1887

Abstract

The sudden and explosive expansion of Zika virus (ZIKV) from the African continent through Oceania and culminating in the outbreak in South America has highlighted the importance of new rapid point-of-care diagnostic tools for the control and prevention of transmission. ZIKV infection has devastating consequences, such as neurological congenital malformations in infants born to infected mothers and GuillainBarré syndrome in adults. Additionally, its potential for transmission through vector bites, as well as from person to person through blood transfusions and sexual contact, are important considerations for prompt diagnosis. Recombinase polymerase amplification (RPA), an isothermal method, was developed as an alternative field-applicable assay to PCR. Here we report the development of a novel ZIKV real-time reverse transcriptase RPA (RT-RPA) assay capable of detecting a range of different ZIKV strains from a variety of geographical locations. The ZIKV RT-RPA was shown to be highly sensitive, being capable of detecting as few as five copies of target nucleic acid per reaction, and suitable for use with a battery-operated portable device. The ZIKV RT-RPA demonstrated 100 % specificity and 83 % sensitivity in clinical samples. Furthermore, we determined that the ZIKV RT-RPA is a versatile assay that can be applied to crude samples, such as saliva and serum, and can be used as a vector surveillance tool on crude mosquito homogenates. Therefore, the developed ZIKV RT-RPA is a useful diagnostic tool that can be transferred to a resource-limited location, eliminating the need for a specialized and sophisticated laboratory environment and highly trained staff.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001083
2018-06-13
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/8/1012.html?itemId=/content/journal/jgv/10.1099/jgv.0.001083&mimeType=html&fmt=ahah

References

  1. Musso D, Gubler DJ. Zika virus. Clin Microbiol Rev 2016;29:487–524 [CrossRef][PubMed]
    [Google Scholar]
  2. Dick GW, Kitchen SF, Haddow AJ. Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg 1952;46:509–520 [CrossRef][PubMed]
    [Google Scholar]
  3. MacNamara FN. Zika virus: a report on three cases of human infection during an epidemic of jaundice in Nigeria. Trans R Soc Trop Med Hyg 1954;48:139–145 [CrossRef][PubMed]
    [Google Scholar]
  4. Marchette NJ, Garcia R, Rudnick A. Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia. Am J Trop Med Hyg 1969;18:411–415 [CrossRef][PubMed]
    [Google Scholar]
  5. Monlun E, Zeller H, Le Guenno B, Traoré-Lamizana M, Hervy JP et al. Surveillance of the circulation of arbovirus of medical interest in the region of eastern Senegal. Bull Soc Pathol Exot 1993;86:21–28[PubMed]
    [Google Scholar]
  6. Diallo D, Sall AA, Diagne CT, Faye O, Faye O et al. Zika virus emergence in mosquitoes in southeastern Senegal, 2011. PLoS One 2014;9:e109442 [CrossRef][PubMed]
    [Google Scholar]
  7. Faye O, Faye O, Diallo D, Diallo M, Weidmann M et al. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virol J 2013;10:311 [CrossRef][PubMed]
    [Google Scholar]
  8. Weinbren MP, Williams MC. 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 [CrossRef][PubMed]
    [Google Scholar]
  9. Haddow AJ, Williams MC, Woodall JP, Simpson DI, Goma LK et al. 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]
  10. Berthet N, Nakouné E, Kamgang B, Selekon B, Descorps-Declère S et al. Molecular characterization of three Zika flaviviruses obtained from sylvatic mosquitoes in the Central African Republic. Vector Borne Zoonotic Dis 2014;14:862–865 [CrossRef][PubMed]
    [Google Scholar]
  11. McCrae AW, Kirya BG. Yellow fever and Zika virus epizootics and enzootics in Uganda. Trans R Soc Trop Med Hyg 1982;76:552–562 [CrossRef][PubMed]
    [Google Scholar]
  12. Grard G, Caron M, Mombo IM, Nkoghe D, Mboui Ondo S et al. Zika virus in Gabon (Central Africa)–2007: a new threat from Aedes albopictus?. PLoS Negl Trop Dis 2014;8:e2681 [CrossRef][PubMed]
    [Google Scholar]
  13. Olson JG, Ksiazek TG, Suhandiman, Triwibowo. Zika virus, a cause of fever in Central Java, Indonesia. Trans R Soc Trop Med Hyg 1981;75:389–393 [CrossRef][PubMed]
    [Google Scholar]
  14. 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. Emerg Infect Dis 2008;14:1232–1239 [CrossRef][PubMed]
    [Google Scholar]
  15. Duffy MR, Chen TH, Hancock WT, Powers AM, Kool JL et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 2009;360:2536–2543 [CrossRef][PubMed]
    [Google Scholar]
  16. Cao-Lormeau V-M et al. Zika Virus, French Polynesia, South Pacific, 2013. Emerg Infect Dis 2014;20:1960–1966 [CrossRef]
    [Google Scholar]
  17. Musso D, Nilles EJ, Cao-Lormeau VM. Rapid spread of emerging Zika virus in the Pacific area. Clin Microbiol Infect 2014;20:O595–O596 [CrossRef][PubMed]
    [Google Scholar]
  18. Campos GS, Bandeira AC, Sardi SI. Zika virus outbreak, Bahia, Brazil. Emerg Infect Dis 2015;21:1885–1886 [CrossRef][PubMed]
    [Google Scholar]
  19. Healy JM, Burgess MC, Chen TH, Hancock WT, Toews KE et al. Notes from the Field: Outbreak of Zika Virus Disease – American Samoa, 2016. MMWR Morb Mortal Wkly Rep 2016;65:1146–1147 [CrossRef][PubMed]
    [Google Scholar]
  20. Hennessey M, Fischer M, Staples JE. Zika virus spreads to new areas - region of the Americas, May 2015–January 2016. MMWR Morb Mortal Wkly Rep 2016;65:55–58 [CrossRef][PubMed]
    [Google Scholar]
  21. Rodriguez-Morales AJ. Zika: the new arbovirus threat for Latin America. J Infect Dev Ctries 2015;9:684–685 [CrossRef][PubMed]
    [Google Scholar]
  22. Araujo LM, Ferreira ML, Nascimento OJ. Guillain-Barré syndrome associated with the Zika virus outbreak in Brazil. Arq Neuropsiquiatr 2016;74:253–255 [CrossRef][PubMed]
    [Google Scholar]
  23. Cao-Lormeau V-M, Blake A, Mons S, Lastère S, Roche C et al. Guillain-Barré syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. The Lancet 2016;387:1531–1539 [CrossRef]
    [Google Scholar]
  24. Nascimento OJM, da Silva IRF. Guillain-Barré syndrome and Zika virus outbreaks. Curr Opin Neurol 2017;30:500–507 [CrossRef][PubMed]
    [Google Scholar]
  25. Savino W, Messias CV, Mendes-da-Cruz DA, Passos P, Ferreira AC et al. Zika virus infection in the elderly: possible relationship with Guillain-Barré syndrome. Gerontology 2017;63:210–215 [CrossRef][PubMed]
    [Google Scholar]
  26. Dub T, Fontanet A. Zika virus and Guillain-Barré syndrome. Rev Neurol 2017;173:361–363 [CrossRef][PubMed]
    [Google Scholar]
  27. Miller E, Becker Z, Shalev D, Lee CT, Cioroiu C et al. Probable Zika virus-associated Guillain-Barré syndrome: challenges with clinico-laboratory diagnosis. J Neurol Sci 2017;375:367–370 [CrossRef][PubMed]
    [Google Scholar]
  28. Uncini A, Shahrizaila N, Kuwabara S. Zika virus infection and Guillain-Barré syndrome: a review focused on clinical and electrophysiological subtypes. J Neurol Neurosurg Psychiatry 2017;88:266–271 [CrossRef][PubMed]
    [Google Scholar]
  29. Villamil-Gomez WE, Sánchez-Herrera ÁR, Hernandez H, Hernández-Iriarte J, Díaz-Ricardo K et al. Guillain-Barré syndrome during the Zika virus outbreak in Sucre, Colombia, 2016. Travel Med Infect Dis 2017;16:62–63 [CrossRef][PubMed]
    [Google Scholar]
  30. 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 [CrossRef][PubMed]
    [Google Scholar]
  31. Panchaud A, Stojanov M, Ammerdorffer A, Vouga M, Baud D et al. Emerging role of Zika virus in adverse fetal and neonatal outcomes. Clin Microbiol Rev 2016;29:659–694 [CrossRef][PubMed]
    [Google Scholar]
  32. Anaya JM, Rodríguez Y, Monsalve DM, Vega D, Ojeda E et al. A comprehensive analysis and immunobiology of autoimmune neurological syndromes during the Zika virus outbreak in Cúcuta, Colombia. J Autoimmun 2017;77:123–138 [CrossRef][PubMed]
    [Google Scholar]
  33. Song BH, Yun SI, Woolley M, Lee YM. Zika virus: history, epidemiology, transmission, and clinical presentation. J Neuroimmunol 2017;308:50–64 [CrossRef][PubMed]
    [Google Scholar]
  34. Şahiner F, Siğ AK, Savaşçi Ü, Tekin K, Akay F et al. Zika virus-associated ocular and neurologic disorders: the emergence of new evidence. Pediatr Infect Dis J 2017;36:e341-e346 [CrossRef][PubMed]
    [Google Scholar]
  35. de Oliveira Dias JR, Ventura CV, Borba PD, de Paula Freitas B, Pierroti LC et al. Infants with congenital zika syndrome and ocular findings from São Paulo, Brazil: spread of infection. Retin Cases Brief Rep 2017; [CrossRef][PubMed]
    [Google Scholar]
  36. Wen Z, Song H, Ming GL. How does Zika virus cause microcephaly?. Genes Dev 2017;31:849–861 [CrossRef][PubMed]
    [Google Scholar]
  37. Duarte G, Moron A, Timerman A, Fernandes C, Mariani Neto C et al. Zika virus infection in pregnant women and microcephaly. Rev Bras Ginecol Obstet 2017;39:235–248 [CrossRef]
    [Google Scholar]
  38. Centers for Disease Control and Prevention Protect yourself & others from Zika. 2017
  39. Folkers KM, Caplan AL, Igel LH. Zika, sexual transmission and prudent public health policy. Public Health 2017;148:66–68 [CrossRef][PubMed]
    [Google Scholar]
  40. Hastings AK, Fikrig E. Zika virus and sexual transmission: a new route of transmission for mosquito-borne Flaviviruses. Yale J Biol Med 2017;90:325–330[PubMed]
    [Google Scholar]
  41. Baud D, Gubler DJ, Schaub B, Lanteri MC, Musso D. An update on Zika virus infection. Lancet 2017;390:2099–2109 [CrossRef][PubMed]
    [Google Scholar]
  42. Motta IJ, Spencer BR, Cordeiro da Silva SG, Arruda MB, Dobbin JA et al. Evidence for transmission of Zika virus by platelet transfusion. N Engl J Med 2016;375:1101–1103 [CrossRef][PubMed]
    [Google Scholar]
  43. Zika virus (ZIKV): clinical and travel guidance. 2017; Available fromwww.gov.uk/government/collections/zika-virus-zikv-clinical-and-travel-guidance
  44. Landry ML, St George K. Laboratory diagnosis of Zika virus infection. Arch Pathol Lab Med 2017;141:60–67 [CrossRef][PubMed]
    [Google Scholar]
  45. Zika virus: sample testing advice. 2017; Available fromwww.gov.uk/guidance/zika-virus-sample-testing-advice
  46. Diagnostic tests for Zika virus. 2017; Available fromwww.cdc.gov/zika/hc-providers/types-of-tests.html
  47. Sharma S, Zapatero-Rodríguez J, Estrela P, O'Kennedy R. Point-of-care diagnostics in low resource settings: present status and future role of microfluidics. Biosensors 2015;5:577–601 [CrossRef][PubMed]
    [Google Scholar]
  48. Elston JW, Cartwright C, Ndumbi P, Wright J. The health impact of the 2014–15 Ebola outbreak. Public Health 2017;143:60–70 [CrossRef][PubMed]
    [Google Scholar]
  49. Maffert P, Reverchon S, Nasser W, Rozand C, Abaibou H et al. New nucleic acid testing devices to diagnose infectious diseases in resource-limited settings. Eur J Clin Microbiol Infect Dis 2017;36:1717–1731 [CrossRef][PubMed]
    [Google Scholar]
  50. Giuffrida MC, Spoto G. Integration of isothermal amplification methods in microfluidic devices: recent advances. Biosens Bioelectron 2017;90:174–186 [CrossRef][PubMed]
    [Google Scholar]
  51. Whitesides GM. The origins and the future of microfluidics. Nature 2006;442:368–373 [CrossRef][PubMed]
    [Google Scholar]
  52. Hamon M, Hong JW. New tools and new biology: recent miniaturized systems for molecular and cellular biology. Mol Cells 2013;36:485–506 [CrossRef][PubMed]
    [Google Scholar]
  53. Craw P, Mackay RE, Naveenathayalan A, Hudson C, Branavan M et al. A simple, low-cost platform for real-time isothermal nucleic acid amplification. Sensors 2015;15:23418–23430 [CrossRef][PubMed]
    [Google Scholar]
  54. Chang CC, Chen CC, Wei SC, Lu HH, Liang YH et al. Diagnostic devices for isothermal nucleic acid amplification. Sensors 2012;12:8319–8337 [CrossRef][PubMed]
    [Google Scholar]
  55. Fakruddin M, Mannan KS, Chowdhury A, Mazumdar RM, Hossain MN et al. Nucleic acid amplification: alternative methods of polymerase chain reaction. J Pharm Bioallied Sci 2013;5:245–252 [CrossRef][PubMed]
    [Google Scholar]
  56. Piepenburg O, Williams CH, Stemple DL, Armes NA. DNA detection using recombination proteins. PLoS Biol 2006;4:e204 [CrossRef][PubMed]
    [Google Scholar]
  57. Shukla S, Hong SY, Chung SH, Kim M. Rapid detection strategies for the global threat of Zika virus: current state, new hypotheses, and limitations. Front Microbiol 2016;7:1685 [CrossRef][PubMed]
    [Google Scholar]
  58. Demidov VV. Rolling-circle amplification in DNA diagnostics: the power of simplicity. Expert Rev Mol Diagn 2002;2:542–548 [CrossRef][PubMed]
    [Google Scholar]
  59. Li Y, Fan P, Zhou S, Zhang L. Loop-mediated isothermal amplification (LAMP): a novel rapid detection platform for pathogens. Microb Pathog 2017;107:54–61 [CrossRef][PubMed]
    [Google Scholar]
  60. Mori Y, Notomi T. Loop-mediated isothermal amplification (LAMP): a rapid, accurate, and cost-effective diagnostic method for infectious diseases. J Infect Chemother 2009;15:62–69 [CrossRef][PubMed]
    [Google Scholar]
  61. Niemz A, Ferguson TM, Boyle DS. Point-of-care nucleic acid testing for infectious diseases. Trends Biotechnol 2011;29:240–250 [CrossRef][PubMed]
    [Google Scholar]
  62. Yan L, Zhou J, Zheng Y, Gamson AS, Roembke BT et al. Isothermal amplified detection of DNA and RNA. Mol Biosyst 2014;10:970–1003 [CrossRef][PubMed]
    [Google Scholar]
  63. Daher RK, Stewart G, Boissinot M, Bergeron MG. Recombinase polymerase amplification for diagnostic applications. Clin Chem 2016;62:947–958 [CrossRef][PubMed]
    [Google Scholar]
  64. Baronti C, Piorkowski G, Charrel RN, Boubis L, Leparc-Goffart I et al. Complete coding sequence of zika virus from a French polynesia outbreak in 2013. Genome Announc 2014;2:e00500-14 [CrossRef][PubMed]
    [Google Scholar]
  65. Cunha MS, Esposito DL, Rocco IM, Maeda AY, Vasami FG et al. First complete genome sequence of Zika virus (Flaviviridae, Flavivirus) from an autochthonous transmission in Brazil. Genome Announc 2016;4:e00032-16 [CrossRef][PubMed]
    [Google Scholar]
  66. Lanciotti RS, Lambert AJ, Holodniy M, Saavedra S, Signor LC et al. Phylogeny of Zika virus in western Hemisphere, 2015. Emerg Infect Dis 2016;22:933–935 [CrossRef][PubMed]
    [Google Scholar]
  67. Azevedo RSS, Cruz ACR, Nunes BTD, Quieroz ALN, Oliveira RS et al. Genome sequences of four Zika virus isolates from Brazil. Unpublished (NCBI). 2016
  68. Lewandowski K, Miles R, Liberty L, Pullan S. Direct submission: Zika virus strain MP1751, complete genome. Genomics of rare and emerging human pathogens, Public Health England, Manor farm road, Porton Down, Salisbury, Wilts SP4 0JG, UK. 2016
  69. Drosten C, Göttig S, Schilling S, Asper M, Panning M et al. Rapid detection and quantification of RNA of Ebola and Marburg viruses, Lassa virus, Crimean-Congo hemorrhagic fever virus, Rift Valley fever virus, dengue virus, and yellow fever virus by real-time reverse transcription-PCR. J Clin Microbiol 2002;40:2323–2330 [CrossRef][PubMed]
    [Google Scholar]
  70. Edwards CJ, Welch SR, Chamberlain J, Hewson R, Tolley H et al. Molecular diagnosis and analysis of Chikungunya virus. J Clin Virol 2007;39:271–275 [CrossRef][PubMed]
    [Google Scholar]
  71. Musso D, Roche C, Nhan TX, Robin E, Teissier A et al. Detection of Zika virus in saliva. J Clin Virol 2015;68:53–55 [CrossRef][PubMed]
    [Google Scholar]
  72. Bonaldo MC, Ribeiro IP, Lima NS, dos Santos AA, Menezes LSR et al. Isolation of infective Zika virus from urine and saliva of patients in Brazil. PLoS Negl Trop Dis 2016;10:e0004816 [CrossRef][PubMed]
    [Google Scholar]
  73. Pompon J, Morales-Vargas R, Manuel M, Huat Tan C, Vial T et al. A Zika virus from America is more efficiently transmitted than an Asian virus by Aedes aegypti mosquitoes from Asia. Sci Rep 2017;7:1215 [CrossRef][PubMed]
    [Google Scholar]
  74. Coffey LL, Pesavento PA, Keesler RI, Singapuri A, Watanabe J et al. Zika virus tissue and blood compartmentalization in acute infection of Rhesus Macaques. PLoS One 2017;12:e0171148 [CrossRef][PubMed]
    [Google Scholar]
  75. Xie X, Yang Y, Muruato AE, Zou J, Shan C et al. Understanding Zika virus stability and developing a chimeric vaccine through functional analysis. MBio 2017;8:e02134-16 [CrossRef][PubMed]
    [Google Scholar]
  76. Xu MY, Liu SQ, Deng CL, Zhang QY, Zhang B et al. Detection of Zika virus by SYBR green one-step real-time RT-PCR. J Virol Methods 2016;236:93–97 [CrossRef][PubMed]
    [Google Scholar]
  77. Joguet G, Mansuy JM, Matusali G, Hamdi S, Walschaerts M et al. Effect of acute Zika virus infection on sperm and virus clearance in body fluids: a prospective observational study. Lancet Infect Dis 2017;17:1200–1208 [CrossRef][PubMed]
    [Google Scholar]
  78. Haddow AD, Woodall JP. Distinguishing between Zika and Spondweni viruses. Bull World Health Organ 2016;94:711–711A [CrossRef][PubMed]
    [Google Scholar]
  79. Rossini G, Gaibani P, Vocale C, Cagarelli R, Landini MP et al. Comparison of Zika virus (ZIKV) RNA detection in plasma, whole blood and urine – case series of travel-associated ZIKV infection imported to Italy, 2016. J Infect 2017;75:242–245 [CrossRef][PubMed]
    [Google Scholar]
  80. Abd El Wahed A, Sanabani SS, Faye O, Pessôa R, Patriota JV et al. Rapid molecular detection of zika virus in acute-phase urine samples using the recombinase polymerase amplification assay. PLoS Curr 2017;9: [CrossRef][PubMed]
    [Google Scholar]
  81. Añez G, Heisey DA, Volkova E, Rios M. Complete genome sequences of dengue virus type 1 to 4 strains used for the development of CBER/FDA RNA reference reagents and WHO International standard candidates for nucleic acid testing. Genome Announc 2016;4:e01583-15 [CrossRef][PubMed]
    [Google Scholar]
  82. Kinney RM, Butrapet S, Chang GJ, Tsuchiya KR, Roehrig JT et al. Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 1997;230:300–308 [CrossRef][PubMed]
    [Google Scholar]
  83. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M et al. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 1999;286:2333–2337 [CrossRef][PubMed]
    [Google Scholar]
  84. Netto M, Shirako Y, Strauss EG, Carvalho MGC, Strauss JH. Direct submission: Mayaro virus, complete genome. National Center for Biotechnology Information, NIH, Bethesda, MD 20894, USA 2012
  85. Grard G, Brisbarre N, Moureau G, Lamballerie de X. Phylogeny of the tick-borne flavivirus group. St. Louis encephalitis virus isolate MSI-7 from USA polyprotein gene, complete cds. Unpublished (NCBI) 2006
  86. Hughes MT, Kempf BJ, Blair CD, Beaty BJ. Complete sequence of the Bunyavirus, La Crosse virus, Human/78 strain. Unpublished (NCBI) 2009
  87. Grard G, Moureau G, Charrel RN, Holmes EC, Gould EA et al. Genomics and evolution of Aedes-borne flaviviruses. J Gen Virol 2010;91:87–94 [CrossRef][PubMed]
    [Google Scholar]
  88. Maher-Sturgess SL, Forrester NL, Wayper PJ, Gould EA, Hall RA et al. Universal primers that amplify RNA from all three flavivirus subgroups. Virol J 2008;5:16 [CrossRef][PubMed]
    [Google Scholar]
  89. Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G et al. A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 2007;7:467–478 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001083
Loading
/content/journal/jgv/10.1099/jgv.0.001083
Loading

Data & Media loading...

Supplementary File 2

PDF

Most Cited This Month

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