Disparities in Immunotherapy Access for Advanced Pancreatic Cancer across the United States

doi:10.21203/rs.3.rs-4892439/v1

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Disparities in Immunotherapy Access for Advanced Pancreatic Cancer across the United States

https://doi.org/10.21203/rs.3.rs-4892439/v1

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Background:

Pancreatic ductal adenocarcinoma (PDAC), a highly lethal cancer with a poor prognosis, is expected to become the second deadliest cancer in the United States by 2030. Despite advancements in treatment modalities, the survival rates of patients with PDAC have remained low. Immunotherapy has emerged as a promising treatment for various cancers; however, its utilization in PDAC has been limited due to various challenges, including resistance mechanisms and the advanced stage at which most patients are diagnosed.

Methods:

We analyzed data from the National Cancer Database (NCDB) from 2010 to 2017, focusing on the impact of race, insurance status, and socioeconomic factors among patients with stage IV PDAC using logistic regression analyses.

Results:

Among 109,663 patients with stage IV PDAC, 421 (0.38%) received immunotherapy. The recipients were younger (median age 63 vs. 68 years, p < 0.001) and more likely to be white (87.4% vs. 82.1%). Patients with private insurance or Medicare (p < 0.001), and those earning more than $60k annually (51.0% vs. 36.4%, p < 0.001) were more likely to receive immunotherapy. Treatment was more likely in academic/research programs than in community cancer programs (53.0% vs. community, p < 0.001). On multivariate analysis, Black patients had lower odds of receiving immunotherapy than Caucasian patients (OR: 0.74 [95% CI: 0.601–0.882], p = 0.019). Higher income was also a significant predictor of immunotherapy utilization (highest vs. lowest income quartile: OR, 2.228 [95% CI: 1.422–3.491], p < 0.001).

Conclusions:

This study revealed significant disparities in immunotherapy access for stage IV PDAC based on race, socioeconomic status, and geographic location in the United States, highlighting the need for intervention to promote equitable access to this promising treatment modality.

Pancreatic cancer

Immunotherapy

Health disparities

Access to care

Socioeconomic factors

Pancreatic ductal adenocarcinoma (PDAC) is one of the most challenging malignancies to treat, and is projected to become the second deadliest cancer in the United States by 2030 [1]. Despite advances in cancer therapy, the five-year survival rate remains less than 10% [2], and over the past decade, mortality rates have continual to increase [3]. This trend can be attributed to the advanced stage at which PDAC is typically identified, along with the absence of effective screening methods for early detection. Moreover, poor prognosis is exacerbated by the development of resistance to chemotherapy and a high rate of cancer recurrence [4, 5].

Currently, surgery is the only curative option available for PDAC patients, but only possible in < 20% of PDAC patients [6]. This is often due to the presence of synchronous metastatic disease during the initial diagnosis or classification of the tumor as borderline resectable or locally advanced. Even when PDAC is deemed resectable, the probability of survival for up to 5 years remains low at around 10–25% [5]. Collective efforts in research and clinical practice are yet to significantly impact the long-term outcomes of individuals with PDAC.

Immunotherapy has been established as a treatment modality for many solid tumors. Immunotherapy approaches include immune checkpoint inhibitors, cancer vaccines, adoptive cell transfer, and targeted molecular agents [11, 13]. Numerous preclinical and clinical studies are currently assessing the effectiveness of those various immunotherapeutic approaches in PDAC, although at this time none has been implemented in standards of care [11, 12].

Studies have identified significant racial and socioeconomic disparities in the delivery of immunotherapy across different cancer types, including non–small cell lung cancer (NSCLC), metastatic melanoma, and hepatobiliary cancer, underscoring uninsured and underinsured populations, and African Americans as less likely to receive immunotherapy-type compounds (ICs) [14]. These disparities have raised concerns about equitable access to emerging cancer therapies, particularly as the utilization of immunotherapy is expected to increase.

Given the poor prognosis associated with advanced PDAC and the potential of immunotherapy to improve outcomes, it is important to understand the extent and determinants of disparities in the utilization of immunotherapy. Our study aimed to shed light on disparities in immunotherapy utilization for stage IV PDAC, focusing on the impact of race, insurance status, and other socioeconomic factors on treatment access and outcomes.

The National Cancer Database (NCDB) encompasses more than 70% of newly diagnosed cancer cases from over 1,500 hospitals in the United States [15]. For this study, we queried the NCDB, to identify patients diagnosed with primary PDAC between January 1, 2010, and December 31, 2017. PDAC patients were identified by using the International Classification of Diseases for Oncology 3rd Edition code C22.0, and histology codes 8000, 8010, 8020–8022, 8140, 8141, 8211, 8230, 8500, 8521, 8050, 8260, 8441, 8450, 8453, 8470–8473, 8480, 8481, and 8503. For each patient, PDAC stage was determined using the American Joint Committee on Cancer (AJCC) tumor-node-metastasis (TNM) classification system. Patients with unknown stage were excluded. Of the patients with known stage disease, only those with clinical stage IV disease were included in this study. The treatment status of the patients with stage IV PDAC was assessed. Patients who received immunotherapy during their first treatment course or in addition to other treatment modalities (chemotherapy and radiation therapy), were included. Patients with missing treatment status data were excluded from logistic analysis. We grouped stage IV PDAC patients in two categories, depending on whether they had received immunotherapy or not (Fig. 1). As only de-identified data were used, the Northwell Health IRB deemed this study exempt from human subjects research approval.

In addition to the primary cancer type, clinical stage, and treatment type, we also collected data on age, sex, race, period of cancer diagnosis, insurance status, facility type, facility location, median income, residential setting, and distance between the patient’s residence and the treating hospital. Facility-related characteristics included facility type (academic versus non-academic), distance to the facility, and facility volume. Treatment variables were also analyzed, including receipt of immunotherapy, chemotherapy, or radiation therapy; reason for no administration of immunotherapy; receipt and type of palliative care; surgical procedure performed; and clinical trial participation.

Data for descriptive variables are presented as median values with the inner quartile range for continuous variables and frequency as a percentage for categorical variables for patients who received immunotherapy and for patients who did not receive immunotherapy. Chi-squared tests were performed to determine potential associations between categorical variables and the receipt of immunotherapy, whereas Wilcoxon rank-sum tests were performed to determine potential associations between continuous variables and immunotherapy receipt. Bivariate and multivariate logistic regression analyses were performed to predict immunotherapy use. Statistical significance was set at P < 0.05. Statistical analysis was performed using SPSS™ 21.0 (IBM Corp, Armonk, NY, USA).

Among the study population of 109,663 individuals diagnosed with stage IV PDAC, only 421 (0.38%) underwent immunotherapy (Fig. 1). Rationales for avoidance of immunotherapy are summarized in Table 1. The majority of patients (n = 108,530, 98.97%), did not receive systemic immunotherapy as it was not included in their planned first course of treatment. Contraindications to immunotherapy were identified in 124 patients (0.11%), while 84 (0.08%) patients died before the opportunity for surgical intervention. The decision against immunotherapy was also influenced by the refusal of the treatment by the patient, their family, or guardian in 150 cases (0.14%).

Table 1

Management of patients with stage IV Pancreatic Adenocarcinoma.
Management	Stage IV Pancreatic Cancer (n = 109,663)
Systemic immunotherapy administered	421 (0.38%)
Reason for no administration of systemic immunotherapy
Was not part of the planned first course treatment	108,530 (98.97%)
Patient had contraindications	124 (0.11%)
Patient died prior to surgery	84 (0.08%)
No reason was documented	65 (0.06%)
Refusal by the patient, family, or guardian	150 (0.14%)
Others	285 (0.26%)

Comparison of patients who received and did not receive immunotherapy is summarized in Table 2. Patients who received immunotherapy were younger (median age 63 vs. 68 years, p < 0.001). Gender distribution (56.5% vs. 52.7% males, p = 0.115), as well as racial composition (87.4% vs. 82.1% white patients and 8.3% vs. 13.1% black patients, p = 0.939) were similar. Patients with private insurance or Medicare were more likely to be treated with immunotherapy than uninsured patients (p < 0.001). Individuals earning more than $60k annually were more likely to undergo immunotherapy treatment (51.0% vs. 36.4%, p < 0.001). Patients in academic or research programs were significantly more likely to receive immunotherapy (53.0% versus 35.1%, p < 0.001) than those in community cancer programs (p < 0.001). Facility locations such as New England and the Pacific demonstrated higher immunotherapy rates (p = 0.002). Patients who underwent immunotherapy were also more likely to receive concurrent chemotherapy (92.9% vs. 53.5%, p < 0.001) (Table 2).

Table 2

Demographic and clinical characteristics of patients with and without immunotherapy.
Variable	No immunotherapy (n = 109,242, 99.62%)	Immunotherapy (n = 421, 0.38%)	p-value
Age, median [IQR]	68 (11)	63 (10)	< 0.001
Sex			0.115
Male	57,559 (52.7%)	238 (56.5%)
Female	51,683 (47.3%)	183 (43.5%)
Race			0.939
White	89,672 (82.1%)	368 (87.4%)
Black or African American	14,276 (13.1%)	35 (8.3%)
Other	4,311 (3.8%)	16 (3.7%)
Insurance Status			< 0.001
Not Insured	3,422 (3.1%)	4 (1.0%)
Private Insurance	32,201 (29.5%)	199 (47.3%)
Medicaid	6,927 (6.3%)	21 (5.0%)
Medicare	63,393 (58.0%)	179 (42.5%)
Other Government	1,292 (1.2%)	9 (2.1%)
Insurance status unknown	2,007 (1.8%)	9 (2.1%)
Median income			< 0.001
Less than $40k	18,159 (18.7%)	38 (10.5%)
$40-50k	20,845 (21.4%)	69 (19.0%)
$50-60k	22,841 (23.5%)	71 (19.6%)
>$60k	35,425 (36.4%)	185 (51.0%)
Facility Type			< 0.001
Community Cancer Program	7,604 (7.0%)	26 (6.3%)
Comprehensive Community Cancer Program	41,216 (38.0%)	112 (27.1%)
Academic/Research Program	38,031 (35.1%)	219 (53.0%)
Integrated Network Cancer Program	21,597 (19.9%)	56 (13.6%)
Facility Location			0.002
New England	6,225 (5.7%)	17 (4.1%)
Middle Atlantic	18,781 (17.3%)	81 (19.6%)
South Atlantic	23,219 (21.4%)	96 (23.2%)
East North Central	18,941 (17.5%)	48 (11.6%)
East South Central	6,703 (6.2%)	23 (5.6%)
West North Central	8,012 (7.4%)	26 (6.3%)
West South Central	8,891 (8.2%)	34 (8.2%)
Mountain	4,686 (4.3%)	32 (7.7%)
Pacific	12,990 (12.0%)	56 (13.6%)
Grade			0.068
Well differentiated	1,605 (1.5%)	9 (2.1%)
Moderately differentiated	7,548 (6.9%)	42 (10.0%)
Poorly differentiated	11,854 (10.9%)	49 (11.6%)
Chemotherapy	56,795 (53.5%)	391 (92.9%)	< 0.001
Radiation therapy	417 (0.4%)	2 (0.5%)	0.763

Regression analysis exploring the determinants of immunotherapy among patients with stage IV pancreatic adenocarcinoma is detailed in Table 3. On multivariate analysis, Black or African American patients were less likely to receive immunotherapy than Caucasian patients (OR, 0.74; 95% CI: 0.601–0.882, p = 0.019). Patients diagnosed in more recent years exhibited substantially higher odds of receiving immunotherapy, and those diagnosed in 2017 had a significantly increased likelihood compared to those diagnosed in 2010 (OR: 4.385, 95% CI: 2.573–7.474, p < 0.001). Patients in the Mountain and South Atlantic regions were more likely to receive immunotherapy than those in New England (OR: 3.296, 95% CI: 1.499–7.249, p = 0.003 and OR: 2.007, 95% CI: 1.013–3.978, p = 0.046, respectively). Patients in the highest income quartile had significantly higher odds of receiving immunotherapy compared to those in the lowest income quartile (OR: 2.228, 95% CI: 1.422–3.491, p < 0.001),

Table 3

Regression analysis of predictors of immunotherapy receipt.
Variable	Univariate Regression Analysis	p-value	Multivariate Regression Analysis	p-value
Age (years)
< 65	Reference		Reference
≥ 65	1.699 (1.369–2.109)	< 0.001	0.764 (0.541–1.077)	0.125
Gender
Male	Reference		Reference
Female	0.874 (0.702–1.087)	0.225	0.864 (0.674–1.107)	0.247
Race
Caucasian	Reference		Reference
Black or African American	0.588 (0.399–0.867)	0.007	0.74 (0.601–0.882)	0.019
American Indian or Alaska Native	1.693 (0.418–6.856)	0.460	1.101 (0.151–8.022)	0.925
Asian	1.022 (0.505–2.067)	0.952	1.045 (0.504–2.168)	0.905
Other minorities	0.213 (0.053–0.855)	0.029	0.224 (0.055–0.905)	0.036
Period of Diagnosis
2010	Reference		Reference
2011	1.065 (0.543–2.090)	0.854	1.054 (0.537–2.069)	0.878
2012	0.899 (0.450–1.799)	0.764	0.849 (0.419–1.718)	0.648
2013	2.042 (1.138–3.663)	0.017	1.897 (1.049–3.431)	0.034
2014	2.199 (1.238–3.906)	0.007	1.952 (1.085–3.513)	0.026
2015	3.963 (2.318–6.774)	< 0.001	3.529 (2.049–6.077)	< 0.001
2016	4.656 (2.746–7.894)	< 0.001	3.622 (2.107–6.226)	< 0.001
2017	4.699 (2.777–7.950)	< 0.001	4.385 (2.573–7.474)	< 0.001
Insurance Status
Not insured	Reference		Reference
Private Insurance/Managed Care	3.347 (1.239–9.044)	0.017	2.765 (0.871–8.78)	0.084
Medicaid	1.314 (0.432-4.0)	0.63	1.232 (0.336–4.518)	0.753
Medicare	1.611 (0.596–4.358)	0.347	1.909 (0.587–6.205)	0.283
Other Government	4.364 (1.339–14.221)	0.014	4.087 (1.041–16.047)	0.044
Facility Location
New England	Reference		Reference
Middle Atlantic	2.158 (1.142–4.078)	0.018	1.935 (0.985–3.799)	0.055
South Atlantic	1.596 (0.842–3.026)	0.152	2.007 (1.013–3.978)	0.046
East North Central	1.142 (0.584–2.233)	0.697	1.512 (0.739–3.094)	0.257
East South Central	1.46 (0.688–3.096)	0.324	2.144 (0.945–4.866)	0.068
West North Central	1.449 (0.698–3.01)	0.32	1.229 (0.533–2.833)	0.629
West South Central	1.526 (0.746–3.119)	0.247	1.838 (0.844–4.001)	0.125
Mountain	3.239 (1.609–6.518)	0.001	3.296 (1.499–7.249)	0.003
Pacific	1.934 (0.999–3.745)	0.05	1.996 (0.987–4.037)	0.055
Residential Setting
Rural	Reference		Reference
Urban	1.085 (0.382–3.080)	0.878	0.956 (0.283–3.224)	0.942
Metropolitan	1.469 (0.547–3.951)	0.446	1.555 (0.476–5.078)	0.465
Distance between the patient's residence and the hospital (miles)
> 40	Reference		Reference
30.1–40	1.620 (1.183–2.218)	0.003	1.814 (1.231–2.672)	0.003
20.1–30	1.555 (0.967-2.5)	0.069	1.717 (1.036–2.844)	0.036
10.1–20	1.324 (0.881–1.988)	0.176	1.186 (0.767–1.835)	0.442
0–10	1.200 (0.877–1.643)	0.254	1.024 (0.736–1.424)	0.890
Median Income
< $40,227	Reference		Reference
$40,227 - $50,353	1.462 (0.924–2.311)	0.105	1.251 (0.771–2.032)	0.365
$50,354 - $63,332	1.489 (0.949–2.337)	0.083	1.285 (0.791–2.09)	0.311
≥$63,333	2.494 (1.673–3.718)	< 0.001	2.228 (1.422–3.491)	< 0.001

In this study, we found that only 0.38% of patients with stage IV PDAC received immunotherapy between 2010–2017. Utilization of immunotherapy was not uniform; factors such as the patient's race, insurance status, socioeconomic background, and geographic location within the US influenced type of treatment. These disparities not only mirrored the broader inequities ingrained within our healthcare system, but also highlight a critical barrier in the quest for equitable cancer care. By focusing on these disparities, our study contributes to an essential dialogue on how systemic challenges in healthcare access and delivery can impede the adoption of disease-modifying treatments.

Immunotherapy utilization was significantly more likely among white people than among black patients (OR, 0.74 [95% CI: 0.601–0.882], p = 0.019). African Americans have been shown to be more commonly diagnosed with PDAC and experience lower survival rates when compared to other racial groups [16]. The survival rates for black patients with PDAC are estimated to be 10–20% lower than those of white patients [17, 18]. Non-modifiable risk factors, including genetic variations and social determinants of health, have been implicated in the disparities observed in PDAC outcomes [19]. Barriers to progress include the low inclusion of minorities in research studies, pointing to the need for increased recruitment and representation of African American patients in clinical trials to better understand and address these disparities [20, 21].

The observed regional disparities found in our analysis may be influenced by several factors, including variations in healthcare infrastructure, the availability of specialized cancer treatment centers, and differences in healthcare policies at the state level [22, 23]. For example, patients receiving care at academic institutions are often at an advantage as these centers are more likely to offer personalized treatments. This is particularly relevant for immunotherapy, which necessitates precise alignment between the treatment and the patient's unique cancer profile [24]. These academic and research institutions are, in turn, more prevalent in certain regions [25], suggesting that patients in regions with higher concentrations of such institutions may have better access to emerging treatments. The variation in immunotherapy access across regions underscores the need for policy interventions and healthcare resource allocation that consider regional disparities. Ensuring equitable access to advanced cancer treatment requires a multifaceted approach that addresses the unique challenges faced by different regions. This may include increasing the availability of specialized care centers in underserved areas, enhancing healthcare infrastructure, and implementing policies aimed at reducing economic barriers to care.

The overall findings suggest that while immunotherapy has a limited proven role in PDAC treatment, with possible exceptions for specific patient subsets such as those involved in phase 1 vaccine trials, the disparities in its administration are noteworthy [26]. The extremely low percentage (only 0.38%) of patients receiving immunotherapy within the entire cohort makes it difficult to argue for disparities when the treatment is not a standard of care. However, our findings do indicate that certain socioeconomic groups did not receive immunotherapy, which, despite its current status as non-standard care outside clinical trials, underscores a broader issue of inequitable access to experimental treatments. It is crucial to link the use or lack thereof of immunotherapy to clinical trial participation, highlighting disparities in the inclusion of certain groups in these trials. This perspective raises concerns that the observed administration of immunotherapy may reflect instances of nonstandard or unindicated therapy.

Limitations of our study include reliance on area-level socioeconomic status (SES) measures, such as education and income, which may not accurately reflect the individual circumstances of each PDAC patient. This approach could confound variations in SES within geographic areas, potentially leading to an underestimation of the true impact of individual socioeconomic factors on the likelihood of receiving immunotherapy for PDAC. Additionally, our analysis lacked detailed data on the specific types of immunotherapy regimens administered, number of cycles completed, and any associated toxicities among patients with PDAC receiving immunotherapy. The absence of granular treatment data limits our ability to fully comprehend the nuances of immunotherapy and its outcomes across different patient groups.

In conclusion, our study highlights notable discrepancies in the adoption of immunotherapy for PDAC. Despite a general uptick in the utilization of immunotherapy, individuals belonging to a minority ethnic group, certain regions in the US, having lower financial resources, and those with reduced income levels exhibited a lower likelihood of receiving this treatment. These disparities underscore the necessity for holistic approaches aimed at overcoming socioeconomic obstacles and ensuring equitable access to advanced cancer therapies for all patients with PDAC.

Conflict of interest: None

Financial Disclosures: None

Acknowledgements: None

Authors’ Contributions: All authors contributed to the study's conception and design. Material preparation, data collection, and analysis were performed by Abdullah Khalid and Zohaa Faiz. Abdullah Khalid wrote the first draft of the manuscript, and all authors commented on previous versions. All authors read and approved the final manuscript.

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No competing interests reported.

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Disparities in Immunotherapy Access for Advanced Pancreatic Cancer across the United States

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