{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,1]],"date-time":"2026-11-01T11:08:11Z","timestamp":1793531291521,"version":"4.5.0"},"reference-count":36,"publisher":"National Academy of Sciences","issue":"12","license":[{"start":{"date-parts":[[2019,2,28]],"date-time":"2019-02-28T00:00:00Z","timestamp":1551312000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004963","name":"EC | Seventh Framework Programme","doi-asserted-by":"publisher","award":["F3-2012-304875"],"award-info":[{"award-number":["F3-2012-304875"]}],"id":[{"id":"10.13039\/501100004963","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004963","name":"EC | Seventh Framework Programme","doi-asserted-by":"publisher","award":["F3-2012-304875"],"award-info":[{"award-number":["F3-2012-304875"]}],"id":[{"id":"10.13039\/501100004963","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000265","name":"RCUK | Medical Research Council","doi-asserted-by":"publisher","award":["13056"],"award-info":[{"award-number":["13056"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000265","name":"RCUK | Medical Research Council","doi-asserted-by":"publisher","award":["CO485"],"award-info":[{"award-number":["CO485"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000272","name":"DH | National Institute for Health Research","doi-asserted-by":"publisher","award":["CBRC85"],"award-info":[{"award-number":["CBRC85"]}],"id":[{"id":"10.13039\/501100000272","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2019,3,19]]},"abstract":"<jats:p>\n                    Recent sequencing efforts have led to estimates of human cytomegalovirus (HCMV) genome-wide intrahost diversity that rival those of persistent RNA viruses [Renzette N, Bhattacharjee B, Jensen JD, Gibson L, Kowalik TF (2011)\n                    <jats:italic>PLoS Pathog<\/jats:italic>\n                    7:e1001344]. Here, we deep sequence HCMV genomes recovered from single and longitudinally collected blood samples from immunocompromised children to show that the observations of high within-host HCMV nucleotide diversity are explained by the frequent occurrence of mixed infections caused by genetically distant strains. To confirm this finding, we reconstructed within-host viral haplotypes from short-read sequence data. We verify that within-host HCMV nucleotide diversity in unmixed infections is no greater than that of other DNA viruses analyzed by the same sequencing and bioinformatic methods and considerably less than that of human immunodeficiency and hepatitis C viruses. By resolving individual viral haplotypes within patients, we reconstruct the timing, likely origins, and natural history of superinfecting strains. We uncover evidence for within-host recombination between genetically distinct HCMV strains, observing the loss of the parental virus containing the nonrecombinant fragment. The data suggest selection for strains containing the recombinant fragment, generating testable hypotheses about HCMV evolution and pathogenesis. These results highlight that high HCMV diversity present in some samples is caused by coinfection with multiple distinct strains and provide reassurance that within the host diversity for single-strain HCMV infections is no greater than for other herpesviruses.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1818130116","type":"journal-article","created":{"date-parts":[[2019,2,28]],"date-time":"2019-02-28T19:45:27Z","timestamp":1551383127000},"page":"5693-5698","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":126,"title":["Human cytomegalovirus haplotype reconstruction reveals high diversity due to superinfection and evidence of within-host recombination"],"prefix":"10.1073","volume":"116","author":[{"given":"Juliana","family":"Cudini","sequence":"first","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sunando","family":"Roy","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlotte J.","family":"Houldcroft","sequence":"additional","affiliation":[{"name":"Infection, Immunity, Inflammation and Physiological Medicine, Institute of Child Health, University College London, London WC1N 1EH, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josephine M.","family":"Bryant","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel P.","family":"Depledge","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena","family":"Tutill","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Veys","sequence":"additional","affiliation":[{"name":"Great Ormond Street Hospital for Children, London WC1N 3JH, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachel","family":"Williams","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Austen J. J.","family":"Worth","sequence":"additional","affiliation":[{"name":"Great Ormond Street Hospital for Children, London WC1N 3JH, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asif U.","family":"Tamuri","sequence":"additional","affiliation":[{"name":"Research Computing, University College London, London WC1E 6BT, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5148-4672","authenticated-orcid":false,"given":"Richard A.","family":"Goldstein","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8246-0534","authenticated-orcid":false,"given":"Judith","family":"Breuer","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, University College London, London WC1E 6BT, United Kingdom;"},{"name":"Infection, Immunity, Inflammation and Physiological Medicine, Institute of Child Health, University College London, London WC1N 1EH, United Kingdom;"},{"name":"Great Ormond Street Hospital for Children, London WC1N 3JH, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2019,2,28]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1128\/CMR.13.1.83","article-title":"New strategies for prevention and therapy of cytomegalovirus infection and disease in solid-organ transplant recipients","volume":"13","author":"Sia IG","year":"2000","unstructured":"IG Sia, R Patel, New strategies for prevention and therapy of cytomegalovirus infection and disease in solid-organ transplant recipients. Clin Microbiol Rev 13, 83\u2013121 (2000).","journal-title":"Clin Microbiol Rev"},{"key":"e_1_3_4_2_2","doi-asserted-by":"crossref","first-page":"e1001344","DOI":"10.1371\/journal.ppat.1001344","article-title":"Extensive genome-wide variability of human cytomegalovirus in congenitally infected infants","volume":"7","author":"Renzette N","year":"2011","unstructured":"N Renzette, B Bhattacharjee, JD Jensen, L Gibson, TF Kowalik, Extensive genome-wide variability of human cytomegalovirus in congenitally infected infants. PLoS Pathog 7, e1001344 (2011).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"e1003735","DOI":"10.1371\/journal.pgen.1003735","article-title":"Rapid intrahost evolution of human cytomegalovirus is shaped by demography and positive selection","volume":"9","author":"Renzette N","year":"2013","unstructured":"N Renzette, , Rapid intrahost evolution of human cytomegalovirus is shaped by demography and positive selection. 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J Infect Dis 215, 1673\u20131683 (2017).","journal-title":"J Infect Dis"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1038\/nrmicro.2016.182","article-title":"Clinical and biological insights from viral genome sequencing","volume":"15","author":"Houldcroft CJ","year":"2017","unstructured":"CJ Houldcroft, MA Beale, J Breuer, Clinical and biological insights from viral genome sequencing. Nat Rev Microbiol 15, 183\u2013192 (2017).","journal-title":"Nat Rev Microbiol"},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"E16","DOI":"10.3390\/pathogens7010016","article-title":"On the demographic and selective forces shaping patterns of human cytomegalovirus variation within hosts","volume":"7","author":"Sackman AM","year":"2018","unstructured":"AM Sackman, SP Pfeifer, TF Kowalik, JD Jensen, On the demographic and selective forces shaping patterns of human cytomegalovirus variation within hosts. Pathogens 7, E16 (2018).","journal-title":"Pathogens"},{"key":"e_1_3_4_8_2","first-page":"e01031","article-title":"Complexities of viral mutation rates","volume":"92","author":"Peck KM","year":"2018","unstructured":"KM Peck, AS Lauring, Complexities of viral mutation rates. J Virol 92, e01031 (2018).","journal-title":"J Virol"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"vew017","DOI":"10.1093\/ve\/vew017","article-title":"Islands of linkage in an ocean of pervasive recombination reveals two-speed evolution of human cytomegalovirus genomes","volume":"2","author":"Lassalle F","year":"2016","unstructured":"F Lassalle, , Islands of linkage in an ocean of pervasive recombination reveals two-speed evolution of human cytomegalovirus genomes. 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J Infect Dis 204, 1003\u20131007 (2011).","journal-title":"J Infect Dis"},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"161","DOI":"10.18388\/abp.2015_1162","article-title":"Multiplex real-time PCR to identify a possible reinfection with different strains of human cytomegalovirus in allogeneic hematopoietic stem cell transplant recipients","volume":"63","author":"Zawilinska B","year":"2016","unstructured":"B Zawilinska, S Szostek, J Kopec, B Piatkowska-Jakubas, M Kosz-Vnenchak, Multiplex real-time PCR to identify a possible reinfection with different strains of human cytomegalovirus in allogeneic hematopoietic stem cell transplant recipients. Acta Biochim Pol 63, 161\u2013166 (2016).","journal-title":"Acta Biochim Pol"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1086\/421496","article-title":"Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients","volume":"39","author":"Coaquette A","year":"2004","unstructured":"A Coaquette, , Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin Infect Dis 39, 155\u2013161 (2004).","journal-title":"Clin Infect Dis"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1111\/j.1399-3062.2011.00685.x","article-title":"Analysis and clinical correlation of genetic variation in cytomegalovirus","volume":"14","author":"Lisboa LF","year":"2012","unstructured":"LF Lisboa, , Analysis and clinical correlation of genetic variation in cytomegalovirus. Transpl Infect Dis 14, 132\u2013140 (2012).","journal-title":"Transpl Infect Dis"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1002\/(SICI)1096-9071(199805)55:1<75::AID-JMV12>3.0.CO;2-Z","article-title":"Glycoprotein B genotype correlates with cell tropism in vivo of human cytomegalovirus infection","volume":"55","author":"Meyer-K\u00f6nig U","year":"1998","unstructured":"U Meyer-K\u00f6nig, , Glycoprotein B genotype correlates with cell tropism in vivo of human cytomegalovirus infection. J Med Virol 55, 75\u201381 (1998).","journal-title":"J Med Virol"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"e00332","DOI":"10.1128\/mBio.00332-13","article-title":"Human cytomegalovirus (HCMV) glycoprotein gB promotes virus entry in trans acting as the viral fusion protein rather than as a receptor-binding protein","volume":"4","author":"Wille PT","year":"2013","unstructured":"PT Wille, TW Wisner, B Ryckman, DC Johnson, Human cytomegalovirus (HCMV) glycoprotein gB promotes virus entry in trans acting as the viral fusion protein rather than as a receptor-binding protein. MBio 4, e00332 (2013).","journal-title":"MBio"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/molbev\/msx304","article-title":"PHYLOSCANNER: Inferring transmission from within- and between-host pathogen genetic diversity","volume":"35","author":"Wymant C","year":"2018","unstructured":"C Wymant, , PHYLOSCANNER: Inferring transmission from within- and between-host pathogen genetic diversity. Mol Biol Evol 35, 719\u2013733 (2018).","journal-title":"Mol Biol Evol"},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1186\/1471-2105-12-119","article-title":"ShoRAH: Estimating the genetic diversity of a mixed sample from next-generation sequencing data","volume":"12","author":"Zagordi O","year":"2011","unstructured":"O Zagordi, A Bhattacharya, N Eriksson, N Beerenwinkel, ShoRAH: Estimating the genetic diversity of a mixed sample from next-generation sequencing data. 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J Virol 78, 10023\u201310033 (2004).","journal-title":"J Virol"},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1099\/0022-1317-82-6-1429","article-title":"In vitro selection of human cytomegalovirus variants unable to transfer virus and virus products from infected cells to polymorphonuclear leukocytes and to grow in endothelial cells","volume":"82","author":"Grazia Revello M","year":"2001","unstructured":"M Grazia Revello, , In vitro selection of human cytomegalovirus variants unable to transfer virus and virus products from infected cells to polymorphonuclear leukocytes and to grow in endothelial cells. J Gen Virol 82, 1429\u20131438 (2001).","journal-title":"J Gen Virol"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.meegid.2017.03.013","article-title":"Evolution of the ability to modulate host chemokine networks via gene duplication in human cytomegalovirus (HCMV)","volume":"51","author":"Scarborough JA","year":"2017","unstructured":"JA Scarborough, JR Paul, JV Spencer, Evolution of the ability to modulate host chemokine networks via gene duplication in human cytomegalovirus (HCMV). Infect Genet Evol 51, 46\u201353 (2017).","journal-title":"Infect Genet Evol"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1093\/infdis\/jiy323","article-title":"Use of whole-genome sequencing of adenovirus in immunocompromised pediatric patients to identify nosocomial transmission and mixed-genotype infection","volume":"218","author":"Houldcroft CJ","year":"2018","unstructured":"CJ Houldcroft, , Use of whole-genome sequencing of adenovirus in immunocompromised pediatric patients to identify nosocomial transmission and mixed-genotype infection. J Infect Dis 218, 1261\u20131271 (2018).","journal-title":"J Infect Dis"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"e27805","DOI":"10.1371\/journal.pone.0027805","article-title":"Specific capture and whole-genome sequencing of viruses from clinical samples","volume":"6","author":"Depledge DP","year":"2011","unstructured":"DP Depledge, , Specific capture and whole-genome sequencing of viruses from clinical samples. PLoS One 6, e27805 (2011).","journal-title":"PLoS One"},{"key":"e_1_3_4_32_2","unstructured":"J Breuer Final report summary\u2013PATHSEEK (automated next eneration sequencing for diagnostic microbiology) (European Union FP7 Health London). (2016)."},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"2470","DOI":"10.1128\/JCM.00330-16","article-title":"Comparison of next-generation sequencing technologies for comprehensive assessment of full-length hepatitis C viral genomes","volume":"54","author":"Thomson E","year":"2016","unstructured":"E Thomson, , Comparison of next-generation sequencing technologies for comprehensive assessment of full-length hepatitis C viral genomes. J Clin Microbiol; STOP-HCV Consortium 54, 2470\u20132484 (2016).","journal-title":"J Clin Microbiol"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"10389","DOI":"10.1128\/JVI.01654-13","article-title":"Mode of virus rescue determines the acquisition of VHS mutations in VP22-negative herpes simplex virus 1","volume":"87","author":"Ebert K","year":"2013","unstructured":"K Ebert, DP Depledge, J Breuer, L Harman, G Elliott, Mode of virus rescue determines the acquisition of VHS mutations in VP22-negative herpes simplex virus 1. J Virol 87, 10389\u201310393 (2013).","journal-title":"J Virol"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"2530","DOI":"10.1128\/JCM.01052-16","article-title":"Norovirus whole-genome sequencing by SureSelect target enrichment: A robust and sensitive method","volume":"54","author":"Brown JR","year":"2016","unstructured":"JR Brown, , Norovirus whole-genome sequencing by SureSelect target enrichment: A robust and sensitive method. 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