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Added sugar and sugar-sweetened foods and beverages and the risk of pancreatic cancer in the National Institutes of Health–AARP Diet and Health Study^1,2,3

¹ From the Department of Epidemiology, Harvard School of Public Health, Boston, MA (YB and DSM); the Divisions of Cancer Epidemiology and Genetics (RSS, LJ, DTS, YP, MFL, AS, and DSM) and Cancer Control and Population Sciences (AFS), National Cancer Institute, Rockville, MD; AARP, Washington, DC (AH); and the Department of Epidemiology and Public Health, Imperial College London, United Kingdom (DSM)

² Supported by the Intramural Research Program of the National Cancer Institute, National Institutes of Health.

³ Reprints not available. Address correspondence to Y Bao, Department of Epidemiology, Harvard School of Public Health, 677 Huntington Avenue, Kresge 911, Boston, MA 02115. E-mail: ybao{at}hsph.harvard.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: Although it has been hypothesized that hyperglycemia, hyperinsulinemia, and insulin resistance are involved in the development of pancreatic cancer, results from epidemiologic studies of added sugar intake are inconclusive.

Objective: Our objective was to investigate whether the consumption of total added sugar and sugar-sweetened foods and beverages is associated with pancreatic cancer risk.

Design: In 1995 and 1996, we prospectively examined 487 922 men and women aged 50–71 y and free of cancer and diabetes. Total added dietary sugar intake (in tsp/d; based on the US Department of Agriculture's Pyramid Servings Database) was assessed with a food-frequency questionnaire. Relative risks (RRs) and 95% CIs were calculated with adjustment for total energy and potential confounding factors.

Results: During an average 7.2 y of follow-up, 1258 incident pancreatic cancer cases were ascertained. The median intakes for the lowest and highest quintiles of total added sugar intake were 12.6 (3 tsp/d) and 96.2 (22.9 tsp/d) g/d, respectively. No overall greater risk of pancreatic cancer was observed in men or women with high intake of total added sugar or sugar-sweetened foods and beverages. For men and women combined, the multivariate RRs of the highest versus lowest intake categories were 0.85 (95% CI: 0.68, 1.06; P for trend = 0.07) for total added sugar, 1.01 (0.82,1.23; P for trend = 0.58) for sweets, 0.98 (0.82,1.18; P for trend = 0.49) for dairy desserts, 1.12 (0.91,1.39; P for trend = 0.35) for sugar added to coffee and tea, and 1.01 (0.77,1.31; P for trend = 0.76) for regular soft drinks.

Conclusion: Our results do not support the hypothesis that consumption of added sugar or of sugar-sweetened foods and beverages is associated with overall risk of pancreatic cancer.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Pancreatic cancer is the fourth leading cause of cancer death in the United States; it has a 5-y survival rate of <5% and a fatality rate of nearly 100% (1). Hyperglycemia and hyperinsulinemia have been shown to be important in the development of this malignancy, probably by the stimulatory effect of insulin on cell proliferation (2, 3). Many of the recognized risk factors for pancreatic cancer, including obesity and type 2 diabetes mellitus, have been related to abnormal glucose tolerance and insulin resistance (4-6). High sugar intake increases blood glucose and insulin response, which may contribute to a favorable environment for the development of pancreatic cancer (7).

Several prospective studies have investigated the influence of sugar or carbohydrate intake on the risk of pancreatic cancer, but the findings are inconsistent, ranging from an inverse association (8) or no association (9-12) to a positive association (13, 14). In contrast, most case-control studies have shown a positive association with sugar or carbohydrate intake (15). Glycemic load, a quantitative measure of glycemic effect, was associated with a greater risk of pancreatic cancer in the Nurses’ Health Study (NHS) (13), whereas no association was found in other cohorts (9-12). Sugar-sweetened soft drinks, the leading source of added sugars in the US diet (16), have been linked with weight gain and type 2 diabetes (17) and to pancreatic cancer (18).

These conflicting results could be partly due to relatively small numbers of cases (8-11, 13, 14, 18), inadequate control for diabetes (9), and incomplete exposure information (14), all of which may distort the true association between sugar consumption and the risk of pancreatic cancer. We therefore examined the consumption of sugar and sugar-sweetened foods and beverages in relation to the risk of pancreatic cancer in the National Institutes of Health (NIH)–AARP Diet and Health Study, a large prospective cohort study of >500 000 US men and women with wide dietary intake distributions and detailed information on potential risk factors for pancreatic cancer.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Study population
Details of the NIH-AARP Diet and Health Study have been described elsewhere (19). Briefly, the cohort was initiated in 1995–1996 when a self-administered baseline food-frequency questionnaire (FFQ) was mailed to 3.5 million AARP members. The baseline questionnaire also collected information on participants’ demographic characteristics and other potential cancer risk factors (eg, smoking, physical activity, family history of cancer, and medical conditions). Recipients were 50–71 y old, and they resided in 1 of 6 states (CA, FL, LA, NJ, NC, or PA) or 1 of 2 metropolitan areas (Atlanta, GA, or Detroit, MI). Although the response rate to the baseline questionnaire was low (17.6%), that would not affect the internal validity of our study, given the prospective design. Of the 617 119 persons who returned the questionnaire, 567 169 provided satisfactory dietary data. We excluded respondents who had completed duplicate questionnaires (n = 179) and persons who moved out of the study areas before returning the questionnaire (n = 321), who died before study entry (n = 261), or who withdrew (n = 6). From the remaining 566 402 participants, we excluded proxy respondents (n = 15 760), prevalent cancer cases identified through cancer registries at baseline (n = 8583), persons with a history of diabetes (n = 49 817)—because diabetes patients often reduce their sugar intake after diagnosis—and persons with extreme energy intake (ie, >2 interquartile ranges above the 75th percentile or below the 25th percentile) (n = 4320). After these exclusions, the study cohort consisted of 487 922 participants (284 076 men and 203 846 women).

All subjects gave informed consent by virtue of completing the questionnaire. The NIH-AARP Diet and Health Study was approved by the Special Studies Institutional Review Board of the National Cancer Institute.

Cancer ascertainment
Incident cases of pancreatic cancer through December 31, 2003, were identified through the 11 state cancer registries. In addition to the participants who resided in the 8 initial study areas, participants who moved to Texas, Nevada, and Arizona were followed-up for outcomes. We estimated that 90% of all cancer cases in our cohort were validly identified by linkage to state cancer registries (20). In addition, deaths due to pancreatic cancer were identified through the National Death Index. For our analyses, we included only incident cases of primary adenocarcinoma of the exocrine pancreas (International Classification of Diseases for Oncology, Third Edition: ICD-O-3 codes C25.0–C25.3 and C25.7–C25.9). We excluded endocrine pancreatic tumors (ICD-O-3 code C25.4) because the etiology of those cancers is thought to be different (2).

Dietary assessment
Dietary intakes were derived from the baseline 124-item FFQ. Participants were queried about their usual frequency of consumption and portion size over the previous year by using 10 categories of frequency ranging from never to 6 times/d for beverages and from never to 2 times/d for foods and 3 categories of portion size (19, 21). Participants were also asked whether they usually drank the sugar-free (diet) or the regular-calorie type of a particular beverage. From these responses, daily consumption of foods, beverages, and nutrients were calculated by using data from the US Department of Agriculture (USDA) 1994–1996 Continuing Survey of Food Intake by Individuals (21).

Total added sugar (in tsp/d) was defined by using the USDA Pyramid Servings Database, which enabled us to estimate added sugar intake from all foods in the FFQ (22). Added sugar included sugars that were eaten separately and sugars used as ingredients in processed or prepared foods. Naturally occurring sugars, such as lactose in milk or fructose in fruit, were not included. One teaspoon added sugar was defined as 4.2 g table sugar (sucrose) (23).

The performance of the FFQ was evaluated by using 2 nonconsecutive 24-h recalls among a subgroup of the cohort consisting of 2053 persons (24). The energy-adjusted Pearson correlation coefficients for carbohydrate between the FFQ and the 24-h recall were 0.71 for men and 0.64 for women.

Statistical analysis
To facilitate analysis, sugar-sweetened foods and beverages were grouped into sugar-sweetened beverages (ie, regular soft drinks and regular fruit drinks), sugar added to coffee and tea, sweets (eg, candy, cookie, cake, pie, donut, and sweet roll), dairy desserts (ie, ice cream and frozen yogurt), and other sugar-sweetened foods (eg, muffin, cornbread, and pancake). Although total added sugar was derived from all foods in the FFQ, not all possible foods with added sugars were included in the food groups. Spearman correlation coefficients were computed among these sugar-sweetened food and beverage groups.

Consumption of total added sugar and sugar-sweetened food groups was analyzed in quintiles. This approach reduces the influence of extreme observations on the effect estimates. For analyses combining men and women, quintiles were based on the intake distribution of the entire cohort. For sex-specific analyses, quintiles were based on the sex-specific intake distributions. Because of the large number of participants who did not regularly consume sugar-sweetened beverages or sugar added to coffee or tea, they were assigned to the lowest intake quintile. We then evenly divided the remainder of the participants into 4 categories and treated them as quintiles 2–5. For total, regular, and diet soft drinks, we assigned never drinkers to the lowest categories and then divided the remainder of the participants into quintiles. We used the lowest intake categories as the reference throughout the analyses. We then estimated the power to detect a specified relative risk (RR) for the highest versus the lowest categories of intake of total added sugar, regular soft drinks, and diet soft drinks with a 2-sided level at 0.05 (25).

Person-years of follow-up were calculated from the scan date of the baseline questionnaire to the date of pancreatic cancer diagnosis, death, emigration out of the study areas, or December 31, 2003—whichever occurred first. RRs and 95% CIs were estimated by using Cox proportional hazards regression models with age as the primary time-scale. The proportional hazards assumption was verified by modeling interaction terms of age and our main exposures as well as other fixed covariates.

We analyzed data by using 2 energy-adjustment methods. Intakes of our main exposures were included as the absolute daily amount (standard model) or the daily amount per 1000 kcal (density model). When the 2 methods yielded similar results, we presented risk estimates only for absolute daily amount, to allow direct comparison with previous publications. In multivariate models, we adjusted for sex, race (white; black; Hispanic; Asian, Pacific Islander, American Indian or Alaskan Native; and missing), education (11 y, 12 y or completed high school, post-high school or some college, college or postgraduate, and missing), body mass index [(BMI; in kg/m²): <18.5, 18.5 to <25, 25 to <30, 30 to <35, 35, and missing), alcohol (g/d, in quintiles), smoking (never, quit 10 y ago, quit 5–9 y ago; quit 1–4 y ago, quit <1 y ago, or current and smoking 20 or >20 cigarettes/d; and missing), physical activity (never, rarely, <3 times/mo, 1–2 times/wk, 3–4 times/wk, 5 times/wk, and missing), total energy (continuous), energy-adjusted total fat intake (quintiles), energy-adjusted saturated fat intake (quintiles), energy-adjusted red meat (quintiles), energy-adjusted folate (quintiles), and use of multivitamins (yes or no). In the final multivariate models, we kept only those variables that altered the ratio of sugar to pancreatic cancer risk by 5%. For sugar-sweetened beverages, we also adjusted for diet beverage consumption (never drinkers and quartiles of the remaining participants). Similarly, regular soft drinks and diet soft drinks were adjusted for each other. Because BMI may mediate the association between sugar and pancreatic cancer, we repeated our analysis without control for BMI. An indicator variable for missing values of each covariate was created. Linear trends were tested by using the Wald test of a score variable that contained median values of intake categories.

We further conducted stratified analyses by strong risk factors of pancreatic cancer including sex and smoking (never smokers or quit 10 y compared with current smokers or quit <10 y, because the previous study (26) showed that the risks of pancreatic cancer were similar for never smokers and former smokers who quit 10 y ago.) Persons who are obese and those who are less active tend to have a greater insulin response to their diet than do lean or active persons (5, 18), and therefore we also examined whether the association of added sugar or soft drink consumption with pancreatic cancer varied across strata of BMI (<30 compared with 30 and <35 compared with 35) and physical activity (<3 compared with 3 times/wk). Tests for interaction were performed by using the likelihood ratio test comparing models with and without cross-product terms. To further examine whether the associations of our interest are more apparent among persons with greater insulin resistance, we analyzed the associations among subgroups defined by the combination of BMI and physical activity.

In sensitivity analyses, we excluded the first 2 y of follow-up for all participants to rule out an effect of subclinical pancreatic cancer on added sugar intake. Because patients with cardiovascular disease or those with poor health may change their diet, we assessed the influence of those conditions on the main study results in 2 additional sensitivity analyses: one that excluded subjects with heart disease at baseline (12.5% of the whole cohort) and a second that was restricted to subjects who reported their health status as excellent or very good (54.4% of the whole cohort).

In addition, we repeated our analyses by excluding those participants who did not report smoking status, those who reported cancer history at baseline that was not recorded in cancer registries, and those who had extreme intake of total added sugar. The estimates were similar to those of the main analysis. Moreover, we analyzed our main exposures in quartiles or categories defined by previously specified cutoffs of intakes, which also yielded results consistent with those based on quintiles. Analysis using reported frequencies of intake made little difference.

We used SAS statistical software (version 9.1; SAS Institute, Inc, Cary, NC) for all analyses. All statistical tests were 2-sided; P < 0.05 was considered statistically significant.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
During 3 521 088 person-years of follow-up (mean: 7.2 y), we identified 1258 incident cases of pancreatic cancer (808 men and 450 women). For men and women combined, the median intake in the lowest and highest quintiles of total added sugar intake was 3.0 tsp/d (12.6 g/d) and 22.9 tsp/d (96.2 g/d), respectively. Compared with participants with low intakes of total added sugar, those with high sugar intake were younger; more likely to be black, less educated, and physically inactive; and more likely to smoke and to consume more fat but less alcohol, folate, and multivitamins (Table 1). Forty-eight percent of men and 36% of women were drinkers of regular soft drinks; 42% of men and 49% of women were drinkers of diet soft drinks. Persons with high consumption of regular soft drinks generally had characteristics similar to those with high sugar intake. In contrast, persons who drank diet soft drinks were more educated and less likely to smoke, and they consumed more folate and multivitamins than did those who never drank diet soft drinks.

Table 2

After adjustment for potential confounders, consumption of sugar-sweetened beverages, sugar added to coffee or tea, sweets, dairy desserts, and other sugar-sweetened foods showed no trends for pancreatic cancer risk (Table 2). Neither regular nor diet soft drinks had a significant trend toward greater risk of pancreatic cancer (Table 3). Separate analyses in men and women showed similar associations (data not shown). The results for sugar-sweetened foods and beverages did not change after exclusion of the first 2 y of follow-up. Analyzing energy-adjusted intake as g/1000 kcal instead of as an absolute amount of sugar-sweetened foods and beverages had no significant effect on the risk ratios (data not shown). The above findings remained the same after removal of BMI from the multivariate models, exclusion of participants with heart disease, or restriction to participants who reported their health status as excellent or very good (data not shown).

Table 4

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
In this large cohort of US men and women, we found no overall associations of total added sugar or sugar-sweetened foods and beverages with pancreatic cancer risk. This lack of overall associations is not likely to be due to lack of statistical power. Given the cohort's large size, we had sufficient power (80%) to detect a moderate association between pancreatic cancer and the highest intake category of total added sugar (RR > 1.26) and regular soft drinks (RR > 1.35). In addition, because of the study's prospective design and the completeness of follow-up, neither selection bias nor differential case ascertainment is likely to be responsible for the null findings.

Misclassification of total added sugar and sweetened food consumption is inevitable because dietary intakes were self-reported, but misclassification is unlikely to dramatically attenuate the estimates, given the high correlation for carbohydrate observed in the validation study (24). The study ascertained histologically confirmed incident cases from 11 cancer registries with 90% completeness (20), which indicates that the observed null associations are not likely to result from misclassification of pancreatic cancer cases.

Residual confounding by measured factors may be of minor importance in the present study, because the age- or sex-adjusted models and multivariate models yielded very similar results. Furthermore, although obesity may mediate the association between dietary intake and pancreatic cancer, the null relations are not likely to be the result of overcontrol for BMI, because our sensitivity analyses showed that adjustment for BMI did not make a difference in the risk estimates.

One possible explanation for the lack of overall associations is that dietary intake may be changed by preclinical disease at baseline. To rule out the possibility of change in sugar intake due to undiagnosed pancreatic cancer, we excluded the first 2 y of follow-up for all participants in sensitivity analyses. The results did not change. Because patients with diabetes usually limited their sugar intake, which would bias the estimates downward, we excluded from analysis those with history of diabetes at baseline, so that the observed association of dietary intake with pancreatic cancer risk would not be due to preexistent diabetes. In addition to diabetes, prediabetic status is a reason for people to change their diet and lifestyle. Therefore, a change in dietary intake after a diagnosis of a prediabetic condition would result in measurement error (ie, would not be representative of long-term diet) and thus may underestimate the true risk. Unfortunately, the influence of a prediabetic condition cannot be eliminated from this study and could potentially explain the lack of association. We attempted to address this issue by restricting the analysis to those who reported their health status as excellent or very good; no changes in overall risk estimates were observed.

The lack of overall associations for added sugar intake and pancreatic cancer risk in the present study is consistent with data from most prospective studies (9-12). Although high glycemic load and fructose were associated with a nonsignificant increase in pancreatic cancer risk in the Nurses’ Health Study (NHS), the null relations observed for carbohydrate and sucrose in the same cohort are consistent with our findings (13). In contrast, carbohydrate was inversely associated with pancreatic cancer risk in Finnish male smokers (8). However, the Finnish diet, particularly during the mid-1980s, may not be comparable to the American diet, in that the carbohydrate consumed by the Finns did not tend to be from sweets or soft drinks, as in American populations, but from a rye bread that was high in fiber and phytochemicals (8). We were unable to confirm the positive association for 5 tsp sugar/d added to coffee or tea (RR =1.69; 0.99, 2.89) reported in a recent prospective study in Sweden (14). However, that study included only 131 cases of pancreatic cancer. In addition, as noted by the authors (14), the components or recipes of sweet foods and beverages in US and Swedish populations may be different, which could make the Swedish and the present studies difficult to compare.

The association of soft drink intake with pancreatic cancer risk was examined in 3 previous cohort studies. The Multiethnic Cohort Study showed no association (12). A study by Larsson et al (14) found an elevated risk of pancreatic cancer for 2 glasses total soft drink/d (RR 1.93; 95% CI: 1.18, 3.14). In addition to the limitations mentioned above, information on the type of soft drink was not available in that study. In a study of 2 US cohorts, women who consumed >3 servings sugar-sweetened soft drink/wk appeared to have a significant increase in risk (RR = 1.57; 95% CI: 1.02, 2.41), whereas no association was observed among men (18). The main strength of that study is that the dietary intake was cumulatively updated during 20 y of follow-up. We are uncertain whether the long follow-up and repeated dietary assessments could explain the different results obtained.

A few studies showed that the adverse effect of glycemic load or of sucrose or regular soft drink consumption was more pronounced among those with greater insulin resistance (12, 13, 18). Although total added sugar intake was not associated with overall risk of pancreatic cancer in the present study, risks were elevated in those with BMIs 35 and those who were extremely obese and less active. Nonetheless, subgroup analyses increase the chance of false-positive findings, and, because of the small number of cases in the subgroups, we lacked statistical power to detect these associations. Therefore, these findings should be interpreted with caution, although we cannot exclude the possibility of a greater risk among those with greater insulin resistance.

Several study limitations should be considered. Dietary changes during the follow-up period cannot be addressed in the present study because intakes were measured only at baseline. However, we do not expect that a significant number of participants in the analysis cohort would change their dietary intake in such a relatively short follow-up period (average: 7.2 y). On the other hand, if added sugar intake has a long latent period for pancreatic cancer, the short duration of follow-up is insufficient to detect the effects of long-term sugar intake. Unmeasured confounding by unknown factors cannot be completely ruled out; however, to have a great effect, such confounding factors would have to be relatively prevalent, to be highly correlated with dietary intake in this cohort, and to be strong risk factors for pancreatic cancer. Although the cohort members appeared to have a healthier lifestyle than does the general US population (19), the added sugar intake was comparable to that in the Multiethnic Cohort Study (12). Finally, because the cohort in the present study is predominantly composed of white subjects, our results may not be generalizable to other ethnic populations.

In conclusion, this large, prospective cohort study suggests that total added sugar and sugar-sweetened foods and beverages do not raise the overall risk of pancreatic cancer. Further work is needed to confirm the effect modification by BMI and physical activity to elucidate the role of insulin resistance and provide a more in-depth understanding of the association.

	ACKNOWLEDGMENTS

 
We are grateful to Edward Giovannucci, Charles Fuchs, Donna Spiegelman, Anne CM Thiébaut, and Unhee Lim for their contribution to the data analysis and interpretation of findings. We are indebted to all participants for their commitment to the NIH-AARP Diet and Health Study.

The authors’ responsibilities were as follows—AS, AFS, and AH: contributed to the design and data collection; AFS and YP: data management; YB, DSM, RS-S, and LJ: contributed to the statistical analysis; YB and DSM: wrote the manuscript; RS-S, LJ, DTS, and MFL: helped with the interpretation of results; and all authors: provided a critical review of the manuscript. None of the authors had a personal or financial conflict of interest.

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TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Google Scholar Articles by Bao, Y. Articles by Michaud, D. S PubMed PubMed Citation Articles by Bao, Y. Articles by Michaud, D. S Agricola Articles by Bao, Y. Articles by Michaud, D. S