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Diet quality and pancreatic cancer incidence in the multiethnic cohort

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Diet quality and pancreatic cancer incidence in the multiethnic cohort

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DIET QUIALITY AND PANCREATIC CANCER INCIDENCE IN THE MULTIETHNIC
COHORT

By

Heather Steel

A Thesis Presented to the
FACULTY OF THE USC KECK SCHOOL OF MEDICINE
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF SCIENCE
(APPLIED BIOSTATISTICS AND EPIDEMIOLOGY)
May 2022

Copyright 2022 Heather Steel
ii
Acknowledgments
This project would not have been possible without the dedication, patience and support of
my thesis committee: Dr. Setiawan, Dr. Wu and Dr. Stram. I would also like to pay special
regards to Dr. Park and Tiffany Lim for their tireless efforts and guidance. Finally, I would like
to thank all of my friends and family that have continued to encourage me throughout my
academic journey. It truly takes a village, and this would not have been possible without all of
you.

iii
Table of Contents
Acknowledgements………………………………………………………………….…………….ii
List of Tables……………………………………………………………………………………..iv
List of Figures…………………………………………………………………………………..…v
Abstract…………………………………………………………………………………………...vi
Chapter 1: Introduction and Background………………………………….….….….….…..……..1
Chapter 2: Materials and Methods……………………….….….….….….….….….….….…...….2
Study Population………………………………………………………………..…2
Diet Quality Indices……………………………………………………………….2
Case Identification………………………………………….…………………..…4
Statistical Analysis.………………………………………….………………….....4
Chapter 3: Results……………………….….….….….….….….….….….….….….……..………6
Chapter 4: Discussion……………………………………….….….…………..…………….…..15
References………………………………………….….….….….….….….….….….….….….…18

iv
Tables

Table 1: Baseline Characteristics of Participants from the Multiethnic Cohort (MEC)
by Quintile of the Dietary Approaches to Stopping Hypertension (DASH) Score…………....8-10

Table 2: Diet Quality Indices and Pancreatic Cancer Risk…..……..…………………......…11-12

Supplementary Table S1: Diet Quality Indices and Pancreatic Cancer Risk among
Racial and Ethnic Groups Studied in the MEC………………………………………....…....20-21

Supplementary Table S2: Diet Quality Indices and Pancreatic Cancer Risk by
Smoking Status……………………………….………………………………………………22-23

Supplementary Table S3: Diet Quality Indices and Pancreatic Cancer Risk by
Body Mass Index…………………………………………………………….……………….24-25

v
Figures
Figure 1: Diet Quality Indices and Pancreatic Cancer Risk by Smoking Status……………......13
Figure 2: Diet Quality Indices and Pancreatic Cancer Risk by Body Mass Index…………..….14

vi
Abstract
Background: Pancreatic cancer is one of the deadliest cancers, and its incidence has been
increasing steadily in the past decade. While some dietary components have been implicated as
risk factors for pancreatic cancer, epidemiological data on the role of overall diet quality in
pancreatic cancer etiology are limited, especially from population-based prospective studies.
This study examined the relationship between diet quality and pancreatic cancer incidence in the
Multiethnic Cohort Study (MEC).

Methods: Data were analyzed from 177,313 African American, Japanese American, Latino,
Native Hawaiian and White men and women aged 45-75 years who completed a quantitative
food frequency questionnaire at cohort entry. Diet quality was assessed by previously developed
and validated diet quality indices (DQIs): the Healthy Eating Index-2015 (HEI-2015), the
Alternative Healthy Eating Index-2010 (AHEI-2010), the alternate Mediterranean Diet (aMED)
score, the Dietary Approaches to Stop Hypertension (DASH) score, and the Dietary
Inflammatory Index (DII®). These five DQIs were investigated because of their potential to
capture differences in various nutritional patterns across different racial and ethnic groups.
Multivariate Cox proportional hazard models were used to calculate hazard ratios (HRs) and
95% confidence intervals (CIs) for the DQIs and pancreatic cancer incidence adjusted for age,
sex, race and ethnicity, education, history of diabetes, family history of pancreatic cancer,
vigorous physical activity, smoking status with pack years, total energy intake, body mass index
(BMI) and alcohol consumption. Stratified analyses by sex, race and ethnicity, smoking status
and BMI were conducted. Tests for heterogeneity were preformed to identify differences in
associations among the subgroup categories.

Results: During an average follow up of 19.3 years, 1,782 incident pancreatic cancer cases were
identified. Overall, we did not observe statistically significant associations between the DQIs and
pancreatic cancer risk. In subgroup analyses comparing the highest vs. lowest quintiles of the
scores, an inverse association was observed with the DASH score for ever smokers (HR = 0.75,
95% CI: 0.60-0.92) and individuals with BMI ≥25 kg/m
2
(HR = 0.77, 95% CI: 0.63-0.94), but
not for never smokers (HR = 1.04, 95% CI: 0.82-1.31, P for heterogeneity = 0.004) or those with
BMI <25 kg/m
2
(HR = 1.21, 95% CI: 0.94-1.56, P for heterogeneity = 0.097). There were no
differences in associations by sex or race and ethnicity (all Ps for heterogeneity ≥0.43).

Conclusion: In this large prospective study, we did not find evidence of pancreatic cancer risk
reduction with healthier diet as assessed by the 5 DQIs. Adherence to the DASH diet may confer
beneficial effects against pancreatic cancer among ever smokers or among overweight or obese
individuals; further investigations are needed to confirm these findings.
1
Introduction and Background
Pancreatic cancer is widely regarded as one of the most lethal cancers. The 5-year
survival rate of 10% is among the lowest; it is the third leading cause of cancer death in
individuals between the age of 40 and 79 and the fourth leading cause of death across all age
groups (1). The late onset of symptoms coupled with a lack of available screening tools have
resulted in very poor outcomes (2). The American Cancer Society estimates that there will be
62,210 new cases of pancreatic cancer in the United States in 2022 with 49,830 deaths (3). The
clinical, societal and economic burden of pancreatic cancer is 3.9% of all disability-adjusted life
years for cancers (4).
There is a clear need to identify reliable preventive measures in an attempt to reduce
disease burden. Specifically, individuals in high-risk categories may benefit from modifiable
measures that they can incorporate into their lifestyles to reduce risk. Modifiable risk factors for
pancreatic cancer including smoking, diabetes, increased body mass index (BMI) and physical
inactivity are well-established (5), but the association between diet and pancreatic cancer
remains unclear, as results from cohort studies have been particularly mixed (6-9).
In this study, we aimed to address this research gap across diverse populations by
examining the relationship between overall diet quality and pancreatic cancer incidence in the
Multiethnic Cohort Study (MEC). We also investigated if this relationship varied by sex, race
and ethnicity, smoking status or BMI since the impact of diet may be particularly important for
specific high-risk subgroups.

2
Materials and Methods
I. Study Population
The MEC is a population-based cohort study that was established to elucidate lifestyle
factors and incidence of cancer and other chronic diseases across various races and ethnicities
(10). The five races and ethnicities included in this study were African American, Japanese-
American, Latino, Native Hawaiian, and White. The cohort was assembled between 1993 and
1996 using a mailed questionnaire that was specifically designed to assess the participants’
lifestyle habits including a food frequency questionnaire (FFQ), consisting of over 180 food
items that accounted for greater than 85% of the major nutrients of interest. The FFQ showed
satisfactory correlations with three 24-hour recalls for all sex-ethnic groups in a calibration study
(11). The baseline questionnaire also collected information on key demographic and lifestyle
history and habits including personal and family medical history, anthropometry, cigarette
smoking, and physical activity.
Of the more than 215,000 MEC participants, this analysis included 177,313 participants
after the following exclusions: previous history of pancreatic cancer (n = 58), not in one of the
five main racial and ethnic groups (n = 12,295), and missing information on covariates: smoking
status or intensity (n = 7,835), BMI (n = 1,866), history of diabetes (n = 2), education (n = 861),
physical activity (n = 8,833) and invalid diet based on total caloric intake or individual dietary
components (n = 6,638).

II. Diet Quality Indices
Diet quality was assessed by previously developed and validated diet quality indices
(DQIs): the Healthy Eating Index-2015 (HEI-2015), the Alternative Healthy Eating Index-2010
3
(AHEI-2010), the alternate Mediterranean Diet (aMED) score, the Dietary Approaches to Stop
Hypertension (DASH) score and the Dietary Inflammatory Index (DII®). The HEI-2015 is based
on a 13-component system of food groups, food intake variability and nutrients (12). It has a
maximum score of 100 accumulated from a score of 0 to 5 on 6 of the components and a score of
0 to 10 on each of the 7 components; a higher score represents adherence to a healthier diet. The
AHEI-2010, a measure of dietary patterns consistently associated with lower risk of chronic
disease, is based on 11 components each scored from 0 (non-adherence) to 10 with a maximum
score of 110 (13). The aMED is an adaptation of the Mediterranean diet that was originally
developed by Trichopoulou et al. (14). It is scored based on nine components, each component
was assigned 1 point for intakes above the median and 0 point for intakes below the median,
resulting in an overall score between 0 and 9 (15). The DASH diet score is based on 8
components. For components where higher intake was desired, such as fruits, vegetables and
whole grains, quintiles with the lowest adherence were given 1 point while the highest received 5
points; since red or processed meats, added sugars and intake of sodium were meant to be
minimized by the use of this diet, these components were reverse coded resulting in an overall
score of 8 to 40 (16). The DII was developed based on an extensive literature review; it aimed to
measure the entire diet on a scale from maximally anti-inflammatory to maximally
proinflammatory based on individual nutrients and other dietary constituents as well as 6
inflammatory markers (17). Only 28 of the 45 food components of the DII were included in the
DII calculations for the MEC (18). In contrast with the other DQIs, a lower DII score denotes a
more anti-inflammatory diet while a higher score represents a more proinflammatory diet and is
indicative of poorer diet quality.

4
III. Case Identification
Incident cases of pancreatic cancer were identified by linkage of the MEC with statewide
Surveillance, Epidemiology and End Results (SEER) cancer registries in Hawaii and California.
Cases were defined based on the International Classification of Diseases for Oncology, 3rd
Edition [ICD-O-3] codes C25.0-C25.9. Deaths were identified based on state death certificate
files and the National Death Index. A total of 1,782 cases of pancreatic cancer were identified
among 177,313 eligible participants after an average of 19.3 years of follow-up through
December 31, 2017.

IV. Statistical Analyses
Hazard ratios (HRs) and 95% confidence intervals (CIs) were calculated using Cox
proportional hazards regression with age as the time metric to estimate an association between
the dietary indices and pancreatic cancer risk. Each DQI was assessed using quintiles based on
distributions across the entire cohort where the quintile representing the poorest diet was used as
a reference for the other four quintiles of each diet separately. For the HEI-2015, the AHEI-2010,
the aMED and the DASH, the poorest diet was represented by the lowest quintile whereas for the
DII, the poorest diet was the highest quintile. Multivariate analyses were adjusted for the
following covariates: age at cohort entry, history of diabetes (yes or no), family history of
pancreatic cancer (yes or no), total energy intake (log-transformed kcal/day), BMI (< 25, 25 to
29.9 and ≥ 30 kg/m
2
) and education (≤ 12 years of schooling, some college or vocational training
and college graduate and above). Sex (male or female), race and ethnicity (African American,
Japanese American, Latino, Native Hawaiian and White), vigorous physical activity (hours of
vigorous activity per day categorized as 0, below the median number of hours or above) and
5
pack-years of smoking for former and current smokers (never, past with < 20 pack-years, past
with ≥ 20 pack-years, current with < 20 pack-years and current with ≥ 20 pack-years) were used
as strata variables in evaluating baseline hazard functions. Models for the HEI-2015 and the
DASH were further adjusted for alcohol use (<14, 14 to 28 and ≥ 28 g/day) as alcohol was not
included in these two indices. Proportional hazard assumptions were tested using Schoenfeld
residuals (19); covariates that violated the assumptions were included as strata. Heterogeneity
was tested using the Wald statistics for cross-product terms.
Stratified analysis was performed for sex, race and ethnicity, smoking status and BMI
category. For the analysis by smoking status, current and past smokers were grouped together as
ever smokers and compared to never smokers. Only smoking intensity was adjusted for in this
model since smoking status was accounted for during grouping. Similarly, for analysis involving
BMI, participants were divided into two groups based on their BMI (> 25 or ≤ 25 kg/m
2
), and
BMI was not further adjusted for in this model. All analyses were performed with SAS Studio
3.8 on SAS 9.4 (SAS Institute, Inc., Cary, NC, USA). All P-values were two-sided.

6
Results
Of the 177,313 participants 81,408 (46%) were men and 95,905 (54%) were women. The
largest racial or ethnic group was Japanese Americans (n = 51,682), followed by Whites (n =
44,791), Latinos (n = 39,208), African Americans (n = 28,670) and the smallest group was
Native Hawaiians (n = 12,962). Compared with men and women in the lowest quintile of DASH
score, both men and women in the highest quintile tended to be Whites followed by Japanese
Americans and Latinos. Participants with the highest DASH scores also tended to be older, more
educated and less obese; men in this quintile were more likely to be former smokers with less
than 20 pack years followed by never smokers, while women were primarily never smokers. All
key baseline characteristics are shown in Table 1.
There was no association between healthier diets, as defined by the five DQIs, and
pancreatic cancer risk after controlling for covariates (Table 2). Results were similar in men and
women; tests for heterogeneity showed no sex differences in association (all Ps for heterogeneity
≥ 0.50, Table 2). No significant associations were found among the DQIs and pancreatic cancer
incidence in racial and ethnic-specific analysis (Supplementary Table S1). Tests for
heterogeneity were not statistically significant across the five racial and ethnic groups (all Ps for
heterogeneity ≥ 0.43)
In the subgroup analysis by smoking status, risk of pancreatic cancer tended to be lower
among ever smokers who adhered to the DASH diet. Ever smokers in the highest quintile of the
DASH diet compared to those in the lowest quintile had a 25% decrease in pancreatic cancer risk
(95% CI: 0.60-0.92, p for trend = 0.01) while no decrease in risk was found among never
smokers (P for heterogeneity = 0.004). For the other four dietary indices we investigated,
7
reduction of risk was not observed among either never or ever smokers, and testing for
heterogeneity did not show differences in associations (Figure 1, Supplementary Table S2).
Participants were divided by BMI as underweight or normal weight (< 25 kg/m
2
) and as
overweight or obese (≥ 25 kg/m
2
) for subgroup analysis. Among overweight or obese individuals
(BMIs ≥ 25 kg/m
2
), the highest quintile of the DASH diet was associated with a 22% reduction
in pancreatic cancer risk (95% CI: 0.63-0.94, p for trend = 0.049, Figure 2) compared to those in
the lowest quintile. No statistically significant associations were observed when testing for
heterogeneity (P for heterogeneity = 0.097, Supplementary Table S3).

8

9

10

11

12

13

14
15
Discussion
In this large prospective study, diet quality was not associated with pancreatic cancer risk
overall. This null association was similar in men and women and across racial and ethnic groups.
However, we found that the DASH diet was associated with reduced pancreatic cancer risk in
participants who were current or former smokers at cohort entry. Our results also suggest an
inverse association between the DASH diet and pancreatic cancer risk among overweight or
obese individuals although testing for heterogeneity was not statistically significant.
Past studies have shown mixed results when examining pancreatic cancer risk with
various dietary patterns, with most cohort studies showing no association as in the current study.
Our findings on DII are consistent with null results from two U.S. cohort studies which
examined energy-adjusted DII scores (E-DII™) as the dietary index of interest (6, 7). The PLCO
cohort study (6) with a small number of cases (n=328) as well as the much larger NIH-AARP
prospective cohort study (7) (n=2,824) found no association between the E-DII and risk of
pancreatic cancer. When comparing the highest versus lowest quintile of HEI-2005 in the NIH-
AARP study (9) (n=2,383), there was an inverse association with pancreatic cancer risk (HR:
0.85, 95% CI: 0.74-0.97). A slightly stronger association was seen among obese individuals
(BMIs ≥ 25 kg/m
2
, HR: 0.81, 95% CI: 0.69-0.96) than among those with a normal weight.
Results from the Singapore Chinese Health Study (8) based on 311 pancreatic cancers found that
the highest quartiles of the AHEI-2010, aMED and DASH diets were associated with decreased
pancreatic cancer risk overall (all p for trend < 0.05). In subgroup analysis, adherence to the
DASH diet showed a protective effect among ever smokers but not in never smokers (P for
heterogeneity = 0.02) but this was based on only 3 cases of pancreatic cancer among ever
smokers in the highest quartile of DASH. The authors suggested that pancreatic cancer risk
16
maybe mitigated by the protective effects of a high-quality diet more robustly in individuals with
a higher risk for pancreatic cancer such as smokers. In the Women’s Health Initiative (WHI)
study (20), adherence to a low-fat diet, similar to the DASH diet, was not associated with a
decreased risk for all women in the study (HR: 0.86, 95% CI: 0.67-1.11). However, risk
reduction was statistically significant (HR: 0.71, 95% CI: 0.53-0.96) among overweight (BMI
>25 kg/m
2
) postmenopausal women.
A 2017 systematic review of a priori dietary patterns as measured by the Mediterranean
diet, the HEI-2005 or DII showed that 8 case-control and cohort studies, including Arem et al
(9), consistently suggested an inverse association between diet quality and pancreatic cancer risk
(21). Adjusted risk ratios ranged from 0.27 and 0.98. However, a stronger association was
observed in case-control studies versus in cohort studies. Biases inherent to case-control studies
could help explain the discrepancy. Selection and information bias can lead to differential
misclassification biasing the results away from the null.
There are inherent limitations to using self-reported dietary questionnaires such as
reporting bias which can lead to measurement error (22). Other limitations include the potential
for residual confounding from unmeasured factors, such as smoking information, that could be
associated with pancreatic cancer risk. Additionally, dietary patterns could be associated with
other lifestyle factors and risks that were not properly adjusted for in the models. Due to the
rarity of pancreatic cancer, most previous studies had a modest number of cases. This study
benefited from a large number of cases (n = 1,782), a long follow up time, its prospective nature
and the availability of potentially confounding variables in analyses. To our knowledge, this
study is the first study to include a racially and ethnically diverse population and provided risk
association analyses with five different dietary indices.
17
In summary, these findings show limited evidence to believe that there is an association
between overall diet quality and pancreatic cancer risk in both men and women in the MEC.
There is some indication, however, that the DASH diet may potentially be protective among
current and former smokers or individuals classified as overweight or obese. Additional research
is needed to draw more definitive conclusions as previous literature is ambiguous when
examining the association between diet quality and pancreatic cancer risk.

18
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7. Zheng J, Wirth MD, Merchant AT, et al. Inflammatory Potential of Diet, Inflammation-
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21. Zheng, Jiali et al. “Dietary patterns and risk of pancreatic cancer: a systematic
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Abstract (if available)

Abstract Background: Pancreatic cancer is one of the deadliest cancers, and its incidence has been increasing steadily in the past decade. While some dietary components have been implicated as risk factors for pancreatic cancer, epidemiological data on the role of overall diet quality in pancreatic cancer etiology are limited, especially from population-based prospective studies. This study examined the relationship between diet quality and pancreatic cancer incidence in the Multiethnic Cohort Study (MEC).
Methods: Data were analyzed from 177,313 African American, Japanese American, Latino, Native Hawaiian and White men and women aged 45-75 years who completed a quantitative food frequency questionnaire at cohort entry. Diet quality was assessed by previously developed and validated diet quality indices (DQIs): the Healthy Eating Index-2015 (HEI-2015), the Alternative Healthy Eating Index-2010 (AHEI-2010), the alternate Mediterranean Diet (aMED) score, the Dietary Approaches to Stop Hypertension (DASH) score, and the Dietary Inflammatory Index (DII®). These five DQIs were investigated because of their potential to capture differences in various nutritional patterns across different racial and ethnic groups. Multivariate Cox proportional hazard models were used to calculate hazard ratios (HRs) and 95% confidence intervals (CIs) for the DQIs and pancreatic cancer incidence adjusted for age, sex, race and ethnicity, education, history of diabetes, family history of pancreatic cancer, vigorous physical activity, smoking status with pack years, total energy intake, body mass index (BMI) and alcohol consumption. Stratified analyses by sex, race and ethnicity, smoking status and BMI were conducted. Tests for heterogeneity were preformed to identify differences in associations among the subgroup categories.
Results: During an average follow up of 19.3 years, 1,782 incident pancreatic cancer cases were identified. Overall, we did not observe statistically significant associations between the DQIs and pancreatic cancer risk. In subgroup analyses comparing the highest vs. lowest quintiles of the scores, an inverse association was observed with the DASH score for ever smokers (HR = 0.75, 95% CI: 0.60-0.92) and individuals with BMI ≥25 kg/m2 (HR = 0.77, 95% CI: 0.63-0.94), but not for never smokers (HR = 1.04, 95% CI: 0.82-1.31, P for heterogeneity = 0.004) or those with BMI <25 kg/m2 (HR = 1.21, 95% CI: 0.94-1.56, P for heterogeneity = 0.097). There were no differences in associations by sex or race and ethnicity (all Ps for heterogeneity ≥0.43).
Conclusion: In this large prospective study, we did not find evidence of pancreatic cancer risk reduction with healthier diet as assessed by the 5 DQIs. Adherence to the DASH diet may confer beneficial effects against pancreatic cancer among ever smokers or among overweight or obese individuals; further investigations are needed to confirm these findings.

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Creator Steel, Heather (author)

Core Title Diet quality and pancreatic cancer incidence in the multiethnic cohort

School Keck School of Medicine

Degree Master of Science

Degree Program Applied Biostatistics and Epidemiology

Degree Conferral Date 2022-05

Publication Date 04/12/2024

Defense Date 04/12/2022

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag cohort,diet quality,multiethnic population,OAI-PMH Harvest,pancreatic cancer

Format application/pdf (imt)

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Setiawan, V. Wendy (committee chair), Stram, Daniel O. (committee member), Wu, Anna H. (committee member)

Creator Email hj02728@usc.edu,jheat@umich.edu

Permanent Link (DOI) https://doi.org/10.25549/usctheses-oUC110939609

Unique identifier UC110939609

Document Type Thesis

Format application/pdf (imt)

Rights Steel, Heather

Type texts

Source 20220413-usctheses-batch-923 (batch), University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the author, as the original true and official version of the work, but does not grant the reader permission to use the work if the desired use is covered by copyright. It is the author, as rights holder, who must provide use permission if such use is covered by copyright. The original signature page accompanying the original submission of the work to the USC Libraries is retained by the USC Libraries and a copy of it may be obtained by authorized requesters contacting the repository e-mail address given.

Repository Name University of Southern California Digital Library

Repository Location USC Digital Library, University of Southern California, University Park Campus MC 2810, 3434 South Grand Avenue, 2nd Floor, Los Angeles, California 90089-2810, USA

Repository Email cisadmin@lib.usc.edu