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Original Investigation |

Anthropometric Measures, Body Mass Index, and Pancreatic Cancer:  A Pooled Analysis From the Pancreatic Cancer Cohort Consortium (PanScan) FREE

Alan A. Arslan, MD; Kathy J. Helzlsouer, MD, MHS; Charles Kooperberg, PhD; Xiao-Ou Shu, MD, PhD; Emily Steplowski, BS; H. Bas Bueno-de-Mesquita, MD, PhD, MPH; Charles S. Fuchs, MD, MPH; Myron D. Gross, PhD; Eric J. Jacobs, PhD; Andrea Z. LaCroix, PhD; Gloria M. Petersen, PhD; Rachael Z. Stolzenberg-Solomon, PhD, MPH; Wei Zheng, MD, PhD; Demetrius Albanes, MD; Laufey Amundadottir, PhD; William R. Bamlet, MS; Aurelio Barricarte, MD, PhD; Sheila A. Bingham, PhD; Heiner Boeing, PhD, MSPH; Marie-Christine Boutron-Ruault, MD, PhD; Julie E. Buring, ScD; Stephen J. Chanock, MD; Sandra Clipp, MPH, MA; J. Michael Gaziano, MD, MPH; Edward L. Giovannucci, MD, ScD; Susan E. Hankinson, ScD; Patricia Hartge, ScD, MA; Robert N. Hoover, MD, ScD; David J. Hunter, ScD; Amy Hutchinson, MS; Kevin B. Jacobs, PhD; Peter Kraft, PhD; Shannon M. Lynch, MPH; Jonas Manjer, MD, PhD; JoAnn E. Manson, MD, DrPH; Anne McTiernan, MD, PhD; Robert R. McWilliams, MD; Julie B. Mendelsohn, JD, MPH; Dominique S. Michaud, ScD; Domenico Palli, MD; Thomas E. Rohan, MD, PhD; Nadia Slimani, MSc, PhD; Gilles Thomas, MD, PhD; Anne Tjønneland, PhD, DMSc; Geoffrey S. Tobias, BS; Dimitrios Trichopoulos, MD, PhD; Jarmo Virtamo, MD, PhD; Brian M. Wolpin, MD, MPH; Kai Yu, PhD; Anne Zeleniuch-Jacquotte, MD, MS; Alpa V. Patel, PhD
[+] Author Affiliations

Financial Disclosure: None reported.


Arch Intern Med. 2010;170(9):791-802. doi:10.1001/archinternmed.2010.63.
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Background  Obesity has been proposed as a risk factor for pancreatic cancer.

Methods  Pooled data were analyzed from the National Cancer Institute Pancreatic Cancer Cohort Consortium (PanScan) to study the association between prediagnostic anthropometric measures and risk of pancreatic cancer. PanScan applied a nested case-control study design and included 2170 cases and 2209 control subjects. Odds ratios (ORs) and 95% confidence intervals (CIs) were estimated using unconditional logistic regression for cohort-specific quartiles of body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]), weight, height, waist circumference, and waist to hip ratio as well as conventional BMI categories (underweight, <18.5; normal weight, 18.5-24.9; overweight, 25.0-29.9; obese, 30.0-34.9; and severely obese, ≥35.0). Models were adjusted for potential confounders.

Results  In all of the participants, a positive association between increasing BMI and risk of pancreatic cancer was observed (adjusted OR for the highest vs lowest BMI quartile, 1.33; 95% CI, 1.12-1.58; Ptrend < .001). In men, the adjusted OR for pancreatic cancer for the highest vs lowest quartile of BMI was 1.33 (95% CI, 1.04-1.69; Ptrend < .03), and in women it was 1.34 (95% CI, 1.05-1.70; Ptrend = .01). Increased waist to hip ratio was associated with increased risk of pancreatic cancer in women (adjusted OR for the highest vs lowest quartile, 1.87; 95% CI, 1.31-2.69; Ptrend = .003) but less so in men.

Conclusions  These findings provide strong support for a positive association between BMI and pancreatic cancer risk. In addition, centralized fat distribution may increase pancreatic cancer risk, especially in women.

Figures in this Article

Pancreatic adenocarcinoma is the fourth leading cause of cancer death in the United States1 and is responsible for about 227 000 deaths per year worldwide.2 Because of the lack of effective screening tests for pancreatic cancer, it is often diagnosed at an advanced stage, contributing to a 5-year survival rate that is less than 5%.3 The incidence of pancreatic cancer is higher in men than in women, and in the United States, it is higher in blacks than in whites.3 Smoking, diabetes mellitus, and a family history of pancreatic cancer are known risk factors,4,5 but these factors do not account for all the cases of pancreatic cancer.

Obesity and high body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) have been proposed as additional risk factors for pancreatic cancer. Prospective studies have yielded conflicting results concerning the association between BMI and risk of pancreatic cancer. Most prospective epidemiological studies615 have found that a high BMI and a lack of physical activity are associated with an increased risk of pancreatic cancer incidence or mortality, independent of a history of diabetes mellitus. However, several prospective studies have not confirmed a significant role of BMI in pancreatic cancer1623 or have found that effect of BMI varied according to smoking status24,25 or sex.2628

The objective of the present study was to examine the association between BMI, other anthropometric factors, and pancreatic cancer risk by pooling data from nested case-control studies included in the National Cancer Institute (NCI) Pancreatic Cancer Cohort Consortium (PanScan). With 2170 cases, this is one of the largest analyses to date of BMI and pancreatic cancer.

STUDY POPULATION

PanScan is an initiative that was funded jointly by the NCI's Division of Cancer Control and Population Sciences and the Division of Cancer Epidemiology and Genetics in 2006. PanScan includes investigators from 12 prospective epidemiological cohorts and 1 case-control study and was created to identify genetic markers of susceptibility through a genome-wide association scan and to investigate environmental, lifestyle, and genetic causes of pancreatic cancer.

Studies in the pooled analysis included the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study (ATBC)29; CLUE II30; Cancer Prevention Study II (CPS II)31; European Prospective Investigation Into Cancer and Nutrition (EPIC)32; the Health Professionals Follow-up Study33; the Mayo Clinic study34; the New York University Women's Health Study,35 the Nurses' Health Study36; the Physicians' Health Study37; the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial38; Shanghai Men's and Women's Health Studies (SMWHS)39,40; the Women's Health Initiative 41; and the Women's Health Study.42 A total of 2170 cases and 2209 controls were eligible for the present study (Table 1).

Table Graphic Jump LocationTable 1. Characteristics of the 13 Cohorts Included in the PanScan Pooled Analysis
CASE ASCERTAINMENT AND DATA COLLECTION

Cases included all incident primary pancreatic adenocarcinoma (International Classification of Diseases for Oncology, Third Edition, codes C25.0-C25.3 and C25.7-C25.9). Endocrine pancreatic tumors (International Classification of Diseases for Oncology, Third Edition, code C25.4, histologic types 8150, 8151, 8153, 8155, 8240, and 8246) were excluded because the etiology of these cancers is thought to be different from that of exocrine tumors, which account for most pancreatic tumors. Case ascertainment varied among studies but included linking participants to cancer registries and national death indices and self-report and next-of-kin reports. Most cases were histologically confirmed (ATBC, CLUE II, EPIC, New York University Women's Health Study, SMWHS, and the Women's Health Initiative) or were confirmed through cancer registries (ATBC, CPS II, EPIC, and SMWHS), death certificates (CPS II and EPIC), or review of medical records by medical personnel (ATBC; CPS II; EPIC; Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial; and SMWHS).

Controls were incidence density sampled with a 1:1 control to case ratio and were alive and cancer free on the date of diagnosis of the matched case. At a minimum, controls were matched to cases on calendar year of birth (±5 years), sex, race, and ethnicity. Some cohorts used more stringent matching on age and, in addition, on other relevant factors (for comparisons of blood levels of analytes of interest), such as age at baseline or age at blood collection (±5 years), date and time of day of blood collection, fasting blood collection, and length of follow-up (Table 1).

Data on anthropometric measures, demographics, and possible confounders were collected through self-administered written questionnaires or in-person interviews. Detailed descriptions of data collection methods have been published previously by the individual studies.29,30,32,33,3544 From each study, baseline information on BMI, weight, height, waist circumference, waist to hip ratio (WHR), history of cigarette smoking, sex, age, race, family history of pancreatic cancer, alcohol consumption, pancreatitis, and history of diabetes mellitus was requested. Individual data sets were checked for consistency with previously published results. Forty cases and 46 controls had missing data on BMI, resulting in 2130 cases and 2163 controls available for the main analyses.

The Special Studies Institutional Review Board of the NCI approved the pooled PanScan. Each study also was approved by its local institutional review board.

STATISTICAL ANALYSIS

Odds ratios (ORs) and 95% confidence intervals (95% CIs) for pancreatic cancer risk were calculated using unconditional logistic regression, adjusting for cohort, age (categorical), sex, BMI source (self-reported vs measured), and smoking (never, former, or current) (model 1). Several multivariate models were assessed to control the effects of potential confounders. Model 2 was additionally adjusted for diabetes mellitus history (yes or no). In model 3, cases diagnosed in the first 2 years of follow-up were excluded to address the possibility of an effect of early undiagnosed disease. In model 4, current smokers (at baseline) were excluded, and in model 5, cases diagnosed in the first 2 years of follow-up and current smokers were excluded. Furthermore, models including waist circumference and WHR were additionally adjusted for height to remove extraneous variation due to body size. No adjustment was made for family history of pancreatic cancer because few cohorts had this information. Trend tests were conducted using cohort-specific quartiles of BMI, weight, height, waist circumference, and WHR as well as descriptive BMI categories (underweight, <18.5; normal weight, 18.5-24.9; overweight, 25.0-29.9; obese, 30.0-34.9; and severely obese, ≥35.0). To test for heterogeneity, BMI quartile categories were modeled as a continuous variable, and the risk estimates and standard errors from the cohort-specific models were used to generate the Q statistic.

The association between BMI and time of onset for pancreatic cancer was also examined using logistic regression modeling. Differences in time of onset were examined for normal vs overweight vs obese categories of BMI and in a combined category of overweight and obese. The analyses were conducted using a software program (SAS version 9.1.3; SAS Institute Inc, Cary, North Carolina).

The study included 2170 pancreatic cancer cases and 2209 controls aged 37 to 94 years (Table 1). Of the 2170 pancreatic cancer cases, 1059 were men and 1111 were women. Cases and controls were similar for age and racial distribution (Table 2). Most participants were white, and 86% of the study population was 60 years or older. Compared with controls, cases had a higher prevalence of current smoking (18% and 25%), diabetes mellitus (7% and 14%), history of pancreatitis (0.4% and 11%), and family history of pancreatic cancer (4% and 6%) based on data from cohorts with available information. The average age at pancreatic cancer onset in cases was 68.3 years, and the average lag time between cohort enrollment and diagnosis of pancreatic cancer in cases was 6.3 years.

Table Graphic Jump LocationTable 2. Participant Characteristics: the PanScan

Table 3 describes baseline anthropometric characteristics of cases and controls. Weight, height, and corresponding BMI were self-reported in approximately 50% of participants, measured in 29%, and measured and subsequently adjusted for difference in clothing in approximately 20%. Thirty-six percent of cases and 39% of controls had BMI in the normal range, 41% of cases and 39% of controls were overweight, and 21% of cases and 19% of controls were obese (Table 3). Cases had slightly higher mean weight compared with controls (76.8 and 75.5 kg) and a larger mean waist circumference (86.9 and 85.7 cm). Mean WHR and height were similar.

Table Graphic Jump LocationTable 3. Baseline Anthropometric Characteristics by Sex: the PanScana

Table 4 displays ORs and 95% CIs for pancreatic cancer according to baseline anthropometric factors for all individuals in the study. In all of the participants, a positive association between increasing BMI and risk of pancreatic cancer was observed (adjusted OR for the highest vs lowest BMI quartile, 1.33; 95% CI, 1.12-1.58; Ptrend < .001 in model 1). Statistically significant trends of increasing risk of pancreatic cancer with increasing BMI (both quartiles and clinical categories) were observed in all 5 models analyzed.

Table Graphic Jump LocationTable 4. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in All the Study Participants: the PanScan

The figures demonstrate the individual study results (model 1) and pooled risk estimates for overweight (Figure 1), obese (Figure 2), and severely obese individuals (Figure 3). Further adjustment for diabetes mellitus history (model 2) resulted in attenuation of risk estimates compared with model 1, but P values for trend were statistically significant for BMI quartiles and categories (Table 4). In addition, waist circumference and WHR were positively associated with risk of pancreatic cancer in all participants with top vs bottom quartile ORs of 1.23 (95% CI, 0.94-1.62) and 1.71 (95% CI, 1.27-2.30), respectively (Table 4). Stratification by BMI source (self-reported vs measured) resulted in similar risk estimates: ORs (95% CIs) for obese vs normal-weight BMI were 1.24 (0.92-1.68) for measured BMI and 1.21 (0.95-1.53) for self-reported BMI. The OR per BMI increase of 5 was 1.13 (95% CI, 1.11-1.14).

Place holder to copy figure label and caption
Figure 1.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for overweight people (BMI, 25 to <30) compared with normal-weight people (BMI, <25). ATBC indicates Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study; CI, confidence interval; CLUE II CPS II, Cancer Prevention Study II; EPIC, European Prospective Investigation Into Cancer and Nutrition; HPFS, Health Professionals Follow-up Study; MAYO, Mayo Clinic study; NHS, Nurses' Health Study; NYUWHS, New York University Women's Health Study; PHSI, Physicians' Health Study; PLCO, Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial; SMWHS, Shanghai Men's and Women's Health Studies; WHI, Women's Health Initiative; and WHS, Women's Health Study.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for obese people (30 to <35) compared with normal-weight people (<25). See the legend for Figure 1 for an explanation of the abbreviations.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for severely obese people (>35) compared with normal-weight people (<25). See the legend for Figure 1 for an explanation of the abbreviations.

Graphic Jump Location

The risk estimates did not change significantly in the sensitivity analysis excluding the Mayo Clinic case-control study (data not shown); therefore, we decided to include the Mayo participants in the final analyses. There was no evidence of significant heterogeneity between different cohorts for the BMI–pancreatic cancer results (Pheterogeneity = .36).

Table 5 and Table 6 provide ORs and 95% CIs for pancreatic cancer in men and women, respectively. In men, the adjusted risk estimate (model 1) for the top vs bottom quartile of BMI was 1.33 (95% CI, 1.04-1.69). Higher risk estimates were observed after the exclusion of current smokers (model 4). In men who never smoked, there was a significant trend of increasing risk with increasing BMI (Ptrend = .007) with the top vs bottom quartile (OR, 1.51; 95% CI, 1.13-2.03). Height, waist circumference, and WHR ratio were not significantly associated with pancreatic cancer in men (Table 5).

Table Graphic Jump LocationTable 5. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in Men: the PanScan
Table Graphic Jump LocationTable 6. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in Women: the PanScan

In women, statistically significant trends of increasing risk of pancreatic cancer with increasing BMI were observed overall (model 1) and after the exclusion of cases diagnosed in the first 2 years of follow-up (model 3) or current and former smokers (model 4) (Table 6). Compared with normal-weight BMI (model 1), the ORs for pancreatic cancer were 1.31 (95% CI = 1.07-1.60) for overweight women and 1.61 (95% CI, 1.12-2.33; Ptrend = .003) for severely obese women. Increasing waist circumference and WHR were significantly associated with pancreatic cancer risk in women. Compared with the reference group, women in the highest quartile of WHR had an OR of 1.87 (95% CI, 1.31-2.69) after adjustment for cohort, age, BMI source, and smoking status. Inclusion of BMI (categorical) and WHR (quartiles) in the same model suggested that the effect of increasing WHR is stronger (P = .006) compared with that of BMI categories (P = .44) after adjustment for cohort, age, sex, BMI source, smoking, and diabetes mellitus history.

We did not observe clinically meaningful differences in time of onset for pancreatic cancer between normal-weight and overweight/obese individuals. Overweight and obese individuals together were diagnosed approximately 4 months earlier than were normal-weight individuals (data not shown). When comparing obese individuals only with normal-weight individuals, obese participants were diagnosed on average approximately 1 year earlier than were normal-weight individuals, and the difference was significant (P = .03).

The results of this large pooled set of studies support the hypothesis that obesity is associated with an increased risk of pancreatic cancer. The present findings are consistent with most previous epidemiological studies that found a positive association between BMI and pancreatic cancer risk45 and support the conclusion from a recent review panel from the World Cancer Research Fund45 that the strength of the evidence supporting an association between obesity and pancreatic cancer is convincing.

Previous studies that did not observe a positive association between BMI and pancreatic cancer were often limited by the use of proxy respondents4649 or by inadequate statistical power to examine associations at BMI levels that correspond with obesity (<10 cases with BMI >30.0).7,10,17,50 Controversy regarding the role of smoking in the BMI and pancreatic cancer relationship still remains. Many previous studies7,47,48,50 that did not observe an association with obesity did not properly control for smoking history. It is possible that residual confounding due to improper adjustment for smoking history may have biased the association between BMI and pancreatic cancer toward the null. When stratifying on smoking status, some previous studies found that the relationship between BMI and pancreatic cancer was strongest in never smokers.24,25 The present findings are consistent with previous reports that the association between BMI and pancreatic cancer is stronger in nonsmokers (adjusted OR for BMI ≥30, 1.37; 95% CI, 1.06-1.78) than in smokers (adjusted OR for BMI ≥30, 1.14; 95% CI, 0.91-1.78).

Unlike a recent study51 in which the authors reported that individuals who were overweight or obese from age 20 to 49 years had earlier onset of pancreatic cancer compared with those with normal body weight, we did not find a substantial difference in age at diagnosis between normal-weight and the combined group of overweight and obese individuals.

In this study, BMI was assessed between ages 37 and 94 years, and overweight or obese individuals were diagnosed a mean of 4 months earlier than were normal-weight individuals. The study by Li et al,51 using a hospital-based case-control study design, found that overweight or obese patients aged 20 to 49 years had a median age at pancreatic cancer onset 2 to 6 years earlier than that of normal-weight patients. However, these differences were based on BMI as recalled from early adulthood and may have been subject to recall bias. Nevertheless, as suggested by Li et al,51 obesity at younger ages might have a more profound effect on risk and age at onset of pancreatic cancer than would obesity at older ages.

There are established biologic pathways to support a relationship between excess body weight and the development of pancreatic cancer. Body fatness has a direct linear relationship with insulin production and is related to the development of insulin resistance.52 Furthermore, insulin resistance and abnormal glucose metabolism, even in the absence of diabetes mellitus, is associated with pancreatic cancer risk.8,53,54 In vitro studies have also shown that insulin has growth-promoting effects in the pancreas.55A hyperinsulinemic state allows increased insulin to pass through the pancreas and trigger mitotic activity.8,53,56 In addition, excess insulin can also downregulate insulinlike growth factor I–binding proteins, which would result in more bioavailable insulinlike growth factor I, which has been associated with cell proliferation and pancreatic cancer risk.54,57

The results of this study also support a specific role of central adiposity in pancreatic cancer risk, especially in women. In addition to general body fatness, there is a direct linear relationship between intra-abdominal fat deposits, insulin production, and the development of insulin resistance.52

The present study has several strengths, including the very large sample size, the wide range of BMI, and the ability to control for most known or suspected pancreatic cancer risk factors. In addition, the study population was largely a nested sample from various prospective cohort studies so that BMI was measured before pancreatic cancer diagnosis, thus reducing differential reporting of past exposure information. Limitations include the use of some self-reported exposure information; however, adjusting for source of exposure information (self-reported or measured) did not alter the association. Another potential limitation is the wide range of lag periods between BMI measurement (collected at baseline for each cohort) and the date of diagnosis; however, sensitivity analyses examining this lag time by excluding the first 2 years of follow-up did not change the point estimates appreciably, thus arguing against an effect of prediagnostic disease-related changes in anthropometric measures (reverse causation). Participating cohorts had different coding systems for physical activity that were not readily comparable; therefore, we could not assess whether the association between BMI and pancreatic cancer varies by level of physical activity. To address potential residual confounding by smoking, we performed the analyses in never smokers and found a slightly stronger association between BMI and pancreatic risk. Last, only a few cohorts had data available on waist and hip circumference so that there was limited statistical power to examine these relationships.

In summary, the results of this study provide additional evidence that obesity is associated with increased risk of pancreatic cancer. In addition, the association between waist circumference and pancreatic cancer risk, especially in women, suggests a possible association with the distribution of body fat. These findings, along with those from previous studies, strongly support the role of obesity in pancreatic cancer development.

Correspondence: Alan A. Arslan, MD, Department of Obstetrics and Gynecology, New York University School of Medicine, 550 First Ave, TH-528, New York, NY 10016 (alan.arslan@nyumc.org).

Accepted for Publication: October 31, 2009.

Author Contributions: Dr Arslan had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analyses. Study concept and design: Kooperberg, Shu, Bueno-de-Mesquita, Fuchs, Stolzenberg-Solomon, Zheng, Amundadottir, Barricarte, Bingham, Chanock, Hartge, Hoover, K. B. Jacobs, Manson, McTiernan, Mendelsohn, Palli, Slimani, Tjønneland, and Tobias. Acquisition of data: Helzlsouer, Kooperberg, Shu, Bueno-de-Mesquita, Fuchs, E. J. Jacobs, LaCroix, Petersen, Stolzenberg-Solomon, Albanes, Bamlet, Barricarte, Boeing, Buring, Clipp, Gaziano, Giovannucci, Hankinson, Hartge, Hoover, Hunter, Hutchinson, K. B. Jacobs, Lynch, Manson, McWilliams, Michaud, Palli, Thomas, Tjønneland, Trichopoulos, Virtamo, Wolpin, and Zeleniuch-Jacquotte. Analysis and interpretation of data: Arslan, Helzlsouer, Kooperberg, Shu, Steplowski, Fuchs, Gross, E. J. Jacobs, Boutron-Ruault, Giovannucci, Hankinson, Hartge, K. B. Jacobs, Kraft, Manjer, Rohan, Trichopoulos, Yu, and Patel. Drafting of the manuscript: Arslan, Helzlsouer, Kooperberg, and Patel. Critical revision of the manuscript for important intellectual content: Arslan, Helzlsouer, Kooperberg, Shu, Steplowski, Bueno-de-Mesquita, Fuchs, Gross, E. J. Jacobs, LaCroix, Petersen, Stolzenberg-Solomon, Zheng, Albanes, Amundadottir, Bamlet, Barricarte, Bingham, Boeing, Boutron-Ruault, Buring, Chanock, Clipp, Gaziano, Giovannucci, Hankinson, Hartge, Hunter, Hutchinson, K. B. Jacobs, Kraft, Lynch, Manson, McTiernan, McWilliams, Mendelsohn, Michaud, Palli, Rohan, Slimani, Thomas, Tjønneland, Tobias, Trichopoulos, Virtamo, Wolpin, Yu, and Zeleniuch-Jacquotte. Statistical analysis: Kooperberg, Shu, E. J. Jacobs, Bamlet, Hunter, K. B. Jacobs, Manjer, and Yu. Obtained funding: Shu, Bueno-de-Mesquita, Fuchs, Petersen, Stolzenberg-Solomon, Albanes, Boeing, Gaziano, Giovannucci, Hoover, Kraft, Lynch, Palli, Tjønneland, Trichopoulos, and Zeleniuch-Jacquotte. Administrative, technical, and material support: Arslan, Kooperberg, Steplowski, Fuchs, Gross, Petersen, Zheng, Albanes, Amundadottir, Bingham, Boeing, Chanock, Clipp, Gaziano, Hartge, Hunter, K. B. Jacobs, Lynch, Manjer, Manson, Mendelsohn, Slimani, Thomas, Tobias, Trichopoulos, and Virtamo. Study supervision: Arslan, Helzlsouer, Kooperberg, Bueno-de-Mesquita, Hankinson, Hartge, and Hoover.

Funding/Support: This project was funded in whole or in part by contract HHSN261200800001E from the NCI, National Institutes of Health. The ATBC was supported by contracts N01-CN-45165, N01-RC-45035, and N01-RC-37004 from the Intramural Research Program of the NCI and the US Public Health Service. CLUE II was supported by grant 5U01AG018033 from the National Institute on Aging and by grants CA105069 and CA73790 from the NCI. The EPIC was supported by the European Commission: Public Health and Consumer Protection Directorate 1993-2004; Research Directorate-General 2005; Ligue contre le Cancer; Societé 3M; Mutuelle Générale de l’Education Nationale; Institut National de la Santé et de la Recherche Médicale (France); German Cancer Aid, German Cancer Research Center, Federal Ministry of Education and Research (Germany); Danish Cancer Society (Denmark); Health Research Fund of the Spanish Ministry of Health, participating regional governments and institutions (Spain); Cancer Research UK, Medical Research Council, Stroke Association, British Heart Foundation, Department of Health, Food Standards Agency, the Wellcome Trust (United Kingdom); Greek Ministry of Health and Social Solidarity, Hellenic Health Foundation and Stavros Niarchos Foundation (Greece); Italian Association for Research on Cancer (Italy); Dutch Ministry of Public Health, Welfare and Sports, Dutch Prevention Funds, LK Research Funds, Dutch ZON (Zorg Onderzoek Nederland) (the Netherlands); Swedish Cancer Society, Swedish Scientific Council, Regional Government of Skane and Västerbotten (Sweden); and World Cancer Research Fund. The New York University Women's Health Study is supported by research grants R01CA034588, R01CA098661, and P30CA016087 from the NCI and by grant ES000260 from the National Institute of Environmental Health Sciences. The Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial was supported by contracts from the NCI (University of Colorado: NO1-CN-25514; Georgetown University: NO1-CN-25522; Pacific Health Research Institute: NO1-CN-25515; Henry Ford Health System: NO1-CN-25512; University of Minnesota: NO1-CN-25513; Washington University: NO1-CN-25516; University of Pittsburgh: NO1-CN-25511; University of Utah: NO1-CN-25524; Marshfield Clinic Research Foundation: NO1-CN-25518; University of Alabama at Birmingham: NO1-CN-75022; Westat Inc: NO1-CN-25476; and University of California, Los Angeles: NO1-CN-25404). The SMWHS were supported by extramural research grants R01 CA82729 and R01 CA70867 from the NCI and by the Intramural Research Program of the NCI (Division of Cancer Epidemiology and Genetics). The Women's Health Initiative is funded by contracts N01WH22110, 24152, 32100-2, 32105-6, 32108-9, 32111-13, 32115, 32118-32119, 32122, 42107-26, 42129-32, and 44221 from the National Heart, Lung, and Blood Institute.

Role of the Sponsors: The funding agencies had no role in the conduct of the study, the interpretation of the data, or the decision to submit the manuscript for publication.

PanScan Writing Committee Members: Alan A. Arslan, MD; Kathy J. Helzlsouer, MD, MHS; Charles Kooperberg, PhD; Xiao-Ou Shu, MD, PhD; Emily Steplowski, BS; and Alpa V. Patel, PhD.

Steering Committee Members: Alan A. Arslan, MD; Kathy J. Helzlsouer, MD, MHS; H. Bas Bueno-de-Mesquita, MD, PhD, MPH; Charles S. Fuchs, MD, MPH; Myron D. Gross, PhD; Eric J. Jacobs, PhD; Andrea Z. LaCroix, PhD; Gloria M. Petersen, PhD; Rachael Z. Stolzenberg-Solomon, PhD, MPH; and Wei Zheng, MD, PhD.

Disclaimer: The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, and neither does the mention of trade names, commercial products, or organizations imply endorsement by the US government.

Additional Contributions: We thank the investigators from the PanScan centers and the study participants, without whom this study would not have been possible.

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Calle  EERodriguez  CWalker-Thurmond  KThun  MJ Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348 (17) 1625- 1638
PubMed Link to Article
Patel  AVRodriguez  CBernstein  LChao  AThun  MJCalle  EE Obesity, recreational physical activity, and risk of pancreatic cancer in a large U.S. cohort. Cancer Epidemiol Biomarkers Prev 2005;14 (2) 459- 466
PubMed Link to Article
Rapp  KSchroeder  JKlenk  J  et al.  Obesity and incidence of cancer: a large cohort study of over 145,000 adults in Austria. Br J Cancer 2005;93 (9) 1062- 1067
PubMed Link to Article
Larsson  SCPermert  JHåkansson  NNäslund  IBergkvist  LWolk  A Overall obesity, abdominal adiposity, diabetes and cigarette smoking in relation to the risk of pancreatic cancer in two Swedish population-based cohorts. Br J Cancer 2005;93 (11) 1310- 1315
PubMed Link to Article
Berrington de González  ASpencer  EABueno-de-Mesquita  HB  et al.  Anthropometry, physical activity, and the risk of pancreatic cancer in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev 2006;15 (5) 879- 885
PubMed Link to Article
Stolzenberg-Solomon  RZPietinen  PTaylor  PRVirtamo  JAlbanes  D A prospective study of medical conditions, anthropometry, physical activity, and pancreatic cancer in male smokers (Finland). Cancer Causes Control 2002;13 (5) 417- 426
PubMed Link to Article
Lee  IMSesso  HDOguma  YPaffenbarger  RS  Jr Physical activity, body weight, and pancreatic cancer mortality. Br J Cancer 2003;88 (5) 679- 683
PubMed Link to Article
Kuriyama  STsubono  YHozawa  A  et al.  Obesity and risk of cancer in Japan. Int J Cancer 2005;113 (1) 148- 157
PubMed Link to Article
Sinner  PJSchmitz  KHAnderson  KEFolsom  AR Lack of association of physical activity and obesity with incident pancreatic cancer in elderly women. Cancer Epidemiol Biomarkers Prev 2005;14 (6) 1571- 1573
PubMed Link to Article
Batty  GDShipley  MJJarrett  RJBreeze  EMarmot  MGSmith  GD Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study. Int J Obes (Lond) 2005;29 (10) 1267- 1274
PubMed Link to Article
Oh  SWYoon  YSShin  SA Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 2005;23 (21) 4742- 4754
PubMed Link to Article
Lukanova  ABjör  OKaaks  R  et al.  Body mass index and cancer: results from the Northern Sweden Health and Disease Cohort. Int J Cancer 2006;118 (2) 458- 466
PubMed Link to Article
Nöthlings  UKolonel  LN Risk factors for pancreatic cancer in the Hawai'i-Los Angeles Multiethnic Cohort Study. Hawaii Med J 2006;65 (1) 26- 28
PubMed
Samanic  CChow  WHGridley  GJarvholm  BFraumeni  JF  Jr Relation of body mass index to cancer risk in 362,552 Swedish men. Cancer Causes Control 2006;17 (7) 901- 909
PubMed Link to Article
Stolzenberg-Solomon  RZAdams  KLeitzmann  M  et al.  Adiposity, physical activity, and pancreatic cancer in the National Institutes of Health-AARP Diet and Health Cohort. Am J Epidemiol 2008;167 (5) 586- 597
PubMed Link to Article
Nöthlings  UWilkens  LRMurphy  SPHankin  JHHenderson  BEKolonel  LN Body mass index and physical activity as risk factors for pancreatic cancer: the Multiethnic Cohort Study. Cancer Causes Control 2007;18 (2) 165- 175
PubMed Link to Article
Lin  YKikuchi  STamakoshi  A  et al. JACC Study Group, Obesity, physical activity and the risk of pancreatic cancer in a large Japanese cohort. Int J Cancer 2007;120 (12) 2665- 2671
PubMed Link to Article
Luo  JIwasaki  MInoue  M  et al. JPHC Study Group, Body mass index, physical activity and the risk of pancreatic cancer in relation to smoking status and history of diabetes. Cancer Causes Control 2007;18 (6) 603- 612
PubMed Link to Article
ATBC Cancer Prevention Study Group, The Alpha-Tocopherol, Beta-Carotene Lung Cancer Prevention Study. Ann Epidemiol 1994;4 (1) 1- 10
PubMed Link to Article
Huang  HYAlberg  AJNorkus  EPHoffman  SCComstock  GWHelzlsouer  KJ Prospective study of antioxidant micronutrients in the blood and the risk of developing prostate cancer. Am J Epidemiol 2003;157 (4) 335- 344
PubMed Link to Article
Calle  EERodriguez  CJacobs  EJ  et al.  The American Cancer Society Cancer Prevention Study II Nutrition Cohort. Cancer 2002;94 (9) 2490- 2501
PubMed Link to Article
Riboli  EHunt  KJSlimani  N  et al.  European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr 2002;5 (6B) 1113- 1124
PubMed Link to Article
Rimm  EBGiovannucci  ELWillett  WC  et al.  Prospective study of alcohol consumption and risk of coronary disease in men. Lancet 1991;338 (8765) 464- 468
PubMed Link to Article
McWilliams  RRBamlet  WRde Andrade  MRider  DNCunningham  JMPetersen  GM Nucleotide excision repair pathway polymorphisms and pancreatic cancer risk: evidence for role of MMS19L. Cancer Epidemiol Biomarkers Prev 2009;18 (4) 1295- 1302
PubMed Link to Article
Toniolo  PGLevitz  MZeleniuch-Jacquotte  A  et al.  A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J Natl Cancer Inst 1995;87 (3) 190- 197
PubMed Link to Article
Colditz  GAHankinson  SE The Nurses' Health Study. Nat Rev Cancer 2005;5 (5) 388- 396
PubMed Link to Article
Hennekens  CHBuring  JE Methodologic considerations in the design and conduct of randomized trials. Control Clin Trials 1989;10 (4) ((suppl)) 142S- 150S
PubMed Link to Article
Gohagan  JKProrok  PCHayes  RBKramer  BSProstate, Lung, Colorectal and Ovarian Cancer Screening Trial Project Team, The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: history, organization, and status. Control Clin Trials 2000;21 (6) ((suppl)) 251S- 272S
PubMed Link to Article
Cai  HZheng  WXiang  YB  et al.  Dietary patterns and their correlates among middle-aged and elderly Chinese men: a report from the Shanghai Men's Health Study. Br J Nutr 2007;98 (5) 1006- 1013
PubMed Link to Article
Zheng  WChow  WHYang  G  et al.  The Shanghai Women's Health Study: rationale, study design, and baseline characteristics. Am J Epidemiol 2005;162 (11) 1123- 1131
PubMed Link to Article
The Women's Health Initiative Study Group, Design of the Women's Health Initiative clinical trial and observational study. Control Clin Trials 1998;19 (1) 61- 109
PubMed Link to Article
Buring  JEHennekens  CH The Women's Health Study: rationale and background. J Myocardial Ischemia 1992;430- 40
Garfinkel  L Selection, follow-up, and analysis in the American Cancer Society prospective studies. Natl Cancer Inst Monogr 1985;6749- 52
PubMed
Haakenson  CPVickers  KSCha  SS  et al.  Efficacy of a simple, low-cost educational intervention in improving knowledge about risks and benefits of screening mammography. Mayo Clin Proc 2006;81 (6) 783- 791
PubMed Link to Article
World Cancer Research Fund, Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. 2nd ed. Washington, DC American Institute for Cancer Research2007;215- 216
Bueno de Mesquita  HBMoerman  CJRunia  SMaisonneuve  P Are energy and energy-providing nutrients related to exocrine carcinoma of the pancreas? Int J Cancer 1990;46 (3) 435- 444
PubMed Link to Article
Howe  GRJain  MMiller  AB Dietary factors and risk of pancreatic cancer: results of a Canadian population-based case-control study. Int J Cancer 1990;45 (4) 604- 608
PubMed Link to Article
Zatonski  WPrzewozniak  KHowe  GRMaisonneuve  PWalker  AMBoyle  P Nutritional factors and pancreatic cancer. Int J Cancer 1991;48 (3) 390- 394
PubMed Link to Article
Ghadirian  PSimard  ABaillargeon  JMaisonneuve  PBoyle  P Nutritional factors and pancreatic cancer in the francophone community in Montreal, Canada. Int J Cancer 1991;47 (1) 1- 6
PubMed Link to Article
Nilsen  TIVatten  LJ A prospective study of lifestyle factors and the risk of pancreatic cancer in Nord-Trondelag, Norway. Cancer Causes Control 2000;11 (7) 645- 652
PubMed Link to Article
Li  DMorris  JSLiu  J  et al.  Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA 2009;301 (24) 2553- 2562
PubMed Link to Article
International Agency for Research on Cancer, IARC Handbook of Cancer Prevention: Weight Control and Physical Activity. Vol 6. Lyon, France IARC Press2002;
Fisher  WEBoros  LGSchirmer  WJ Insulin promotes pancreatic cancer: evidence for endocrine influence on exocrine pancreatic tumors. J Surg Res 1996;63 (1) 310- 313
PubMed Link to Article
McCarty  MF Insulin secretion as a determinant of pancreatic cancer risk. Med Hypotheses 2001;57 (2) 146- 150
PubMed Link to Article
Mössner  JLogsdon  CDGoldfine  IDWilliams  JA Do insulin and the insulin like growth factors (IGFs) stimulate growth of the exocrine pancreas? Gut 1987;28 ((suppl)) 51- 55
PubMed Link to Article
Williams  JAGoldfine  ID The insulin-pancreatic acinar axis. Diabetes 1985;34 (10) 980- 986
PubMed Link to Article
Conover  CALee  PDKanaley  JAClarkson  JTJensen  MD Insulin regulation of insulin-like growth factor binding protein-1 in obese and nonobese humans. J Clin Endocrinol Metab 1992;74 (6) 1355- 1360
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for overweight people (BMI, 25 to <30) compared with normal-weight people (BMI, <25). ATBC indicates Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study; CI, confidence interval; CLUE II CPS II, Cancer Prevention Study II; EPIC, European Prospective Investigation Into Cancer and Nutrition; HPFS, Health Professionals Follow-up Study; MAYO, Mayo Clinic study; NHS, Nurses' Health Study; NYUWHS, New York University Women's Health Study; PHSI, Physicians' Health Study; PLCO, Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial; SMWHS, Shanghai Men's and Women's Health Studies; WHI, Women's Health Initiative; and WHS, Women's Health Study.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for obese people (30 to <35) compared with normal-weight people (<25). See the legend for Figure 1 for an explanation of the abbreviations.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Risk estimates for pancreatic cancer associated with body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]) by study for severely obese people (>35) compared with normal-weight people (<25). See the legend for Figure 1 for an explanation of the abbreviations.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Characteristics of the 13 Cohorts Included in the PanScan Pooled Analysis
Table Graphic Jump LocationTable 2. Participant Characteristics: the PanScan
Table Graphic Jump LocationTable 3. Baseline Anthropometric Characteristics by Sex: the PanScana
Table Graphic Jump LocationTable 4. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in All the Study Participants: the PanScan
Table Graphic Jump LocationTable 5. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in Men: the PanScan
Table Graphic Jump LocationTable 6. Risk of Pancreatic Cancer According to Baseline Anthropometric Factors in Women: the PanScan

References

American Cancer Society, Cancer Facts & Figures 2009.  Atlanta, GA American Cancer Society2009;
Parkin  DMBray  FFerlay  JPisani  P Global cancer statistics, 2002. CA Cancer J Clin 2005;55 (2) 74- 108
PubMed Link to Article
Edwards  BKBrown  MLWingo  PA  et al.  Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment. J Natl Cancer Inst 2005;97 (19) 1407- 1427
PubMed Link to Article
Gapstur  SMGann  P Is pancreatic cancer a preventable disease? JAMA 2001;286 (8) 967- 968
PubMed Link to Article
Li  DXie  KWolff  RAbbruzzese  JL Pancreatic cancer. Lancet 2004;363 (9414) 1049- 1057
PubMed Link to Article
Friedman  GDvan den Eeden  SK Risk factors for pancreatic cancer: an exploratory study. Int J Epidemiol 1993;22 (1) 30- 37
PubMed Link to Article
Shibata  AMack  TMPaganini-Hill  ARoss  RKHenderson  BE A prospective study of pancreatic cancer in the elderly. Int J Cancer 1994;58 (1) 46- 49
PubMed Link to Article
Gapstur  SMGann  PHLowe  WLiu  KColangelo  LDyer  A Abnormal glucose metabolism and pancreatic cancer mortality. JAMA 2000;283 (19) 2552- 2558
PubMed Link to Article
Michaud  DSGiovannucci  EWillett  WCColditz  GAStampfer  MJFuchs  CS Physical activity, obesity, height, and the risk of pancreatic cancer. JAMA 2001;286 (8) 921- 929
PubMed Link to Article
Isaksson  BJonsson  FPedersen  NLLarsson  JFeychting  MPermert  J Lifestyle factors and pancreatic cancer risk: a cohort study from the Swedish Twin Registry. Int J Cancer 2002;98 (3) 480- 482
PubMed Link to Article
Calle  EERodriguez  CWalker-Thurmond  KThun  MJ Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348 (17) 1625- 1638
PubMed Link to Article
Patel  AVRodriguez  CBernstein  LChao  AThun  MJCalle  EE Obesity, recreational physical activity, and risk of pancreatic cancer in a large U.S. cohort. Cancer Epidemiol Biomarkers Prev 2005;14 (2) 459- 466
PubMed Link to Article
Rapp  KSchroeder  JKlenk  J  et al.  Obesity and incidence of cancer: a large cohort study of over 145,000 adults in Austria. Br J Cancer 2005;93 (9) 1062- 1067
PubMed Link to Article
Larsson  SCPermert  JHåkansson  NNäslund  IBergkvist  LWolk  A Overall obesity, abdominal adiposity, diabetes and cigarette smoking in relation to the risk of pancreatic cancer in two Swedish population-based cohorts. Br J Cancer 2005;93 (11) 1310- 1315
PubMed Link to Article
Berrington de González  ASpencer  EABueno-de-Mesquita  HB  et al.  Anthropometry, physical activity, and the risk of pancreatic cancer in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev 2006;15 (5) 879- 885
PubMed Link to Article
Stolzenberg-Solomon  RZPietinen  PTaylor  PRVirtamo  JAlbanes  D A prospective study of medical conditions, anthropometry, physical activity, and pancreatic cancer in male smokers (Finland). Cancer Causes Control 2002;13 (5) 417- 426
PubMed Link to Article
Lee  IMSesso  HDOguma  YPaffenbarger  RS  Jr Physical activity, body weight, and pancreatic cancer mortality. Br J Cancer 2003;88 (5) 679- 683
PubMed Link to Article
Kuriyama  STsubono  YHozawa  A  et al.  Obesity and risk of cancer in Japan. Int J Cancer 2005;113 (1) 148- 157
PubMed Link to Article
Sinner  PJSchmitz  KHAnderson  KEFolsom  AR Lack of association of physical activity and obesity with incident pancreatic cancer in elderly women. Cancer Epidemiol Biomarkers Prev 2005;14 (6) 1571- 1573
PubMed Link to Article
Batty  GDShipley  MJJarrett  RJBreeze  EMarmot  MGSmith  GD Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study. Int J Obes (Lond) 2005;29 (10) 1267- 1274
PubMed Link to Article
Oh  SWYoon  YSShin  SA Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 2005;23 (21) 4742- 4754
PubMed Link to Article
Lukanova  ABjör  OKaaks  R  et al.  Body mass index and cancer: results from the Northern Sweden Health and Disease Cohort. Int J Cancer 2006;118 (2) 458- 466
PubMed Link to Article
Nöthlings  UKolonel  LN Risk factors for pancreatic cancer in the Hawai'i-Los Angeles Multiethnic Cohort Study. Hawaii Med J 2006;65 (1) 26- 28
PubMed
Samanic  CChow  WHGridley  GJarvholm  BFraumeni  JF  Jr Relation of body mass index to cancer risk in 362,552 Swedish men. Cancer Causes Control 2006;17 (7) 901- 909
PubMed Link to Article
Stolzenberg-Solomon  RZAdams  KLeitzmann  M  et al.  Adiposity, physical activity, and pancreatic cancer in the National Institutes of Health-AARP Diet and Health Cohort. Am J Epidemiol 2008;167 (5) 586- 597
PubMed Link to Article
Nöthlings  UWilkens  LRMurphy  SPHankin  JHHenderson  BEKolonel  LN Body mass index and physical activity as risk factors for pancreatic cancer: the Multiethnic Cohort Study. Cancer Causes Control 2007;18 (2) 165- 175
PubMed Link to Article
Lin  YKikuchi  STamakoshi  A  et al. JACC Study Group, Obesity, physical activity and the risk of pancreatic cancer in a large Japanese cohort. Int J Cancer 2007;120 (12) 2665- 2671
PubMed Link to Article
Luo  JIwasaki  MInoue  M  et al. JPHC Study Group, Body mass index, physical activity and the risk of pancreatic cancer in relation to smoking status and history of diabetes. Cancer Causes Control 2007;18 (6) 603- 612
PubMed Link to Article
ATBC Cancer Prevention Study Group, The Alpha-Tocopherol, Beta-Carotene Lung Cancer Prevention Study. Ann Epidemiol 1994;4 (1) 1- 10
PubMed Link to Article
Huang  HYAlberg  AJNorkus  EPHoffman  SCComstock  GWHelzlsouer  KJ Prospective study of antioxidant micronutrients in the blood and the risk of developing prostate cancer. Am J Epidemiol 2003;157 (4) 335- 344
PubMed Link to Article
Calle  EERodriguez  CJacobs  EJ  et al.  The American Cancer Society Cancer Prevention Study II Nutrition Cohort. Cancer 2002;94 (9) 2490- 2501
PubMed Link to Article
Riboli  EHunt  KJSlimani  N  et al.  European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr 2002;5 (6B) 1113- 1124
PubMed Link to Article
Rimm  EBGiovannucci  ELWillett  WC  et al.  Prospective study of alcohol consumption and risk of coronary disease in men. Lancet 1991;338 (8765) 464- 468
PubMed Link to Article
McWilliams  RRBamlet  WRde Andrade  MRider  DNCunningham  JMPetersen  GM Nucleotide excision repair pathway polymorphisms and pancreatic cancer risk: evidence for role of MMS19L. Cancer Epidemiol Biomarkers Prev 2009;18 (4) 1295- 1302
PubMed Link to Article
Toniolo  PGLevitz  MZeleniuch-Jacquotte  A  et al.  A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J Natl Cancer Inst 1995;87 (3) 190- 197
PubMed Link to Article
Colditz  GAHankinson  SE The Nurses' Health Study. Nat Rev Cancer 2005;5 (5) 388- 396
PubMed Link to Article
Hennekens  CHBuring  JE Methodologic considerations in the design and conduct of randomized trials. Control Clin Trials 1989;10 (4) ((suppl)) 142S- 150S
PubMed Link to Article
Gohagan  JKProrok  PCHayes  RBKramer  BSProstate, Lung, Colorectal and Ovarian Cancer Screening Trial Project Team, The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: history, organization, and status. Control Clin Trials 2000;21 (6) ((suppl)) 251S- 272S
PubMed Link to Article
Cai  HZheng  WXiang  YB  et al.  Dietary patterns and their correlates among middle-aged and elderly Chinese men: a report from the Shanghai Men's Health Study. Br J Nutr 2007;98 (5) 1006- 1013
PubMed Link to Article
Zheng  WChow  WHYang  G  et al.  The Shanghai Women's Health Study: rationale, study design, and baseline characteristics. Am J Epidemiol 2005;162 (11) 1123- 1131
PubMed Link to Article
The Women's Health Initiative Study Group, Design of the Women's Health Initiative clinical trial and observational study. Control Clin Trials 1998;19 (1) 61- 109
PubMed Link to Article
Buring  JEHennekens  CH The Women's Health Study: rationale and background. J Myocardial Ischemia 1992;430- 40
Garfinkel  L Selection, follow-up, and analysis in the American Cancer Society prospective studies. Natl Cancer Inst Monogr 1985;6749- 52
PubMed
Haakenson  CPVickers  KSCha  SS  et al.  Efficacy of a simple, low-cost educational intervention in improving knowledge about risks and benefits of screening mammography. Mayo Clin Proc 2006;81 (6) 783- 791
PubMed Link to Article
World Cancer Research Fund, Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. 2nd ed. Washington, DC American Institute for Cancer Research2007;215- 216
Bueno de Mesquita  HBMoerman  CJRunia  SMaisonneuve  P Are energy and energy-providing nutrients related to exocrine carcinoma of the pancreas? Int J Cancer 1990;46 (3) 435- 444
PubMed Link to Article
Howe  GRJain  MMiller  AB Dietary factors and risk of pancreatic cancer: results of a Canadian population-based case-control study. Int J Cancer 1990;45 (4) 604- 608
PubMed Link to Article
Zatonski  WPrzewozniak  KHowe  GRMaisonneuve  PWalker  AMBoyle  P Nutritional factors and pancreatic cancer. Int J Cancer 1991;48 (3) 390- 394
PubMed Link to Article
Ghadirian  PSimard  ABaillargeon  JMaisonneuve  PBoyle  P Nutritional factors and pancreatic cancer in the francophone community in Montreal, Canada. Int J Cancer 1991;47 (1) 1- 6
PubMed Link to Article
Nilsen  TIVatten  LJ A prospective study of lifestyle factors and the risk of pancreatic cancer in Nord-Trondelag, Norway. Cancer Causes Control 2000;11 (7) 645- 652
PubMed Link to Article
Li  DMorris  JSLiu  J  et al.  Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA 2009;301 (24) 2553- 2562
PubMed Link to Article
International Agency for Research on Cancer, IARC Handbook of Cancer Prevention: Weight Control and Physical Activity. Vol 6. Lyon, France IARC Press2002;
Fisher  WEBoros  LGSchirmer  WJ Insulin promotes pancreatic cancer: evidence for endocrine influence on exocrine pancreatic tumors. J Surg Res 1996;63 (1) 310- 313
PubMed Link to Article
McCarty  MF Insulin secretion as a determinant of pancreatic cancer risk. Med Hypotheses 2001;57 (2) 146- 150
PubMed Link to Article
Mössner  JLogsdon  CDGoldfine  IDWilliams  JA Do insulin and the insulin like growth factors (IGFs) stimulate growth of the exocrine pancreas? Gut 1987;28 ((suppl)) 51- 55
PubMed Link to Article
Williams  JAGoldfine  ID The insulin-pancreatic acinar axis. Diabetes 1985;34 (10) 980- 986
PubMed Link to Article
Conover  CALee  PDKanaley  JAClarkson  JTJensen  MD Insulin regulation of insulin-like growth factor binding protein-1 in obese and nonobese humans. J Clin Endocrinol Metab 1992;74 (6) 1355- 1360
PubMed

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