Outcomes of resected pancreatic cancer in patients age ≥70

Abstract

Objective:
To determine outcomes of patients ≥70 years with resected pancreatic cancer.

Methods:
A study was conducted to identify pancreatic cancer patients ≥70 years who underwent surgery for pancreatic carcinoma from 2000 to 2012. Patients were excluded if they had neoadjuvant therapy. The primary endpoint was overall survival (OS).

Results:
We identified 112 patients with a median follow-up of surviving patients of 36 months. The median patient age was 77 years. The median and 5 year OS was 20.5 months and 19%, respectively. Univariate analysis (UVA) showed a significant correlation for increased mortality with N1 (P=0.03) as well as post-op CA19-9 >90 (P<0.001), with a trend towards decreased mortality with adjuvant chemoradiation (P=0.08). Multivariate analysis (MVA) showed a statistically significant increased mortality associated with N1 (P=0.008), post-op CA19-9 >90 (P=0.002), while adjuvant chemoradiation (P=0.04) was associated with decreased mortality.

Conclusions:
These data show that in patients ≥70, nodal status, post-op CA19-9, and adjuvant chemoradiation, were associated with OS. The data suggests that outcomes of patients ≥70 years who undergo upfront surgical resection are not inferior to younger patients.

Full text

© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
Introduction
Pancreatic cancer remains the fourth leading cause of
cancer-associated deaths in the United States (1,2). Despite
advancements in multi-modality therapy pancreatic cancer
remains extraordinarily lethal with a 5-year overall survival
(OS) of approximately 5% (1,3). Furthermore in the United
States the incidence of pancreatic cancer has continued to
increase since the 1930s (4). There are greater than 43,000
cases diagnosed annually in the United States, with a large
proportion dying of their disease (5).
The current accepted standard of care for resectable
pancreatic cancer remains resection followed by adjuvant
therapy consisting of chemotherapy. The use of post-
operative radiotherapy (PORT) continues to be a topic of
controversy (6). Several studies have shown an increase in
OS compared to surgery alone (7-9), whereas others have
shown no benet (10-12).
In the United States the elderly population has continued
to grow with a 30% increase from 2000 to 2010 (13).
Additionally, the average life span has increased secondary
to advancements in public health, nutrition, early detection
of diseases, and continued medical progress. This increase
in average life expectancy as well as advancements in cancer
Original Article
Outcomes of resected pancreatic cancer in patients age ≥70
Thomas J. Hayman1, Tobin Strom2, Gregory M. Springett3, Lodovico Balducci4, Sarah E. Hoffe2,
Kenneth L. Meredith5, Pamela Hodul3, Mokenge Malafa3, Ravi Shridhar2
1University of South Florida Morsani College of Medicine, Tampa, FL, USA; 2Department of Radiation Oncology, 3Gastrointestinal Tumor
Program, 4Senior Adult Oncology Program, Moftt Cancer Center, Tampa, FL, USA; 5Gastrointestinal Oncology, Sarasota Memorial Hospital,
Sarasota, FL, USA
Contributions: (I) Conception and design: All authors; (II) Administrative support: None; (III) Provision of study materials or patients: None; (IV)
Collection and assembly of data: T Strom; (V) Data analysis and interpretation: T Strom; (VI) Manuscript writing: R Shridhar, TJ Hayman; (VII)
Final approval of manuscript: All authors.
Correspondence to: Ravi Shridhar, MD, PhD. Department of Radiation Oncology, Gastrointestinal Tumor Program, Moftt Cancer Center, 12902
Magnolia Dr, Tampa, FL 33612, USA. Email: ravi0421@yahoo.com.
Objective: To determine outcomes of patients ≥70 years with resected pancreatic cancer.
Methods: A study was conducted to identify pancreatic cancer patients ≥70 years who underwent surgery
for pancreatic carcinoma from 2000 to 2012. Patients were excluded if they had neoadjuvant therapy. The
primary endpoint was overall survival (OS).
Results: We identified 112 patients with a median follow-up of surviving patients of 36 months. The
median patient age was 77 years. The median and 5 year OS was 20.5 months and 19%, respectively.
Univariate analysis (UVA) showed a signicant correlation for increased mortality with N1 (P=0.03) as well
as post-op CA19-9 >90 (P<0.001), with a trend towards decreased mortality with adjuvant chemoradiation
(P=0.08). Multivariate analysis (MVA) showed a statistically signicant increased mortality associated with
N1 (P=0.008), post-op CA19-9 >90 (P=0.002), while adjuvant chemoradiation (P=0.04) was associated with
decreased mortality.
Conclusions: These data show that in patients ≥70, nodal status, post-op CA19-9, and adjuvant
chemoradiation, were associated with OS. The data suggests that outcomes of patients ≥70 years who
undergo upfront surgical resection are not inferior to younger patients.
Keywords: Pancreatic cancer; surgery; elderly; adjuvant therapy; chemoradiation
Submitted Feb 09, 2015. Accepted for publication Feb 28, 2015.
doi: 10.3978/j.issn.2078-6891.2015.038
View this article at: http://dx.doi.org/10.3978/j.issn.2078-6891.2015.038

499Journal of Gastrointestinal Oncology Vol 6, No 5 October 2015
© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
screening has led to a growing number of cancer diagnoses
in the elderly (14).
Pancreatic cancer tends to occur at an older age, with
relatively rare occurrence before the age of 45 and a sharp
increase in its incidence thereafter (4). Incidence of the
disease increases with advancing age, with an incidence of
29 per 100,000 in patients aged 60-64 and 91 per 100,000
in patients aged 80-84 years (15). In the United States the
median age for patients diagnosed with pancreatic cancer
is 72 (16). Increasing age is a well-known risk factor for
the development of pancreatic cancer (17,18). In fact,
approximately two-thirds of cases are diagnosed in patients
greater than 65 years old (4,15). As such, more elderly
patients are being diagnosed with pancreatic cancer and
being considered for multi-disciplinary treatment (19).
However, elderly cancer patients remain underrepresented
in many clinical studies, with age greater than 70 years as a
frequent exclusion criterion (20,21). As such the question
remains as to whether these data can be extrapolated to the
elderly population. The aim of this study was to determine
the outcomes of age ≥70 patients with resected pancreatic
cancer at our institution.
Materials and methods
Patients
An analysis of pancreatic cancer patients ≥70 years who
underwent upfront surgical resection for pancreatic
carcinoma from 2000 to 2012 was conducted to determine
outcomes. Patients were excluded if they had M1 disease,
lack of surgical resection, use of neoadjuvant therapy, or
age <70, and unusual histologies including lymphoma,
cystadenoma, intraductal palpillary mucinous neoplasm,
signet ring cell carcinoma, neuroendocrine tumors, islet cell
tumors such as gastrinoma, insulinoma, glucagonoma and
VIPoma.
Treatment
Surgery
Patients with pancreatic head tumors underwent
pancreaticoduodenectomy with or without a pylorus-sparing
procedure. A minority of patients with pancreatic body or
tail tumors underwent pancreaticoduodenectomy, complete
pancreatectomy, or partial pancreatectomy with or without
splenectomy, and/or vein resection/repair depending on
the size and location of the tumor with respect to regional
organs and vasculature.
Adjuvant therapy
Following surgery, patients received chemoradiation
with or without neoadjuvant or adjuvant chemotherapy,
chemotherapy alone, or no adjuvant therapy. Adjuvant
therapy was initiated within 4 months from the time of
surgery in all cases.
Patients treated with chemotherapy alone received single-
agent gemcitabine. Patients treated with chemotherapy
followed by radiation were treated in a similar fashion
to the radiation therapy oncology group (RTOG) 9,704
protocol with 1 month of gemcitabine followed by
concurrent chemoradiation with continuous infusion 5-FU
or gemcitabine, followed by adjuvant gemcitabine. Patients
treated with chemoradiation alone received concurrent
radiation with 5-FU or gemcitabine. The median radiation
dose was 50 Gy (range, 43.2-63 Gy) in 180 to 200 cGy daily
fractions for a median of 28 fractions (range, 24-35 fractions)
to the pancreatic tumor bed and regional lymphatics; a
minority of patients received a boost to the tumor bed
(median 0 Gy; range, 0-14.4 Gy).
Statistical analysis
The primary endpoint was OS, defined as the interval
from surgery to date of death. Statistical analysis was
performed using SPSS® version 21.0 (IBM®, Chicago, IL,
USA). Progression-free survival (PFS) was also analyzed
and dened as the interval from surgery to rst recurrence
or death. Continuous variables were compared using both
Wilcoxon rank sum test and the Kruskal Wallis test as
appropriate. Pearson’s Chi-square test was used to compare
categorical variables. Actuarial rates of OS were calculated
using the Kaplan-Meier method and the log-rank test. A
Cox multivariate model was performed for OS, including
all clinical, histopathologic, and treatment variables.
Continuous variables for inclusion in the multivariate model
were split at clinically meaningful cut-points; post-operative
CA19-9 level was split at <90 and ≥90. All statistical tests
were two-sided and an α (type I) error <0.05 was considered
statistically signicant.
Results
Patient characteristics are shown in Table 1. A total of
112 patients age ≥70 who underwent upfront pancreatic
resection were analyzed with a median follow-up of

500 Hayman et al. Pancreas cancer surgery age ≥70
© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
surviving patients of 36 months. The median patient age
was 77 years and the majority of patients presented with
advanced disease and received adjuvant treatment.
Postoperative complications are presented in Table 2.
The most common complications were pancreatic leak
(14.3%) and wound infection (12.5%). Postoperative 30, 60,
and 90 day mortality was 2.7%, 3.6%, and 4.5%.
Figure 1 shows the OS and PFS Kaplan Meier curves for
the patients included in this analysis. The median, 3 and
5 year OS was 20.5 months, 36%, and 19% respectively
(Figure 1A). The median, 3 and 5 year PFS was 14.6 months,
24%, and 17% respectively (Figure 1B).
Table 3 illustrates the univariate analysis (UVA) and
multivariate analysis (MVA) for OS. On UVA, increased
mortality was associated with N1 status [hazard ratio (HR)
1.64: 1.05-2.56; P=0.03], post-operative CA19-9 >90 (HR
2.78: 1.56-4.93; P<0.001). There was a trend towards
decreased mortality associated with adjuvant treatment
with chemoradiation (HR 0.64: 0.39-1.05; P=0.08). On
MVA, increased mortality was associated with N1 status
(HR 1.91: 1.19-3.07; P=0.008) and postop CA19-9 >90
(HR 2.68: 1.45-4.94; P=0.002), while decreased mortality
was significantly associated with adjuvant chemoradiation
(HR 0.5: 0.26-0.95; P=0.04). Interestingly, there was no
correlation associated with adjuvant chemotherapy alone.
Age, tumor stage, interval from diagnosis to surgery, margin
status, tumor site, and gender were not prognositic on UVA
or MVA.
Discussion
This is one of the first studies to document outcomes
and prognostic factors in patients ≥70 with pancreatic
cancer treated with upfront resection with or without
adjuvant therapy. Interestingly, adjuvant chemoradiation
was associated with decreased mortality on MVA, whereas
adjuvant chemotherapy was not prognostic. On both UVA
and MVA, patients with N1 disease and post-operative
Table 1 Patient characteristics
Variable Level Age ≥70 y; N (%)
Gender Male 59 (52.7)
Female 53 (47.3)
Site Head 87 (77.7)
Body 7 (6.3)
Tail 18 (16.1)
Days from diagnosis to
surgery
≤30 83 (74.1)
>30 29 (25.9)
Median path tumor size
(cm, range)
3.0 (0.5, 8.5)
Pathologic tumor stage T1/2 24 (21.4)
T3/4 88 (78.6)
Median nodes positive
(range)
1 (0, 25)
Median nodes removed
(range)
11 (0, 49)
Pathologic nodal stage N0 49 (43.8)
N1 63 (56.3)
Tumor grade Well 12 (10.7)
Moderate 75 (67.0)
Poor 18 (16.1)
Unknown 7 (6.3)
Surgical margins Negative 94 (83.9)
Positive 18 (16.1)
Post-op CA19-9 >90 No 64 (57.1)
Yes 19 (17.0)
Unknown 29 (25.9)
Adjuvant treatment None 34 (30.4)
Chemoradiation 53 (47.3)
Chemotherapy 25 (22.3)
Table 2 Post-operative complications
Post-op complications N (%)
Pancreatic leak 16 (14.3)
Gastrojejunostomy leak 1 (0.9)
Atrial fibrillation 6 (5.4)
Pulmonary embolus 2 (1.8)
Abscess 2 (1.8)
Wound infection 14 (12.5)
Wound dehiscence 1 (0.9)
Anastomotic bleed 4 (3.6)
Stricture 1 (0.9)
Enterocutaneous fistula 0 (0)
SMA clot with bowel necrosis 1 (0.9)
Peritonitis 3 (2.7)
30 day mortality 3 (2.7)
60 day mortality 4 (3.6)
90 day mortality 5 (4.5)
SMA, superior mesenteric artery.

501Journal of Gastrointestinal Oncology Vol 6, No 5 October 2015
© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
Overall survival (%)
Time (years)
0 1 2 3 4 5
100
80
60
40
20
0
100
80
60
40
20
0
0 1 2 3 4 5
Subjects
112
Subjects
108
Events
83
Events
84
Censored
29
Censored
24
Median OS (mo, 95% CI)
20.5 (17.6, 23.4)
Median OS (mo, 95% CI)
14.6 (12.0, 17.2)
Time (years)
Progression-free survival (%)
AB
Figure 1 Kaplan-Meier survival curve of (A) overall survival (OS); (B) progression-free survival (PFS).
Table 3 Univariate and multivariate analysis for overall survival
Variable Level Median OS (m) UV HR (95% CI) P value MV HR (95% CI) P value
Age* 1.02 (0.98, 1.07) 0.37 1.01 (0.96, 1.06) 0.76
Gender Male 20.5 Ref
Female 19.9 0.92 (0.60-1.41) 0.70 0.86 (0.55, 1.36) 0.53
Diagnosis to surgery (days) ≤30 19.8 Ref
>30 21.9 0.93 (0.57-1.51) 0.76 0.85 (0.48, 1.49) 0.57
Tumor site Head 20.8 Ref
Body 65.9 0.54 (0.20, 1.50) 0.24 1.03 (0.32, 3.35) 0.96
Tail 15.6 1.26 (0.70, 2.24) 0.44 1.62 (0.84, 3.13) 0.15
Tumor grade Well 28.9 Ref
Moderate 18.7 1.24 (0.63, 2.45) 0.53 1.13 (0.52, 2.47) 0.75
Poor 19.1 1.17 (0.51, 2.69) 0.71 1.04 (0.42, 2.62) 0.93
Unknown 48.2 0.66 (0.23, 1.94) 0.45 0.52 (0.14, 2.01) 0.35
Pathologic tumor stage T1/2 19.8 Ref
T3/4 20.8 1.19 (0.70-2.02) 0.53 1.27 (0.67, 2.41) 0.47
Pathologic nodal status N0 28.8 Ref
N1 18.2 1.64 (1.05-2.56) 0.03 1.91 (1.19, 3.07) 0.008
Surgical margins Negative 19.9 Ref
Positive 21.1 0.75 (0.40-1.42) 0.38 0.94 (0.46, 1.93) 0.87
Post-op CA19-9 ≤90 26.4 Ref
>90 10.1 2.78 (1.56-4.93) <0.001 2.68 (1.45, 4.94) 0.002
Unknown 20.5 1.31 (0.79-2.17) 0.29 1.13 (0.64, 1.98) 0.68
Adjuvant treatment None 15.6 Ref
Chemoradiation 21.1 0.64 (0.39-1.05) 0.08 0.50 (0.26, 0.95) 0.04
Chemotherapy 20.5 1.05 (0.58-1.90) 0.87 0.67 (0.33, 1.33) 0.25
*, continuous variable; OS, overall survival; m, months; HR, hazard ratio; CI, confidence interval; UV, univariate; MV, multivariate;
Ref, reference (HR 1.00).

502 Hayman et al. Pancreas cancer surgery age ≥70
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CA19-9 >90 were prognostic for increased mortality.
The elderly population continues to remain
underrepresented in clinical literature, representing only
25-30% of study participants (20). Secondary to this dearth
of data there has been recent interest in dening the roles
of different therapies in the elderly with pancreatic cancer.
A retrospective study by Sehgal et al. (n=16,694) reported
the rates of chemotherapy delivered and associated survival
in different age groups in all patients with pancreatic cancer
from the Cancer Information Resource files registry (4).
They found that elderly patients with pancreatic cancer
receive treatment less frequently than younger patients.
Additionally, median OS was significantly less in the
age >70 group (4.21 vs. 7.07 months and 7.89 months
for age >70, 51-70, and ≤50 years respectively), however
these patients were shown to have a comparable or
better survival benefit from chemotherapy. In their UVA,
age >70 was not prognostic for OS. This study also showed
an OS benefit in all patients treated with radiotherapy
(HR 0.47, P<0.001). Our results are in general agreement
with this study, suggesting that elderly patients with
pancreatic cancer do derive a benefit from treatment,
specically chemoradiotherapy (CRT).
There continues to be controversy regarding the role of
PORT in resected pancreatic cancer patients (6). Several
trials have shown benefit from the used of PORT in
pancreatic cancer. In Gastrointestinal Tumor Study Group
(GITSG) 9,173 (n=43) patients who had undergone curative
resection were randomized to observation or CRT with
40 Gy split course radiation and concurrent 5-uorouracil
(5-FU) chemotherapy (9). The median survival in the
CRT arm was significantly improved compared to the
observation arm (20 vs. 11 months, P=0.035). Additionally,
the 2-year survival rates were significantly improved with
CRT vs. the observation group (42% vs. 15%; P=0.035).
This initial study has led to adjuvant CRT being adopted
in the United States. The European Organisation for
Research and Treatment of Cancer (EORTC)-40,891
(n=218) phase III study sought to conrm these results and
as such randomized patients with resected pancreatic cancer
or periampullary cancer to observation or 5-FU based
CRT (12). The initial data showed no difference in median
survival between the two groups, (19 vs. 24.5 months;
P=0.208). However, further subgroup analysis of just
pancreatic tumor showed use of adjuvant CRT improved
2-year OS (23% vs. 37%; P=0.049) (22).
While these studies support the use of PORT in the
treatment of pancreatic cancer there are additional data
that do not support its use. The European Organisation for
Research and Treatment of Cancer (ESPAC)-1 trial (n=541)
compared observation, chemotherapy alone or CRT (11).
They reported that adjuvant CRT worsened the median
survival compared to those who did not receive CRT (16 vs.
18 months) as well as reported an inferior 2-year survival
(29% vs. 49%; P=0.05). However, this study has been
widely criticized for lack of quality assurance and the split-
course treatment techniques. The study allowed radiation
oncologists to choose their dose with a range of 40-60 Gy.
Moreover, only 53% of patients enrolled in the study were
included in the nal analysis. Lastly the physician was able
to choose how the patient was randomized and prescribe
chemotherapy or “background” CRT.
While the previously mentioned trials included elderly
patients, but did not specically analyze this population, there
have been two other trials that have specifically examined
the elderly population. Miyamoto et al. examined pancreatic
cancer patients age ≥75 (n=42) treated with CRT as adjuvant
or definitive therapy (23). Median OS for the patients that
received surgery followed by CRT was 20.6 months vs.
8.6 months for CRT as denitive therapy. Importantly, they
showed that in this elderly population outcomes after CRT
were similar to historic controls, although many patients
experienced substantial treatment-related toxicity. Another
study, Horowitz et al. from Johns Hopkins analyzed 655
patients from their prospectively collected database of
patients who underwent resection and 5-FU based CRT
(n=313) or no adjuvant treatment (n=342) (24). They
showed that the 2-year survival for elderly patients receiving
adjuvant CRT was significantly greater than those who
received surgery alone (49% vs. 31.6%; P=0.013); however,
the 5-year survival in both groups was similar (11.7% vs.
19.8% respectively; P=0.310). Upon MVA adjuvant CRT had
protective effect with respect to 2-year survival [relative risk
(RR) 0.59; P=0.44].
Our study differs from the aforementioned studies in
the fact that we examined patients who underwent upfront
surgical resection followed by no treatment, chemotherapy,
and CRT. The study by Horowitz et al. compared surgery
alone to CRT, and the Miyamoto et al. study compared only
CRT as an adjuvant therapy to CRT as denitive therapy.
While these differences do exist it appears that our data is
in general agreement that elderly patients with pancreatic
cancer benet from treatment, specically chemoradiation
in the adjuvant setting.
Our study does present several inherent limitations
based on the fact that this is a retrospective analysis, a time

503Journal of Gastrointestinal Oncology Vol 6, No 5 October 2015
© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
period spanning 12 years, including that fact that patient
selection may inuence survival. Overall, our study suggests
that elderly patients with resected pancreatic cancer
benefit from therapy and specifically that adjuvant CRT,
however, conclusion drawn from this analysis are hypothesis
generating and not denitive.
Conclusions
Our study begins to dene prognostic variables associated
with OS in elderly patients, a group that continues to be
underrepresented in clinical research. Our data shows an
increase in OS in patients that were treated with adjuvant
CRT but not chemotherapy alone.
Acknowledgements
None.
Footnote
Conicts of Interest: The authors have no conicts of interest
to declare.
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504 Hayman et al. Pancreas cancer surgery age ≥70
© Journal of Gastrointestinal Oncology. All rights reserved. J Gastrointest Oncol 2015;6(5):498-504www.thejgo.org
Cite this article as: Hayman TJ, Strom T, Springett GM,
Balducci L, Hoffe SE, Meredith KL, Hodul P, Malafa M,
Shridhar R. Outcomes of resected pancreatic cancer in patients
age ≥70. J Gastrointest Oncol 2015;6(5):498-504. doi: 10.3978/
j.issn.2078-6891.2015.038
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