Genome AnnouncGenome AnnouncgagaGAGenome Announcements2169-8287American Society for Microbiology1752 N St., N.W., Washington, DC254144994239354genomeA01178-1410.1128/genomeA.01178-14VirusesReidentification of Ebola Virus E718 and ME as Ebola Virus/H.sapiens-tc/COD/1976/Yambuku-EcranKuhnJens H.http://orcid.org/0000-0002-7800-6045aLoftsLoreen L.bKugelmanJeffrey R.bSmitherSophie J.cLeverMark S.cvan der GroenGuidodJohnsonKarl M.eRadoshitzkySheli R.http://orcid.org/0000-0001-8976-8056bBavariSinabJahrlingPeter B.http://orcid.org/0000-0002-9775-3724aTownerJonathan S.fNicholStuart T.fPalaciosGustavohttp://orcid.org/0000-0001-5062-1938bIntegrated Research Facility at Fort Detrick (IRF-Frederick), National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, Maryland, USAUnited States Army Medical Research Institute of Infectious Diseases (USAMRIID), Fort Detrick, Frederick, Maryland, USABiomedical Sciences Department, Dstl, Porton Down, Salisbury, Wiltshire, United KingdomPrins Leopold Instituut voor Tropische Geneeskunde (ITG), Antwerp, BelgiumRetired, Portland, Oregon, USAViral Special Pathogens Branch, Division of High-Consequence Pathogens Pathology, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Georgia, USAAddress correspondence to Jens H. Kuhn, kuhnjens@mail.nih.gov.20112014Nov-Dec201426e01178-1411020148102014Copyright © 2014 Kuhn et al.2014Kuhn et al.This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.

Ebola virus (EBOV) was discovered in 1976 around Yambuku, Zaire. A lack of nomenclature standards resulted in a variety of designations for each isolate, leading to confusion in the literature and databases. We sequenced the genome of isolate E718/ME/Ecran and unified the various designations under Ebola virus/H.sapiens-tc/COD/1976/Yambuku-Ecran.

cover-dateNovember/December 2014access-typefree
GENOME ANNOUNCEMENT

Ebola virus (EBOV) was discovered in 1976 around Yambuku, Équateur Province, Zaire (the present-day Democratic Republic of the Congo). Of the 318 people that became infected with the virus, 280 died (1). At least three EBOV isolates (Ecran, de Roover, and Mayinga) were obtained and distributed among laboratories for further characterization. Due to a lack of nomenclature standards, individual institutes assigned a variety of names to each individual isolate, thereby leading to confusion in the literature and in databases.

Filovirus experts recently established a naming scheme for filoviruses (2, 3) and have designated reference isolates and sequences for each filovirus to facilitate research, automatic genome annotation, and database searches (4). Among these efforts are attempts to identify and remove possibly redundant isolate designations.

Isolate E718 (known as 718 [5], E718 [614), E-718 [1517], and E 718 [6, 15, 1821]) is one of the EBOV isolates found in 1976. The origin of E718 is usually not mentioned, or it is stated only that E718 was derived from an acute-phase human blood sample (5, 1014, 16, 17, 20, 21). Other authors elaborate that the isolate was obtained by S. R. Pattyn (Instituut voor Tropische Geneeskunde [ITG], Antwerp, Belgium) (6, 15, 18). One article refers to the isolate as the Zaire prototype (8), whereas a very recent publication states that “E718 [is] … one of four isolates (including … Mayinga)” (9). Finally, one publication states that E718 “was derived from a Zairean patient (ME) during the Zairean outbreak” (7). One of two publications detailing isolate ME states that this virus was “isolated by… Pattyn … Bowen, and … Webb from serum of adult female human being manifesting severe … illness” and that “[d]isease [was] contracted in Yambuku … and case transported to mission hospital in Kinshasa” (22). Other publications specify that patient ME was a 42-year-old woman who fell ill on 23 September 1976 in Yambuku and was transported by air to Kinshasa (23, 24). She died on 30 September 1976 (25, 26).

From a review of internal documents at institutes that still store E718 cultures (CDC, Defence Science and Technology Laboratory [Dstl], ITG, and the United States Army Medical Research Institute of Infectious Diseases [USAMRIID]), detailed descriptions of the 1976 outbreak (25, 26), and personal observations of authors who participated in its control (K.M.J. and G.v.d.G.), we conclude that E718 is a synonym of ME. Both designations are, in all likelihood, synonyms of the EBOV variant designation Ecran (often incorrectly spelled Eckron in the literature), which is derived from the name of Sister Myriam (Louise Ecran), who was one of two nurses that were transported from Yambuku to Kinshasa (the other one being Sister Edmonda [Jeanne de Roover]) (25, 26).

We sequenced E718 using infected cell-culture supernatant originally frozen at USAMRIID on 19 May 1978. Following sample preparation performed as described in Kugelman et al. (27), its sequence was determined with Ion Torrent PGM and Applied Biosystems Sanger technology with EBOV-specific oligonucleotides. The consensus genome was generated via reference alignment to that of RefSeq accession no. NC_002549 (Ebola virus/H.sapiens-tc/COD/1976/Yambuku-Mayinga [4]) using SeqMan Pro (DNAStar). As expected, the obtained sequence was nearly identical with that of RefSeq accession no. NC_002549 and has been deposited under the unifying designation Ebola virus/H.sapiens-tc/COD/1976/Yambuku-Ecran.

Nucleotide sequence accession numbers.

The GenBank accession no. of EBOV E718, now designated Ebola virus/H.sapiens-tc/COD/1976/Yambuku-Ecran, is KM655246.

Citation Kuhn JH, Lofts LL, Kugelman JR, Smither SJ, Lever MS, van der Groen G, Johnson KM, Radoshitzky SR, Bavari S, Jahrling PB, Towner JS, Nichol ST, Palacios G. 2014. Reidentification of Ebola virus E718 and ME as Ebola virus/H.sapiens-tc/COD/1976/Yambuku-Ecran. Genome Announc. 2(6):e01178-14. doi:10.1128/genomeA.01178-14.

ACKNOWLEDGMENTS

J.H.K. performed this work as an employee of Tunnell Government Services, Inc., a subcontractor to Battelle Memorial Institute under its prime contract with NIAID (HHSN272200700016I).

We thank Laura Bollinger (IRF-Frederick) for editing the manuscript.

The content of this publication does not necessarily reflect the views or policies of the U.S. Department of Health and Human Services, the U.S. Department of Defense, the U.S. Department of the Army, or of the institutions and companies affiliated with the authors.

REFERENCES World Health Organization 1978 Ebola haemorrhagic fever in Zaire, 1976. Bull. World Health Organ. 56:271293.307456 KuhnJHBeckerSEbiharaHGeisbertTWJohnsonKMKawaokaYLipkinWINegredoAINetesovSVNicholSTPalaciosGPetersCJTenorioAVolchkovVEJahrlingPB 2010 Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch. Virol. 155:20832103. 10.1007/s00705-010-0814-x.21046175 KuhnJHBaoYBavariSBeckerSBradfuteSBristerJRBukreyevAAChandranKDaveyRADolnikODyeJMEnterleinSHensleyLEHonkoANJahrlingPBJohnsonKMKobingerGLeroyEMLeverMSMühlbergerENetesovSVOlingerGGPalaciosGPattersonJLPaweskaJTPittLRadoshitzkySRSaphireEOSmitherSJSwanepoelRTownerJSvan der GroenGVolchkovVEWahl-JensenVWarrenTKWeidmannMNicholST 2013 Virus nomenclature below the species level: a standardized nomenclature for natural variants of viruses assigned to the family Filoviridae. Arch. Virol. 158:301311. 10.1007/s00705-012-1454-0.23001720 KuhnJHAndersenKGBàoYBavariSBeckerSBennettRSBergmanNHBlinkovaOBradfuteSBristerJRBukreyevAChandranKChepurnovAADaveyRADietzgenRGDoggettNADolnikODyeJMEnterleinSFenimorePWFormentyPFreibergANGarryRFGarzaNLGireSKGonzalezJPGriffithsAHappiCTHensleyLEHerbertASHeveyMCHoenenTHonkoANIgnatyevGMJahrlingPBJohnsonJCJohnsonKMKindrachukJKlenkHDKobingerGKochelTJLackemeyerMGLacknerDFLeroyEMLeverMSMühlbergerENetesovSVOlingerGGOmilabuSAPalaciosG 2014 Filovirus RefSeq entries: evaluation and selection of filovirus type variants, type sequences, and Names. Viruses 6:36633682. 10.3390/v6093663.25256396 van der GroenGJacobWPattynSR 1979 Ebola virus virulence for newborn mice. J. Med. Virol. 4:239240. 10.1002/jmv.1890040309.536744 BowenETWLloydGPlattGMcArdellLBWebbPASimpsonDIH 1978 Virological studies on a case of Ebola virus infection in man and in monkeys, p 95102 In PattynSR (ed), Ebola virus haemorrhagic fever: proceedings of an international colloquium on Ebola virus infection and other haemorrhagic fevers held in Antwerp, Belgium, 6–8 December, 1977. Elsevier/North-Holland Biomedical Press, Amsterdam, the Netherlands. EllisDSStamfordSLloydGBowenETPlattGSWayHSimpsonDI 1979 Ebola and Marburg viruses: I. Some ultrastructural differences between strains when grown in Vero cells. J. Med. Virol. 4:201211. 10.1002/jmv.1890040306.94087 BowenETPlattGSLloydGRaymondRTSimpsonDI 1980 A comparative study of strains of Ebola virus isolated from southern Sudan and northern Zaire in 1976. J. Med. Virol. 6:129138. 10.1002/jmv.1890060205.6165800 PiercyTJSmitherSJStewardJAEastaughLLeverMS 2010 The survival of filoviruses in liquids, on solid substrates and in a dynamic aerosol. J. Appl. Microbiol. 109:15311539. 10.1111/j.1365-2672.2010.04778.x.20553340 SmitherSJPiercyTJEastaughLStewardJALeverMS 2011 An alternative method of measuring aerosol survival using spiders’ webs and its use for the filoviruses. J. Virol. Methods 177:123127. 10.1016/j.jviromet.2011.06.021.21762730 LeverMSPiercyTJStewardJAEastaughLSmitherSJTaylorCSalgueroFJPhillpottsRJ 2012 Lethality and pathogenesis of airborne infection with filoviruses in A129 α/β -/- interferon receptor-deficient mice. J. Med. Microbiol. 61:815. 10.1099/jmm.0.036210-0.21852521 SmitherSJEastaughLSStewardJANelsonMLenkRPLeverMS 2014 Post-exposure efficacy of oral T-705 (favipiravir) against inhalational Ebola virus infection in a mouse model. Antiviral Res. 104:153155. 10.1016/j.antiviral.2014.01.012.24462697 Fisher-HochSPPlattGSLloydGSimpsonDINeildGHBarrettAJ 1983 Haematological and biochemical monitoring of Ebola infection in rhesus monkeys: implications for patient management. Lancet 2:10551058.6138602 Fisher-HochSPPlattGSNeildGHSoutheeTBaskervilleARaymondRTLloydGSimpsonDI 1985 Pathophysiology of shock and hemorrhage in a fulminating viral infection (Ebola). J. Infect. Dis. 152:887894. 10.1093/infdis/152.5.887.4045253 EllisDSBowenETSimpsonDIStamfordS 1978 Ebola virus: a comparison, at ultrastructural level, of the behaviour of the Sudan and Zaire strains in monkeys. Br. J. Exp. Pathol. 59:584593.106868 MoeJBLambertRDLuptonHW 1981 Plaque assay for Ebola virus. J. Clin. Microbiol. 13:791793.7014628 LuptonHWLambertRDBumgardnerDLMoeJBEddyGA 1980 Inactivated vaccine for Ebola virus efficacious in guineapig model. Lancet 2:12941295.6108462 BowenETPlattGSSimpsonDIMcArdellLBRaymondRT 1978 Ebola haemorrhagic fever: experimental infection of monkeys. Trans. R. Soc. Trop. Med. Hyg. 72:188191. 10.1016/0035-9203(78)90058-5.418537 BowenETWBaskervilleACantellKMannGFSimpsonDIHZuckermanAJ 1978 The effect of interferon on experimental Ebola virus infection in rhesus monkeys, p 245253 In PattynSR (ed), Ebola virus haemorrhagic fever: proceedings of an international colloquium on Ebola virus infection and other haemorrhagic fevers held in Antwerp, Belgium, 6–8 December, 1977. Elsevier/North-Holland Biomedical Press, Amsterdam, the Netherlands. LuptonHW 1981 Inactivation of Ebola virus with 60Co irradiation. J. Infect. Dis. 143:291. 10.1093/infdis/143.2.291.7217722 BaskervilleAFisher-HochSPNeildGHDowsettAB 1985 Ultrastructural pathology of experimental Ebola haemorrhagic fever virus infection. J. Pathol. 147:199209. 10.1002/path.1711470308.4067737 PattynSR 1978 Ebola (EBO): strain: ME. Am. J. Trop. Med. Hyg. 27:383384. PattynSvan der GroenGCourteilleGJacobWPiotP 1977 Isolation of Marburg-like virus from a case of haemorrhagic fever in Zaire. Lancet 1:573574.65663 PattynSRBowenETWWebbPA 1985 Ebola, p 379380 In KarabatsosN (ed), International Catalogue of Arboviruses 1985 including certain other viruses of Vertebrates, 3rd ed. American Society of Tropical Medicine and Hygiene, San Antonio, TX. GarrettL 1994 Yambuku—Ebola, p 100152 In GarrettL (ed), The coming plague: newly emerging diseases in a world out of balance. Farrar, Straus & Giroux, New York, NY. SureauP 1977 Yambuku. A novel African hemorrhagic fever. The discovery of the Ebola virus. The Yambuku epidemic, Zaire, September–October 1976. Travel log book. Paris, France. KugelmanJRLeeMSRossiCAMcCarthySERadoshitzkySRDyeJMHensleyLEHonkoAKuhnJHJahrlingPBWarrenTKWhitehouseCABavariSPalaciosG 2012 Ebola virus genome plasticity as a marker of its passaging history: a comparison of in vitro passaging to non-human primate infection. PLoS One 7:e50316. 10.1371/journal.pone.0050316.23209706