Disparities in Pancreas Cancer Care

10

Click here to load reader

Transcript of Disparities in Pancreas Cancer Care

Page 1: Disparities in Pancreas Cancer Care

ORIGINAL ARTICLE – PANCREATIC TUMORS

Disparities in Pancreas Cancer Care

Anasooya Abraham1, Waddah B. Al-Refaie1,2, Helen M. Parsons1, Vikas Dudeja1, Selwyn M. Vickers1,

and Elizabeth B. Habermann1,3

1The Minnesota Surgical Outcomes Workgroup, University of Minnesota Surgical Outcomes Research Center, University

of Minnesota, Minneapolis, MN; 2Minneapolis Veterans Affairs Health Care System, Minneapolis, MN; 3Department of

Surgery, University of Minnesota, Minneapolis, MN

ABSTRACT

Background. Prior literature shows demographic differ-

ences in patients surgically treated for pancreatic cancer

(PC). We hypothesized that socioeconomic disparities also

exist across all aspects of PC care, in both surgically and

non-surgically treated patients.

Methods. We identified a cohort of patients with Ameri-

can Joint Committee on Cancer (AJCC) stage I–IV PC in

the 1994–2008 California Cancer Registry. We used mul-

tivariate logistic regression to examine the impact of race,

sex, and insurance status on (1) resectability (absence of

advanced disease), (2) receipt of surgery, and (3) receipt of

adjuvant/primary chemotherapy (?/– radiotherapy).

Results. Among 20,312 patients, 7,585 (37 %) had

resectable disease; 40 % who met this definition received

surgery (N = 3,153). On multivariate analysis, males were

less likely to present with resectable tumors [odds ratio

(OR) 0.91, 95 % confidence interval (CI) 0.85–0.96], but

sex did not otherwise predict treatment. Black patients

were as likely as White patients to show resectable disease,

yet were less likely to receive surgery (OR 0.66, 95 % CI

0.54–0.80), and adjuvant (OR 0.75, 95 % CI 0.58–0.98) or

primary chemotherapy ?/– radiation. Compared with

Medicaid recipients, non-Medicare/Medicaid enrollees

were more likely to receive surgery (OR 1.7, 95 % CI 1.4–

2.2), and the uninsured were less likely to receive adjuvant

therapy (OR 0.54, 95 % CI 0.30–0.98).

Conclusions. Though Black patients appear to present

with comparable rates of resectability, they receive care

that deviates from current guidelines. Insurance status is

associated with inferior profiles of resectability and treat-

ments. Future policies and research should identify

effective strategies to ensure receipt of standard care.

While over 40,000 new cases of pancreatic cancer are

diagnosed each year, 5-year survival is nominal and has

remained low for 30 years.1–3 Prior studies show that the

epidemiology, treatment, and survival of this malignancy

vary by demographics such as race and socioeconomic

status (SES).4,5 Black males suffer the highest incidence of

pancreatic cancer, yet Blacks are less likely to receive

specialty referral, surgical evaluation, cancer-directed sur-

gery, and treatment at high-volume centers compared with

Whites.1,6–8 Similarly, several studies have demonstrated

that pancreas cancer patients with lower SES have worse

postoperative mortality and survival.6,9,10 These disparities

also exist in access to and participation in clinical trials.

While much of the existing literature examines disparities

in the subset of patients with locoregional PC amenable to

surgery, nearly 75 % of pancreatic cancer patients present

with advanced disease.1 We build upon previous disparities

research and examine differences in treatment of pancreatic

cancer patients presenting with all disease stages.

Current National Comprehensive Cancer Network rec-

ommendations for locoregional disease include resection

and adjuvant therapy. Unresectable patients with good

performance status are offered chemoradiation. We

hypothesized that sociodemographic differences (age, sex,

race, insurance status) in the management of pancreatic

cancer exist along all points of care, from presentation to

treatment (Appendix 1). We examined variations by race,

sex, and insurance status on:

1. Resectability at presentation

2. Surgical resection in those with resectable disease

3. Chemotherapy receipt (with and without radiation)

after pancreatectomy

� Society of Surgical Oncology 2013

First Received: 10 February 2012;

Published Online: 12 April 2013

E. B. Habermann

e-mail: [email protected]

Ann Surg Oncol (2013) 20:2078–2087

DOI 10.1245/s10434-012-2843-z

Page 2: Disparities in Pancreas Cancer Care

4. Chemotherapy receipt [with and without radiotherapy

(RT)] as primary treatment in nonresectable PC

(locally advanced/metastatic)

The delivery of guideline-recommended care remains

paramount as more effective therapies are explored in

clinical trial settings to promote a combined approach to

improving population-based outcomes for pancreatic can-

cer in the USA.

METHODS

Study Design and Database

We used the 1994–2008 California Cancer Registry (CCR)

to conduct our retrospective, observational study. The CCR is

a statewide, population-based cancer surveillance system.

Abstractors collect data from 10 regional registries encom-

passing 58 counties according to documented standards on

demographics, cancer type, extent of disease, treatment, and

survival. Information on first course of therapy is provided but,

regarding chemotherapy, does not include specific agents,

dosages or duration/completion of therapy.

Patients

We limited our cohort to patients with adenocarcinomas

of the pancreatic head, body, and tail, International Clas-

sification of Disease site codes C250–C252; histology

codes 8010, 8020–8022, 8000, 8070–8078, 814–815 8210–

8211, 8230, 8260–8263, 8470–8471, 8480–8481, 8490,

8500–8503, 8560, 8562, 8570, 8574–8575, 8262, 8310,

8323, 8440, 8571–8573, 8576.

We excluded patients younger than 18 and older than

95 years at diagnosis (as there are no published guidelines

on age thresholds for offering therapies). Our upper and

lower age limits were chosen to allow appropriate and

reportable cell size for analysis and to preserve anonymity.

The race variable used in this study codes Hispanics as

White. As our focus was on differences in comparison with

Blacks, we felt this was an appropriate classification. We

excluded patients who had more than one prior cancer (any

site) and those with unknown disease extent, surgery

receipt, nodal status or chemotherapy status. Patients

treated with radiation alone were excluded due to inade-

quate cell size for analysis. Cases identified via death

certificates, nursing home records or coroner’s reports were

excluded. CCR data were censored on December 31, 2008.

Definition of Resectable Disease

In CCR, extent of disease is abstracted from pre- and/or

postoperative clinical and pathological data. We adhered to

National Comprehensive Cancer Network and American

College of Surgeons definitions of resectable disease.

While we cannot be sure that every clinician abides by

these definitions, they are generally established. Though all

data to achieve these definitions are not provided in CCR,

we utilized what was available to approximate the concept

of resectability. Accordingly, we defined tumors involving

major blood vessels (aorta, celiac axis, superior mesenteric

artery or vein), liver or diaphragm as unresectable. All

other localized disease or that involving stomach, spleen,

omentum, urologic organs, adrenal glands, colon or small

bowel was classified as resectable.

Adjuvant Chemotherapy and Radiation Definitions

CCR defines the first course of therapy as all therapy

received before disease progression or treatment failure; if

disease progression or treatment failures are not docu-

mented, first course is considered to be any treatment

received 1 year from diagnosis. Radiation and chemo-

therapy receipt are coded separately. Radiation was defined

as none versus beam/implants/isotopes/not otherwise

specified. Radiation alone was excluded from the study

since few persons received only radiation.

If data indicated that chemotherapy was (1) contraindi-

cated, (2) recommended, but not given, or (3) refused, or

(4) the patient died prior to administration, patients were

coded as not having received chemotherapy. Chemother-

apy and radiation receipt were examined separately among

patients who had and had not undergone surgery in order to

evaluate trends in adjuvant therapy versus primary che-

moradiotherapy receipt.

Constructed Variables

Surgery was defined as any pancreatectomy or local

excision. Local excision in CCR could include any partial

pancreatic excision and therefore could include the stan-

dard, curative pancreaticoduodenectomy.

We categorized age as 18–65 (a non-Medicare-eligible

subgroup), 65–69, 70–74, 75–79, and 80–95 years and race

as Black, White, and other. We classified insurance as

Medicare, Medicaid, non-Medicare/Medicaid [including

health maintenance organization (HMO), preferred pro-

vider organization (PPO), other managed care, Veterans

Affairs, TRICARE, Military, Indian/Public Health Service,

and county insurance], unknown, and no insurance.

Another method of managing unknown insurance status

would have been to exclude these cases. However, this

would result in loss of valuable information regarding

demographics and treatment (e.g., patients for whom race

and treatment factors were known but insurance status was

unknown). Unknown insurance status represents a distinct

Pancreas Cancer Care 2079

Page 3: Disparities in Pancreas Cancer Care

entity which we felt should be included in statistical

analysis.

Well-differentiated and moderately well-differentiated

tumors were classified as low grade, while poorly differ-

entiated and undifferentiated tumors were classified as high

grade. Finally, we classified disease extent as peripancre-

atic, beyond the pancreas or metastatic.

To examine therapy trends, patients were classified as

having undergone surgery alone, adjuvant chemotherapy

only, or both adjuvant chemotherapy and radiotherapy. As

radiation alone is not standard treatment for pancreatic cancer

and represented too small a group for analysis, this group was

excluded. Non-surgically treated patients were classified by

chemotherapy or chemoradiotherapy receipt. CCR does not

provide information on specific indications for chemoradia-

tion therapy in metastatic disease. However, these modalities

are frequently used as palliation and so were included.

Finally, in the analysis of chemoradiation receipt (as

adjuvant and primary therapy), persons who received

chemotherapy only or radiation only were classified as

having received no chemoradiation.

Statistical Analyses

We compared patient- and tumor-related factors by

resectability, surgery, and chemotherapy with or without

RT using the v2 test. The Cochran–Armitage method was

used to test trends. We used multivariate logistic regression

to predict the following: (1) resectability at diagnosis, (2)

receipt of surgery in those classified as resectable, (3)

adjuvant chemotherapy receipt with and without radiation,

and (4) chemotherapy (with or without RT) in those with

unresectable PC (locally advanced/metastatic), while

adjusting for covariates [age category, sex, race, insurance

status, grade, extent of disease, disease site (head, body,

tail), tumor size, and nodal positivity].

When main effects were significant, interactions for all

binary combinations of age group, sex, race, and insurance

status were tested. Interactions were considered significant

at p = 0.1 level, and all other results were significant at

p = 0.05 level using two-sided tests, when applicable. All

analyses were performed using SAS version 9.2 (SAS

Institute, Cary, NC). The study was approved by the

institutional Human Subjects Committee of the University

of Minnesota and by the California Cancer Registry.

RESULTS

Cohort Characteristics

During our study period, 20,312 patients with stage I–IV

pancreatic adenocarcinoma were identified (Table 1 and

Appendix 2). Median age at diagnosis was 70 years, and 51 %

were female. The majority of our population was White (82 %)

and insured (88 %). Up to 46 % of cases were metastatic.

Resectability at Diagnosis and Pancreatic Resection

While 37 % (N = 7,585) of the cohort were identified to

have resectable disease, only 42 % (N = 3,153) of these cases

underwent surgery. In other words, only 15 % (N = 3,153) of

the cohort underwent surgery. On bivariate analyses, we found

no significant differences in resectability across patient race

(38 % White, 37 % Black, 36 % other, p = 0.412) (Table 1).

However, a higher proportion of Whites underwent pancreatic

resection compared with Blacks (42 vs 36 %, p = 0.002).

After adjusting for covariates, increasing age, female sex,

non-Medicare/Medicaid insurance, and pancreatic head

tumors predicted presentation with resectable disease. Race

did not predict resectable disease (Table 2).

Among those with resectable disease, White race,

younger age, and non-Medicare/Medicaid and Medicare

insurance predicted undergoing pancreatectomy. Blacks

were 34 % less likely to undergo pancreatic resection as

compared with Whites (OR 0.66, 95 % CI 0.54–0.80).

However, sex did not predict surgery receipt (Table 3).

Adjuvant Chemotherapy (With or Without Radiation)

Among surgically treated PC patients, excluding those

who received radiation alone, 51 % (N = 1,999) received

chemotherapy alone and 32 % (N = 1,260) received che-

moradiotherapy (Table 4).

After adjusting for covariates, age, race, extent of dis-

ease, and nodal positivity all continued to predict

chemotherapy receipt. However, Black patients were 25 %

less likely to receive adjuvant chemotherapy (OR 0.75,

95 % CI 0.58–0.98). Sex was not a significant predictor of

receiving this treatment (Table 5).

Black patients were 30 % less likely to receive adjuvant

chemoradiation than Whites (OR 0.71. 95 % CI 0.53–

0.95). Furthermore, uninsured patients were half as likely

to receive adjuvant therapy. Again, sex did not predict this

treatment (Table 6).

Unresectable PC: Chemotherapy With or Without

Radiation, as Primary Treatment

Among persons with unresectable PC (N = 11,986),

42 % (N = 5,008) received chemotherapy and 10 %

(N = 1,140) received chemoradiotherapy. Whites received

primary chemotherapy and chemoradiation more fre-

quently than Blacks (42 vs 37 %, p = 0.001; 10 vs 6.0 %,

p \ 0.001). Only 32 % of uninsured patients received

primary chemotherapy compared with 50 % of non-

Medicare/Medicaid patients (p \ 0.001), and only 3.7 % of

2080 A. Abraham et al.

Page 4: Disparities in Pancreas Cancer Care

uninsured patients received primary chemoradiotherapy

compared with 12 % of non-Medicare/Medicaid patients

(p \ 0.001). Table 7 summarizes demographic and tumor

features of the unresectable, non-surgically treated cohort

receiving chemotherapy and chemoradiation.

Black patients were 30 % less likely to receive primary

chemotherapy compared with White patients (OR 0.69,

95 % CI 0.60–0.80). Additionally, we found a significant

age–sex interaction (p = 0.005) in the model predicting

primary chemotherapy (unresectable, non-surgically treated

patients). Stratification by age demonstrated that the oldest

males (age C80 years) were 1.5 times as likely (95 % CI

1.2–1.9) as females to receive primary chemotherapy. In

70–74-year-olds, males were 1.3 times as likely (95 % CI

1.1–1.6) and in 74–79-year-olds, males were also 1.3 times

as likely (95 % CI 1.0–1.5) to receive primary chemother-

apy. For those aged less than 65 years and 65–69 years, this

association was not significant. Table 8 summarizes the

adjusted odds of primary chemotherapy receipt.

Black patients were 50 % less likely to receive primary

chemoradiation, and uninsured patients were 70 % less

likely to receive primary chemoradiation than Medicaid

recipients (OR 0.31, 95 % CI 0.17–0.58). Increasing age

was associated with decreasing odds of both adjuvant and

primary chemoradiation. Sex did not predict primary che-

moradiation (Table 9).

TABLE 1 Demographic and

tumor features by resectability

and receipt of surgery

a Among those classified as

resectableb We classified insurance as

Medicare, Medicaid, non-

Medicare/Medicaid (including

HMO, PPO, other managed

care, Veterans Affairs,

TRICARE, Military, Indian/

Public Health Service, and

county insurance), unknown,

and no insurance

N (%), total cohort (N = 20,312)

Variable Resectable

disease, 7,585 (37)

p value Receipt of

surgery,a3,153 (42)

p value

Age (years) \0.001 \0.001

18–65 2,352 (31) 1,433 (45)

65–69 1,036 (14) 545 (17)

70–74 1,221 (16) 556 (18)

75–79 1,214 (16) 392 (12)

80–95 1,762 (23) 227 (7.0)

Sex \0.001 0.001

Female 4,079 (54) 1,624 (52)

Male 3,506 (46) 1,529 (48)

Race 0.412 0.008

Black 602 (7.9) 215 (6.8)

White 6,239 (82) 2,633 (84)

Other 744 (9.8) 305 (9.7)

Insurance status \0.001 \0.001

Non-Medicare/Medicaidb 3,345 (44) 1,603 (51)

Medicare 3,024 (40) 1,044 (33)

Medicaid 427 (5.6) 185 (5.9)

None 146 (1.9) 58 (1.8)

Unknown 643 (8.5) 263 (8.3)

Extent of disease \0.001 \0.001

Peripancreatic 6,646 (88) 2,946 (93)

Beyond the pancreas 939 (12) 207 (7.0)

Metastatic 0 (0) 0 (0)

Tumor size \0.001 \0.001

\2 cm 483 (6.0) 352 (11)

C2 cm 5,395 (71) 2,601 (82)

Unknown 1,707 (23) 200 (6.3)

Grade \0.001 \0.001

Low 2,739 (36) 1,864 (59)

High 1,679 (22) 1,036 (33)

Unknown 3,167 (42) 253 (8.0)

Pancreas Cancer Care 2081

Page 5: Disparities in Pancreas Cancer Care

Sensitivity Analyses

We carried out several additional analyses to test whe-

ther our findings resulted from modeling decisions. On

multivariate analysis reported above, we found that age,

sex, and insurance status predicted higher nonadherence to

resection when indicated. Next, as surgery, chemotherapy,

and radiation may not be offered in the context of short life

expectancy or poor postoperative course, we repeated our

analyses excluding those who died within 2 months of

diagnosis. These estimates remained comparable (data not

shown). Finally, we repeated our analyses after adding

‘‘prior cancer’’ as a covariate. Prior cancer was a strong

predictor of presenting with resectable disease (OR 3.3,

95 % CI 2.6–4.2) and of receipt of surgery (OR 2.4, 95 %

CI 1.7–3.4); however, this variable did not alter adjuvant

chemotherapy or chemoradiation therapy receipt after

pancreatectomy or in those with nonresectable PC.

DISCUSSION

In this population-based analysis we have shown that

sociodemographic factors impact pancreatic cancer care

from presentation to therapy. While Black race did not

predict resectable disease, it consistently predicted

decreased rates of pancreatic resection when indicated,

adjuvant chemoradiation, and primary chemoradiation

receipt in unresectable disease. Non-Medicare/Medicaid

insurance predicted resectability, and receipt of surgery and

primary chemoradiation. To our knowledge, the present

study is the first to evaluate disparities in the continuum of

PC care for both those receiving and not receiving surgery.

In agreement with prior studies, our results confirm that

extent of disease at presentation does not vary by patient

race. This has been previously reported using the Alabama

Cancer Registry and Surveillance, Epidemiology, and End

Results (SEER) data, among others.7,11–13 Whether resec-

tion rates vary by race, however, appears debatable. In

work by Shaver et al., race did not predict cancer-directed

surgery;12 however, other studies have reported that Black

race is associated with lower relative odds of resection.7,13

Previous work with SEER and SEER-Medicare demon-

strated that Black patients were 0.64 times as likely (95 %

CI 0.49–0.84) to receive surgery compared with Whites.7

We have validated these inequalities in resection among

Black patients within the context of comparable stage at

presentation.

With respect to chemotherapy and radiation, much of

the existing literature does not distinguish between adju-

vant therapy versus primary therapy for nonresectable (i.e.,

locally advanced or metastatic) PC. Nevertheless, prior

literature would suggest that, overall, Black patients

receive chemotherapy for pancreatic cancer less often than

Whites; For example, Shaver’s group reports an adjusted

odds ratio of 0.61 (95 % CI 0.37–0.95) for chemotherapy

receipt among Black patients compared with White

patients, though no distinction is made as to whether this

therapy was after pancreatic resection or for those with

TABLE 2 Predictors of resectability at diagnosis

Odds ratio 95 % CI p-Value

Race

Black versus white 1.0 0.91–1.1 0.859

Other versus white 0.97 0.88–1.1

Sex

Male versus female 0.91 0.85–0.96 0.001

Insurance status

Medicaid Referent

Non-Medicare/Medicaid 1.1 1.0–1.3 0.045

Medicare 1.1 0.96–1.3 0.017

None 0.89 0.71–1.1 0.334

Unknown 1.1 0.96–1.3 0.155

Age group (years)

\65 Referent

65–69 1.2 1.0–1.3 0.005

70–74 1.2 1.1–1.3 0.001

75–79 1.4 1.2–1.5 \0.001

80–95 1.7 1.5–1.8 \0.001

After adjusting for patient and tumor factors

TABLE 3 Predictors of surgery, in resectable cases

Odds ratio 95 % CI p value

Race

Black versus white 0.66 0.54–0.80 \0.001

Other versus white 0.93 0.78–1.1 0.441

Sex

Male versus female 0.95 0.85–1.1 0.375

Insurance status

Medicaid Referent

Non-Medicare/Medicaid 1.7 1.4–2.2 \0.001

Medicare 1.8 1.4–2.4 \0.001

None 0.83 0.54–1.3 0.386

Unknown 1.8 1.4–2.5 \0.001

Age group (years)

\65 Referent

65–69 0.66 0.55–0.78 \0.001

70–74 0.46 0.39–0.55 \0.001

75–79 0.26 0.22–0.31 \0.001

80–95 0.071 0.059–0.087 \0.001

After adjusting for patient and tumor factors

2082 A. Abraham et al.

Page 6: Disparities in Pancreas Cancer Care

locally advanced/metastatic PC.12 Eloubeidi’s group offers

an unadjusted analysis indicating that 27 % of Black

patients compared with 32 % of White patients (p = 0.02)

received chemotherapy across all stages. Further, they

report that this difference persisted in distant disease when

the cohort was stratified by stage.11 In our analysis, how-

ever, we go beyond previous studies and identify that, in

both the adjuvant and primary setting, after adjusting for

covariates, Black race predicts lower chemotherapy receipt

compared with White race.

While the indications for palliative therapy may be

variable, to our knowledge, the present study is also the

first to evaluate disparities in chemoradiation considered as

either combined-modality adjuvant therapy or primary

treatment for those with unresectable PC. Prior research

has suggested that there are no differences in radiation

receipt by race in adjusted and unadjusted analyses.11,12 On

the other hand, recent analysis of the Florida Cancer

Registry suggests that patients from less affluent areas with

higher proportions of Black population were less likely to

receive radiation therapy (14 vs 17 %, p = 0.003).9

However, specific poverty and race interactions and mul-

tivariate modeling of radiation receipt were not reported.

We observed that Black patients and those without insur-

ance coverage receive chemoradiation, as adjuvant therapy

or as primary therapy, less frequently; however, we found

no interaction of insurance with race in our regression

models.

Though surrogates for SES have been studied, there is a

general paucity of literature on the associations of

TABLE 4 Demographic and

tumor features by chemotherapy

and chemoradiation receipt in

surgically treated patients

N (%)

Variable Chemotherapy

receipt,

1,999 (51)

p value Chemoradiation

receipt,

1,260 (32)

p value

Age (years) \0.001 \0.001

\65 1,097 (55) 714 (57)

65–69 359 (18) 228 (18)

70–74 311 (16) 188 (15)

75–79 168 (8.0) 99 (8.0)

80–95 64 (3.0) 31 (3.0)

Sex 0.066 0.212

Female 995 (50) 627 (50)

Male 1,004 (50) 633 (50)

Race 0.383 \0.178

Black 123 (6.2) 73 (6.0)

White 1,683 (84) 1,071 (85)

Other 193 (9.8) 116 (9.0)

Insurance status \0.001 \0.001

Non-Medicare/Medicaid 1,104 (55) 703 (56)

Medicare 598 (30) 342 (27)

Medicaid 128 (6.0) 88 (7.0)

None 34 (2.0) 20 (2.0)

Unknown 135 (7.0) 107 (9.0)

Extent of disease \0.001 \0.001

Peripancreatic 1,460 (73) 980 (78)

Beyond the pancreas 405 (20) 248 (20)

Metastatic 134 (7.0) 32 (3.0)

Tumor size 0.003 \0.093

\2 cm 180 (9.0) 120 (10)

C2 cm 1,689 (84) 1,060 (84)

Unknown 130 (6.0) 80 (6.0)

Grade 0.010 \0.001

Low 1,162 (58) 771 (61)

High 679 (34) 415 (33)

Unknown 158 (8.0) 74 (6.0)

Pancreas Cancer Care 2083

Page 7: Disparities in Pancreas Cancer Care

insurance status with pancreatic cancer care. One recent

study reported that uninsured patients were 0.07 times less

likely (95 % CI 0.01–0.49) to receive surgery compared

with insured patients.12 However, only 23 patients in that

study were uninsured, reducing the analytic power of these

results. In comparison, the present study offers 486 unin-

sured patients and identifies differences in adjusted

resectability rates, rates of pancreatic resections, and

adjuvant and primary chemoradiation receipt by insurance

status.

We report several limitations to this study inherent in

the database. CCR does not collect information on

comorbidities and performance status, both of which are

variables used in determining oncologic treatment and have

been reported to vary by sociodemographic factors.7,14

Confounding by comorbidity would likely result in over-

estimation of odds ratios reported in this study. Second,

California counties span the extremes of dense urban cities

to rural farmlands. It is possible that, in one or the other,

disparities are more pronounced. Third, prior researchers

have reported demographic differences in patient referral to

high-volume centers for pancreatic resection.15–18 This

element of confounding could also affect our results such

that, potentially, the lower odds of therapy receipt in Black

patients could be accounted for by biased referral to low-

volume centers. Fourth, our conservative definition of

resectable disease may have under- or overestimated those

with resectable cancers. Finally, the diverse population in

the State of California and statewide treatment trends may

not necessarily reflect trends in other regions of the USA.

The current study provides valuable contributions to the

disparities literature in pancreatic cancer care. First, much

of the prior literature has focused on patients with surgi-

cally resectable disease, who represent less than 30 % of

pancreatic cancer patients. Identifying disparities in the

remaining majority is crucial to equitable delivery of care.

Furthermore, the distinction between adjuvant chemoradi-

ation and primary chemoradiation is an important one, as

the populations to which these therapies are prescribed are

fundamentally different. As we reported, disparities exist-

ing in one of these populations do not necessarily exist in

the other. Finally, our relatively recent cohort, spanning

through 2008, reiterates that disparities continue to exist in

the continuum of pancreas cancer care.

The presumption of our work is that treatment dispari-

ties translate to survival disparities, or conversely that the

latter can be explained by the former. Many prior studies

have suggested that race-based survival differences are at

least partly explained by variations in treatment and

SES.13,19–21 The implication, then, is that reducing treat-

ment disparities will reduce survival disparities. In fact, a

lack of association between sociodemographics and cancer

survival under universal access systems perhaps begs this

argument.22,23 Perhaps not coincidentally, these popula-

tions of racial/ethnic minorities and socioeconomically

disadvantaged continue to be underenrolled in clinical tri-

als, calling into question the applicability of trial results to

these populations. Our results highlight specific popula-

tions (Black patients, females, underinsured) in which we

TABLE 5 Predictors of chemotherapy in surgically treated patients

Odds ratio 95 % CI p value

Race

Black versus white 0.75 0.58–0.98 \0.037

Other versus white 0.91 0.73–1.1 0.409

Sex

Male versus female 1.0 0.91–1.2 0.375

Insurance status

Medicaid Referent

Non-Medicare/Medicaid 1.0 0.77–1.4 0.854

Medicare 1.2 0.87–1.7 0.258

None 0.58 0.34–0.99 0.046

Unknown 0.75 0.52–1.1 0.116

Age group (years)

\65 Referent

65–69 0.67 0.55–0.82 \0.0001

70–74 0.48 0.39–0.58 \0.0001

75–79 0.29 0.23–0.37 \0.0001

80–95 0.16 0.12–0.23 \0.0001

After adjusting for patient, tumor, and treatment factors

TABLE 6 Predictors of chemoradiotherapy in surgically treated

patients

Odds ratio 95 % CI p value

Race

Black versus white 0.71 0.53–0.95 0.023

Other versus white 0.87 0.69–1.1 0.262

Sex

Male versus female 1.0 0.88–1.2 0.898

Age group (years)

\65 Referent

65–69 0.76 0.62–0.94 0.010

70–74 0.55 0.45–0.69 \0.001

75–79 0.37 0.28–0.48 \0.001

80–95 0.18 0.12–0.28 \0.001

Insurance status

Medicaid Referent

Non-Medicare/Medicaid 0.91 0.68–1.2 0.524

Medicare 0.93 0.67–1.3 0.647

None 0.54 0.30–0.98 0.044

Unknown 0.96 0.66–1.4 0.821

After adjusting for patient, tumor, and treatment factors

2084 A. Abraham et al.

Page 8: Disparities in Pancreas Cancer Care

must ensure not only availability and accessibility of

standard treatments but also the opportunities to participate

in clinical trials.

In conclusion, in this large population-based study, we

found that patient race, insurance status, and sex influence

pancreatic cancer care. Our findings provide insight into

previously observed treatment disparities, call for future

studies to identify barriers to treatment in at-risk popula-

tions, and support the need for specific efforts geared

toward ensuring the equitable delivery of recommended

care.

ACKNOWLEDGMENT This study was supported by Enhancing

Minority Participation in Clinical Trials (Empact), National Institute

on Minority Health and Health Disparities. Project Number:

5RC2MD004797-02. Recipient of the 2011 American Society of

Clinical Oncology Foundation Merit Award and 2011 Pancreas Club

meeting Poster of Note.

TABLE 7 Demographic and tumor features in inoperable, non-sur-

gically treated patients (N = 11,986)

N (%) (column percents do not add to 100)

Variable Chemotherapy

receipt, 5,008

(41.8)

p value Chemoradiation

receipt, 1,140

(9.5)

p value

Age (years) \0.001 \0.001

\65 2,508 (50) 613 (54)

65–69 811 (16) 171 (15)

70–74 791 (16) 163 (14)

75–79 552 (11) 121 (11)

80–95 346 (7.0) 72 (6.0)

Sex \0.001 0.101

Female 2,256 (45) 540 (47)

Male 2,752 (55) 600 (53)

Race \0.004 \0.001

Black 371 (8.0) 60 (5.0)

White 4,127 (82) 942 (83)

Other 510 (10) 138 (12)

Insurance status \0.001 \0.001

Non-Medicare/

Medicaid

2,727 (54) 637 (56)

Medicare 1,586 (32) 324 (28)

Medicaid 295 (6.0) 84 (7.0)

None 102 (2.0) 12 (1.0)

Unknown 298 (6.0) 83 (7.0)

Extent of disease \0.001 \0.001

Peripancreatic 0 (0) 0 (0)

Beyond the

pancreas

1,520 (30) 775 (68)

Metastatic 3,488 (70) 365 (32)

Tumor size \0.001 \0.001

\2 cm 105 (2.1) 18 (2.0)

C2 cm 3,577 (71) 871 (76)

Unknown 1,326 (26) 251 (22)

Grade \0.001 \0.001

Low 921 (18) 272 (24)

High 892 (18) 197 (17)

Unknown 3,195 (64) 671 (59)

TABLE 8 Predictors of chemotherapy for inoperable, non-surgically

treated patients

Odds ratio 95 % CI p value

Race

Black versus white 0.69 0.60–0.80 \0.001

Other versus white 0.92 0.86–1.1 0.777

Sex

Male versus female 1.1 1.0–1.2 0.001

Age group (years)

\65 Referent

65–69 0.60 0.53–0.68 \0.001

70–74 0.45 0.40–0.51 \0.001

75–79 0.32 0.28–0.36 \0.001

80–95 0.13 0.11–0.15 \0.001

Insurance status

Medicaid Referent Medicaid Referent

Non-Medicare/Medicaid 2.1 1.8–2.5 \0.001

Medicare 2.3 1.9–2.7 \0.001

None 0.70 0.53–0.93 0.014

Unknown 0.97 0.79–1.2 0.749

After adjusting for patient and tumor factors

TABLE 9 Predictors of chemoradiotherapy among inoperable, non-

surgically treated patients

Odds ratio 95 % CI p value

Race

Black versus white 0.53 0.41–0.70 \0.001

Other versus white 1.2 0.98–1.4 0.072

Sex

Male versus female 0.95 0.84–1.1 0.440

Age group (years)

\65 Referent

65–69 0.65 0.53–0.79 0.010

70–74 0.53 0.43–0.65 \0.001

75–79 0.44 0.35–0.55 \0.001

80–95 0.20 0.16–0.27 \0.001

Insurance status

Medicaid Referent

Non-Medicare/Medicaid 1.3 1.0–1.7 0.039

Medicare 1.3 0.97–1.7 0.079

None 0.31 0.17–0.58 0.002

Unknown 0.98 0.71–1.4 0.909

After adjusting for patient and tumor factors

Pancreas Cancer Care 2085

Page 9: Disparities in Pancreas Cancer Care

APPENDIX 1

Continuum of pancreas cancer care

APPENDIX 2

See Table 10.REFERENCES

1. Fast Stats: An interactive tool for access to SEER cancer statis-

tics. Surveillance Research Program, National Cancer Institute.

http://seer.cancer.gov/faststats. Accessed 20 Dec 2010.

2. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CACancer J Clin. 2010;60(5): 277–300.

3. Baxter NN, Whitson BA, Tuttle TM. Trends in the treatment and

outcome of pancreatic cancer in the United States. Ann SurgOncol. 2007;14(4): 1320–6.

4. DeLancey JOL, Thun MJ, Jemal A, Ward EM. Recent trends in

black-white disparities in cancer mortality. Cancer EpidemiolBiomark Prev. 2008;17(11): 2908–12.

5. Bilimoria KY, Bentrem DJ, Ko CY, Stewart AK, Winchester DP,

Talamonti MS. National failure to operate on early stage pan-

creatic cancer. Ann Surg. 2007;246(2): 173–80.

6. Cress RD, Yin DX, Clarke L, Bold R, Holly EA. Survival among

patients with adenocarcinoma of the pancreas: A population-based

study (United States). Cancer Causes Control. 2006;17(4): 403–09.

7. Riall T, Townsend CJ, Kuo Y, Freeman J, Goodwin J. Dissecting

racial disparities in the treatment of patients with locoregional

pancreatic cancer: a 2-step process. Cancer. 2010;116(4): 930–9.

8. Lucas F, Stukel T, Morris A, Siewers A, Birkmeyer J. Race and

surgical mortality in the United States. Ann Surg. 2006;243(2): 281–6.

9. Cheung M, Yang R, Byrne M, Solorzano C, Nakeeb A, Koniaris L. Are

patients of low socioeconomic status receiving suboptimal manage-

ment for pancreatic adenocarcinoma?. Cancer. 2010;116(3): 723–33.

10. Krzyzanowska M, Weeks J, Earle C. Treatment of locally

advanced pancreatic cancer in the real world: population-based

practices and effectiveness. J Clin Oncol. 2003;21(18): 3409–14.

11. Eloubeidi MA, Desmond RA, Wilcox CM, et al. Prognostic

factors for survival in pancreatic cancer: a population-based

study. Am J Surg. 2006;192(3): 322–29.

12. Shavers VL, Harlan LC, Jackson M, Robinson J. Racial/ethnic

patterns of care for pancreatic cancer. J Palliative Med. 2009;12(7):

623–30.

13. Murphy MM, Simons JP, Hill JS, et al. Pancreatic resection a key

component to reducing racial disparities in pancreatic adenocar-

cinoma. Cancer. 2009;115(17): 3979–90.

14. Arnold L, Patel A, Yan Y, et al. Are racial disparities in pan-

creatic cancer explained by smoking and overweight/obesity?.

Cancer Epidemiol Biomark Prev. 2009;18(9): 2397–405.

15. Chang D, Zhang Y, Mukherjee D, et al. Variations in referral

patterns to high-volume centers for pancreatic cancer. J Am CollSurg. 2009;209(6): 720–6.

16. Riall T, Eschbach K, Townsend CJ, Nealon W, Freeman J, Goodwin

J. Trends and disparities in regionalization of pancreatic resection. JGastrointest Surg. 2007;11(10): 1242–51; discussion 51-2.

TABLE 10 Demographic and tumor characteristics of total cohort

(N = 20,312)

Variable N (%)

Age (years)

18–65 7,218 (36)

65–69 2,887 (14)

70–74 3,306 (16)

75–79 3,006 (15)

80–95 3,895 (19)

Sex

Female 10,404 (51)

Male 9,908 (49)

Race

Black 1,650 (8.0)

White 16,613 (82)

Other 2,049 (10)

Insurance status

Non-Medicare/Medicaida 9,206 (45)

Medicare 7,645 (38)

Medicaid 1,267 (6.2)

None 486 (2.4)

Unknown 1,708 (8.4)

Extent of disease

Peripancreatic 6,646 (33)

Beyond the pancreas 4,336 (21)

Metastatic 9,330 (46)

Tumor size

\2 cm 756 (4.0)

C2 cm 13,989 (69)

Unknown 5,566 (27)

Grade

Low 4,930 (24)

High 4,079 (20)

Unknown 11,303 (56)

a We classified insurance as Medicare, Medicaid, non-Medicare/Medicaid

(including HMO, PPO, other managed care, Veterans Affairs, TRICARE,

Military, Indian/Public Health Service, and county insurance), unknown, and

no insurance

Disease Diagnosis

Stage-Specific First Course of Therapy

Surgical Therapies

Non-Surgical Therapies

Adjuvant Therapy

Survival Death

2086 A. Abraham et al.

Page 10: Disparities in Pancreas Cancer Care

17. Epstein A, Gray B, Schlesinger M. Racial and ethnic differences

in the use of high-volume hospitals and surgeons. Arch Surg.2010;145(2): 179–86.

18. Liu J, Zingmond D, McGory M, et al. Disparities in the utiliza-

tion of high-volume hospitals for complex surgery. JAMA.

2006;296(16): 1973–80.

19. Murphy M, Simons J, Ng S, et al. Racial differences in cancer spe-

cialist consultation, treatment, and outcomes for locoregional

pancreatic adenocarcinoma. Ann Surg Oncol. 2009;16(11): 2968–77.

20. Zell J, Rhee J, Ziogas A, Lipkin S, Anton-Culver H. Race,

socioeconomic status, treatment, and survival time among pan-

creatic cancer cases in California. Cancer Epidemiol Biomark.Prev 2007;16(3): 546–52.

21. Komenaka IK, Martinez ME, Pennington RE, et al. Race and

ethnicity and breast cancer outcomes in an underinsured popu-

lation. J Natl Cancer Inst. 2010;102(15): 1178–87.

22. Kuhn Y, Koscielny A, Glowka T, Hirner A, Kalff J, Standop J.

Postresection survival outcomes of pancreatic cancer according to

demographic factors and socio-economic status. Eur J SurgOncol. 2010;36(5): 496–500.

23. Mulligan CR, Meram AD, Proctor CD, Wu H, Zhu K, Marrogi

AJ. Unlimited access to care: effect on racial disparity and

prognostic factors in lung cancer. Cancer Epidemiol BiomarkPrev. 2006;15(1): 25–31.

Pancreas Cancer Care 2087