Socioeconomic Status is Globally a Prognostic Factor for Overall Survival of Multiple Myeloma Patients: Synthesis of Studies and Review of the Literature
Received: August 17, 2020
Accepted: December 7, 2020
Mediterr J Hematol Infect Dis 2021, 13(1): e2021006 DOI 10.4084/MJHID.2021.006
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Socioeconomic status (SES) is reflecting differences in
sociodemographic factors affecting cancer survivorship. Deprived, low
SES populations have a higher prevalence of multiple myeloma and worst
survival, a condition which widens over time.
Despite all this progress, disparities in myeloma care are globally noted, with not all myeloma patients finally achieving the expected survival benefit. A primary reason for inequalities in myeloma care is differences in social resources. The socioeconomic status (SES) is an index calculated based on education, social support, and income but, actually, is a surrogate marker reflecting differences in factors like ethnicity or race, availability of new treatment options, access to health system facilities, disparities in insurance status/ refurbishment of anti-myeloma drugs, occupation and place of living (rural or urban vs. metropolitan). Racial or ethnic differences in myeloma reflect differences in factors that interfere with the SES status and disease biology during all stages of myeloma evolution (from monoclonal gammopathy to symptomatic myeloma).
Ethnicity/Racial Disparities in Myeloma Care
Disease characteristics like myeloma-related events or high-risk features are different across racial/ethnic subgroups. African American patients are thought to have a lower incidence of specific high-risk cytogenetics abnormalities (deletion of 17p) but higher rates of t(11;14) and 1q amp. A mutational study recently showed that A.A. myeloma patients had a lower prevalence of the high risk p53 mutation, while across all ethnic groups, NRAS and KRAS are the most frequently occurred mutations. Furthermore, the incidence of myeloma-related end-organ damage (e.g., need for kidney dialysis), factors that can delay therapy or put limitations in drug choice, has been reported with varying incidence according to racial/ethnic subgroups, affecting thus disease outcome and prognosis.
A.A. patients with MM, examined on the treatment offered, were less likely to undergo ASCT and be treated with bortezomib, leading to a potential association with the worst prognosis. The age-adjusted odds of receiving ASCT for MM were significantly higher for white than for A.A. patients (odds ratio, 1.75; 95% CI, 1.64–1.86; p=0,01)[11,12] although a recent study from a single center in Minnesota reported that SES was in less than 2% of cases a barrier in order patients to be referred for ASCT. Another single-center study reported that A.A. patients have a time since referral to ASCT longer than Whites. Data from SEER-Medicare data from 2003-2017 shows that ASCT use rates during first-year increases for A.As. Notably, African American patients compared to white Americans after receiving autologous transplant have no difference in disease outcome (PFS or O.S.), meaning that ASCT can overcome biological differences among racial subgroups or that equality of treatment overcomes all racial disparities.[16,17,18] A recent study by Munshi et al. conducted on army veterans showed that O.S. disparities across different races are lost and possibly reversed when all patients have the same insurance and access to health system providers.
Similarly, access to new agents is not equal across ethnic/racial subgroups in health systems where these agents are approved. During the first year after MM diagnosis, White and African American patients had higher bortezomib-only usage, but A.A. had lower lenalidomide usage, whereas Hispanic and Asian patients had higher immunomodulatory drug-only utilization. Furthermore, a substantial increase was seen over the years for both lenalidomide and bortezomib use for all subgroups except Hispanic patients, and a notable increase in bortezomib use was noted for all subgroups except Asian patients. Notably, even today use of novel agents is more distanced from diagnosis for patients with A.A. and Hispanic origin (5,2 and 4,6 months, respectively) compared to Whites (2,7 months).
Novel Anti-Myeloma Agents and Disparities in Myeloma Care According to Race/Ethnicity
1. Data extracted from studies and included in this meta-analysis.
Single-center Experience on Myeloma Care in the Muslim Minority of Thrace, Greece
Access to Medical Centers and Availability of Best Anti-Myeloma Care
Outside the USA in 15 Latin American countries, the FISH analysis was available in 67% of patients, MRI in 44%, and PET/CT was offered in 66,7% of patients. Treatment availability queries showed that ASCT was available in 11/13 countries, bortezomib, and lenalidomide in more than 90% of reported physicians, and pomalidomide, carfilzomib, and daratumumab is accessible in around 60% of physicians participating in this study. Maintenance therapy was prescribed in almost all indicated patients. However, there were significant differences in access to tests and treatments for multiple myeloma between public and private systems. Although patients can be referred to the private or public center for anti-myeloma care, that does not significantly impact patients' survival when the same protocols were utilized. All physicians reported having access to thalidomide and bortezomib. Autologous stem cell transplant (ASCT) is available in most countries (11/13). Lenalidomide is commercially available in 97.9% (96), melphalan in 92.7% (94), daratumumab in 68% (65), pomalidomide in 67% (57), carfilzomib in 60% (57), and ixazomib in 18%. Nevertheless, the commercial availability of these drugs does not mean patients have access to them, as reimbursement issues and local health policies often do not provide them due to their high cost.
Socioeconomic Status and Cancer Survivorship
Socioeconomic Status and Hematological Malignancies
Considering the impact of SES on myeloma survival, many data exist in the literature that supports SES as a prognostic survival factor globally and across all decades.[40,41,42] Some studies are relating to SES and the incidence of myeloma.
Socioeconomic Status and Incidence of Multiple Myeloma
Socioeconomic Status and Myeloma Survival
Search Strategy and Statistical Analysis
2. Studies flow diagram and final selection of studies included in this
We separated subgroups according to the geographical area of the study. To synthesize data from different cohort studies, we used the Mosteller and Bush formula, which is the generalization of the z-test. This formula gives weight to each study concerning the number of patients. Under the null hypothesis, the weighted sum still has a normal distribution with mean 0 and variance equals the sum of the weights' square. So we have the formula:
In some studies (n=10), Hazzard Ratio (H.R.), and 95% confidence interval for O.S. in High SES and Low SES myeloma patients were reported. By using the RevMan software, a Cochrane tool, we performed a meta-analysis of the reported H.R.
Combined from Eleven Studies Hazzard Ratio for Death in High SES and Low SES Myeloma Patients
Socioeconomic Status and Disparities in 5 Years Overall Survival of Myeloma Patients According to Geography
USA: Health System Disparities and the Impact of SES on Myeloma Survival
The health care system in the USA is characterized by broad economic inequalities. The life expectancy of the wealthiest Americans now exceeds that of the poorest by 10-15 years. Poor Americans have worse access to health care than do wealthy Americans because many remain uninsured despite coverage expansions since 2010 due to the Affordable Care Act (ACA). Significantly, more than 37 million Americans do not have health insurance, and 41 million more have inadequate access to care.
According to SEER registry reporting data from over than 30.000 myeloma patients diagnosed from 1981 to 2010 in the USA, gap on survival rates according to SES has widened over time (affluent to deprived: 26,1%, 26,8% and 24,8% in the first decade, 31,2%, 28,1%, and 25,9% in the second decade and 44,2%, 40,5%, and 34,8% in the third decade). The Kaplan–Meier survival analyses confirmed the widening survival gaps among SES groups, with p values of 0,0016 during the last decade when more effective anti-myeloma treatments became available.
This decade's focus was made by Costa et al., reporting data from 10,161 cases of MM diagnosed before the age of 65 years from 2007 t0 2012 and included in the SEER-18 registry. In the Cox proportional hazards model, only marital status, insurance status, and county-level income significantly influenced O.S. The cumulative effect of sociodemographic factors associated with shorter survival in the multivariable analysis was statistically significant (p<0,0001). The 4 years OS% reported 71,1%, 63,2% 53,4% and 46,5% for patients with 0, 1, 2, 3 adverse sociodemographic factors.
Fiala et al. reported retrospectively from five-hundred-sixty-two patients eligible for analysis included in medical records from Washington University School of Medicine.
High-SES patients were less likely to have comorbidities at diagnosis than middle-SES and low-SES patients (58% compared to 72% and 76%, p=0.007) and were more likely to have private insurance at diagnosis. High-SES patients were more likely to undergo ASCT than middle-SES and low-SES patients (72% compared to 59% and 52%, respectively, p<0.001). In multivariate analysis of SES, age at diagnosis, year of diagnosis, race, comorbidity score, ASCT utilization, and insurance provider, all other variables except insurance provider, were independently associated with survival.
The same group tested their patients' results in SEER-18 registry reporting from patients recorded until November 2012. 45.505 MM patients were identified for analysis. The median age at diagnosis was 69 years (range 18–85+), and 18 percent were black. In a multivariate model, SES was associated with O.S. [HR 1.18 (95% CI 1.15–1.22) for low-SES relative to high-SES; HR 1.10 (95% CI 1.07–1.13) for middle-SES relative to high-SES].
Hong et al. reported data from 354 transplant eligible patients from the USA, and they did not observe any significant differences in O.S. or Progression-Free Survival (PFS) and relapse rate based on recipient SES at ASCT in univariate analyses or multivariable analysis after adjusting for significant patient-, disease-, and transplantation-related variables.
There is also a small study from Harlem Hospital reporting from 1980 to 1985 and found out that low socioeconomic index resulted in a significantly lower five-year O.S. rate (27 vs. 18%; p=0,01).
We performed the synthesis of p values coming from these six studies (n=89807 pts) by using the Mosteller and Bush formula, and the extracted p-value was <0.0001, meaning that in the USA, there is a statistically significant association between low SES and O.S. across all age groups and decades (Figure 3B).
Australia: Health System Disparities and the Impact of SES on Myeloma Survival
Primary care is mostly provided in the community by general practitioners (GPs) who are generally self-employed. G.P.s also operate as 'gatekeepers', referring patients to specialist medical services where needed. The national public health insurance scheme «Medicare» provides subsidies for most medical and diagnostic and some other health services.
Public hospital treatment is free for people but can be subject to long waiting times for elective surgery. Private hospitals cater to patients who want a choice of doctor and private ward accommodation. For private hospitals, Medicare pays 75 percent of the Medicare schedule fee, with the balance met by private health insurance.
A range of free or low-cost public health services, including immunization and mental health services, are provided by community health facilities. Prescription medicines are dispensed by private community pharmacists paid by the Australian government (under a Pharmacy Agreement) to dispense medicines subsidized under the Pharmaceutical Benefits Scheme (PBS).
An older study from Australia reported data from 249 myeloma patients diagnosed from 1975 through 1984 and found no difference in O.S. according to SES p=0,2 in this decade where chemotherapy was the most effective treatment. Another study from Australia reporting survival data from more than 6000 myeloma patients diagnosed between 1981 to 2014 found that five-year relative survival across all treatment eras for disadvantaged patients was 39% (95% CI 0,36–0,42) vs. affluent patients 46% (95% CI 0,42–0,49) (p<0.001). There was no significant difference in relative survival for the middle class in multivariate analysis than affluent SES patients. Importantly, residence and SES were significant in multivariate testing, demonstrating that each was independently predictive of O.S.
New Zealand: Health System Disparities and the Impact of SES on Myeloma Survival
The health care system is has been funded by the government since the early 1940s, and public funding currently accounts for 83% of total health expenditure Government-owned hospitals provide accident and emergency, inpatient, outpatient, and community care free of charge to all New Zealanders.
Primary health care services such as general practitioner (G.P.), pharmacy, and diagnostic services have traditionally been delivered through privately owned, small independent businesses funded by the government.
A recent study from the New Zealand Cancer Registry performed in the era of modern drugs from 2004 to 2016 has reported in multivariate analysis age [hazard ratio (HR) 1,06, 95% CI 1,05-1,07], socio-economic deprivation (HR 1,10, 95% CI 1,04- 1,16) and 4 regions of the country (HR 1,12, 95% CI 1,05 - 1,19) as negative, and treatment with ASCT (HR 0,66, 95% CI 0,51- 0,87) or bortezomib (HR 0,74, 95% CI 0,64 - 0,86) as positive independent prognostic factors for OS. The most deprived groups had an inferior 3-year OS compared to others (57 vs. 63%; p=0,026) and experienced no improvement in survival following the funding of bortezomib despite similar uptake of first line bortezomib.
Synthesis of p values from two cohorts from Australia and a New Zealand cohort (n=10196 pts) returned a p-value of 0,022 indicated SES as a prognostic factor and in Oceania (Figure 3B).
United Kingdom: Health System Disparities and the Impact of SES on Myeloma Survival
Life expectancy has increased steadily across the United Kingdom, but health inequalities have proved resistant to improvement, and the gap between the most deprived and the most privileged continues to widen rather than close.
Renshaw et al. reported data from 10,015 myeloma patients diagnosed from 1985 through 2004 and included in the Thames Cancer Registry. When considering patients with myeloma diagnosed in the era of targeted therapies from 2000 to 2004 in both males and females, there was a tendency for higher survival in patients resident in the most affluent areas (males trend p= 0,09, females trend p= 0,07).
Rachet et al., in another U.K. study, reported data from 40.000 myeloma patients according to the year of diagnosis and relative deprivation of social supporting factors (social gap). They found out that the equal myeloma survival for deprived women noted in the late 1980s had wholly reversed by the late 1990s. These vast differences among deprivation groups in survival trends, with no improvement at all in 5-year survival among the most deprived group, but an increase of more than 10% for the most affluent groups expected to be further widened in the future.
Greece: Health System Disparities and the Impact of SES on Myeloma Survival
The National Organization for the Provision of Health Services (Greek acronym EOPYY) negotiates contracts and remunerates health professionals. At the Pharmacist's, there is usually a co-payment of 25% of medicinal products' cost. Some patients' groups, such as cancer patients, the chronically ill, and pregnant women, receive medicines free of charge or pay a reduced co-payment.
In a recently published study, we retrospectively collected data from 223 myeloma patients treated in our department from January 2005 till December 2019. Based on the intention to treat (ITT), 78 patients were considered transplant eligible (T.E.), and 145 were non-transplant eligible (NTE). In Kaplan Mayer survival analysis, including all MM patients of our cohort, the Low SES group n=100 had inferior survival compared to High SES patients n=123 [Median O.S. (95% CI) for Low SES: 28 months (18-37,9) High SES: 68 months (55,6-80,4), Long Rank p=0,000). The Low SES effect on O.S. is more evident in the non-transplant eligible (NTE) elderly myeloma patients and those diagnosed at I stage ISS.
The synthesis of p values from the U.K. and Greece studies (n=18533 pts) returned a p-value of <0,0001 suggested that SES remains an important prognostic factor of survival in Europe (Figure 3B).
Asia and Africa
Synthesis of 2 studies from Asia (n=915 pts) returned a p-value of< 0,0001 showing a better survival for high SES myeloma patients compared to low SES and in this part of the world (Figure 3B).
Financial Toxicity of Myeloma Treatment
After patients are diagnosed with cancer, the purchase of therapies affects their personal economics (pocket cost) by two ways; first, contributing to calculations of the cost of insurance premiums and second through cost-sharing mechanisms imposed by insurers. Furthermore, employment issues due to myeloma are arising. In a recently published study, five hundred (66%) of the respondents reported that they were employed at the time of diagnosis and treatment onset. However, by the time they completed the study questionnaire, only 33% were employed. In the same study, 29% of participants changed or lost coverage after myeloma diagnosis, including 10% unable to obtain replacement insurance and 35% applied for disability support programs. Considering the ability to work, this is affected by the choice of an anti-myeloma treatment plan. Merola et al. reported that patients who received injectable therapy missed an average of 110 workdays in the one year after diagnosis, compared with 87 for patients receiving only oral therapy.
Myeloma care's financial toxicity is increasing for both health system payers and for patients' as well. Disparities in myeloma care will widen since the most deprived will fail to meet the need for continuous administration of expensive therapies.
This work was supported by an unrestricted educational grant from the pharmaceutical company FARAN Hellas.
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