{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T20:05:54Z","timestamp":1785787554044,"version":"3.56.0"},"reference-count":35,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T00:00:00Z","timestamp":1737676800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,5,19]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Patients with haematological malignancies are at increased risk of developing skin cancer and often experience worse skin cancer-related outcomes. However, there is a lack of nationwide, population-based data with long-term follow-up on the incidence and risks of different skin cancer types across all haematological malignancies.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Objectives<\/jats:title>\n                  <jats:p>To assess population-based risk estimates for cutaneous squamous cell carcinoma (cSCC), malignant melanoma (MM), Merkel cell carcinoma (MCC) and basal cell carcinoma (BCC) among patients with haematological malignancies, stratified by skin cancer type and haematological malignancy subgroup. These estimates can serve as a base for surveillance guidelines and patient education.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>This nationwide population-based epidemiological cohort study used data from 210 794 patients diagnosed with a haematological malignancy between 1989 and 2020 from the Netherlands Cancer Registry (NCR). In addition, data on each type of histopathologically confirmed skin cancer per patient after haematological malignancy diagnosis were retrieved from the NCR. Patients with a history of skin cancer prior to their haematological malignancy were excluded. Cumulative incidences, standardized incidence ratios (SIRs) and absolute excess risks for each of the four skin cancers were calculated and stratified by haematological malignancy subgroup, age, sex, follow-up and primary treatment.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>The overall 10-year cumulative incidence of developing a first skin cancer was 2.6% for cSCC, 0.5% for MM, 0.05% for MCC and 4.8% for BCC. Compared with the general population, nearly all haematological malignancy subgroups showed more than a twofold increased risk of cSCC, MM, MCC and BCC. Patients with chronic lymphocytic leukaemia (CLL) showed the highest risks for each of the four skin cancers, with SIRs of 4.4 for cSCC, 2.7 for MM, 9.3 for MCC, and 2.6 for BCC. These elevated risks persisted for &amp;gt; 30\u2005years after haematological malignancy diagnosis.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Patients with all types of haematological malignancies, and especially those with CLL, have a lifetime increased risk of developing different types of skin cancer. These findings highlight the importance of creating awareness among patients and care providers about this increased risk and promoting sun-protective measures and regular skin self-examinations in this high-risk population.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/bjd\/ljaf027","type":"journal-article","created":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T18:29:36Z","timestamp":1737743376000},"page":"1029-1037","source":"Crossref","is-referenced-by-count":13,"title":["Skin cancer risk in more than 200 000 patients with haematological malignancies over 30\u2005years: a nationwide population-based study in the Netherlands"],"prefix":"10.1093","volume":"192","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1669-0283","authenticated-orcid":false,"given":"Celeste J","family":"Eggermont","sequence":"first","affiliation":[{"name":"Department of Dermatology, Erasmus MC Cancer Institute, University Medical Center , Rotterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9211-822X","authenticated-orcid":false,"given":"Andrya","family":"Hollatz","sequence":"additional","affiliation":[{"name":"Department of Dermatology, Erasmus MC Cancer Institute, University Medical Center , Rotterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8578-901X","authenticated-orcid":false,"given":"Marlies","family":"Wakkee","sequence":"additional","affiliation":[{"name":"Department of Dermatology, Erasmus MC Cancer Institute, University Medical Center , Rotterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9011-6741","authenticated-orcid":false,"given":"Marieke","family":"Louwman","sequence":"additional","affiliation":[{"name":"Department of Research and Development, Netherlands Comprehensive Cancer Organization (IKNL) , Utrecht ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4767-6716","authenticated-orcid":false,"given":"Avinash\u00a0G","family":"Dinmohamed","sequence":"additional","affiliation":[{"name":"Department of Public Health, Erasmus MC, University Medical Center , Rotterdam ,","place":["the Netherlands"]},{"name":"Department of Hematology, Amsterdam University Medical Center, Cancer Center Amsterdam , Amsterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0882-2346","authenticated-orcid":false,"given":"Eduardus F M","family":"Posthuma","sequence":"additional","affiliation":[{"name":"Department of Research and Development, Netherlands Comprehensive Cancer Organization (IKNL) , Utrecht ,","place":["the Netherlands"]},{"name":"Department of Internal Medicine, Reinier de Graaf Hospital , Delft ,","place":["the Netherlands"]},{"name":"Department of Hematology, Leiden University Medical Center , Leiden ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9940-2875","authenticated-orcid":false,"given":"Tamar","family":"Nijsten","sequence":"additional","affiliation":[{"name":"Department of Dermatology, Erasmus MC Cancer Institute, University Medical Center , Rotterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8922-6791","authenticated-orcid":false,"given":"Loes","family":"Hollestein","sequence":"additional","affiliation":[{"name":"Department of Dermatology, Erasmus MC Cancer Institute, University Medical Center , Rotterdam ,","place":["the Netherlands"]},{"name":"Department of Research and Development, Netherlands Comprehensive Cancer Organization (IKNL) , Utrecht ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,1,24]]},"reference":[{"key":"2025052712580684000_ljaf027-B1","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1111\/ijd.12208","article-title":"Lymphoma-associated skin cancer: incidence, natural history, and clinical management","volume":"53","author":"Brewer","year":"2014","journal-title":"Int J Dermatol"},{"key":"2025052712580684000_ljaf027-B2","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1038\/s41408-021-00574-5","article-title":"Risk of second primary malignancies in patients with follicular lymphoma: a \u00adpopulation-based study in the Netherlands, 1989\u20132018","volume":"11","author":"Dinnessen","year":"2021","journal-title":"Blood Cancer J"},{"key":"2025052712580684000_ljaf027-B3","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.clml.2018.05.021","article-title":"Trends in the risks of secondary cancers in patients with Hodgkin lymphoma","volume":"18","author":"Kumar","year":"2018","journal-title":"Clin Lymphoma Myeloma Leuk"},{"key":"2025052712580684000_ljaf027-B4","doi-asserted-by":"crossref","first-page":"e121","DOI":"10.1038\/bcj.2013.19","article-title":"Patterns of second primary malignancy risk in multiple myeloma patients before and after the introduction of novel therapeutics","volume":"3","author":"Razavi","year":"2013","journal-title":"Blood Cancer J"},{"key":"2025052712580684000_ljaf027-B5","doi-asserted-by":"crossref","first-page":"3204","DOI":"10.1080\/10428194.2019.1620941","article-title":"Risk factors for skin cancer and solid tumors in newly diagnosed patients with chronic lymphocytic leukemia and the impact of skin surveillance on survival","volume":"60","author":"Ishdorj","year":"2019","journal-title":"Leuk Lymphoma"},{"key":"2025052712580684000_ljaf027-B6","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1038\/s41408-023-00784-z","article-title":"Risk of second primary malignancies in patients with chronic lymphocytic leukemia: a population-based study in the Netherlands, 1989\u20132019","volume":"13","author":"van der Straten","year":"2023","journal-title":"Blood Cancer J"},{"key":"2025052712580684000_ljaf027-B7","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1111\/ijd.15813","article-title":"Cutaneous squamous cell carcinoma in patients with chronic lymphocytic leukemia: a systematic review of the literature","volume":"61","author":"Lai","year":"2022","journal-title":"Int J Dermatol"},{"key":"2025052712580684000_ljaf027-B8","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1200\/JCO.2011.34.9605","article-title":"Chronic lymphocytic leukemia is associated with decreased survival of patients with malignant melanoma and Merkel cell carcinoma in a SEER \u00adpopulation-based study","volume":"30","author":"Brewer","year":"2012","journal-title":"J Clin Oncol"},{"key":"2025052712580684000_ljaf027-B9","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1001\/jama.1975.03250030023012","article-title":"Subsequent neoplasia in chronic lymphocytic leukemia","volume":"232","author":"Manusow","year":"1975","journal-title":"JAMA"},{"key":"2025052712580684000_ljaf027-B10","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1016\/j.jaad.2014.10.028","article-title":"Increased incidence and recurrence rates of nonmelanoma skin cancer in patients with non-Hodgkin lymphoma: a Rochester Epidemiology Project \u00adpopulation-based study in Minnesota","volume":"72","author":"Brewer","year":"2015","journal-title":"J Am Acad Dermatol"},{"key":"2025052712580684000_ljaf027-B11","doi-asserted-by":"crossref","first-page":"e0258423","DOI":"10.1371\/journal.pone.0258423","article-title":"Detailing the epidemiological and clinical characteristics of chronic lymphocytic leukaemia in Portugal \u2013 results from a population-based cancer registry cohort study","volume":"16","author":"Cardoso Borges","year":"2021","journal-title":"PLOS ONE"},{"key":"2025052712580684000_ljaf027-B12","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1111\/ejh.12748","article-title":"Risk of skin cancer in multiple myeloma patients: a retrospective cohort study","volume":"97","author":"Robinson","year":"2016","journal-title":"Eur J Haematol"},{"key":"2025052712580684000_ljaf027-B13","doi-asserted-by":"crossref","first-page":"2203","DOI":"10.1038\/s41375-018-0027-y","article-title":"Second malignancies in patients with myeloproliferative neoplasms: a \u00adpopulation-based cohort study of 9379 patients","volume":"32","author":"Landtblom","year":"2018","journal-title":"Leukemia"},{"key":"2025052712580684000_ljaf027-B14","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1093\/ije\/23.6.1111","article-title":"The capture-\u00adrecapture method for estimation of cancer registry \u00adcompleteness: a useful tool?","volume":"23","author":"Schouten","year":"1994","journal-title":"Int J Epidemiol"},{"key":"2025052712580684000_ljaf027-B15","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1111\/bjd.20871","article-title":"A nationwide study of the incidence and trends of first and multiple basal cell carcinomas in the Netherlands and prediction of future incidence","volume":"186","author":"Schreuder","year":"2022","journal-title":"Br J Dermatol"},{"key":"2025052712580684000_ljaf027-B16","volume-title":"Jack A","author":"Fritz","year":"2000"},{"key":"2025052712580684000_ljaf027-B17","first-page":"1","volume-title":"Statistical methods in cancer research. Volume II--The design and analysis of cohort studies","author":"Breslow","year":"1987"},{"key":"2025052712580684000_ljaf027-B18","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1136\/bmj.39335.541782.AD","article-title":"Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies","volume":"335","author":"von Elm","year":"2007","journal-title":"BMJ"},{"key":"2025052712580684000_ljaf027-B19","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1136\/bmj.310.6993.1491","article-title":"Evidence of an association between non-Hodgkin's lymphoma and skin cancer","volume":"310","author":"Adami","year":"1995","journal-title":"BMJ"},{"key":"2025052712580684000_ljaf027-B20","doi-asserted-by":"crossref","first-page":"1847","DOI":"10.1038\/bjc.1996.642","article-title":"Non-Hodgkin's lymphomas, chronic lymphocytic leukaemias and skin cancers","volume":"74","author":"Levi","year":"1996","journal-title":"Br J Cancer"},{"key":"2025052712580684000_ljaf027-B21","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1158\/1055-9965.EPI-05-0895","article-title":"Merkel cell carcinoma and multiple primary cancers","volume":"15","author":"Howard","year":"2006","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"2025052712580684000_ljaf027-B22","doi-asserted-by":"crossref","first-page":"e287","DOI":"10.1111\/ijd.12564","article-title":"Increased incidence of malignant melanoma and other rare cutaneous cancers in the setting of chronic lymphocytic leukemia","volume":"54","author":"Brewer","year":"2015","journal-title":"Int J Dermatol"},{"key":"2025052712580684000_ljaf027-B23","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1001\/jamadermatol.2015.5152","article-title":"Competing risk of death in Kaplan\u2013Meier curves when analyzing subsequent keratinocyte cancer","volume":"152","author":"Verkouteren","year":"2016","journal-title":"JAMA Dermatol"},{"key":"2025052712580684000_ljaf027-B24","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1001\/jamadermatol.2022.0036","article-title":"Spectrum of nonkeratinocyte skin cancer risk among solid organ transplant recipients in the US","volume":"158","author":"Sargen","year":"2022","journal-title":"JAMA Dermatol"},{"key":"2025052712580684000_ljaf027-B25","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.jaad.2023.10.036","article-title":"Cumulative incidence and timing of subsequent cutaneous squamous cell carcinomas stratified for patients with organ transplantation and hematologic malignancies: a nationwide cohort study","volume":"90","author":"Eggermont","year":"2024","journal-title":"J Am Acad Dermatol"},{"key":"2025052712580684000_ljaf027-B26","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.ejca.2022.03.043","article-title":"Diagnosis and treatment of Merkel cell carcinoma: European consensus-based interdisciplinary guideline \u2013 update 2022","volume":"171","author":"Gauci","year":"2022","journal-title":"Eur J Cancer"},{"key":"2025052712580684000_ljaf027-B27","doi-asserted-by":"crossref","first-page":"20","DOI":"10.3389\/fonc.2019.00020","article-title":"Merkel cell polyoma viral load and intratumoral CD8+ lymphocyte infiltration predict overall survival in patients with Merkel cell carcinoma","volume":"9","author":"von der Grun","year":"2019","journal-title":"Front Oncol"},{"key":"2025052712580684000_ljaf027-B28","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1126\/science.1152586","article-title":"Clonal integration of a polyomavirus in human Merkel cell carcinoma","volume":"319","author":"Feng","year":"2008","journal-title":"Science"},{"key":"2025052712580684000_ljaf027-B29","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1001\/jamadermatol.2013.6249","article-title":"Association of advanced leukemic stage and skin cancer tumor stage with poor skin cancer outcomes in patients with chronic lymphocytic leukemia","volume":"150","author":"Velez","year":"2014","journal-title":"JAMA Dermatol"},{"key":"2025052712580684000_ljaf027-B30","doi-asserted-by":"crossref","first-page":"113251","DOI":"10.1016\/j.ejca.2023.113251","article-title":"European \u00adconsensus-based interdisciplinary guideline for invasive cutaneous squamous cell carcinoma. Part 1: Diagnostics and prevention\u00a0\u2013 update 2023","volume":"193","author":"Stratigos","year":"2023","journal-title":"Eur J Cancer"},{"key":"2025052712580684000_ljaf027-B31","doi-asserted-by":"crossref","first-page":"113254","DOI":"10.1016\/j.ejca.2023.113254","article-title":"European \u00adconsensus-based interdisciplinary guideline for diagnosis and treatment of basal cell carcinoma \u2013 update 2023","volume":"192","author":"Peris","year":"2023","journal-title":"Eur J Cancer"},{"key":"2025052712580684000_ljaf027-B32","doi-asserted-by":"crossref","first-page":"108226","DOI":"10.1016\/j.envint.2023.108226","article-title":"Global, regional and national burdens of non-melanoma skin cancer attributable to occupational exposure to solar ultraviolet radiation for 183 countries, 2000\u20132019: a systematic analysis from the WHO\/ILO Joint Estimates of the Work-related Burden of Disease and Injury","volume":"181","author":"Pega","year":"2023","journal-title":"Environ Int"},{"key":"2025052712580684000_ljaf027-B33","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.blre.2005.01.007","article-title":"Chronic graft-versus-host disease","volume":"20","author":"Horwitz","year":"2006","journal-title":"Blood Rev"},{"key":"2025052712580684000_ljaf027-B34","doi-asserted-by":"crossref","first-page":"3802","DOI":"10.1182\/blood-2004-09-3411","article-title":"Impact of chronic GVHD therapy on the development of squamous-cell cancers after hematopoietic stem-cell transplantation: an international case-control study","volume":"105","author":"Curtis","year":"2005","journal-title":"Blood"},{"key":"2025052712580684000_ljaf027-B35","doi-asserted-by":"crossref","first-page":"3667","DOI":"10.1038\/s41467-018-06027-1","article-title":"The genomic landscape of cutaneous SCC reveals drivers and a novel azathioprine associated mutational signature","volume":"9","author":"Inman","year":"2018","journal-title":"Nat Commun"}],"container-title":["British Journal of Dermatology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bjd\/advance-article-pdf\/doi\/10.1093\/bjd\/ljaf027\/61621810\/ljaf027.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bjd\/article-pdf\/192\/6\/1029\/61621810\/ljaf027.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bjd\/article-pdf\/192\/6\/1029\/61621810\/ljaf027.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,27]],"date-time":"2025-05-27T16:59:22Z","timestamp":1748365162000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bjd\/article\/192\/6\/1029\/7978933"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,24]]},"references-count":35,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2025,1,24]]},"published-print":{"date-parts":[[2025,5,19]]}},"URL":"https:\/\/doi.org\/10.1093\/bjd\/ljaf027","relation":{},"ISSN":["0007-0963","1365-2133"],"issn-type":[{"value":"0007-0963","type":"print"},{"value":"1365-2133","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,6]]},"published":{"date-parts":[[2025,1,24]]}}}