
SudreB.
Chikungunya: its history in Africa and Asia and its spread to new regions in 2013–2014. J Infect Dis2016; 214:S436–S440 [View Article]
WilliamsM,
WoodallJ,
CorbetPS,
GillettJ.
O’nyong-nyong fever: an epidemic virus disease in East Africa. VIII. Virus isolations from Anopheles mosquitoes. Trans R Soc Trop Med Hyg1965; 59:
VanlandinghamDL,
HongC,
KlinglerK,
TsetsarkinK,
McElroyKL et al. Differential infectivities of o’nyong-nyong and chikungunya virus isolates in Anopheles gambiae and Aedes aegypti mosquitoes. Am J Trop Med Hyg2005; 72:616–621 [View Article] [PubMed]
HaddowA,
DaviesC,
WalkerA.
O’nyong-nyong fever: an epidemic virus disease in East Africa. I. Introduction. In Transactions of the Royal Society of Tropical Medicine and Hygiene Vol 54(61960
KiwanukaN,
SandersEJ,
RwagumaEB,
KawamataJ,
SsengoobaFP et al. O’nyong-nyong fever in south-central Uganda, 1996-1997: clinical features and validation of a clinical case definition for surveillance purposes. Clin Infect Dis1999; 29:1243–1250 [View Article] [PubMed]
KayiwaJT,
NankyaAM,
AtalibaIJ,
MosselEC,
CrabtreeMB et al. Confirmation of Zika virus infection through hospital-based sentinel surveillance of acute febrile illness in Uganda, 2014-2017. J Gen Virol2018; 99:1248–1252 [View Article] [PubMed]
SteinhagenK,
ProbstC,
RadzimskiC,
Schmidt-ChanasitJ,
EmmerichP et al. Serodiagnosis of Zika virus (ZIKV) infections by a novel ns1-based elisa devoid of cross-reactivity with dengue virus antibodies: A multicohort study of assay performance, 2015 to 2016. Euro Surveill2016; 21:50–30426 [View Article]
BrinkmannA,
NitscheA,
KohlC.
Viral metagenomics on blood-feeding arthropods as a tool for human disease surveillance. Int J Mol Sci2016; 17:10 [View Article]
JeromeH,
TaylorC,
SreenuVB,
KlymenkoT,
FilipeADS et al. Metagenomic next-generation sequencing aids the diagnosis of viral infections in febrile returning travellers. J Infect2019; 79:383–388 [View Article]
Osei‐PokuJ,
MbogoC,
PalmerW,
JigginsF.
Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from K enya. Mol Ecol2012; 21:5138–5150
WilliamsMC,
WoodallJP,
CorbetPS,
GillettJD.
O’nyong-Nyong eever: an epidemic virus disease in East Africa. 8. virus isolations from Anopheles mosquitoes. Trans R Soc Trop Med Hyg1965; 59:300–306 [View Article] [PubMed]
NyakarahukaL,
Ade S,
PurpuraL,
ErvinE,
BalinandiS et al. Prevalence and risk factors of rift valley fever in humans and animals from Kabale District in southwestern Uganda, 2016. PLoS Negl Trop Dis2018; 12:e0006412 [View Article]
MoniniM,
FalconeE,
BusaniL,
RomiR,
RuggeriFM.
West nile virus: characteristics of an african virus adapting to the third millennium world. Open Virol J2010; 4:42–51 [View Article] [PubMed]
AlthouseBM,
GuerboisM,
CummingsDA,
DiopOM,
FayeO et al. Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal. Nat Commun2018; 9:1–10 [View Article]
Bosco-LauthAM,
HartwigAE,
BowenRA.
Reptiles and amphibians as potential reservoir hosts of Chikungunya virus. Am J Trop Med Hyg2018; 98:841–844 [View Article] [PubMed]
MathiotCC,
GrimaudG,
GarryP,
BouquetyJC,
MadaA et al. An outbreak of human Semliki Forest virus infections in Central African Republic. Am J Trop Med Hyg1990; 42:386–393 [View Article] [PubMed]
AtkinsGJ,
SheahanBJ,
LiljeströmP.
The molecular pathogenesis of Semliki forest virus: A model virus made useful?. J Gen Virol1999; 80:2287–2297 [View Article]
KadingRC,
KityoRM,
MosselEC,
BorlandEM,
NakayikiT et al. Neutralizing antibodies against flaviviruses, babanki virus, and rift valley fever virus in ugandan bats. Infect Ecol Epidemiology2018; 8:1439215
LaineM,
LuukkainenR,
ToivanenA.
Sindbis viruses and other alphaviruses as cause of human arthritic disease. J Intern Med2004; 256:457–471 [View Article] [PubMed]
WoodallJP,
WilliamsMC,
CorbetPS,
HaddowAJ.
The isolation of Sindbis virus from the mosquito Mansonia (Coquillettidia) Fuscopennata (theobald) in Uganda. Ann Trop Med Parasitol1964; 58:383–389 [View Article] [PubMed]
KokernotR,
SmithburnK,
PatersonH,
McIntoshB.
Isolation of Germiston virus, a hitherto unknown agent, from culicine mosquitoes, and a report of infection in two laboratory workers. Am J Trop Med Hyg1960; 9:62–69 [View Article] [PubMed]
DialloM,
NabethP,
BaK,
SallA,
BaY et al. Mosquito vectors of the 1998–1999 outbreak of Rift Valley Fever and other arboviruses (Bagaza, Sanar, Wesselsbron and West Nile) in Mauritania and Senegal. Med Vet Entomol2005; 19:119–126 [View Article] [PubMed]