Abstract
Dietary fiber intake has been implicated as a protective factor for several human cancers in multiple epidemiologic studies. However, little is known about the effect of fiber intake on bladder cancer. This study examines the association between dietary fiber intake and bladder cancer risk among participants in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial. A total of 101 721 participants were included in this study as they completed both the baseline questionnaire and the diet history questionnaire (cancer free before completion of the diet history questionnaire). Hazard ratios (HRs) and the corresponding 95% confidence intervals (CIs) were estimated using the Cox proportional hazards regression model. After a median of 12.5 years of follow-up, 776 new cases of bladder cancer were identified. Higher intake of total fiber, insoluble fiber and soluble fiber were not significantly associated with a reduced risk of bladder cancer. The multi-adjusted HRs (95 CIs) of highest versus lowest tertile of intake were 0.83 (0.66–1.04) for total fiber (P for trend = 0.098), 0.83 (95% CI: 0.67–1.03) for insoluble fiber (P for trend = 0.092) and 0.86 (95% CI: 0.68–1.08) for soluble fiber (P for trend = 0.168), respectively. There was no significant interaction of potential confounders, including education, body mass index and smoking status, with total fiber intake on bladder cancer risk. In summary, the findings of this prospective study show that there is no obvious evidence for a link between dietary fiber consumption and bladder cancer risk. Further large cohort studies are warranted to confirm these findings.
Introduction
Bladder cancer is the 9th most common cancer worldwide with around 430 000 new cases diagnosed annually and the 13th most common cause of cancer deaths (1). Well-established risk factors for bladder cancer are cigarette smoking and exposure to certain chemicals such as benzidine and 4-aminobiphenyl in the working and general environments (2). Additionally, emerging evidence suggests that certain dietary factors have anticancer properties and thus may reduce the risk of bladder cancer (2), including higher intakes of vitamin A, vitamin E, folate, vegetables, citrus fruit and cruciferous vegetables (3), although controversy still exists.
Dietary fiber intake has numerous health benefits. A higher consumption of dietary fiber has been reported to be associated with lower risks of cardiovascular diseases, diabetes and obesity (4). Additionally, there is strong evidence that a high intake of dietary fiber is associated with a lower risk of colorectal cancer (5) and renal cell carcinoma (6). The role of fiber intake in the development of bladder cancer remains inconclusive. There are only two prospective cohort studies that have investigated this association with inconsistent results (7,8). In this study, we evaluated the association between consumption of fiber and the risk of bladder cancer based on the data from the Prostate, Lung, Colorectal and Ovarian (PLCO) cohort.
Materials and methods
Subjects and study design
The PLCO study is a large prospective population-based cohort aimed to determine whether selected screening methods reduce mortality from PLCO cancer (9). Briefly, the participants were enrolled from 1993 to 2001 at 10 screening centers across the United States. At entry, participants were randomly assigned to the intervention arm (n = 77 444) and the control arm (n = 77 453). A total of 101 721 participants were eligible in this study as they had completed both the baseline questionnaire and the diet history questionnaire. In addition, no cancer occurred before completion of the diet history questionnaire. The subjects were followed until 31 December 2009. The PLCO study was approved by the Institutional Review Boards of the United States National Cancer Institute. Informed consent agreement for participation in the research study was also obtained. The number of this approved PLCO project is PLCO-446.
Data collection
The baseline questionnaire is self-administrated and collected information on demographics (e.g. age, sex, ethnicity and education), smoking status, family history of any cancer and medical history. Dietary data were collected using the diet history questionnaire, which included the portion size and frequency of intake of 124 food items and supplement use during the past year.
The amount of dietary fiber intake was estimated based on the Nutrition Data System for Research (NDS-R). The US Department of Agriculture Nutrient Database for Standard Reference and its periodic revisions are the primary data source for NDS-R, which is also supplemented by relevant information from the food manufacturers, literature reports and other published food tables. Specific fiber groups were created according to the pyramid food groups by calculating the fiber content of each food item belonging to the group and multiplying it by the reported amount consumed (10,11). Definitions on soluble and insoluble fiber are provided in Supplemental Text S1, available at Carcinogenesis Online.
Ascertainment of bladder cancer
Study participants were mailed a questionnaire annually to ascertain cancer cases. Participants were asked whether they were diagnosed with any type of cancer and the date of diagnosis in the previous year. Cancer diagnoses were ascertained through medical record review. The methods of vital statistics consist of the administration of annual questionnaires, reports from relatives, friends or physicians, and searches of the National Death Index.
Statistical analysis
Cox proportional hazards regression model was used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs). Follow-up started at cohort entry and ended at the earliest of the following events: diagnosis of bladder cancer, death or study closure. Models were adjusted for various confounding variables including randomization arm (intervention versus control), age (categorical), sex (male versus female), race (White, Non-Hispanic versus Other), body mass index at the time of enrollment (<25 kg/m2 versus ≥25 kg/m2), education status (≤high school versus ≥some college), smoking status (never versus former ≤15 years since quit versus former >15 years since quit versus former year since quit unknown versus current smoker ≤1 pack per day versus current smoker >1 pack per day versus current smoker intensity unknown), alcohol drinking status (never versus former versus current), total energy intake (continuous), family history of any cancer (yes versus no) and marital status (married versus not married). Repeated measurements on potential confounders are not available in this study. Missing values for variables were regarded as dummy variables in the analyses. Likelihood-ratio tests were performed to evaluate interactions. The dietary fiber was firstly examined as tertiles. A restricted cubic spline model with three knots (i.e. 10th, 50th and 90th percentiles) was also performed (12). All statistical analyses were carried out using the STATA version 15 (Stata Corp, College Station, TX) with two-sided P values.
Results
After screening, 53 176 subjects including 653 bladder cancer cases in PLCO Cancer Screening Trial were excluded from this study because they did not meet the inclusion criteria. The main characteristics comparison between those who were in this study and those not are summarized in Supplemental Tables S1 and S2, available at Carcinogenesis Online. Participants included in this study had higher proportions of never smokers, non-Hispanic White and being married compared those not included in this study. Table 1 shows the main characteristics of 101 721 subjects eligible for this study by total fiber intake. The median dietary fiber consumption and energy intake in the total cohort were 16.5 g/day and 1607.5 kcal/day, respectively. Participants who consumed lower amounts of dietary fiber were less educated and more likely to be female. After a median of 12.5 years of follow-up, 776 newly diagnosed bladder cancer cases were identified. The incidence rate of bladder cancer was 6.65 (95% CI 6.20–7.13) per 10 000 person-years.
Table 1.
Main characteristics of 101 721 subjects in the PLCO Cancer Screening Trial by total fiber intake
| Variables | Q1 (n = 33 941) | Q2 (n = 33 884) | Q3 (n = 33 896) | P value |
|---|---|---|---|---|
| Age (years), mean ± SD | 62.40 ± 5.30 | 62.43 ± 5.28 | 62.38 ± 5.27 | 0.579 |
| Female (n, %) | 19 774 (58.3%) | 17 961 (53.0%) | 14 512 (42.8%) | <0.001 |
| Smoking status (n, %) | <0.001 | |||
| Never | 15 511 (45.7%) | 16 505 (48.7%) | 16 536 (48.8%) | |
| Former ≤15 years since quit | 5805 (17.1%) | 5385 (15.9%) | 5154 (15.2%) | |
| Former >15 years since quit | 8096 (23.9%) | 8881 (26.2%) | 9614 (28.4%) | |
| Former year since quit unknown | 308 (0.9%) | 250 (0.7%) | 268 (0.8%) | |
| Current smoker ≤1 pack per day | 2623 (7.7%) | 1768 (5.2%) | 1421 (4.2%) | |
| Current smoker >1 pack per day | 1584 (4.7%) | 1082 (3.2%) | 890 (2.6%) | |
| Current smoker intensity unknown | 11 (0.0%) | 10 (0.0%) | 6 (0.0%) | |
| Missing | 3 (0.0%) | 3 (0.0%) | 7 (0.0%) | |
| Education (n, %) | <0.001 | |||
| ≤High school | 15 659 (46.1%) | 14 021 (41.4%) | 13 248 (39.1%) | |
| ≥Some college | 18 207 (53.6%) | 19 812 (58.5%) | 20 577 (60.7%) | |
| Missing | 75 (0.2%) | 51 (0.2%) | 71 (0.2%) | |
| BMI (n, %) | 0.7406 | |||
| <25.0 kg/m2 | 11 282 (33.2%) | 11 227 (33.1%) | 11 230 (33.1%) | |
| ≥25.0 kg/m2 | 22 192 (65.4%) | 22 229 (65.6%) | 22 227 (65.6%) | |
| Missing | 467 (1.4%) | 428 (1.3%) | 439 (1.3%) | |
| Race (n, %) | <0.001 | |||
| White, Non-Hispanic | 30 459 (89.7%) | 31 230 (92.2%) | 30 814 (90.9%) | |
| Other | 3472 (10.2%) | 2642 (7.8%) | 3067 (9.0%) | |
| Missing | 10 (0.0%) | 12 (0.0%) | 15 (0.0%) | |
| Alcohol drinking status (n, %) | <0.001 | |||
| Never | 3428 (10.1%) | 3274 (9.7%) | 3411 (10.1%) | |
| Former | 4906 (14.5%) | 4742 (14.0%) | 5107 (15.1%) | |
| Current | 24 616 (72.5%) | 24 946 (73.6%) | 24 410 (72.0%) | |
| Missing | 991 (2.9%) | 922 (2.7%) | 968 (2.9%) | |
| Total energy (kcal/day), mean ± SD | 1212.56 ± 422.13 | 1676.82 ± 482.36 | 2327.11 ± 767.52 | <0.001 |
| Control arm (n, %) | 16 839 (49.6%) | 16 615 (49.0%) | 16 463 (48.6%) | 0.025 |
| Marital status (n, %) | <0.001 | |||
| Married | 25 613 (75.5%) | 26 942 (79.5%) | 27 056 (79.8%) | |
| Not married | 8264 (24.3%) | 6886 (20.3%) | 6774 (20.0%) | |
| Missing | 64 (0.2%) | 56 (0.2%) | 66 (0.2%) | |
| Family history of any cancer (n, %) | 18 938 (56.0%) | 19 030 (56.3%) | 18 870 (55.8%) | 0.419 |
BMI, body mass index; PLCO, prostate, lung, colorectal and ovarian; SD, standard deviation.
The total dietary fiber intake was firstly examined as tertiles. Participants in the 2nd and 3rd tertile groups had a multi-adjusted HR (95% CI) of 0.89 (0.74–1.07) and 0.83 (0.66–1.04), respectively, when compared with participants of the 1st tertile group (Table 2). There was no significant trend across tertiles (P for trend = 0.098). Additionally, when total fiber intake was treated as a continuous variable using a restricted cubic spline model, a reduced but not statistically significant bladder cancer risk was observed as dietary fiber consumption increased (Figure 1). There is no interaction between total fiber intake and education, body mass index and smoking status (Supplemental Table S3, available at Carcinogenesis Online, all P > 0.05).
Table 2.
Fiber intake and the risk of bladder cancer in the PLCO cohort
| Nutrients | Range (g/day) | Mean (g/day) | Cohort | Cases | Incidence rate (95% CI)a | Age-adjusted HR (95% CI), P-value | Multi-adjusted HR (95% CI),bP-value |
|---|---|---|---|---|---|---|---|
| Total fiber | |||||||
| Q1 | <13.57 | 10.06 | 33 941 | 269 | 6.96 (6.18–7.85) | Reference group | Reference group |
| Q2 | ≥13.57 to <20.01 | 16.62 | 33 884 | 252 | 6.46 (5.71–7.31) | 0.92 (0.77–1.09), P = 0.335 | 0.89 (0.74–1.07), P = 0.225 |
| Q3 | ≥ 20.01 | 27.41 | 33 896 | 255 | 6.52 (5.77–7.37) | 0.93 (0.78–1.10), P = 0.380 | 0.83 (0.66–1.04), P = 0.101 |
| P for trend = 0.378 | P for trend = 0.098 | ||||||
| Insoluble fiber | |||||||
| Q1 | <8.86 | 6.51 | 33 931 | 272 | 7.05 (6.26–7.94) | Reference group | Reference group |
| Q2 | ≥8.86 to <13.19 | 10.90 | 33 918 | 251 | 6.43 (5.68–7.28) | 0.90 (0.76–1.07), P = 0.247 | 0.89 (0.74–1.06), P = 0.199 |
| Q3 | ≥13.19 | 18.16 | 33 872 | 253 | 6.47 (5.72–7.32) | 0.91 (0.76–1.08), P = 0.261 | 0.83 (0.67–1.03), P = 0.095 |
| P for trend = 0.259 | P for trend = 0.092 | ||||||
| Soluble fiber | |||||||
| Q1 | <4.54 | 3.37 | 33 955 | 269 | 6.95 (6.17–7.83) | Reference group | Reference group |
| Q2 | ≥4.54 to <6.68 | 5.55 | 33 987 | 245 | 6.26 (5.53–7.10) | 0.89 (0.75–1.06), P = 0.197 | 0.86 (0.72–1.04), P = 0.114 |
| Q3 | ≥6.68 | 9.19 | 33 779 | 262 | 6.73 (5.96–7.60) | 0.96 (0.81–1.14), P = 0.655 | 0.86 (0.68–1.08), P = 0.184 |
| P for trend = 0.653 | P for trend = 0.168 |
aPer 10 000 person-years.
bAdjusted for age (categorical), sex (male versus female), race (White, Non-Hispanic versus Other), body mass index at the time of enrollment (<25 kg/m2 versus ≥25 kg/m2), education (≤high school versus ≥some college), smoking status (never versus former ≤ 15 years since quit versus former >15 years since quit versus former year since quit unknown versus current smoker ≤1 pack per day versus current smoker >1 pack per day versus current smoker intensity unknown), alcohol drinking status (never versus former versus current), total energy intake (continuous), randomization arm (intervention versus control), family history of any cancer (yes versus no) and marital status (married versus not married).
Figure 1.
Dose–response using restricted cubic spline model for the association between total fiber intake and bladder cancer risk in PLCO cohort. Solid line represents point estimates and dashed lines represent 95% CIs. Multivariable risk estimate was calculated by restricted cubic spline regression (using three knots at 10th, 50th and 90th percentiles) adjusting for age (categorical), sex (male versus female), race (White, Non-Hispanic versus Other), body mass index at the time of enrollment (<25 kg/m2 versus ≥25 kg/m2), education (≤high school versus ≥some college), smoking status (never versus former ≤15 years since quit versus former >15 years since quit versus former year since quit unknown versus current smoker ≤1 pack per day versus current smoker >1 pack per day versus current smoker intensity unknown), alcohol drinking status (never versus former versus current), total energy intake (continuous), randomization arm (intervention versus control), family history of any cancer (yes versus no) and marital status (married versus not married). The histograms show the percentage of participants (left y-axis) consuming each level of fiber.
We then examined the association between fiber intake and bladder cancer risk by types of fiber. For insoluble fiber intake, participants in the 2nd and 3rd tertile groups had a multi-adjusted HR (95% CI) of 0.89 (0.74–1.06) and 0.83 (0.67–1.03), respectively, when compared with participants of the 1st tertile group (Table 2). There was no significant trend across tertiles (P for trend = 0.092). Similarly, soluble fiber intake was also not significantly associated with the risk of bladder cancer. Participants within the 2nd and 3rd tertile had an HR of 0.86 (0.72–1.04) and 0.86 (0.68–1.08), respectively (P for trend = 0.168). Finally, we examined the association between fiber intake and bladder cancer risk by gender. No significant association with bladder cancer risk was observed for total fiber intake in men (HR Q3 versus Q1 = 0.89, 95% CI 0.68–1.16; P for trend = 0.322) or in women (HR Q3 versus Q1 = 0.95, 95% CI 0.56–1.60; P for trend = 0.811) after adjusting for potential confounders (Supplemental Table S4, available at Carcinogenesis Online).
Discussion
After adjusting for age, race, smoking and other well-known bladder cancer risk factors, there was no obvious evidence that participants with higher intake of dietary fiber may have a lower risk of bladder cancer compared with those with the lower fiber intake in PLCO study.
To date, only two prospective cohorts and one case–control study have assessed the association between fiber consumption and bladder cancer risk. The Multiethnic Cohort Study (7) observed a total of 581 invasive bladder cancer cases from a cohort of 185 885 participants after a 12.5-year follow-up. An inverse association of total fiber intake with bladder cancer risk was found among women with a borderline significant trend [highest versus lowest quintile: 0.50 (0.26, 0.97), P for trend = 0.07] but not among men [highest versus lowest quintile: 0.89 (0.61, 1.30), P for trend = 0.58]. The European Prospective Investigation into Cancer and Nutrition (8) was the largest prospective cohort study, including 1416 newly diagnosed urothelial cell carcinoma from a cohort of 469 339 men and women over an average 11.3-year of follow-up. The EPIC found a suggestive but not significant inverse association between total fiber intake and bladder cancer risk [highest versus lowest quintile: 0.84 (0.68–1.04), P for trend = 0.12]. The only case–control study (13) conducted in Spain included 432 male cases and 792 matched controls. No significant association was observed between total fiber intake and the risk of bladder cancer [highest versus lowest: 1.01 (0.69–1.48), P for trend = 0.68]. Our study was the third cohort on this topic and we also failed to find a significant association between fiber intake and bladder cancer risk.
Several biological mechanisms have been proposed to support the protective effect of fiber intake on bladder cancer risk. Higher intake of dietary fiber may protect against carcinogenesis by stabilizing blood sugar and lowering insulin levels, which in turn reduces inflammatory biomarkers, and oxidative stress and improves insulin resistance and metabolic regulation (14–16). Our previous studies have shown that diabetes (17) and obesity (18) are significantly associated with the risk of bladder cancer. Additionally, bladder cancer is a highly immunogenic malignancy. Tumor-induced release of excessive amount of proinflammatory cytokines will lead to an ‘inflammatory storm’, which promote the tumorigenicity and metastasis of bladder cancer (19). Emerging evidence has indicated that inflammatory pathways represent potential therapeutic targets to improve the efficacy of chemotherapy agents for bladder cancer (20).
The consumption of dietary fiber is still insufficient worldwide. A study by Garcia-Meseguer et al. (21) investigated the fiber patterns in youngsters from three different counties (USA, Spain and Tunisia). They found that the mean dietary fiber intake was only 17.8 g/day, which was not adequate. Nakaji et al. (22) reported a decline in total dietary fiber intake in Japan using data compiled in the Japanese National Nutrition Survey. Similarly, Casagrande et al. (23) found that fiber intake significantly decreased and remained below recommendations among adults with type 2 diabetes based on the data of National Health and Nutrition Examination Surveys 1988–2012. In our study, the median dietary fiber intake of the total cohort was 16.5 g/day. According to estimates, 6.0% of colorectal cancers or 0.7% of all cancers in Alberta in 2012 can be attributed to insufficient intake of fiber (24).
A unique strength of this study was that the amount of fiber intake was also examined continuously using the cubic spline regression model, which provided more granular information and identified the relationship shape between fiber intake and bladder cancer risk. Additionally, our study has some other strengths. PLCO cohort was a large prospective study and thus avoided the possibility of selection bias and recall bias. Various known confounders associated with fiber intake and bladder cancer risk were adjusted in the multi-analysis, including sex, body mass index, education, smoking status, alcohol drinking status and total energy intake.
This study also has several limitations. First, the exposure was relied on self-reported dietary data, which potentially introduced misclassifications in the assessment of fiber intake. In the present study, misclassification can lead to bias the results in either direction, toward exaggeration or underestimation of the risk estimates. However, food frequency questionnaire used in PLCO study has exhibited acceptable reproducibility and validity for assessing intake of various dietary factors (25,26). Second, the diet assessment in this study was performed at baseline and dietary patterns could change over a 12.5-year follow-up period. As participants are able to enhance or reduce their fiber intake, any dietary changes that occur after the food frequency questionnaire investigations would be expected to attenuate any observed associations. Third, people who eat more fibers have probably a different dietary pattern in many aspects (e.g. meat consumption) and probably even a healthier lifestyle in general, which may distort the real association. Finally, main sources of dietary fiber were cereal/grain, vegetables, fruit and legumes in PLCO study (11). Our study focused on total fiber intake, which represents a heterogeneous group of dietary components and thus may introduce some bias.
In summary, the findings of this study show that there is no obvious evidence for a link between dietary fiber consumption and bladder cancer risk. Further prospective studies are warranted to confirm these findings.
Supplementary Material
Acknowledgements
The authors thank the National Cancer Institute for access to NCI’s data collected by the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial. The statements contained herein are solely those of the authors and do not represent or imply concurrence or endorsement by NCI.
Glossary
Abbreviations
- CI
confidence interval
- HR
hazard ratio
- PLCO
Prostate, Lung, Colorectal and Ovarian
Conflict of Interest Statement: None declared.
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