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Follicular Lymphoma in Sweden: Nationwide Improved Survival in the Rituximab Era, Particularly in Elderly Women: a Swedish Lymphoma Registry Study

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Follicular Lymphoma in Sweden: Nationwide Improved Survival in the Rituximab Era, Particularly in Elderly Women: a Swedish Lymphoma Registry Study Leukemia (2015) 29, 668–676 © 2015 Macmillan Publishers Limited All rights reserved 0887-6924/15 www.nature.com/leu ORIGINAL ARTICLE Follicular lymphoma in Sweden: nationwide improved survival in the rituximab era, particularly in elderly women: a Swedish Lymphoma Registry Study HR Junlén1, S Peterson2, E Kimby1, S Lockmer1, O Lindén3, H Nilsson-Ehle4, M Erlanson5, H Hagberg6, A Rådlund7, O Hagberg2 and BE Wahlin1 Treatment for follicular lymphoma (FL) improved with rituximab. In Sweden, first-line rituximab was gradually introduced between 2003 and 2007, with regional differences. The first national guidelines for FL were published in November 2007, recommending rituximab in first-line therapy. Using the population-based Swedish Lymphoma Registry, 2641 patients diagnosed with FL from 2000 to 2010 were identified and characterized by year and region of diagnosis, age (median, 65 years), gender (50% men), first-line therapy and clinical risk factors. Overall and relative survivals were estimated by calendar periods (2000–2002, 2003–2007 and 2008–2010) and region of diagnosis. With each period, first-line rituximab use and survival increased. Survival was superior in regions where rituximab was quickly adopted and inferior where slowly adopted. These differences were independent in multivariable analyses. Ten-year relative survival for patients diagnosed 2003–2010 was 92%, 83%, 78% and 64% in the age groups 18–49, 50–59, 60–69 and ⩾ 70, respectively. With increasing rituximab use, male sex emerged as an adverse factor. Survival improved in all patient categories, particularly in elderly women. The introduction and the establishment of rituximab have led to a nationwide improvement in FL survival. However, rituximab might be inadequately dosed in younger women and men of all ages. Leukemia (2015) 29, 668–676; doi:10.1038/leu.2014.251 INTRODUCTION MATERIALS AND METHODS Follicular lymphoma (FL), an indolent CD20+ malignancy of Swedish registries germinal B-cell origin, is the most common indolent lymphoma.1 Every clinician and pathologist/cytologist in Sweden is legally obliged to The disease is usually widespread at diagnosis and considered report each occurrence of cancer to the nationwide Swedish Cancer incurable with conventional therapy (although most kinds Registry (SCR). The registry includes diagnosis, gender, date of birth, date of therapy induce remission), because it will relentlessly of diagnosis and the hospital where the diagnosis was made, but no 2 clinical information. The SCR and its diagnostic classification were relapse. fi Rituximab, a chimeric mouse/human anti-CD20 monoclonal introduced in 1958. By the 1990s, they were insuf cient for the proper antibody, was introduced in the 1990s. Its effector mechanisms registration of most lymphoma entities. The Swedish Lymphoma Group therefore commissioned the Swedish Lymphoma Registry (SLR), which include complement-mediated cytotoxicity, antibody-dependent 17 ’ 3 was launched nationwide on 1 January 2000. The SLR s purpose was to cellular cytotoxicity and direct induction of apoptosis. In the amend the lymphoma registration with information on exact subtype, single-agent pivotal study of 1998, rituximab induced complete first-line treatment, localization, stage and other prognostic lymphoma- 4 or partial remission in half of relapsed patients. Several and patient-specific data. The SLR excludes patients o18 years old and first-line treatment trials conducted around the turn of the cases diagnosed at autopsy.17 When a patient with lymphoma is millennium showed that rituximab improved remission rates reported to the SCR, the SLR is notified and sends a form to the and remission durations when combined with conventional attending clinician, requesting additional information. The coverage in fi 5–8 SLR compared with the mandatory SCR has been 95–97% since its chemotherapeutic rst-line regimens and that is was effective 18 as monotherapy.9–12 initiation, according to yearly reports. The SLR has been validated, showing a 95% agreement between the diagnosis reported to the SLR The median overall survival (OS) in FL patients was about 9 fi 18 years in the 1990s.13 Several centers have reported improved and the actual diagnosis in the local patient les. In June 2007, 14–16 additional prognostic factors were added to the report form, allowing survival since rituximab was introduced. The aim of this the calculation of the FL International Prognostic Index (FLIPI)19 and the national population-based study was to assess patterns of FL separation of FL grades 3A and 3B. For every resident in Sweden, date of survival after the introduction of first-line rituximab and to identify death is centrally registered in the Causes of Death Registry, from which important prognostic factors in the rituximab era. survival data was obtained. 1Division of Hematology, Department of Medicine at Huddinge, Karolinska Institutet, and Hematology Center, Karolinska University Hospital, Stockholm, Sweden; 2Department of Statistics, Regional Cancer Center in South Sweden, Lund, Sweden; 3Department of Oncology, Lund University Hospital, Lund, Sweden; 4Section of Hematology and Coagulation, Department of Medicine, The Sahlgrenska Academy at the University of Gothenburg, Gothenburg, Sweden; 5Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden; 6Department of Oncology, Uppsala University Hospital, Uppsala, Sweden and 7Department of Oncology, Ryhov County Hospital, Jönköping, Sweden. Correspondence: Dr BE Wahlin, Division of Hematology, Department of Medicine at Huddinge, Karolinska Institutet, and Hematology Center, Karolinska University Hospital, M54 Hematologiskt Centrum, Karolinska Huddinge, Stockholm 141 86, Sweden. E-mail: [email protected] Received 17 July 2014; revised 11 August 2014; accepted 20 August 2014; accepted article preview online 25 August 2014; advance online publication, 19 September 2014 Follicular lymphoma survival in Sweden 2000–2010 HR Junlén et al 669 Patients population life tables stratified by sex, age and calendar period, expected 32 The studied population includes all patients in the SLR newly diagnosed survival was assessed using the Ederer II method. RSRs were calculated with FL of any grade from 1 January 2000 to 31 December 2010, excluding for patients in the three calendar periods and in four age orders (18–49, patients with a coterminous (within 90 days) diagnosis of aggressive 50–59, 60–69 and ⩾ 70 years). Multivariable models for excess mortality lymphoma. Patients were not excluded because of other diseases. All were constructed using the expectation-maximization algorithm, using a patients were observed from date of diagnosis until death, emigration or smoothed baseline excess hazard, yielding excess mortality rate ratios as 33 end of follow-up (10 February 2014). From the SLR, we obtained estimates. The excess mortality rate ratio denotes excess mortality (the information on first-line therapy, age, gender, World Health Organization difference between observed and expected mortality in the general (WHO) performance status, Ann Arbor stage, lactate dehydrogenase, population); for example, if men show an excess mortality rate ratio of 1.55, B symptoms, bulky disease and the FLIPI. We also investigated the health- it would indicate that they have 55% higher excess mortality than women. care regions: Sweden is divided into six health-care regions, each of which The RS calculations were performed using R software (Maja Pohar Perme has a population between 0.9 and 2.2 million people and a tertiary (2013): relsurv, R package version 2.0–4 (http://CRAN.R-project.org/ lymphoma center. Each region maintained regional guidelines for FL until package = relsurv)); all other calculations with Stata version 9.2 (StataCorp, November 2007, when nationwide guidelines for FL were implemented. College Station, TX, USA). This study was approved by the Ethics Committee, Stockholm, Sweden. RESULTS An overview of treatment for FL in Sweden during the study period A total of 2641 FL patients (1334 women and 1307 men) without concurrent transformation were diagnosed in Sweden from 2000 Since the early 1970 s, local radiation20 for Ann Arbor stage I and limited to 2010 (Table 1). The average number of new patients per year stage II disease was the standard of care, and this did not change during the – study period. Asymptomatic patients with widespread lymphoma have been was 240 (range, 208 266). The age-adjusted incidence rates did managed with wait-and-watch policies since decades,21 and this practice was not increase over time (Supplementary Information). The median also continued through the study period. However, with the advent of age at diagnosis was 65 years (range, 18–100) and age at rituximab, treatment algorithms for symptomatic generalized disease diagnosis increased over time (P = 0.004), whereas the number of changed radically between 2000 and 2010. In the early 2000s, first-line patients who presented at diagnosis with poor WHO performance treatment was similar to the situation in the 1990s, with the most status (P = 0.003) and bulky disease (P = 0.006) decreased. There common regimen being the polychemotherapeutic cyclophosphamide- were no changes in lactate dehydrogenase levels or B symptoms hydroxydaunorubicin-vincristine-prednisone (CHOP) regimen, followed by over time. The median follow-up time was 7.8 years (2000–2002, single oral alkylators, mostly chlorambucil. In Sweden, CHOP was particularly 12.5 years; 2003–2010, 6.6 years (2003–2007, 8.6 years; 2008–2010,
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