1887

Abstract

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 , followed by , , and only one each from family and . 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. Next 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) 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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001680
2021-10-05
2021-10-20
Loading full text...

Full text loading...

References

  1. Bouree P. A New Pandemic: Zika Virus Infection. Rev Prat 2016; 66:641–647 [PubMed]
    [Google Scholar]
  2. Cugola FR, Fernandes IR, Russo FB, Freitas BC, Dias JL et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 2016; 534:267–271 [View Article] [PubMed]
    [Google Scholar]
  3. Hayes CG. West Nile virus: Uganda, 1937, to New York City, 1999. Ann N Y Acad Sci 2001; 951:25–37 [View Article] [PubMed]
    [Google Scholar]
  4. McCrae AW, Kirya BG. Yellow fever and Zika virus epizootics and enzootics in Uganda. Trans R Soc Trop Med Hyg 1982; 76:552–562 [View Article] [PubMed]
    [Google Scholar]
  5. Hrnjakovic Cvjetkovic IB, Cvjetkovic D, Patic A, Nikolic N, Stefan Mikic S et al. Chikungunya - a Serious Threat for Public Health. Med Pregl 2015; 68:122–125 [View Article] [PubMed]
    [Google Scholar]
  6. Theiler M, Downs WG. The arthropod-borne viruses of vertebrates. An account of the Rockefeller Foundation virus program, 1951-1970. The arthropod-borne viruses of vertebrates An account of The Rockefeller Foundation Virus Program; 1973
  7. Abudurexiti A, Adkins S, Alioto D, Alkhovsky SV, Avšič-Županc T et al. Taxonomy of the order Bunyavirales: update 2019. Arch Virol 2019; 164:1949–1965 [View Article] [PubMed]
    [Google Scholar]
  8. Karabatsos N. International catalogue of arboviruses, including certain other viruses of vertebrates, American Society of Tropical Medicine and Hygiene San Antonio, TX: 1985
    [Google Scholar]
  9. Kirya BG. A yellow fever epizootic in Zika forest, Uganda, during 1972: Part 1: Virus isolation and sentinel monkeys. Trans R Soc Trop Med Hyg 1977; 71:254–260 [View Article] [PubMed]
    [Google Scholar]
  10. Mahaffy A, Smithburn K, Jacobs H, Gillett J. Yellow fever in western Uganda. Trans R Soc Trop Med Hyg 1942; 36:9–20 [View Article]
    [Google Scholar]
  11. Sempala SD. Institute profile: the Uganda virus research institute. Trends Microbiol 2002; 10:346–348 [View Article] [PubMed]
    [Google Scholar]
  12. Smithburn K, Mahaffy A, Paul J. Bwamba fever and its causative virus. The American Journal of Tropical Medicine and Hygiene 1941; 1:75–90
    [Google Scholar]
  13. Smithburn K, Hughes T, Burke A, Paul J. A neurotropic virus isolated from the blood of a native of Uganda1. Am J Trop Med Hyg 1940; 1:471–492
    [Google Scholar]
  14. Smithburn K, Haddow A, Mahaffy A. A neurotropic virus isolated from Aedes mosquitoes caught in the Semliki forest. Am J Trop Med Hyg 1946; 1:189–208
    [Google Scholar]
  15. Smithburn K. A hitherto unknown agent isolated from mosquitoes collected in Uganda. Proc Soc Exp Biol Med 1951; 77:130–133 [View Article] [PubMed]
    [Google Scholar]
  16. Kokernot R, Smithburn K, De Meillon B, Paterson H. Isolation of Bunyamwera Virus from a Naturally Infected Human Being and Further Isolations from Aedes (Banksinelld) circumluteolus Theo. American Journal of Tropical Medicine and Hygiene 1958; 7:579–584
    [Google Scholar]
  17. Smithburn K, Haddow A. Semliki Forest virus: I. Isolation and pathogenic properties. The Journal of Immunology 1944; 49:141–157
    [Google Scholar]
  18. Dick GW, Haddow AJ. Uganda S virus; a hitherto unrecorded virus isolated from mosquitoes in Uganda. I. Isolation and pathogenicity. Trans R Soc Trop Med Hyg 1952; 46:600–618 [View Article] [PubMed]
    [Google Scholar]
  19. Dick G. 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 Hyg 1953; 47:13–43 [View Article] [PubMed]
    [Google Scholar]
  20. Carrington LB, Wills B. Lessons from history: viral surveillance in 1940s East Africa: Epidemiological notes on some viruses isolated in Uganda, GWA Dick, Transactions of the Royal Society of Tropical Medicine and Hygiene, 1953; 47 (1): 13–48. Transactions of The Royal Society of Tropical Medicine and Hygiene. 112413–414
  21. Crabtree MB, Kading RC, Mutebi JP, Lutwama JJ, Miller BR. Identification of host blood from engorged mosquitoes collected in western Uganda using cytochrome oxidase I gene sequences. J Wildl Dis 2013; 49:611–626 [View Article] [PubMed]
    [Google Scholar]
  22. Al-Qahtani AA, Nazir N, Al-Anazi MR, Rubino S, Al-Ahdal MN. Zika virus: a new pandemic threat. J Infect Dev Ctries 2016; 10:201–207 [View Article] [PubMed]
    [Google Scholar]
  23. Chancey C, Grinev A, Volkova E, Rios M. The global ecology and epidemiology of West Nile virus. Biomed Res Int 2015; 2015:376230 [View Article] [PubMed]
    [Google Scholar]
  24. Marklewitz M, Zirkel F, Rwego IB, Heidemann H, Trippner P et al. Discovery of a unique novel clade of mosquito-associated bunyaviruses. J Virol 2013; 87:12850–12865 [View Article] [PubMed]
    [Google Scholar]
  25. Edridge AW, Deijs M, Namazzi R, Cristella C, Jebbink MF et al. Novel orthobunyavirus identified in the cerebrospinal fluid of a Ugandan child with severe encephalopathy. Clin Infect Dis 2019; 68:139–142 [View Article] [PubMed]
    [Google Scholar]
  26. Ramesh A, Nakielny S, Hsu J, Kyohere M, Byaruhanga O et al. Metagenomic next-generation sequencing of samples from pediatric febrile illness in Tororo, Uganda. PloS one 2019; 14:e0218318 [View Article] [PubMed]
    [Google Scholar]
  27. McMullan LK, Frace M, Sammons SA, Shoemaker T, Balinandi S et al. Using next generation sequencing to identify yellow fever virus in Uganda. Virology 2012; 422:1–5 [View Article] [PubMed]
    [Google Scholar]
  28. Williams M, Woodall J. O’nyong-nyong fever: an epidemic virus disease in East Africa. II. Isolation and some properties of the virus. Trans R Soc Trop Med Hyg 1961; 55:135–141 [View Article] [PubMed]
    [Google Scholar]
  29. Dick G, Kitchen S, Haddow A. Zika virus (I). Isolations and serological specificity. Trans R Soc Trop Med Hyg 1952; 46:509–520 [View Article] [PubMed]
    [Google Scholar]
  30. Tomori O, Fabiyi A, Murphy F. Characterization of Orungo virus, an orbivirus from Uganda and Nigeria. Arch Virol 1976; 51:285–298 [View Article] [PubMed]
    [Google Scholar]
  31. Haddow AJ, Williams MC, Woodall JP, Simpson DI, Goma LK. Twelve Isolations of Zika Virus from Aedes (Stegomyia) Africanus (Theobald) Taken in and above a Uganda Forest. Bull World Health Organ 1964; 31:57–69 [PubMed]
    [Google Scholar]
  32. Lanciotti RS, Ludwig ML, Rwaguma EB, Lutwama JJ, Kram TM et al. Emergence of epidemic O’nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology 1998; 252:258–268 [View Article] [PubMed]
    [Google Scholar]
  33. Lutwama JJ, Rwaguma EB, Nawanga PL, Mukuye A. Isolations of Bwamba virus from south central Uganda and north eastern Tanzania. Afr Health Sci 2002; 2:24–28 [PubMed]
    [Google Scholar]
  34. Shoemaker TR, Nyakarahuka L, Balinandi S, Ojwang J, Tumusiime A et al. First Laboratory-Confirmed Outbreak of Human and Animal Rift Valley Fever Virus in Uganda in 48 Years. Am J Trop Med Hyg 2019; 100:659–671 [View Article] [PubMed]
    [Google Scholar]
  35. Shakib K. Epidemic of Zika virus and maxillofacial surgery. Br J Oral Maxillofac Surg 2016; 54:355–357 [View Article] [PubMed]
    [Google Scholar]
  36. Lumsden WH. The yellow fever vector situation with reference to Entebbe airport. Bull World Health Organ 1954; 11:485–487 [PubMed]
    [Google Scholar]
  37. McCrae AW, Henderson BE, Kirya BG, Sempala SD. Chikungunya virus in the Entebbe area of Uganda: isolations and epidemiology. Trans R Soc Trop Med Hyg 1971; 65:152–168 [View Article] [PubMed]
    [Google Scholar]
  38. Simpson DI, Haddow AJ, Williams MC, Woodall JP. Yellow Fever in Central Uganda, 1964. Iv. Investigations on Blood-Sucking Diptera and Monkeys. Trans R Soc Trop Med Hyg 1965; 59:449–458 [View Article] [PubMed]
    [Google Scholar]
  39. Weinbren MP, Haddow AJ, Williams MC. The occurrence of Chikungunya virus in Uganda. I. Isolation from mosquitoes. Trans R Soc Trop Med Hyg 1958; 52:253–257 [View Article] [PubMed]
    [Google Scholar]
  40. Wamala JF, Malimbo M, Okot CL, Atai-Omoruto AD, Tenywa E et al. Epidemiological and laboratory characterization of a yellow fever outbreak in northern Uganda, October 2010-January 2011. Int J Infect Dis 2012; 16:e536–42 [View Article] [PubMed]
    [Google Scholar]
  41. Gonzales J, Georges A. Bunyaviral fevers: Bunyamwera, Ilesha, Germiston, Bwamba, and Tataguine. The arboviruses: epidemiology and ecology 1988; 2:87–98
    [Google Scholar]
  42. Smithburn K. Neutralizing antibodies against certain recently isolated viruses in the sera of human beings residing in East Africa. J Immunol 1952; 69:223–234 [PubMed]
    [Google Scholar]
  43. Taylor R, Work T, Hurlbut H, Rizk F. A Study of the Ecology of West Nile Virus in Egypt1. Am J Trop Med Hyg 1956; 5:579–620 [View Article] [PubMed]
    [Google Scholar]
  44. Williams M. Virological studies on birds 1957 pp 1956–1957
    [Google Scholar]
  45. Williams M. Collection of sera from wild birds and neutralization tests with bird sera. Rep E Afr Virus Res Inst 1955; 1956:31–32
    [Google Scholar]
  46. Work TH, Hurlbut HS, Taylor R. Indigenous Wild Birds of the Nile Delta as Potential West Nile Virus Circulating Reservoirs1. Am J Trop Med Hyg 1955; 4:872–888 [View Article] [PubMed]
    [Google Scholar]
  47. Fields BN, Knipe DM, Howley PM. Fields virology Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007
    [Google Scholar]
  48. Woodall JP, Gillett JD, Corbet PS, Weinbren MP, Williams MC. The isolation of West Nile virus from the bird-biting mosquito Mansonia metallica in Uganda. Ann Trop Med Parasitol 1961; 55:398–402 [View Article] [PubMed]
    [Google Scholar]
  49. Mossel EC, Crabtree MB, Mutebi JP, Lutwama JJ, Borland EM et al. Arboviruses Isolated From Mosquitoes Collected in Uganda, 2008-2012. J Med Entomol 2017; 54:1403–1409 [View Article] [PubMed]
    [Google Scholar]
  50. Williams MC, Simpson DI, Haddow AJ, Knight EM. 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 Parasitol 1964; 58:367–374 [View Article] [PubMed]
    [Google Scholar]
  51. Martín-Acebes MA, Saiz J-. C. West Nile virus: a re-emerging pathogen revisited. World J Virol 2012; 1:51 [View Article] [PubMed]
    [Google Scholar]
  52. Haddow A, Smithburn K, Mahaffy A, Bugher J. Monkeys in relation to yellow fever in Bwamba County, Uganda. Trans R Soc Trop Med Hyg 1947; 40:677–700 [View Article] [PubMed]
    [Google Scholar]
  53. Powell JR, Tabachnick WJ. History of domestication and spread of Aedes aegypti-A Review. Mem Inst Oswaldo Cruz 2013; 108:11–17 [View Article] [PubMed]
    [Google Scholar]
  54. Kotsakiozi P, Evans BR, Gloria‐Soria A, Kamgang B, Mayanja M et al. Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa. Ecol Evol 2018; 8:7835–7848 [View Article] [PubMed]
    [Google Scholar]
  55. Gillett J. Further studies on the biting behaviour of Aedes (Stegomyia) simpsoni Theobald in Uganda. Annals of Tropical Medicine & Parasitology 1955; 49:154–157
    [Google Scholar]
  56. Lumsden W, Buxton A. A study of the epidemiology of yellow fever in West Nile District, Uganda. Trans R Soc Trop Med Hyg 1951; 45:53–78 [View Article] [PubMed]
    [Google Scholar]
  57. Ross E, Haddow A, Raper A, Trowell H. A fatal case of yellow fever in a European in Uganda. East Afr Med J 1953; 30:1–11 [PubMed]
    [Google Scholar]
  58. Tulloch J, Patel K. Yellow fever in central Uganda, 1964. Part II. Report of a fatal case. Transactions of the Royal Society of Tropical Medicine and Hygiene; 1965; 59
  59. Haddow AJ. Yellow Fever in Central Uganda, 1964. I. Historical Introduction. Trans R Soc Trop Med Hyg; 1965; 59436–440
  60. Henderson BE, Cheshire PP, Kirya GB, Lule M. Immunologic studies with yellow fever and selected African group B arboviruses in rhesus and vervet monkeys. Am J Trop Med Hyg 1970; 19:110–118 [View Article] [PubMed]
    [Google Scholar]
  61. Haddow A, Dick G, Lumsden W, Smithburn K. Monkeys in relation to the epidemiology of yellow fever in Uganda. Trans R Soc Trop Med Hyg 1951; 45:189–224 [View Article] [PubMed]
    [Google Scholar]
  62. Kirya B, Okia N. A yellow fever epizootic in Zika Forest, Uganda, during 1972: Part 2: Monkey serology. Trans R Soc Trop Med Hyg 1977; 71:300–303 [View Article] [PubMed]
    [Google Scholar]
  63. Kwagonza L, Masiira B, Kyobe-Bosa H, Kadobera D, Atuheire EB et al. Outbreak of yellow fever in central and southwestern Uganda, February-may 2016. BMC Infect Dis 2018; 18:548 [View Article] [PubMed]
    [Google Scholar]
  64. Mukwaya L. Host preference in Aedes simpsoni (Theo.)(Diptera, Culicidae) with special reference to the anthropophilic and non-anthropophilic forms in Uganda. Bulletin of Entomological Research 1974; 64:129–139
    [Google Scholar]
  65. Vasconcelos PF, Monath TP. Yellow Fever Remains a Potential Threat to Public Health. Vector Borne Zoonotic Dis 2016; 16:566–567 [View Article] [PubMed]
    [Google Scholar]
  66. Xavier AR, Freitas GS, Santos CF, Januzzi WA, Lacerda GS et al. Yellow fever: laboratorial diagnosis and clinical manifestations. Jornal Brasileiro de Patologia e Medicina Laboratorial 2018; 54:296–305 [View Article]
    [Google Scholar]
  67. Boyer S, Calvez E, Chouin-Carneiro T, Diallo D, Failloux A-. B. An overview of mosquito vectors of Zika virus. Microbes Infect 2018; 20:646–660 [View Article] [PubMed]
    [Google Scholar]
  68. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerging Infect Dis 2008; 14:1232
    [Google Scholar]
  69. Weinbren M, Williams M. Zika virus: further isolations in the Zika area, and some studies on the strains isolated. Trans R Soc Trop Med Hyg 1958; 52:263–268 [View Article] [PubMed]
    [Google Scholar]
  70. Haddow A, Williams M, Woodall J, Simpson D, Goma L. Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda forest. Bull World Health Organ 1964; 31:57 [PubMed]
    [Google Scholar]
  71. Henderson B, McCrae A, Kirya B, Ssenkubuge Y, Sempala S. Arbovirus epizootics involving man, mosquitoes and vertebrates at Lunyo, Uganda 1968. Annals of Tropical Medicine & Parasitology 1972; 66:343–355
    [Google Scholar]
  72. Kayiwa JT, Nankya AM, Ataliba IJ, Mossel EC, Crabtree MB et al. Confirmation of Zika virus infection through hospital-based sentinel surveillance of acute febrile illness in Uganda, 2014-2017. J Gen Virol 2018; 99:1248–1252 [View Article] [PubMed]
    [Google Scholar]
  73. Haddow AD, Schuh AJ, Yasuda CY, Kasper MR, Heang V et al. Genetic Characterization of Zika Virus Strains: Geographic Expansion of the Asian Lineage. PLoS Negl Trop Dis 2012; 6:e1477 [View Article] [PubMed]
    [Google Scholar]
  74. Laavanya V, Jayasurya R, Kavitha N, Prabakaran G, Jayakumari S. A Review on Microcephaly Associated with Zika Fever in New Born Babies. Research Journal of Pharmacy and Technology 2017; 10:337
    [Google Scholar]
  75. Krauer F, Riesen M, Reveiz L, Oladapo OT, Martínez-Vega R et al. Zika virus infection as a cause of congenital brain abnormalities and Guillain–Barré syndrome: systematic review. PLoS Med 2017; 14:e1002203 [View Article] [PubMed]
    [Google Scholar]
  76. Smithburn K, Haddow A. Isolation of the virus from wild mosquitoes. Br J Exp Pathol 1948; 29:107 [PubMed]
    [Google Scholar]
  77. Mims C. n.d Rift Valley fever protection test surveys. Annual Report of the East African Virus Research Institute 1956:25
    [Google Scholar]
  78. Magona J, Kabi F, Walubengo J, Ssekitto C. Surveillance of Rift Valley fever in cattle, goats and sheep in Uganda Joint FAO/IAEA Programme; 2009
    [Google Scholar]
  79. Tumusiime D, Kihu S, Mutua E, Bett BK. Towards the development of risk-based intervention strategies for Rift Valley fever in Uganda ILRI; 2018
    [Google Scholar]
  80. Daubney R, Hudson J. Enzootic Hepatitis or Rift Valley Fever. An Un-described Virus Disease of Sheep, Cattle and Man from East Africa. Journal of pathology and bacteriology 1931; 34:545–579
    [Google Scholar]
  81. Van den Bergh C. 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
    [Google Scholar]
  82. Mohamed M, Mosha F, Mghamba J, Zaki SR, Shieh W-J et al. Epidemiologic and clinical aspects of a Rift Valley fever outbreak in humans in Tanzania, 2007. Am J Trop Med Hyg 2010; 83:22–27 [View Article] [PubMed]
    [Google Scholar]
  83. Pardigon N. The biology of chikungunya: a brief review of what we still do not know. Pathol Biol (Paris) 2009; 57:127–132 [View Article] [PubMed]
    [Google Scholar]
  84. Powers AM, Brault AC, Tesh RB, Weaver SC. Re-emergence of Chikungunya and O’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 2000; 81:471–479
    [Google Scholar]
  85. Ross R. The Newala epidemic: III. The virus: isolation, pathogenic properties and relationship to the epidemic. Epidemiol Infect 1956; 54:177–191
    [Google Scholar]
  86. Schwartz O, Albert ML. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 2010; 8:491–500 [View Article] [PubMed]
    [Google Scholar]
  87. Mutebi J-P, Crabtree M, Kading R, Powers A, Lutwama J et al. Mosquitoes of Western Uganda. J Med Entomol 2014; 49:1289–1306
    [Google Scholar]
  88. Mutebi J-P, Crabtree M, Kading R, Powers A, Ledermann J et al. Mosquitoes of Northwestern Uganda. J Med Entomol 2018; 55:587–599 [View Article] [PubMed]
    [Google Scholar]
  89. Rodhain F, Gonzalez JP, Mercier E, Helynck B, Larouze B et al. Arbovirus infections and viral haemorrhagic fevers in Uganda: a serological survey in Karamoja district, 1984. Trans R Soc Trop Med Hyg 1989; 83:851–854 [View Article] [PubMed]
    [Google Scholar]
  90. Clements TL, Rossi CA, Irish AK, Kibuuka H, Eller LA et al. Chikungunya and O’nyong-nyong Viruses in Uganda: Implications for Diagnostics. Open forum infectious diseases Oxford University Press US; 2019
    [Google Scholar]
  91. Kalunda M, Lwanga-Ssozi C, Lule M, Mukuye A. Isolation of Chikungunya and Pongola viruses from patients in Uganda. Trans R Soc Trop Med Hyg 1985; 79:567 [View Article] [PubMed]
    [Google Scholar]
  92. Kayiwa JT, Nankya AM, Ataliba I, Nassuna CA, Omara IE et al. Dengue fever and chikungunya virus infections: identification in travelers in Uganda–2017. Trop Dis Travel Med Vaccines 2019; 5:1–5
    [Google Scholar]
  93. Zeller H, Van Bortel W, Sudre B. Chikungunya: its history in Africa and Asia and its spread to new regions in 2013–2014. J Infect Dis 2016; 214:S436–S440 [View Article]
    [Google Scholar]
  94. Spicher T, Delitz M, AdB S, Wolfinger MT. Dynamic molecular epidemiology reveals lineage-associated single-nucleotide variants that alter RNA structure in Chikungunya virus. Genes (Basel) 2021; 12:239 [View Article] [PubMed]
    [Google Scholar]
  95. de Bernardi Schneider A, Ochsenreiter R, Hostager R, Hofacker IL, Janies D et al. Updated phylogeny of Chikungunya virus suggests lineage-specific RNA architecture. Viruses 2019; 11:798
    [Google Scholar]
  96. Williams M, Woodall J, Corbet PS, Gillett J. O’nyong-nyong fever: an epidemic virus disease in East Africa. VIII. Virus isolations from Anopheles mosquitoes. Trans R Soc Trop Med Hyg 1965; 59:
    [Google Scholar]
  97. Porterfield J. Cross-neutralization studies with group A arthropod-borne viruses. Bull World Health Organ 1961; 24:735 [PubMed]
    [Google Scholar]
  98. Vanlandingham DL, Hong C, Klingler K, Tsetsarkin K, McElroy KL et al. Differential infectivities of o’nyong-nyong and chikungunya virus isolates in Anopheles gambiae and Aedes aegypti mosquitoes. Am J Trop Med Hyg 2005; 72:616–621 [View Article] [PubMed]
    [Google Scholar]
  99. Haddow A, Davies C, Walker A. O’Nyong-nyong fever: An epidemic virus disease in East Africa. I introduction. Trans R Soc Trop Med Hyg 1960; 54:
    [Google Scholar]
  100. Williams M, Woodall J, Gillett J. O’Nyong-Nyong fever: An epidemic virus disease in East Africa. Trans R Soc Trop Med Hyg 1965; 59:186–197
    [Google Scholar]
  101. Lutwama JJ, Kayondo J, Savage HM, Burkot TR, Miller BR. Epidemic O’Nyong-Nyong fever in southcentral Uganda, 1996-1997: entomologic studies in Bbaale village. Am J Trop Med Hyg 1999; 61:158–162 [View Article] [PubMed]
    [Google Scholar]
  102. Kiwanuka N, Sanders EJ, Rwaguma EB, Kawamata J, Ssengooba FP 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 Dis 1999; 29:1243–1250 [View Article] [PubMed]
    [Google Scholar]
  103. Rezza G, Chen R, Weaver SC. O’nyong-nyong fever: a neglected mosquito-borne viral disease. Pathog Glob Health 2017; 111:271–275 [View Article] [PubMed]
    [Google Scholar]
  104. Kayiwa JT, Nankya AM, Ataliba IJ, Mossel EC, Crabtree MB et al. Confirmation of Zika virus infection through hospital-based sentinel surveillance of acute febrile illness in Uganda, 2014-2017. J Gen Virol 2018; 99:1248–1252 [View Article] [PubMed]
    [Google Scholar]
  105. Steinhagen K, Probst C, Radzimski C, Schmidt-Chanasit J, Emmerich P 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 Surveill 2016; 21:30426 [View Article] [PubMed]
    [Google Scholar]
  106. Brinkmann A, Nitsche A, Kohl C. Viral metagenomics on blood-feeding arthropods as a tool for human disease surveillance. Int J Mol Sci 2016; 17:10 [View Article]
    [Google Scholar]
  107. Jerome H, Taylor C, Sreenu VB, Klymenko T, Filipe ADS et al. Metagenomic next-generation sequencing aids the diagnosis of viral infections in febrile returning travellers. J Infect 2019; 79:383–388 [View Article]
    [Google Scholar]
  108. Logue K, Keven JB, Cannon MV, Reimer L, Siba P et al. Unbiased characterization of Anopheles mosquito blood meals by targeted high-throughput sequencing. PLoS Negl Trop Dis 2016; 10:e0004512 [View Article] [PubMed]
    [Google Scholar]
  109. Osei‐Poku J, Mbogo C, Palmer W, Jiggins F. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from K enya. Mol Ecol 2012; 21:5138–5150 [View Article] [PubMed]
    [Google Scholar]
  110. Jupatanakul N, Sim S, Dimopoulos G. The insect microbiome modulates vector competence for arboviruses. Viruses 2014; 6:4294–4313 [View Article] [PubMed]
    [Google Scholar]
  111. Smithburn K, Haddow A. Isolation of yellow fever virus from African mosquitoes. American Journal of Tropical Medicine 1946; 26:261–271
    [Google Scholar]
  112. Williams MC, Woodall JP, Corbet PS, Gillett JD. O’nyong-Nyong Fever: An Epidemic Virus Disease in East Africa. 8. Virus Isolations from Anopheles Mosquitoes. Trans R Soc Trop Med Hyg 1965; 59:300–306 [View Article] [PubMed]
    [Google Scholar]
  113. Nyakarahuka L, de St. Maurice A, Purpura L, Ervin E, Balinandi S et al. Prevalence and risk factors of Rift Valley fever in humans and animals from Kabale district in Southwestern Uganda, 2016. PLOS Neglected Tropical Diseases 2018; 12:e0006412 [View Article]
    [Google Scholar]
  114. Smithburn KC, Haddow AJ, Lumsden WH. 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 Parasitol 1949; 43:74–89 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001680
Loading
/content/journal/jgv/10.1099/jgv.0.001680
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error