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Systemic therapy in stage IV pancreatic cancer: a population-based analysis using the National Cancer Data Base:

Systemic therapy in stage IV pancreatic cancer: a population-based analysis using the National... Background: Pancreatic cancer accounts for approximately 7% of all cancer deaths. More than half of all pancreatic cancers are stage IV at diagnosis, where systemic chemotherapy is used with the goal of life prolongation as well as palliation. The patient characteristics and health system factors that drive the use of systemic therapy are unknown. Method: This is a retrospective study of stage IV pancreatic cancer patients (n = 140,210) diagnosed between 2000 and 2011 in the NCDB. NCDB contains approximately 70% of new cancer diagnosis from more than 1500 accredited cancer programs in the United States and Puerto Rico. Chi-squared test was used to determine any differences in characteristics of patients who did or did not receive systemic therapy. Results: Our study demonstrated that only 49.1% of stage IV pancreatic cancer patients received systemic therapy. The use of systemic therapy is significantly lower in female, African American/Hispanic, patients older than 40 years, those without insurance or with Medicare and Medicaid, higher Charlson Comorbidity Score, poor economic and educational status and in nonacademic centers. Conclusions: This is the largest study to evaluate the determinants of systemic therapy use in stage IV pancreatic cancer. The use of systemic therapy was significantly lower in patients older than 40 years, lower educational status, nonprivate insurance and with higher Charlson Correspondence to: Nabin Khanal, MBBS Comorbidity Scores. In addition, the use of systemic therapy was lower with female sex, Department of Internal African Americans/Hispanic, and lower socio-economic status. Understanding the barriers Medicine, Creighton University Medical Center, in the use of systemic therapy as well as appropriate utilization of systemic therapy can both 601 N. 30th Street Suite 5850, Omaha, NE 68131, optimize cancer care. USA nabinkhanal@creighton. edu Keywords: Systemic therapy, stage IV pancreatic cancer, disparities Smrity Upadhyay, MBBS Department of Internal Medicine, Creighton University Medical Center, Introduction [Siegel et  al. 2014]. Even with surgical resection, Omaha, NE, USA In the United States, pancreatic cancer is the the recurrence rate of stage II disease is around Sumit Dahal, MBBS fourth leading cause of cancer-related mortality 40%, and that of stage III is up to 90% [Kayahara Department of Internal Medicine, Interfaith and accounts for about 7% of all cancer-related et al. 1993]. In metastatic pancreatic cancer, chem- Medical Center, Brooklyn, deaths. In 2014, 46,420 new diagnoses and 39,590 otherapy, compared with the best supportive care, NY, USA deaths are expected from pancreatic cancer, improves the median OS [Sultana et  al. 2007; Vijaya Raj Bhatt, MBBS Department of Internal reflecting the high public health burden of the dis- Pelzer et al. 2011; V alsecchi et al. 2014; Ghosn et al. Medicine, Division of ease. The 5-year overall survival (OS) of pancre- 2014] with risk of death reduced by as much as Hematology-Oncology, University of Nebraska atic cancer is 2% for stage IV disease [Siegel et al. 36% [Sultana et al. 2007], and improves quality of Medical Center, Omaha, 2014]. life [Shore et al. 2003; Moinpour et al. 2010]. NE, USA Peter T. Silberstein, MD Department of Internal The only potentially curative therapy for pancre- The use of chemotherapy in pancreatic cancer has Medicine, Division of atic cancer is surgical resection. However, 53% improved significantly in last two decades. In 1997, Hematology-Oncology, Creighton University cases of pancreatic cancer are stage IV at diagnosis, a phase III clinical trial determined that gemcit- Medical Center, Omaha, and hence not a candidate for curative resection abine confers a significant survival advantage NE, USA 198 http://tam.sagepub.com N Khanal, S Upadhyay et al. (5.65 versus 4.41 months, p = 0.0025) and clinical national cancer registries, including the benefit (23.8% versus 4.8%, p = 0.0022) over Surveillance, Epidemiology, and End Results 5-fluorouracil, thus leading to its approval for (SEER) database [Bilimoria et al. 2008]. improvement in symptoms [Burris et  al. 1997]. Afterwards the use of chemotherapy gradually Our study included newly diagnosed stage IV pan- shifted from 5-fluorouracil to gemcitabine for creatic cancer patients, and excluded those who advanced disease for next 10 years and subse- had nonmetastatic disease at diagnosis and later quently gemcitabine became the comparator arm developed metastasis. The Institutional Review in newer trails [Oberstein et  al. 2013]. In 2007, Board waiver was obtained from the University of Moore and colleagues demonstrated that gemcit- Nebraska Medical Center Institutional Review abine and erlotinib prolonged OS (median 6.24 Board. Using NCDB aggregate hospital compari- months versus 5.91 months, p = 0.038) over gem- son benchmark reports, a total of 140,210 patients citabine alone [Moore et  al. 2007]. However, the with stage IV pancreatic cancer were categorized modest prolongation in survival prevented its into two groups: patients, who did versus did not widespread use. receive systemic therapy (chemotherapy, hormone therapy, immunotherapy, or a combination of dif- Prior studies have demonstrated disparities in ther- ferent therapies). The two groups were then com- apy and outcomes of different cancers based on pared in terms of age, race, sex, Charlson demographic features such as age [Goodwin et al. Comorbidity Score, distance traveled, hospital 1993], race [Shavers and Brown, 2002; Murphy type, household income, insurance and educa- et al. 2009], education [Albano et al. 2007], socio- tional status. NCDB uses Charlson Comorbidity economic status [Aarts et  al. 2010] insurance sta- Score to characterize the burden of comorbid con- tus, hospital type [Bilimoria et  al. 2009; Raigani ditions. Educational status in NCDB is recorded et al. 2014] and year of treatment. Such studies on as an aggregate percentage of population without a healthcare disparities have mainly focused on high school degree residing in the zip code of the patients with nonmetastatic pancreatic cancer. patient at the time of diagnosis, using US Census There is a paucity of similar studies in stage IV pan- data from year 2000. [American College of creatic cancer. A prior study on this subject focused Surgeons (2014b)] For the analysis, we classified only on older patients and excluded patients, who hospital type into two main groups: academic cent- died within 30 days of diagnosis [Oberstein et  al. ers (teaching/research hospitals  associated with 2013]. Therefore, we utilized a large database of all university medical schools or designated as stage IV pancreatic cancer patients to analyze any National Cancer Institute Comprehensive Cancer variation in the use of systemic therapy based on Care Programs) and nonacademic centers (other patients’ demographic and other characteristics. hospitals including community cancer programs, comprehensive community cancer programs). [American College of Surgeons (2014a)] Methods This was a retrospective study of stage IV pancre- atic cancer patients diagnosed between 2000 and Statistical analysis 2011 in the National Cancer Data Base (NCDB). Patient characteristics were computed using NCDB is a nationwide oncology database for descriptive statistics. Pearson’s chi-squared test of more than 1500 Commission on Cancer- independence was used to calculate any statistical accredited cancer programs in the United States difference in the distribution of different variables and Puerto Rico. Approximately 70% of all newly between these two groups. The level of statistical diagnosed cases of cancer in the United States are significance was set to a p-value of <0.01. Because captured at the institutional level and reported to the data were presorted into different categories the NCDB [Bilimoria et  al. 2008]. The NCDB, by the NCDB, we were unable to conduct any begun in 1989, now contains approximately 29 patient-level multivariate analyses. million records from hospital cancer registries across the United States. [American College of Surgeons (2014c)] The NCDB requires reporting Results of all new cancer diagnoses from the hospitals that Of 303,534 total patients with pancreatic cancer are approved by the Commission on Cancer, and reported to NCDB between 2000 and 2011, shares common data coding, collection, and accu- 46.2% (n = 140,210) of patients were diagnosed racy assessment mechanisms with state and with stage IV pancreatic cancer. Patients with http://tam.sagepub.com 199 Therapeutic Advances in Medical Oncology 7(4) 54% 52% 50% 48% 46% 44% 42% 40% OO O1 O2 O3 O4 O5 O6 O7 O8 O9 10 11 Figure 1. Percentage of patients with stage IV pancreatic cancer, who received systemic therapy between the years 2000 and 2011. stage IV disease were predominantly elderly centers (52% versus 47%, p < 0.01). Patients with (74.6%; >60 years), White (79%), and male Charlson Comorbidity Score 0 were more likely to (53%). A total of 50% had Charlson Comorbidity receive systemic therapy (52.9%) compared with Score of zero. Only 49.1% (n = 68,848) of stage those with a score of 1 (46.5%) and 2 or more IV pancreatic cancer patients received systemic (34.8%) (p < 0.01). therapy. The use of systemic therapy increased from 47% in 2000 to 52.4% in 2011 (Figure 1). Discussion Men were more likely to receive systemic therapy Our study demonstrated that only 49% of stage IV compared with women (51% versus 47%, p < 0.01; pancreatic cancer patients received systemic ther- Table 1). Utilization of systemic therapy was less apy. The use of systemic therapy was lower among with advancing age (61.8% in age group 50–59 ver- older patients, females and patients with higher sus 56.8% in 60–69, 45.7% in 70–79 and 25.7% in Charlson Comorbidity Score and lower socio- 80–89, p < 0.01). Patients with poor economic sta- economic status, which is consistent with prior tus were less likely to receive systemic therapy studies [Goodwin et  al. 1993; Albano et  al. 2007; (42.2% with an annual income of less than Bilimoria et  al. 2009; Murphy et  al. 2009; Aarts US$28,000 versus 52.6% with an annual income of et  al. 2010]. A large SEER Medicare database more than US$49,000, p < 0.01). Patients with study of stage IV pancreatic cancer patients (n = private insurance (61.5%) were more likely to 3231) demonstrated an increase in the utilization receive systemic therapy compared with those with- of chemotherapy from 53% in 1998–1999 to 57% out insurance (43.5%), with Medicaid (48.7%) in 2004–2005. Patients, who were older, female, and with Medicare (42.2%) (p < 0.01). Patients black, unmarried, lived in suburban areas, or had were more likely to receive systemic therapy if they lower socioeconomic status, poorly differentiated were White (50%) compared with African carcinomas and two or more comorbidities, were Americans (45.2%) and Hispanics (45.7%) less likely to receive gemcitabine [Oberstein et  al. (p < 0.01). Patients with higher educational status 2013]. This study excluded patients, who died were more likely to receive systemic therapy (53.2% within 30 days, which may explain a higher receipt for patients living in an area with >88% with high of chemotherapy than in our study. school degree versus 43.8% for patients living in an area with <69% population with high school The systemic therapy use in our study was sig- degree, p < 0.01). Patients were more likely to nificantly lower in patients >60 years old and receive systemic therapy if they received treatment with higher Charlson Comorbidity Score. Sehgal in academic center compared with nonacademic and colleagues demonstrated that stage I–IV 200 http://tam.sagepub.com N Khanal, S Upadhyay et al. Table 1. Systemic therapy use in stage IV pancreatic cancers. Variables Systemic therapy n (%) No systemic therapy n (%) Age Under 20 22 (71) 9 (29) 20–29 125 (64) 70 (36) 30–39 984 (69.4) 433 (30.6) 40–49 5613 (65.2) 2998 (34.8) 50–59 15,713 (61.8) 9719 (38.2) 60–69 21,701 (56.8) 16,459 (43.2) 70–79 18,692 (45.7) 22,212 (54.3) 80–89 5807 (25.7 ) 16,794 (74.3) 90 and above 191 (6.6) 2668 (93.4) Sex Male 37,922 (51) 36,464 (49) Female 30,926 (47) 34,898 (53) Race White 55,309 (50.1) 55,251 (49.9) Hispanic 3087 (45.7) 3661 (54.3) African American 7853 (45.2) 9506 (54.8) Charlson Comorbidity Score None 37,404 (52.9) 33,355 (47.1) 1 11,976 (46.5) 13,783 (53.5) 2 or more 3210 (34.8) 6016 (65.2) Insurance Private 27,845 (61.5) 17,422 (38.5) Medicaid 3249 (48.7) 43,515 (51.3) Not insured 2099 (43.5) 2722 (56.5) Medicare 31,836 (42.2) 3417 (57.8) Other govt. 1458 (41.3) 2074 (58.7) Annual household income US$ >49,000 23,350 (52.6) 21,036 (47.4) 39,000–48,999 15,598 (49.5) 15,930 (50.5) 33,000–38,999 11,836 (47.8) 12,934 (52.2) 28,000–32,999 8142 (46.5) 9377 (53.5) <28,000 5864 (42.2) 8013 (57.8) Educational status* >88% 18,519 (53.2) 16,285 (46.8) 82.1–88% 16,644 (50.1) 16,630 (49.9) 77.1–82% 10,807 (48.5) 11,463 (51.5) 69.1–77% 10,626 (46.1) 12,405 (53.9) <69% 8189 (43.8) 10,500 (56.2) Hospital type Academic 24,942 (51.9) 23,146 (48.1) Non-academic 43,906 (47.7) 48,216 (52.3) Total 68,848 (49.1) 71,362 (50.9) (p < 0.01 for all comparisons.) *Aggregate percentage of individuals with a high school degree for patient’s zip code. pancreatic cancer patients >70 years old were chemotherapy as younger patients did [Sehgal less likely to receive chemotherapy; however, et al. 2014]. Even in patients with resectable pan- elderly patients derived similar benefits from creatic cancer, patients with older age and higher http://tam.sagepub.com 201 Therapeutic Advances in Medical Oncology 7(4) comorbidities are less likely to be surgical candi- differences or potential influences of gender or dates [Sener et al. 1999; Bilimoria et al. 2007].  racial differences on providers’ decision-making. Elderly patients (age >65 years) are often under- In our study, a higher income status and the represented in clinical trials because of the exclu- availability of a private insurance were associated sion criteria related to age, comorbidities or with a higher receipt of systemic therapy. This is performance status [Conroy et al. 2011; Von Hoff consistent with prior studies on pancreatic can- et al. 2013]. Several studies, however, have shown cer [Oberstein et  al. 2013] as well as metastatic that there is no relationship of age with OS in gastric cancers [Sherman et  al. 2013]. Although patients receiving treatment [Moore et  al. 2007; high cost associated with systemic therapy may Marechal et  al. 2013; Von Hoff et  al. 2013], explain this disparity, prior studies have also although elderly patients may have increased tox- shown that cost consideration can influence icity [Miyamoto et al. 2010]. Nakai and colleagues oncologists’ recommendations. In a survey of evaluated gemcitabine-based therapies in patients 167 oncologists, Schrag and colleagues demon- with advanced pancreatic cancer and demon- strated that one in six oncologists admitted omit- strated that comorbidities, rather than age, pre- ting treatment options based on their perception dicted poor outcomes [Nakai et  al. 2011]. of patients’ ability to afford treatment. However, However, Vickers and colleagues analyzed the one-third of the oncologists were not comforta- impact of comorbidities on patients receiving ble discussing the economic impact of cancer gemcitabine and erlotinib and found that OS was treatment [Schrag and Hanger, 2007]. Prior not affected by the presence of comorbidities studies have also shown that oncologists pre- [Vickers et  al. 2012]. Although elderly patients ferred patients to have access to effective cancer seem to benefit from systemic therapy in pancre- treatment only if the treatments are cost-effective, atic cancer [Hubbard et  al. 2011], a fear of although the cost-effectiveness threshold varied increased toxicity and decreased benefits may among oncologists [Nadler et  al. 2006; Berry lead to less aggressive treatment [Lewis et  al. et al. 2010]. 2003; Hubbard et al. 2011], which could explain lower utilization of systemic therapy with advanc- Our study also demonstrated a positive correlation ing age. between educational status and systemic therapy use. Higher education is associated with better uti- The major trials evaluating gemcitabine and erlo- lization of screening modalities, less exposure to nitib as well as gemcitabine and nab-paclitaxel risk factors and better access to healthcare services did not show any difference in outcomes based on [Mouw et  al. 2008]. Furthermore, Albano and gender [Moore et  al. 2007; Conroy et  al. 2011; colleagues in their analysis of 137,708 cancer Von Hoff et  al. 2013]. In fact, Moore and col- deaths demonstrated that educational status was leagues demonstrated an association between inversely associated with cancer-related mortality female sex and increased survival [Moore et  al. [Albano et  al. 2007]. These findings may suggest 2007]. Hence, it is clear that female patients that education in general as well as patient educa- derive at least similar benefits from chemotherapy tion may improve utilization of systemic therapy. as men do. Despite this, in our study, women were less likely to receive systemic therapy compared In our study, there was comparatively less utiliza- with men (47% versus 51%, p < 0.01). tion of systemic therapy in stage IV pancreatic cancer in nonacademic hospitals than academic Similarly, patients were more likely to receive sys- hospitals which is consistent with prior studies temic therapy if they were White (50%) compared that have analyzed the surgical management of with African Americans (45.2%) and Hispanics pancreatic cancer [Bilimoria et  al. 2007; Raigani (45.7%) (p < 0.01). In a SEER registry study of et  al. 2014]. This may be related to quality of locally advanced pancreatic adenocarcinoma patient counseling [Koedoot et al. 2004] and the patients, African-Americans had lower rates of differences in experience and availability of specialist consultation (p < 0.01), chemotherapy resources between the two settings. use (p < 0.01), and resection (p < 0.01) compared with Whites [Murphy et  al. 2009]. It is unclear Our study has certain limitations, which include whether these gender and racial disparities are sec- retrospective study design, utilization of a large ondary to patients’ preferences, patient–provider secondary database with a potential for miscod- interactions, socio-economic or educational ing, missing data and lack of patient-level data for 202 http://tam.sagepub.com N Khanal, S Upadhyay et al. multivariate analysis. Although the use of sys- lower economic or educational status, and higher temic therapy differed by race and other socio- Charlson Comorbidity Score. Future studies economic factors, minority status and low should focus on identifying the cause for lower sys- socioeconomic status frequently overlap. Hence, temic therapy use in these patient populations. these factors may not necessarily be the separate Disparities in receipt of systemic therapy in pan- drivers of the observed disparity. The differences creatic cancer may get worse with the use of between some of the groups are statistically sig- improved but more intensive and expensive thera- nificant but the actual difference is small. Such pies such as FOLFIRINOX and gemcitabine plus results may be due to the large sample size of our nab-paclitaxel . This highlights a need to under- study. Patients, who initially presented with early stand the barriers in the use of systemic therapy stage pancreatic cancer and later on developed that can improve the OS of the stage IV pancreatic metastasis, were excluded from the study. NCDB cancer. does not include patients seeking care in non- Commission on Cancer-approved hospitals, Acknowledgement which are usually smaller, located away from The study was published as an abstract form in urban locations and have less cancer-related ser- the proceedings of the American Society of vices available to patients. Patients diagnosed Clinical Oncology 50th annual meeting, 31 May with stage IV pancreatic cancer between 2000 2014. and 2011 were selected for this study. Hence, it is unlikely that many patients receiving newer ther- Conflict of interest statement apy options such as FOLFIRINOX or gemcit- Peter T Silberstein reports receiving payment for abine and nab-paclitaxel were included in our lectures  from Bristol Myers and  Celgene in the study. However, disparities in receipt of systemic past. There are no conflicts of interest for any therapy may get worse with the use of more inten- other authors.  sive and expensive therapies such as oxaliplatin, irinotecan, fluorouracil, and leucovorin Funding (FOLFIRINOX) [Conroy et al. 2011] and gem- This research received no specific grant from any citabine plus nab-paclitaxel [Von Hoff et al. 2013]. funding agency in the public, commercial, or not- These newer regimens has been shown to further for-profit sectors. improve survival, hence it becomes even more important to understand these disparities in can- cer treatment. References American College of Surgeons (2014a) NCDB Public A few prior studies have evaluated the receipt of Benchmark Reports. Available from systemic therapy in stage IV pancreatic cancer, however, these studies were small and evaluated http://cromwell.facs.org/bmarks/bmpub/ver10/help/ fewer variables. 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Systemic therapy in stage IV pancreatic cancer: a population-based analysis using the National Cancer Data Base:

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Abstract

Background: Pancreatic cancer accounts for approximately 7% of all cancer deaths. More than half of all pancreatic cancers are stage IV at diagnosis, where systemic chemotherapy is used with the goal of life prolongation as well as palliation. The patient characteristics and health system factors that drive the use of systemic therapy are unknown. Method: This is a retrospective study of stage IV pancreatic cancer patients (n = 140,210) diagnosed between 2000 and 2011 in the NCDB. NCDB contains approximately 70% of new cancer diagnosis from more than 1500 accredited cancer programs in the United States and Puerto Rico. Chi-squared test was used to determine any differences in characteristics of patients who did or did not receive systemic therapy. Results: Our study demonstrated that only 49.1% of stage IV pancreatic cancer patients received systemic therapy. The use of systemic therapy is significantly lower in female, African American/Hispanic, patients older than 40 years, those without insurance or with Medicare and Medicaid, higher Charlson Comorbidity Score, poor economic and educational status and in nonacademic centers. Conclusions: This is the largest study to evaluate the determinants of systemic therapy use in stage IV pancreatic cancer. The use of systemic therapy was significantly lower in patients older than 40 years, lower educational status, nonprivate insurance and with higher Charlson Correspondence to: Nabin Khanal, MBBS Comorbidity Scores. In addition, the use of systemic therapy was lower with female sex, Department of Internal African Americans/Hispanic, and lower socio-economic status. Understanding the barriers Medicine, Creighton University Medical Center, in the use of systemic therapy as well as appropriate utilization of systemic therapy can both 601 N. 30th Street Suite 5850, Omaha, NE 68131, optimize cancer care. USA nabinkhanal@creighton. edu Keywords: Systemic therapy, stage IV pancreatic cancer, disparities Smrity Upadhyay, MBBS Department of Internal Medicine, Creighton University Medical Center, Introduction [Siegel et  al. 2014]. Even with surgical resection, Omaha, NE, USA In the United States, pancreatic cancer is the the recurrence rate of stage II disease is around Sumit Dahal, MBBS fourth leading cause of cancer-related mortality 40%, and that of stage III is up to 90% [Kayahara Department of Internal Medicine, Interfaith and accounts for about 7% of all cancer-related et al. 1993]. In metastatic pancreatic cancer, chem- Medical Center, Brooklyn, deaths. In 2014, 46,420 new diagnoses and 39,590 otherapy, compared with the best supportive care, NY, USA deaths are expected from pancreatic cancer, improves the median OS [Sultana et  al. 2007; Vijaya Raj Bhatt, MBBS Department of Internal reflecting the high public health burden of the dis- Pelzer et al. 2011; V alsecchi et al. 2014; Ghosn et al. Medicine, Division of ease. The 5-year overall survival (OS) of pancre- 2014] with risk of death reduced by as much as Hematology-Oncology, University of Nebraska atic cancer is 2% for stage IV disease [Siegel et al. 36% [Sultana et al. 2007], and improves quality of Medical Center, Omaha, 2014]. life [Shore et al. 2003; Moinpour et al. 2010]. NE, USA Peter T. Silberstein, MD Department of Internal The only potentially curative therapy for pancre- The use of chemotherapy in pancreatic cancer has Medicine, Division of atic cancer is surgical resection. However, 53% improved significantly in last two decades. In 1997, Hematology-Oncology, Creighton University cases of pancreatic cancer are stage IV at diagnosis, a phase III clinical trial determined that gemcit- Medical Center, Omaha, and hence not a candidate for curative resection abine confers a significant survival advantage NE, USA 198 http://tam.sagepub.com N Khanal, S Upadhyay et al. (5.65 versus 4.41 months, p = 0.0025) and clinical national cancer registries, including the benefit (23.8% versus 4.8%, p = 0.0022) over Surveillance, Epidemiology, and End Results 5-fluorouracil, thus leading to its approval for (SEER) database [Bilimoria et al. 2008]. improvement in symptoms [Burris et  al. 1997]. Afterwards the use of chemotherapy gradually Our study included newly diagnosed stage IV pan- shifted from 5-fluorouracil to gemcitabine for creatic cancer patients, and excluded those who advanced disease for next 10 years and subse- had nonmetastatic disease at diagnosis and later quently gemcitabine became the comparator arm developed metastasis. The Institutional Review in newer trails [Oberstein et  al. 2013]. In 2007, Board waiver was obtained from the University of Moore and colleagues demonstrated that gemcit- Nebraska Medical Center Institutional Review abine and erlotinib prolonged OS (median 6.24 Board. Using NCDB aggregate hospital compari- months versus 5.91 months, p = 0.038) over gem- son benchmark reports, a total of 140,210 patients citabine alone [Moore et  al. 2007]. However, the with stage IV pancreatic cancer were categorized modest prolongation in survival prevented its into two groups: patients, who did versus did not widespread use. receive systemic therapy (chemotherapy, hormone therapy, immunotherapy, or a combination of dif- Prior studies have demonstrated disparities in ther- ferent therapies). The two groups were then com- apy and outcomes of different cancers based on pared in terms of age, race, sex, Charlson demographic features such as age [Goodwin et al. Comorbidity Score, distance traveled, hospital 1993], race [Shavers and Brown, 2002; Murphy type, household income, insurance and educa- et al. 2009], education [Albano et al. 2007], socio- tional status. NCDB uses Charlson Comorbidity economic status [Aarts et  al. 2010] insurance sta- Score to characterize the burden of comorbid con- tus, hospital type [Bilimoria et  al. 2009; Raigani ditions. Educational status in NCDB is recorded et al. 2014] and year of treatment. Such studies on as an aggregate percentage of population without a healthcare disparities have mainly focused on high school degree residing in the zip code of the patients with nonmetastatic pancreatic cancer. patient at the time of diagnosis, using US Census There is a paucity of similar studies in stage IV pan- data from year 2000. [American College of creatic cancer. A prior study on this subject focused Surgeons (2014b)] For the analysis, we classified only on older patients and excluded patients, who hospital type into two main groups: academic cent- died within 30 days of diagnosis [Oberstein et  al. ers (teaching/research hospitals  associated with 2013]. Therefore, we utilized a large database of all university medical schools or designated as stage IV pancreatic cancer patients to analyze any National Cancer Institute Comprehensive Cancer variation in the use of systemic therapy based on Care Programs) and nonacademic centers (other patients’ demographic and other characteristics. hospitals including community cancer programs, comprehensive community cancer programs). [American College of Surgeons (2014a)] Methods This was a retrospective study of stage IV pancre- atic cancer patients diagnosed between 2000 and Statistical analysis 2011 in the National Cancer Data Base (NCDB). Patient characteristics were computed using NCDB is a nationwide oncology database for descriptive statistics. Pearson’s chi-squared test of more than 1500 Commission on Cancer- independence was used to calculate any statistical accredited cancer programs in the United States difference in the distribution of different variables and Puerto Rico. Approximately 70% of all newly between these two groups. The level of statistical diagnosed cases of cancer in the United States are significance was set to a p-value of <0.01. Because captured at the institutional level and reported to the data were presorted into different categories the NCDB [Bilimoria et  al. 2008]. The NCDB, by the NCDB, we were unable to conduct any begun in 1989, now contains approximately 29 patient-level multivariate analyses. million records from hospital cancer registries across the United States. [American College of Surgeons (2014c)] The NCDB requires reporting Results of all new cancer diagnoses from the hospitals that Of 303,534 total patients with pancreatic cancer are approved by the Commission on Cancer, and reported to NCDB between 2000 and 2011, shares common data coding, collection, and accu- 46.2% (n = 140,210) of patients were diagnosed racy assessment mechanisms with state and with stage IV pancreatic cancer. Patients with http://tam.sagepub.com 199 Therapeutic Advances in Medical Oncology 7(4) 54% 52% 50% 48% 46% 44% 42% 40% OO O1 O2 O3 O4 O5 O6 O7 O8 O9 10 11 Figure 1. Percentage of patients with stage IV pancreatic cancer, who received systemic therapy between the years 2000 and 2011. stage IV disease were predominantly elderly centers (52% versus 47%, p < 0.01). Patients with (74.6%; >60 years), White (79%), and male Charlson Comorbidity Score 0 were more likely to (53%). A total of 50% had Charlson Comorbidity receive systemic therapy (52.9%) compared with Score of zero. Only 49.1% (n = 68,848) of stage those with a score of 1 (46.5%) and 2 or more IV pancreatic cancer patients received systemic (34.8%) (p < 0.01). therapy. The use of systemic therapy increased from 47% in 2000 to 52.4% in 2011 (Figure 1). Discussion Men were more likely to receive systemic therapy Our study demonstrated that only 49% of stage IV compared with women (51% versus 47%, p < 0.01; pancreatic cancer patients received systemic ther- Table 1). Utilization of systemic therapy was less apy. The use of systemic therapy was lower among with advancing age (61.8% in age group 50–59 ver- older patients, females and patients with higher sus 56.8% in 60–69, 45.7% in 70–79 and 25.7% in Charlson Comorbidity Score and lower socio- 80–89, p < 0.01). Patients with poor economic sta- economic status, which is consistent with prior tus were less likely to receive systemic therapy studies [Goodwin et  al. 1993; Albano et  al. 2007; (42.2% with an annual income of less than Bilimoria et  al. 2009; Murphy et  al. 2009; Aarts US$28,000 versus 52.6% with an annual income of et  al. 2010]. A large SEER Medicare database more than US$49,000, p < 0.01). Patients with study of stage IV pancreatic cancer patients (n = private insurance (61.5%) were more likely to 3231) demonstrated an increase in the utilization receive systemic therapy compared with those with- of chemotherapy from 53% in 1998–1999 to 57% out insurance (43.5%), with Medicaid (48.7%) in 2004–2005. Patients, who were older, female, and with Medicare (42.2%) (p < 0.01). Patients black, unmarried, lived in suburban areas, or had were more likely to receive systemic therapy if they lower socioeconomic status, poorly differentiated were White (50%) compared with African carcinomas and two or more comorbidities, were Americans (45.2%) and Hispanics (45.7%) less likely to receive gemcitabine [Oberstein et  al. (p < 0.01). Patients with higher educational status 2013]. This study excluded patients, who died were more likely to receive systemic therapy (53.2% within 30 days, which may explain a higher receipt for patients living in an area with >88% with high of chemotherapy than in our study. school degree versus 43.8% for patients living in an area with <69% population with high school The systemic therapy use in our study was sig- degree, p < 0.01). Patients were more likely to nificantly lower in patients >60 years old and receive systemic therapy if they received treatment with higher Charlson Comorbidity Score. Sehgal in academic center compared with nonacademic and colleagues demonstrated that stage I–IV 200 http://tam.sagepub.com N Khanal, S Upadhyay et al. Table 1. Systemic therapy use in stage IV pancreatic cancers. Variables Systemic therapy n (%) No systemic therapy n (%) Age Under 20 22 (71) 9 (29) 20–29 125 (64) 70 (36) 30–39 984 (69.4) 433 (30.6) 40–49 5613 (65.2) 2998 (34.8) 50–59 15,713 (61.8) 9719 (38.2) 60–69 21,701 (56.8) 16,459 (43.2) 70–79 18,692 (45.7) 22,212 (54.3) 80–89 5807 (25.7 ) 16,794 (74.3) 90 and above 191 (6.6) 2668 (93.4) Sex Male 37,922 (51) 36,464 (49) Female 30,926 (47) 34,898 (53) Race White 55,309 (50.1) 55,251 (49.9) Hispanic 3087 (45.7) 3661 (54.3) African American 7853 (45.2) 9506 (54.8) Charlson Comorbidity Score None 37,404 (52.9) 33,355 (47.1) 1 11,976 (46.5) 13,783 (53.5) 2 or more 3210 (34.8) 6016 (65.2) Insurance Private 27,845 (61.5) 17,422 (38.5) Medicaid 3249 (48.7) 43,515 (51.3) Not insured 2099 (43.5) 2722 (56.5) Medicare 31,836 (42.2) 3417 (57.8) Other govt. 1458 (41.3) 2074 (58.7) Annual household income US$ >49,000 23,350 (52.6) 21,036 (47.4) 39,000–48,999 15,598 (49.5) 15,930 (50.5) 33,000–38,999 11,836 (47.8) 12,934 (52.2) 28,000–32,999 8142 (46.5) 9377 (53.5) <28,000 5864 (42.2) 8013 (57.8) Educational status* >88% 18,519 (53.2) 16,285 (46.8) 82.1–88% 16,644 (50.1) 16,630 (49.9) 77.1–82% 10,807 (48.5) 11,463 (51.5) 69.1–77% 10,626 (46.1) 12,405 (53.9) <69% 8189 (43.8) 10,500 (56.2) Hospital type Academic 24,942 (51.9) 23,146 (48.1) Non-academic 43,906 (47.7) 48,216 (52.3) Total 68,848 (49.1) 71,362 (50.9) (p < 0.01 for all comparisons.) *Aggregate percentage of individuals with a high school degree for patient’s zip code. pancreatic cancer patients >70 years old were chemotherapy as younger patients did [Sehgal less likely to receive chemotherapy; however, et al. 2014]. Even in patients with resectable pan- elderly patients derived similar benefits from creatic cancer, patients with older age and higher http://tam.sagepub.com 201 Therapeutic Advances in Medical Oncology 7(4) comorbidities are less likely to be surgical candi- differences or potential influences of gender or dates [Sener et al. 1999; Bilimoria et al. 2007].  racial differences on providers’ decision-making. Elderly patients (age >65 years) are often under- In our study, a higher income status and the represented in clinical trials because of the exclu- availability of a private insurance were associated sion criteria related to age, comorbidities or with a higher receipt of systemic therapy. This is performance status [Conroy et al. 2011; Von Hoff consistent with prior studies on pancreatic can- et al. 2013]. Several studies, however, have shown cer [Oberstein et  al. 2013] as well as metastatic that there is no relationship of age with OS in gastric cancers [Sherman et  al. 2013]. Although patients receiving treatment [Moore et  al. 2007; high cost associated with systemic therapy may Marechal et  al. 2013; Von Hoff et  al. 2013], explain this disparity, prior studies have also although elderly patients may have increased tox- shown that cost consideration can influence icity [Miyamoto et al. 2010]. Nakai and colleagues oncologists’ recommendations. In a survey of evaluated gemcitabine-based therapies in patients 167 oncologists, Schrag and colleagues demon- with advanced pancreatic cancer and demon- strated that one in six oncologists admitted omit- strated that comorbidities, rather than age, pre- ting treatment options based on their perception dicted poor outcomes [Nakai et  al. 2011]. of patients’ ability to afford treatment. However, However, Vickers and colleagues analyzed the one-third of the oncologists were not comforta- impact of comorbidities on patients receiving ble discussing the economic impact of cancer gemcitabine and erlotinib and found that OS was treatment [Schrag and Hanger, 2007]. Prior not affected by the presence of comorbidities studies have also shown that oncologists pre- [Vickers et  al. 2012]. Although elderly patients ferred patients to have access to effective cancer seem to benefit from systemic therapy in pancre- treatment only if the treatments are cost-effective, atic cancer [Hubbard et  al. 2011], a fear of although the cost-effectiveness threshold varied increased toxicity and decreased benefits may among oncologists [Nadler et  al. 2006; Berry lead to less aggressive treatment [Lewis et  al. et al. 2010]. 2003; Hubbard et al. 2011], which could explain lower utilization of systemic therapy with advanc- Our study also demonstrated a positive correlation ing age. between educational status and systemic therapy use. Higher education is associated with better uti- The major trials evaluating gemcitabine and erlo- lization of screening modalities, less exposure to nitib as well as gemcitabine and nab-paclitaxel risk factors and better access to healthcare services did not show any difference in outcomes based on [Mouw et  al. 2008]. Furthermore, Albano and gender [Moore et  al. 2007; Conroy et  al. 2011; colleagues in their analysis of 137,708 cancer Von Hoff et  al. 2013]. In fact, Moore and col- deaths demonstrated that educational status was leagues demonstrated an association between inversely associated with cancer-related mortality female sex and increased survival [Moore et  al. [Albano et  al. 2007]. These findings may suggest 2007]. Hence, it is clear that female patients that education in general as well as patient educa- derive at least similar benefits from chemotherapy tion may improve utilization of systemic therapy. as men do. Despite this, in our study, women were less likely to receive systemic therapy compared In our study, there was comparatively less utiliza- with men (47% versus 51%, p < 0.01). tion of systemic therapy in stage IV pancreatic cancer in nonacademic hospitals than academic Similarly, patients were more likely to receive sys- hospitals which is consistent with prior studies temic therapy if they were White (50%) compared that have analyzed the surgical management of with African Americans (45.2%) and Hispanics pancreatic cancer [Bilimoria et  al. 2007; Raigani (45.7%) (p < 0.01). In a SEER registry study of et  al. 2014]. This may be related to quality of locally advanced pancreatic adenocarcinoma patient counseling [Koedoot et al. 2004] and the patients, African-Americans had lower rates of differences in experience and availability of specialist consultation (p < 0.01), chemotherapy resources between the two settings. use (p < 0.01), and resection (p < 0.01) compared with Whites [Murphy et  al. 2009]. It is unclear Our study has certain limitations, which include whether these gender and racial disparities are sec- retrospective study design, utilization of a large ondary to patients’ preferences, patient–provider secondary database with a potential for miscod- interactions, socio-economic or educational ing, missing data and lack of patient-level data for 202 http://tam.sagepub.com N Khanal, S Upadhyay et al. multivariate analysis. Although the use of sys- lower economic or educational status, and higher temic therapy differed by race and other socio- Charlson Comorbidity Score. Future studies economic factors, minority status and low should focus on identifying the cause for lower sys- socioeconomic status frequently overlap. Hence, temic therapy use in these patient populations. these factors may not necessarily be the separate Disparities in receipt of systemic therapy in pan- drivers of the observed disparity. The differences creatic cancer may get worse with the use of between some of the groups are statistically sig- improved but more intensive and expensive thera- nificant but the actual difference is small. Such pies such as FOLFIRINOX and gemcitabine plus results may be due to the large sample size of our nab-paclitaxel . This highlights a need to under- study. Patients, who initially presented with early stand the barriers in the use of systemic therapy stage pancreatic cancer and later on developed that can improve the OS of the stage IV pancreatic metastasis, were excluded from the study. NCDB cancer. does not include patients seeking care in non- Commission on Cancer-approved hospitals, Acknowledgement which are usually smaller, located away from The study was published as an abstract form in urban locations and have less cancer-related ser- the proceedings of the American Society of vices available to patients. Patients diagnosed Clinical Oncology 50th annual meeting, 31 May with stage IV pancreatic cancer between 2000 2014. and 2011 were selected for this study. Hence, it is unlikely that many patients receiving newer ther- Conflict of interest statement apy options such as FOLFIRINOX or gemcit- Peter T Silberstein reports receiving payment for abine and nab-paclitaxel were included in our lectures  from Bristol Myers and  Celgene in the study. However, disparities in receipt of systemic past. There are no conflicts of interest for any therapy may get worse with the use of more inten- other authors.  sive and expensive therapies such as oxaliplatin, irinotecan, fluorouracil, and leucovorin Funding (FOLFIRINOX) [Conroy et al. 2011] and gem- This research received no specific grant from any citabine plus nab-paclitaxel [Von Hoff et al. 2013]. funding agency in the public, commercial, or not- These newer regimens has been shown to further for-profit sectors. improve survival, hence it becomes even more important to understand these disparities in can- cer treatment. References American College of Surgeons (2014a) NCDB Public A few prior studies have evaluated the receipt of Benchmark Reports. Available from systemic therapy in stage IV pancreatic cancer, however, these studies were small and evaluated http://cromwell.facs.org/bmarks/bmpub/ver10/help/ fewer variables. 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Journal

Therapeutic Advances in Medical OncologySAGE

Published: Apr 6, 2015

Keywords: Systemic therapy; stage IV pancreatic cancer; disparities

References