{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T03:52:30Z","timestamp":1780458750943,"version":"3.54.1"},"reference-count":13,"publisher":"Wiley","issue":"3","license":[{"start":{"date-parts":[[2023,12,29]],"date-time":"2023-12-29T00:00:00Z","timestamp":1703808000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/M011194\/1"],"award-info":[{"award-number":["BB\/M011194\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100015570","name":"Blood Cancer UK","doi-asserted-by":"publisher","award":["19010"],"award-info":[{"award-number":["19010"]}],"id":[{"id":"10.13039\/501100015570","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000289","name":"Cancer Research UK","doi-asserted-by":"publisher","award":["CRUK: C8333\/A29707"],"award-info":[{"award-number":["CRUK: C8333\/A29707"]}],"id":[{"id":"10.13039\/501100000289","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["pathsocjournals.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["The Journal of Pathology"],"published-print":{"date-parts":[[2024,3]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Follicular lymphoma (FL) develops through a stepwise acquisition of cooperative genetic changes with t(14;18)(q32;q21)\/\n                    <jats:italic>IGH<\/jats:italic>\n                    ::\n                    <jats:italic>BCL2<\/jats:italic>\n                    occurring early at the pre\u2010B stage of B\u2010cell development. Patients with FL typically show an indolent clinical course, remitting and relapsing with the eventual development of resistance to treatments. Interestingly, the majority of transformed FL do not progress directly from FL but originate from their clonally related lymphoma precursor (CLP) cells. To examine whether such divergent tumour evolution also underpins the relapses in patients with early\u2010stage FL, we investigated by targeted next\u2010generation sequencing 13 cases (stage I\u2009=\u20099, stage II\u2009=\u20094), who showed complete remission (mean: 5\u2009years; range: 1\u201311.5\u2009years) following local radiotherapy but subsequently relapsed (\u22652 in 5). A clonal relationship between the diagnostic FL and relapses was confirmed in 11 cases. In six cases, common and distinct variants were seen between the paired diagnostic and relapsed lymphomas, indicating their divergent evolution from a CLP. In two cases, different B\u2010cell clones were involved in the diagnostic and relapsed lymphomas, including one case involving two different\n                    <jats:italic>BCL2<\/jats:italic>\n                    translocations. In the remaining five cases, the relapsed lymphoma developed via a linear progression (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u20094) or a mixed evolutionary path (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u20091). These findings may bear important implications in the routine diagnosis and management of relapsed FL. \u00a9 2023 The Authors.\n                    <jats:italic>The Journal of Pathology<\/jats:italic>\n                    published by John Wiley &amp; Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.\n                  <\/jats:p>","DOI":"10.1002\/path.6235","type":"journal-article","created":{"date-parts":[[2023,12,29]],"date-time":"2023-12-29T03:48:21Z","timestamp":1703821701000},"page":"289-295","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Relapses in early\u2010stage follicular lymphoma frequently develop via a divergent evolution from their clonally related precursor cells"],"prefix":"10.1002","volume":"262","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5519-3351","authenticated-orcid":false,"given":"Jasmine","family":"Makker","sequence":"first","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew","family":"Wotherspoon","sequence":"additional","affiliation":[{"name":"Histopathology Department The Royal Marsden Hospital  London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria\u2010Myrsini","family":"Tzioni","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zi","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Guo","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Jiang","sequence":"additional","affiliation":[{"name":"East Genomic Laboratory Hub Cambridge University Hospitals NHS Foundation Trust  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Calogero","family":"Casa","sequence":"additional","affiliation":[{"name":"East Genomic Laboratory Hub Cambridge University Hospitals NHS Foundation Trust  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Cucco","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1017-5045","authenticated-orcid":false,"given":"Ming\u2010Qing","family":"Du","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Pathology, Department of Pathology University of Cambridge  Cambridge UK"},{"name":"Department of Histopathology, Addenbrooke's Hospital Cambridge University Hospitals NHS Foundation Trust  Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2023,12,29]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.blre.2022.100992"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1038\/ng.2856"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2013.12.027"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1038\/leu.2016.175"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41375-019-0691-6"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1002\/path.5861"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmoldx.2015.04.008"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2018-03-837039"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.3324\/haematol.2020.254854"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41375-021-01251-z"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20200573"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1158\/2159-8290.CD-23-0111"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.3324\/haematol.2013.094474"}],"container-title":["The Journal of Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pathsocjournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/path.6235","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T18:01:02Z","timestamp":1761069662000},"score":1,"resource":{"primary":{"URL":"https:\/\/pathsocjournals.onlinelibrary.wiley.com\/doi\/10.1002\/path.6235"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,29]]},"references-count":13,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2024,3]]}},"alternative-id":["10.1002\/path.6235"],"URL":"https:\/\/doi.org\/10.1002\/path.6235","archive":["Portico"],"relation":{},"ISSN":["0022-3417","1096-9896"],"issn-type":[{"value":"0022-3417","type":"print"},{"value":"1096-9896","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,29]]},"assertion":[{"value":"2023-05-24","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-11-13","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-12-29","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}