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Research Article
4 December 2020

Impact of socioeconomic status on presentation, treatment and outcomes of patients with pancreatic cancer

Abstract

Objective: To assess the impact of socioeconomic status (SES) on the patterns of care and outcomes of patients with pancreatic cancer. Materials & methods: Surveillance, Epidemiology and End Results specialized SES registry has been accessed and patients with pancreatic cancer diagnosed (2000–2015) were evaluated. The following SES variables were included: employment percentage, percent of people above the poverty line, percent of people identified as working-class, educational level, median rent, median household value and median household income. Within this SES registry, patients were classified according to their census-tract SES into three groups (where group-1 represents the lowest SES category and group-3 represents the highest SES category). Multivariable logistic regression analysis was used to assess the impact of SES on access to surgical resection and multivariable Cox regression analysis was used to assess the impact of SES on pancreatic cancer-specific survival. Kaplan–Meier survival estimates were also used to compare overall survival (OS) outcomes according to SES. Results: A total of 83,902 pancreatic cancer patients were included in the current analysis. Within multivariable logistic regression analysis among patients with a localized/regional disease, patients with lower SES were less likely to undergo surgical resection for pancreatic cancer (odds ratio: 0.719; 95% CI: 0.673–0.767; p < 0.001). Among patients with a localized/regional disease who underwent surgical resection, patients with higher SES have better OS (median OS for group-3: 20.0 vs 17.0 months for group-1; p < 0.001). Moreover, patients with lower SES have worse pancreatic cancer-specific survival compared with patients with higher SES: (hazard ratio for group-1 vs group-3: 1.212; 95% CI: 1.135–1.295; p < 0.001). Conclusion: Poor neighborhood SES is associated with more advanced disease at presentation, less probability of surgical resection and even poorer outcomes after surgical resection.
Socioeconomic status (SES) has been shown to play an important role in health and disease [1,2]. This is particularly relevant among cancer patients where personal and area-based socioeconomic factors have been shown to alter the outcomes of this disease [3,4].
Pancreatic cancer represents one of the most aggressive solid tumors with unfortunately very minimal improvement in survival outcomes over the past three decades [5]. Many studies have evaluated the impact of SES on the outcomes of pancreatic cancer patients; however, there was generally a lack of standardized assessment of SES within these studies, with many of them focusing only on personal characteristics like race and marital status without proper attention to other socioeconomic factors like employment, income and educational status [6,7]. Additionally, the impact of neighborhood-based socioeconomic factors was generally under-evaluated in many of these studies.
In order to address the challenge resulting from lack of dedicated SES registries for cancer patients as well as lack of a standardized comprehensive tool to assess SES, Surveillance, Epidemiology and End Results (SEER) database developed a dedicated registry incorporating baseline clinicopathological information about cancer patients as well as census tract-based socioeconomic information about their neighborhoods. This registry should provide an excellent opportunity to study the interaction between neighborhood SES and outcomes of pancreatic cancer patients.
Results of this analysis should inform healthcare policy decisions; particularly with regards to ensuring equitable access to cancer care among socioeconomically disadvantaged and vulnerable groups of cancer patients.

Objective

To assess the impact of SES on the patterns of care and outcomes of patients with pancreatic cancer.

Materials & methods

SEER census-tract socioeconomic database

In an effort to standardize the way neighborhood SES is reported within the SEER database, a specialized registry has been developed [8]. Based on several parameters, a composite score was produced in this registry to indicate SES. These parameters are employment percentage, percent of people above the poverty line, percent of people identified as working-class, educational level, median rent, median household value and median household income. This scoring system was developed and validated by Yost et al. and Yu et al. [9,10]. Educational level was provided as per the work of Liu et al. [11]. Additional information about data linkage for this registry was detailed elsewhere [12]. As an output of this scoring system, patients will be categorized into three SES categories according to this score (where group 3 represents the highest SES category and group 1 represents the lowest SES category). The SES indices are calculated for 2000–2015 using data from the 2000 US Decennial Census long form survey and a series of American Community Survey 5-year estimates from 2006 to 2016. The indices are then linked to cancer cases at the census tract level by matching the survey year with the cancer diagnosis year. It has to be noted that SES is an aggregate, neighborhood-based measure that is predictive but may not actually represent the patient’s true SES.

Cohort selection

The following eligibility criteria were used to select patients for the current study: patients were included in the SES specialized SEER database; patients have microscopically confirmed pancreatic adenocarcinoma diagnosis; patients were diagnosed (2000–2015); complete information about SES group for each patient. For patients with more than one primary pancreatic carcinoma, first tumor was only included.

Data collection

The following data were extracted from each included patient where available: age at diagnosis, race/ethnicity, sex, stage at diagnosis (using SEER summary stages: localized, regional and distant), location within the pancreas, treatment with surgery, chemotherapy and/or radiation therapy and SES group. For the sake of the current study, any reference in the current study to surgical resection would mean oncologic resection rather than limited resection or ablation. SEER staging system was used to avoid possible confusion from the changes in the TNM staging system across the duration of the study (2000–2015).
End points of the current study included overall survival (OS) and pancreatic cancer-specific survival. OS was defined as the time from pancreatic cancer diagnosis till death (of any cause) and pancreatic cancer-specific survival was defined as the time from pancreatic cancer diagnosis till death due to pancreatic cancer. Follow-up for included patients continued until the cutoff of this database (December 2015).

Statistical analysis

Chi-squared testing was initially used to compare the distribution of baseline and treatment characteristics according to the SES group. Multivariable logistic regression analysis was then used to evaluate factors potentially predicting the use of surgery. This analysis was restricted for patients with a localized/regional disease only and it was adjusted for all the available baseline characteristics including age at diagnosis, sex and race, location of the primary tumor, SES group and stage.
Kaplan–Meier analysis was then used to compare OS outcomes of patients with a localized/regional disease who underwent surgical resection according to the SES group. Multivariable Cox regression analysis was then used to assess the impact of SES group on pancreatic cancer-specific survival among the same subgroup of patients (patients with localized/regional disease who underwent surgical resection). This multivariable analysis was adjusted for all baseline characteristics as above. Chemotherapy and radiotherapy were not included in this multivariable analysis because of uncertainty surrounding the reporting of chemotherapy and radiotherapy in SEER database as well as the absence of technical details (e.g., dose and schedule) for both modalities.
The reason for restricting survival analyses to surgically resected patients only is to partially mitigate the impact of the absence of comorbidity information on the survival analyses (patients with significant comorbidities/poor performance status are less likely to be offered a surgical for pancreatic cancer). All the above statistical analyses were conducted by SPSS software (version 20.0, IBM, NY, USA).

Results

Patients’ characteristics

A total of 83,902 patients fulfilled the eligibility criteria and were included in the current analysis. Comparing the three SES groups together, patients with group 3 SES (highest group) were more likely to have older age (p < 0.001), male sex (p < 0.001), white race (p < 0.001) and less distant disease (p < 0.001). They were also more likely to be treated with surgery (p < 0.001), chemotherapy (p < 0.001) and/or radiation therapy (p < 0.001) (Table 1).
Table 1. Baseline characteristics of included patients in the current study (83,902 patients).
ParameterGroup 1 (23,941 patients)Group 2 (28,380 patients)Group 3 (31,581 patients)p-value
Age
– <40 years
– 40–69 years
– ≥70 years

237 (1%)
12,962 (54.1%)
10,743 (44.9%)

215 (0.8%)
14,011 (49.4%)
14,157 (49.9%)

189 (0.6%)
15,023 (47.6%)
16,373 (51.8%)
<0.001
Sex
– Male
– Female

12,150 (50.7%)
11,791 (49.3%)

14,434 (50.9%)
13,946 (49.1%)

16,667 (52.8%)
14,914 (47.2%)
<0.001
Race
– White non-Hispanic
– Black non-Hispanic
– Hispanic
– Asian-Pacific Islander
– American Indian
– Unknown

13,585 (56.8%)
5399 (22.6%)
3752 (15.7%)
1005 (4.2%)
171 (0.7%)
29 (0.1%)

20,965 (73.9%)
2546 (9%)
2837 (10%)
1885 (6.6%)
108 (0.4%)
39 (0.1%)

25,490 (80.7%)
1307 (4.1%)
1897 (6%)
2774 (8.8%)
74 (0.2%)
39 (0.1%)
<0.001
Location
– Head
– Body
– Tail
– Other specified parts
– Overlapping lesions
– Pancreas, NOS

12,173 (50.8%)
2730 (11.4%)
2884 (12%)
450 (2%)
1663 (6.9%)
4041 (16.9%)

14,483 (51%)
3326 (11.7%)
3400 (12%)
534 (1.9%)
2152 (7.6%)
4485 (15.8%)

15,535 (49.2%)
4089 (12.9%)
4019 (12.7%)
695 (2.2%)
2470 (7.8%)
4773 (15.1%)
<0.001
Stage
– Localized
– Regional
– Distant
– Unknown

1870 (7.8%)
7020 (29.3%)
13,998 (58.5%)
1053 (4.4%)

1982 (7%)
8796 (31%)
16,404 (57.8%)
1198 (4.2%)

2030 (6.4%)
10,043 (31.8%)
18,283 (57.9%)
1225 (3.9%)
<0.001
Surgery
– None
– Limited destruction/excision
– Oncological resection
– Unknown

20,813 (86.9%)
56 (0.2%)
2723 (11.4%)
349 (1.5%)

24,457 (86.2%)
73 (0.3%)
3616 (12.7%)
234 (0.8%)

26,742 (84.7%)
79 (0.3%)
4500 (14.3%)
260 (0.8%)
<0.001
Chemotherapy
– Yes
– No/unknown

11,203 (46.8%)
12,738 (53.1%)

14,553 (51.3%)
13,827 (48.7%)

17,935 (56.8%)
13,646 (43.2%)
<0.001
Radiotherapy
– Yes
– No/unknown

3786 (15.8%)
20155 (84.2%)

4829 (17%)
23551 (83%)

5509 (17.4%)
26072 (82.6%)
<0.001
The following SES variables were included: employment percentage, percent of people above the poverty line, percent of people identified as working-class, educational level, median rent, median household value and median household income.
SES: Socioeconomic status.
Mean follow-up for the entire study cohort is 8.9 months (standard deviation [SD]: 15.10) and for the sub-cohort of patients with a localized/regional disease who underwent resection is 25.74 months (SD: 29.39).

Predictors of surgical resection among patients with localized/regional disease

Multivariable logistic regression analysis was conducted to further elaborate on the impact of SES on referral to surgical resection among patients with localized/regional pancreatic cancer. Within this multivariable analysis, patients with lower SES were less likely to undergo surgical resection for pancreatic cancer (odds ratio: 0.719; 95% CI: 0.673–0.767; p < 0.001; Table 2).
Table 2. Multivariable logistic regression analysis for factors predicting surgical resection among patients with localized/regional disease.
ParameterOR (95% CI)p-value
Socioeconomic group
– Group 3
– Group 1
– Group 2

Reference
0.719 (0.673–0.767)
0.835 (0.788–0.886)


<0.001
<0.001
Sex
– Female
– Male

Reference
1.001 (0.952–1.052)
0.973
Race/ethnicity
– White non-Hispanic
– Black non-Hispanic
– Hispanic

Reference
0.768 (0.702–0.839)
0.808 (0.740–0.883)


<0.001
<0.001
Location
– Head
– Body
– Tail

Reference
0.400 (0.362–0.442)
2.418 (2.159–2.156)


<0.001
<0.001
Stage
– Regional
– Localized

Reference
0.576 (0.536–0.618)


<0.001
Age
– 40–69 years
– <40 years
– ≥70 years

Reference
1.811 (1.339–2.448)
0.490 (0.466–0.516)


<0.001
<0.001
This was adjusted for age at diagnosis, sex, and race, location of the primary tumor, SES group and stage.
All racial and location subgroups were included in the analysis but only the three biggest subgroups were reported here.
OR: Odds ratio; SES: Socioeconomic status.

Survival analyses among patients with localized/regional disease treated with surgical resection

Kaplan–Meier survival analysis was conducted to compare OS outcomes among surgically treated localized/regional pancreatic cancer patients. Patients with higher SES have better OS (median OS for group-3: 20.0 months vs 17.0 months for group-1; p < 0.001; Figure 1).
Figure 1. Kaplan-Meier survival estimates according to socioeconomic status.
SES: Socioeconomic status.
Multivariable Cox regression analysis was then used to evaluate the impact of SES on pancreatic cancer-specific survival among patients with a localized/regional disease treated with surgical resection. Patients with lower SES have worse pancreatic cancer-specific survival compared with patients with higher SES: (hazard ratio for group-1 vs group-3: 1.212; 95% CI: 1.135–1.295; p < 0.001; Table 3).
Table 3. Multivariable Cox regression analysis for factors predicting pancreatic cancer-specific survival among all patients with localized/regional disease who underwent surgical resection.
ParameterHR (95% CI)p-value
Socioeconomic group
– Group 3
– Group 1
– Group 2

Reference
1.212 (1.135–1.295)
1.130 (1.066–1.197)


<0.001
<0.001
Sex
– Female
– Male

Reference
0.962 (0.915–1.012)


0.132
Race/ethnicity
– White non-Hispanic
– Black non-Hispanic
– Hispanic

Reference
1.017 (0.928–1.115)
1.018 (0.927–1.117)


0.712
0.715
Location
– Head
– Body
– Tail

Reference
0.877 (0.779–0.988)
0.892 (0.805–0.988)


0.030
0.029
Stage
– Regional
– Localized

Reference
0.505 (0.463–0.551)


<0.001
Age
– 40–69 years
– <40 years
– ≥70 years

Reference
0.691 (0.522–0.913)
1.240 (1.178–1.305)


0.009
<0.001
This was adjusted for age at diagnosis, sex, and race, location of the primary tumor, SES group and stage.
All racial and location subgroups were included in the analysis but only the three biggest subgroups were reported here.
HR: Hazard ratio; SES: Socioeconomic status.

Pancreatic cancer-specific survival analyses among clinically defined subgroups of localized/regional disease patients treated with surgical resection

Multivariable Cox regression analyses were further conducted among clinically defined patients' subgroups according to race and stage. When stratified by race/ethnicity, SES was most powerful in predicting the outcomes of non-Hispanic white patients (hazard ratio for group-1 vs group-3: 1.207; 95% CI: 1.118–1.302; p < 0.001); while it played no role in the prediction of outcomes of Hispanic patients (hazard ratio for group-1 vs group-3: 1.055; 95% CI: 0.844–1.317; p = 0.640; Table 4). When the analyses were stratified by stage, the impact of SES was clear among both localized and regional disease patients. Hazard ratio for group-1 versus group-3 among localized disease patients was 1.283; 95% CI: 1.040–1.583; p = 0.020; while hazard ratio for group-1 versus group-3 among regional disease patients was 1.208; 95% CI: 1.127–1.295; p < 0.001 (Table 5Figure 2).
Table 4. Impact of socioeconomic group on pancreatic cancer-specific survival among patients with localized/regional disease who underwent resection according to race.
RaceSocioeconomic groupHR (95% CI)p-value
White non-HispanicGroup 3
Group 1
Group 2
Reference
1.207 (1.118–1.302)
1.133 (1.062–1.208)

<0.001
<0.001
Black non-HispanicGroup 3
Group 1
Group 2
Reference
1.415 (1.102–1.817)
1.333 (1.018–1.746)

0.006
0.037
HispanicGroup 3
Group 1
Group 2
Reference
1.055 (0.844–1.317)
0.957 (0.765–1.198)

0.640
0.703
Multivariate Cox regression analysis adjusted for age, stage, sex and location.
HR: Hazard ratio.
Table 5. Impact of socioeconomic group on pancreatic cancer-specific survival among patients with localized/regional disease who underwent resection according to stage.
RaceSocioeconomic groupHR (95% CI)p-value
Localized diseaseGroup 3
Group 1
Group 2
Reference
1.283 (1.040–1.583)
1.329 (1.095–1.614)

0.020
0.004
Regional diseaseGroup 3
Group 1
Group 2
Reference
1.208 (1.127–1.295)
1.113 (1.048–1.183)

<0.001
0.001
Multivariate Cox regression analysis adjusted for age, race, sex and location.
HR: Hazard ratio.
Figure 2. Impact of socioeconomic status (group 1 versus group III) on pancreatic cancer-specific survival.
Three dots in each line represent hazard ratio with 95% CIs.
SES: Socioeconomic status.

Discussion

The current study evaluates the impact of SES on the presentation of patients with pancreatic adenocarcinoma using a validated census-tract SES database. It shows that poor neighborhood SES is associated with more advanced disease at presentation, less probability of surgical resection, chemotherapy and radiation therapy; and even poorer outcomes after surgical resection.
It is interesting to note that although patients with higher SES were more likely to have older age at diagnosis, they were also more likely to be offered surgical resection. Although this might be partially explained by yet unknown comorbidity differences between different SES groups, this also might indicate a potential disparity in the access to surgical resection based on SES. It is also notable that regional disease patients were more likely to have surgical resection in the multivariable logistic regression analysis (as compared with localized disease patients). Possible reasons for this observation might include the fact that staging of patients included in the current study was based on pathological grounds in surgically treated patients (versus clinical grounds in nonsurgically treated patients). Thus, there was a possibility of upstaging among surgically treated patients. It is interesting also to note that Black race (compared with White race) was associated with lower likelihood of undergoing surgical resection. Moreover, race was not associated with a difference in survival outcomes when adjusted for SES.
Several previously published population-based studies have evaluated the impact of SES on the outcomes of pancreatic cancer patients, most of them focused on personal socioeconomic factors (like race, marital status or insurance status) [13,14]. A couple of previous studies evaluated neighborhood SES parameters using state-specific cancer registries in the US [15,16]. The current study provides a national overview (through the SEER database) of the impact of neighborhood SES parameters as a surrogate marker to the social determinants of health in individual patients and this has been done through a validated tool.
The current study has several limitations that need to be recognized; foremost, the absence of comorbidity and performance score information which might have affected treatment selection and outcomes. It should be noted also that prior studies have suggested a higher rate of noncancer comorbidities among patients with low SES [17]. To neutralize this confounding effect, survival analyses were limited to patients who have undergone surgical resection (to ensure patients with significant noncancer morbidity are not included in the survival analyses). Moreover, both overall and pancreatic cancer-specific survivals were evaluated in the current study. While OS may be affected by non-cancer mortality, cancer-specific survival is less likely to be affected by noncancer mortality. Second, the absence of detailed information about perioperative systemic or local treatments the patients might have received is another confounder in the current analysis. Third, it has also to be remembered that the results of the current study are most applicable to patients treated in the US. Whether these results can be applied to other healthcare settings/countries is unknown. Prior studies from a number of European countries have suggested similar impact of SES on outcomes of pancreatic cancer patients [18,19]. That being said, comparing studies conducted in Western European countries (where all residents will receive the same level of care regardless of SES) with studies conducted in the US (where healthcare access depends largely on SES) might be tricky. Fourth, the study is based on group SES assessment (neighborhood); applying the results to individual SES assessments might be associated with the risk of ecological fallacy (this fallacy happen when inferences about individuals are derived from inferences about their groups) [20]. This should be taken into consideration when interpreting the results of the current analysis.
These limitations need to be viewed in light of the clear strengths of the current study; most notably, the reliance on a well-designed, dedicated database for SES which follows the rigorous quality control procedures of the SEER database.
The difference in median survival between patients with low versus patients with high SES in the current study is remarkable. This is in line with prior studies showing significant impact for SES on the survival of other solid tumors [21–23]. Together, these studies call for an action to minimize disparities in cancer care. Health policymakers should prioritize strategies which address cancer care among the underserved and vulnerable populations in the society. That being said, structural problems within the healthcare insurance system within the US needs to be corrected in order for these strategies to work.

Conclusion

Poor neighborhood SES is associated with more advanced disease at presentation, less probability of surgical resection and even poorer outcomes after surgical resection.
Summary points
Surveillance, Epidemiology and End Results specialized socioeconomic status (SES) registry has been accessed and patients with pancreatic cancer diagnosed (2000–2015) were evaluated.
The following SES variables were included: employment percentage, percent of people above the poverty line, percent of people identified as working-class, educational level, median rent, median household value and median household income.
Within this SES registry, patients were classified according to their census-tract SES into three groups (where group-1 represents the lowest SES category and group-3 represents the highest SES category).
Multivariable logistic regression analysis was used to assess the impact of SES on access to surgical resection, and multivariable Cox regression analysis was used to assess the impact of SES on pancreatic cancer-specific survival.
Kaplan–Meier survival estimates were also used to compare overall survival (OS) outcomes according to SES.
A total of 83,902 pancreatic cancer patients were included in the current analysis.
Within multivariable logistic regression analysis among patients with a localized/regional disease, patients with lower SES were less likely to undergo surgical resection for pancreatic cancer (odds ratio: 0.719; 95% CI: 0.673–0.767; p < 0.001).
Among patients with a localized/regional disease who underwent surgical resection, patients with higher SES have better OS (median OS for group-3: 20.0 vs 17.0 months for group-1; p < 0.001).
Moreover, patients with lower SES have worse pancreatic cancer-specific survival compared with patients with higher SES: (hazard ratio for group-1 vs group-3: 1.212; 95% CI: 1.135–1.295; p < 0.001).

Acknowledgments

This study is based on the novel SEER specialized database for census-tract level SES data.

Financial & competing interests disclosure

The author has no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.
No writing assistance was utilized in the production of this manuscript.

Ethical conduct of research

Ethical approval: All procedures performed in studies involving human participants were following the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent: as this study is based on a publicly available database without identifying patient information, informed consent was not needed.

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