Временные модели выживаемости пациентов из числа населения США среди взрослых, которые лечатся химиотерапией и/или иммунной терапией по множеству миелом, 2000-2020.

INTRODUCTION

Over the past two decades in the United States, the age‐standardized incidence rate of multiple myeloma (MM) increased from 5.8/100 000 in 2000 to 6.9/100 000 in 2019, while the age‐standardized death rate decreased from 3.8/100 000 in 2000 to 3.1/100 000 in 2019. 1 Although MM remains incurable with conventional treatment, the introduction of autologous haematopoietic stem cell transplantation in the 1990s and novel therapeutics over the past two decades have contributed to the improved patient survival that has been reported within and outside of the United States. 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 However, population‐based studies of MM evaluating survival among adults of all ages have largely included all affected patients irrespective of treatment status. 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 Although patients with MM generally receive treatment at the time of diagnosis, some may not be candidates for systemic therapy, others may decline therapy and those with smouldering MM may delay therapy until myeloma‐defining events occur. Therefore, evaluation of population‐based cohorts restricted to patients reported to have received chemotherapy and/or immunotherapy (chemo/immunotherapy) at diagnosis provides a unique opportunity to better assess the impact of treatment over time.

Prior population‐based, 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 clinical, 28 , 29 , 30 specialty registry 31 , 32 , 33 , 34 , 35 and institutional studies 36 , 37 , 38 of treated patients with MM have considered various patient groups restricted in age (e.g. ≥65 years) and/or race and ethnicity, with many studies completing follow‐up in the early 2010s or earlier, thereby limiting generalizability to US adults treated during a more recent era of numerous therapeutic advances. Therefore, we sought to characterize the adult MM patient population in the US and evaluate patient survival among those initially treated with chemo/immunotherapy. We assessed calendar trends in patient survival during 2000–2019 when the therapeutic landscape of MM substantially evolved, 39 , 40 and evaluated differences in patient survival by age at diagnosis of MM, sex, race and ethnicity and quintiles of county‐level median household income.

METHODS

We used data from 17 cancer registry areas of the Surveillance, Epidemiology and End Results (SEER) Program that represent approximately 26.5% of the US population, including coverage of White (22.4%), Black (23.1%), Asian (46.5%), Native Hawaiian and Pacific Islander (Pacific Islander) (62.3%) and Hispanic (35.9%) persons. 41 The information collected by SEER Program registries includes tumour characteristics, patient demographics, initial treatment in broad categories [e.g. any chemotherapy (yes vs. no/unknown), any immunotherapy (yes vs. no/unknown)], vital status and county‐level attributes from linkages to Census and American Community Survey data. Tumour morphology is coded according to the International Classification of Diseases for Oncology, 3rd edition (ICD‐O‐3). There is no dedicated ICD‐O‐3 code for smouldering myeloma. SEER defines initial therapy as all treatments administered to the patient as part of the initial treatment plan at time of diagnosis, irrespective of the time it takes to complete. The first course of treatment (initial therapy) ends when the initial treatment plan ends or at the time of documentation of disease progression, relapse or treatment failure, whichever occurs first. For haematopoietic neoplasms, initial ‘treatment’ may involve observation alone (i.e. supportive measures) that do not meet the usual SEER definition of treatment that ‘modifies, controls, removes or destroys proliferating cancer tissue’. Therefore, a patient followed with active surveillance alone following a diagnosis of MM (i.e. smouldering myeloma) would be included within the ‘no/unknown’ chemotherapy and ‘no/unknown’ immunotherapy treatment categories. The SEER Program does not collect information on MM staging, cytogenetic features, patient comorbidities, specific drug names and doses nor treatment administered after initial therapy or for disease relapse or progression (i.e. subsequent therapy). Data on Collaborative Stage Site‐specific Factors for MM and haematopoietic stem cell transplantation are not publicly available.

We identified 102 999 patients diagnosed with MM during 2000–2019 (followed through 2020). For consistency, we included patients diagnosed with plasma cell myeloma (ICD‐O‐3 code 9732) or plasma cell leukaemia (9733). Although plasma cell leukaemia was coded separately from multiple myeloma between 2000 and 2009, the code 9733 became obsolete in 2010 and all cases of plasma cell leukaemia were subsequently coded to 9732. Between 2000 and 2009, plasma cell leukaemia ( n = 235) accounted for 0.76% of total MM cases ( n = 31 056). To best align with the Revised International Myeloma Working Group diagnostic criteria for multiple myeloma that requires ≥10% bone marrow plasma cells or biopsy‐proven plasmacytoma in addition to at least one other MM‐defining event, we limited our study population to patients with first primary, microscopically confirmed MM (Figure 1 ). Our final population included 74 102 adults with MM, and we limited our survival analysis to the 50 288 (67.9%) adults reported to have received initial chemo/immunotherapy.

Similar to other studies, we used calendar year as a proxy for available treatments, recognizing that not all would be administered in the first‐line setting. 42 , 43 , 44 We assessed patient survival according to year of diagnosis within each of four 5‐year calendar periods: 2000–2004 (introduction of the first proteosome inhibitor for relapsed/refractory MM), 2005–2009 (introduction of immunomodulatory drugs for newly diagnosed or relapsed/refractory MM), 2010–2014 (availability of additional proteosome inhibitors and immune modulators for relapsed/refractory MM) and 2015–2019 (introduction of monoclonal antibodies and histone deacetylase inhibitors for newly diagnosed MM or relapsed and/or refractory MM), 40 with progressively increasing use of combination therapies in initial and subsequent lines of therapy, particularly in the most recent decade, as new drugs have been introduced.

To examine temporal patterns in patient survival, we assessed overall and relative survival across calendar periods of diagnosis among patients with newly diagnosed MM treated with initial chemo/immunotherapy. To assess differences in survival within our cohort (i.e. internal comparison), we estimated overall survival (OS) and fitted multivariable Cox proportional hazard regression models with all‐cause mortality as the outcome, using time since diagnosis of MM as the time scale to calculate hazard ratios (HRs) and corresponding 95% confidence intervals (CIs), mutually adjusted for age, sex, race and ethnicity and county‐level median household income. We compared OS across and within calendar periods (2000–2004, 2005–2009, 2010–2014, 2015–2019) in stratified models by age at diagnosis (20–44, 45–64, 65–74, 80–99 years), sex (females, males), race and ethnicity [Hispanic, inclusive of all races; non‐Hispanic Asian (Asian); non‐Hispanic Black (Black); non‐Hispanic Pacific Islander (Pacific Islander); other non‐Hispanic and unknown race; and non‐Hispanic White (White)] and quintiles of county‐level median household income (<$55 000; $55 000–$64 999; $65 000–$69 999; $70 000–$74 999; ≥$75 000). County‐level median household income was defined as household income from the past 12 months, measured in 2019 inflation‐adjusted US dollars. This was ascertained by linkage of an individual's residing county during the year of cancer diagnosis matched to the closest year of the American Community Survey. This variable was used as a proxy for socioeconomic status; quintiles were developed based on the distribution of the cohort and available SEER categories.

To assess survival differences within each calendar period for patients treated with initial chemo/immunotherapy by age, sex, race and ethnicity and county‐level median household income within our cohort, we used adjusted Cox proportional hazards regression models to compare OS by age at diagnosis (45–64 years = reference), sex (males = reference), race and ethnicity (White = reference) and quintiles of county‐level median household income (≥$75 000 = reference). Cox proportional hazard models were generated using SAS (version 9.4, Cary, NC). Two‐sided p ‐values less than 0.05 were considered statistically significant.

In our cohort analysis, we also assessed actuarial relative survival (RS)—a measure of the proportion of observed MM survivors in a population relative to the proportion of expected survivors in the general population matched on age, sex, race and ethnicity and calendar year of diagnosis (i.e. external comparison)—in our patient population treated with initial chemo/immunotherapy. We estimated RS and corresponding 95% CIs using the Survival session in SEER*Stat (version 8.4.3). For each calendar year period (with one additional year of follow‐up), we estimated RS overall and according to age groups, sex, race and ethnicity and quintiles of county‐level median household income described above. Because survival tables in the general population during our study period only consider Asian and Pacific Islander individuals in aggregate, we were unable to provide disaggregated Pacific Islander data for the RS estimates.

RESULTS

The characteristics of all 74 102 adult patients diagnosed with first primary, microscopically confirmed MM during 2000–2019 and the 67.9% ( n = 50 288) that were reported to have received initial chemo/immunotherapy are detailed in Table 1 according to four calendar periods. The proportion of patients receiving initial chemo/immunotherapy increased progressively over time, from 61.2% during 2000–2004 to 72.8% during 2015–2019, with the most notable increase observed among individuals ages 65–79 and ≥80 years. A similar pattern was observed among males and females, for all racial and ethnic groups, and across all county‐level median household income quintiles.

Among adults initially treated with chemo/immunotherapy for MM, we observed improved OS and RS over time, overall and across each patient group. In the multivariable Cox analyses, OS improved significantly in each calendar period compared to 2000–2004 (Figure 2 ; Table S1 ). These gains in OS were also observed for each age and sex group and suggested in most race and ethnicity groups, as well as among MM patients in each county‐level median household income quintile. Consistent with findings of OS, the 5‐year RS improved over time, from 37.7% in 2000–2004 to 60.3% in 2015–2019 (Figure S1 ; Table S2 ). Increases in RS were observed among all age groups, both sexes, all racial and ethnic groups and across all quintiles of county‐level median household income. In general, the most notable rise in RS was observed between 2000–2004 and 2005–2009, with progressive but more attenuated survival increases continuing through 2015–2019.

Despite improvements in survival over time, we observed important mortality differences within each calendar period by age, sex, race and ethnicity and quintiles of county‐level median household income. Compared to those aged 45–64 years, the risk of death was consistently lower among those aged 20–44 years (HR range = 0.65–0.70, all p < 0.0001) and higher among those aged 65–79 (HR range = 1.65–1.78, all p < 0.0001) and ≥80 years (HR range = 2.76–3.32, all p < 0.0001) in each calendar period (Figure 3 ; Table S3 ). Compared with males, females had a consistent and significantly lower risk of death in each of the four time periods (HR range = 0.89–0.92, all p < 0.001). Black, Hispanic and Pacific Islander patients experienced worse survival across nearly all calendar periods compared with White patients, whereas OS was similar among Asian patients. Notably, the risk of death was significantly higher among Pacific Islander patients compared with White patients across all time periods (HR range = 1.37–1.85, all p < 0.05), with the most pronounced risk observed for those diagnosed in the most recent calendar year period (HR Pacific Islander = 1.85, 95% CI = 1.40–2.44, p < 0.0001). Black patients had a higher risk of death in 2000–2004 (HR Black = 1.08, p = 0.0093) and 2015–2019 (HR Black = 1.07, p = 0.0436), with more modest differences in the intervening calendar periods (HR Black = 0.99–1.04; p > 0.05) compared with White patients. Hispanic patients had a higher risk of death compared with White patients in each calendar year period, including in 2015–2019 (White = reference; HR Hispanic = 1.08, 95% CI = 1.00–1.16), although not all HRs reached statistical significance. For each calendar period, patients living in the lowest income counties (<$55 000 HR range = 1.08–1.27, all p < 0.02; $55 000–$64 999 HR range = 1.10–1.19, all p < 0.01) had the highest risk of death compared to those living in the wealthiest (≥$75 000) counties, a finding which was most prominent in the most recent decade (≥$75 000 = reference; 2010–2014: HR <$55 000 = 1.25, 95% CI = 1.18–1.33; 2015–2019: HR <$55 000 = 1.27, 95% CI = 1.18–1.37).

DISCUSSION

This US population‐based study of patient survival among individuals diagnosed with MM and treated with initial chemo/immunotherapy is among the first to comprehensively assess the impact of contemporary treatment on survival and mortality over the past two decades among adults of all ages and across demographic backgrounds. We observed a progressive increase over time in the fraction of patients receiving initial chemo/immunotherapy for newly diagnosed MM, particularly among older age groups. Among treated MM patients, we noted continued and significant survival gains overall and across patients of all age groups, males and females, most racial and ethnic groups and all county‐level median household income quintiles. Multiple factors may have contributed to the improved patient survival noted in our study, including increasing availability of effective therapies for use in first and subsequent lines of MM therapy; effective use of drugs in combination, particularly in the most recent decade; improvement in supportive care measures; and advances in laboratory testing and imaging modalities that could lead to earlier disease detection and more accurate staging. However, despite the improvement in survival, we identified important OS differences by patient subgroups that were persistent across calendar periods, with worse survival observed among older individuals; male patients; Black, Hispanic and Pacific Islander patients; and patients living in counties with lower median household income.

The introduction of new therapies, particularly as drugs are used in combination in initial and subsequent lines of treatment, has been associated with survival improvements in patients with MM. 36 , 38 , 45 In the United States, between 1999 and 2007, the use of new therapies (e.g. immunomodulatory agents, proteosome inhibitors) for MM increased from 3.9% to 75.5%. 39 A large, European, population‐based study using EUROCARE data from 20 countries noted significant improvement in MM/plasmacytoma survival between 1997–1999 and 2006–2008. 46 Although the study included all cancer registry patients irrespective of treatment status, thalidomide and bortezomib were noted to be available in Europe in 1998 and 2003, respectively, similar to the availability of these drugs in the United States. Although thalidomide was first approved in 2006 for treatment of MM in the third‐line setting in the United States, its initial approval was in 1998 for other indications. By limiting our study to adults receiving initial therapy, we show that survival improvements in newly diagnosed patients began in the era of immunomodulatory agents and proteasome inhibitors and continued through the most recent time period, 2015–2019. However, our novel findings of continued survival differences among patient sociodemographic groups within each calendar period suggest that unmet medical needs persist across select patient groups.

We found that the proportion of patients receiving initial chemo/immunotherapy increased progressively during the study period, and most notably for older patients. A prior SEER‐based study of all patients with MM irrespective of treatment status covering an earlier period (1973–2009) found that 5‐year survival had improved across all age groups except those ≥80 years. 6 Focusing on patients ≥80 years, a SEER‐Medicare study between 2007 and 2013 reported a median overall survival of 21.4 months among those receiving systemic therapy in contrast to 6.4 months among those not receiving systemic treatment. 22 Our observations that the fraction of individuals 65–79 and ≥80 years who received initial chemoimmunotherapy increased in excess of 20% in 2015–2019 compared to 2000–2004, along with improved survival estimates in these age groups, indicate that an increasing fraction of older patients are benefiting from treatment, although older age remains an important adverse risk factor for survival.

During 2000–2019, MM patient survival also progressively and significantly improved among males and females treated with initial chemo/immunotherapy, yet males had a higher risk of death than females across each of the four calendar periods. Male sex has been identified as a risk for inferior survival in other registry studies of MM in the United States and Europe 10 , 47 , 48 and in various other databases. 31 , 49 , 50 , 51 Derman and colleagues hypothesized that females with MM may have more health promoting behaviours, fewer comorbidities, distinct disease biology and/or different innate and adaptive immune responses to therapy contributing to their more favourable survival than seen in males. 51 A phase III clinical trial from the United Kingdom found that females were more likely than males to have high risk molecular lesions [e.g. t(14;16) and del(17p)] but did not observe differences in overall survival, despite adverse molecular features. 52 Additional research is needed to understand and address factors potentially underpinning the observed sex differences identified in clinical trials and registry studies of MM.

Reflecting the SEER Program's catchment areas, our study included relatively large numbers of patients from diverse racial and ethnic groups. 41 In contrast, clinical trials of patients with MM, even when results are pooled, often have limited power to detect survival differences among racial and ethnic minoritized populations due to their underrepresentation in clinical trials. 28 , 29 , 30 , 53 Because race is a social construct, the findings from our analysis should be interpreted in the context of underlying social drivers of health, such as socioeconomic status. 53 Due to our focus on patients reported to have received initial chemo/immunotherapy for MM, we can infer that myeloma therapies were available, accessible and acceptable to the patients in our treated study population at the time of initial diagnosis. Prior studies have reported that when treatment access and uptake are equal for White and Black patients, survival among Black patients often exceeds that of White patients. 21 , 23 , 31 , 33 , 35 , 54 We report worse survival for Black patients compared with White patients, most prominently for MM diagnosed in the earliest and most recent time periods. Although we were unable to assess how differences in disease characteristics (e.g. stage, cytogenetics), patient comorbidities and choice of initial or subsequent therapy differed by race and ethnicity or socioeconomic status, prior studies have assessed some of these characteristics. For example, haematopoietic stem cell transplantation utilization in the United States for the treatment of MM increased during 2008–2014 but was significantly lower among Black and Hispanic patients compared with White patients. 34 While data for haematopoietic stem cell transplantation utilization among Pacific Islander patients are limited, we note that Hawaii, a contributing SEER Registry, does not have a haematopoietic stem cell transplant centre for adults. 55 Furthermore, studies from New Zealand and Australia have reported that Māori and other Pacific Islander patients with MM have significantly more comorbidities (e.g. diabetes, renal insufficiency), more chromosomal abnormalities, including t(4;14), and other high‐risk features of MM than non‐Māori and non‐Pacific Islander patients. 9 , 56 Additional research is needed to understand the intersectional complexities between distinct disease characteristics, 56 , 57 differences in drug metabolism 57 and other biological, cultural, social, behavioural, psychosocial and/or physical factors that may influence access to high quality or necessary health care (e.g. barriers to treatment access and adherence, absence or presence of transplantation services, transportation challenges) that could contribute to the observed lower survival among Black, Hispanic and Pacific Islander patients and those living in lower resourced counties.

Strengths of our study include the large numbers and representativeness of our population‐based analysis of adult patients of all ages with MM initially treated with chemo/immunotherapy, thus allowing analyses by age, sex, race and ethnicity and county‐level median household income across four calendar periods. Our study is the first to characterize OS for Pacific Islander patients with MM separately from Asian patients who were treated with chemo/immunotherapy in the United States. This finding is a critical addition to the literature, as research has historically aggregated these races 58 , 59 despite evidence of increased cancer mortality rates 60 and higher mortality rates for most causes of death (e.g. diabetes, heart disease, stroke) for Pacific Islander versus Asian populations. 61 Unfortunately, we were underpowered to examine survival for American Indian/Alaska Native patients and could not disaggregate the heterogeneous Hispanic patient population. We note that capture of initial chemotherapy information in SEER has been found to have a positive predictive value exceeding 85% 62 ; however, completeness of capture of immunotherapy has not been rigorously evaluated, and coding of immunotherapy has evolved over time, with some agents initially coded as chemotherapy prior to 2013. These were among the factors that precluded us from separately evaluating chemotherapy and immunotherapy. Furthermore, we lacked information on specific drug names, subsequent therapies, supportive therapies and select disease (e.g. stage) and patient characteristics (e.g. performance status), because these data are not available in SEER. We cannot determine the extent to which subsequent therapies, supportive therapies and improvements in laboratory testing and diagnostic imaging contributed to improvements in survival over time. While our results are largely generalizable to treated MM patients in the US population as they are not limited by eligibility criteria encountered in clinical trials and incorporate patients treated in community and academic settings, it is important to consider how geographic differences for SEER versus non‐SEER catchment areas might reflect varying racial and ethnic patterns in mortality.

Overall, among adults with newly diagnosed MM in the United States reported to have received initial chemo/immunotherapy, we found progressive and significant improvement in patient survival over the past two decades across patient groups within all demographic characteristics. Nevertheless, we identified patient groups at heightened risk for death, including adults of older age; male sex; Black, Hispanic and Pacific Islander race and ethnicity; and those living in lower income counties. These survival differences remained evident across the four calendar year periods assessed, with persistent disparities in the most recent period, 2015–2019. Whereas disease and biological factors (e.g. stage, cytogenetic profile, age, co‐morbidities) are generally considered in MM risk assessments, additional research is needed to understand the intersection and influence of social, cultural, psychosocial, behavioural and related factors so that all adults with MM can more equally benefit from therapeutic advances positively contributing to patient survival.

AUTHOR CONTRIBUTIONS

GMD, JBV, SJS, LMM, REC and MSL conceived and designed the study and analysis. GMD and REC conducted and oversaw the analysis. GMD wrote the first draft of the manuscript. All authors contributed to the analysis and interpretation of the data, revised and edited the manuscript for scientific content and read and approved the final version of the manuscript.

FUNDING INFORMATION

This work was supported by the Intramural Research Program of the Division of Cancer Epidemiology and Genetics of the National Cancer Institute, National Institutes of Health, Bethesda, MD.

CONFLICT OF INTEREST STATEMENT

The authors have no conflicts of interest to disclose.

ETHICS STATEMENT

This study uses publicly available, de‐identified data and was exempt from Institutional Review Board review.

Supporting information

Data S1.

ACKNOWLEDGEMENTS

The authors thank Jeremy Miller (Information Management Services, Inc., Rockville, MD) for computing support.

Dores GM, Vo JB, Schonfeld SJ, Shing JZ, Taparra K, Morton LM, et al. Temporal patterns in US population‐based patient survival among adults treated with chemotherapy and/or immunotherapy for multiple myeloma, 2000–2020. Br J Haematol. 2025;207(2):417–425. 10.1111/bjh.20192

Rochelle E. Curtis and Martha S. Linet contributed equally to this study.

DATA AVAILABILITY STATEMENT

The data used for this study are publicly available upon application to the SEER Program ( seer.cancer.gov ).

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Associated Data

Supplementary Materials

Data S1.

Data Availability Statement

The data used for this study are publicly available upon application to the SEER Program ( seer.cancer.gov ).