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Yongye Sun, †a,b Jianping Sun,†c Peipei Zhang,a Feng Zhong,a Jing Caia and
Aiguo Ma *a
Current evidence on the relationship between dietary fiber intake and risk of hyperuricemia is limited. The
aim of the present study was to examine their associations in the U.S. general adult population. Data from
the National Health and Nutrition Examination Survey (NHANES) 2009 to 2014 were used. Dietary fiber
intake was extracted through two 24 h dietary recall interviews. Hyperuricemia was defined by cut-off
values of 7.0 mg dL−1 for men and 6.0 mg dL−1 for women. Multivariable logistic regression models and
restricted cubic spline models were applied to explore the associations between dietary intakes of total,
cereal, fruit and vegetable fiber and the risk of hyperuricemia. A total of 12 869 participants aged 20 years
or older were included in the present study. The multivariable odds ratio (OR) and 95% confidence interval
(CI) of hyperuricemia for the highest vs. lowest quartile intake of total fiber were 0.58 (0.46–0.74), 0.61
(0.52–0.74) for cereal fiber, 0.94 (0.76–1.16) for fruit fiber and 0.95 (0.76–1.18) for vegetable fiber. The
inverse associations between dietary intakes of total fiber and cereal fiber and the risk of hyperuricemia
were observed in men. In stratified analysis by age (<45 years, ≥45 years), the inverse association between
total fiber intake and the risk of hyperuricemia was consistent, while cereal fiber intake was only inversely
Received 30th September 2018, associated with hyperuricemia among participants <45 years old. Dose–response analyses showed that
Accepted 4th July 2019
the risk of hyperuricemia was associated with dietary intake of total fiber in a nonlinear manner, whereas
DOI: 10.1039/c8fo01917g the relationship was linear for cereal fiber intake. In conclusion, dietary intakes of total fiber and cereal
rsc.li/food-function fiber were inversely associated with the risk of hyperuricemia in the U.S. adult population.
Methods
Study population for Dietary Studies (FNDDS 2009–2010, 2011–2012 and
Cross-sectional study data from 3 cycles of NHANES (2009–2010, 2013–2014).33 Average dietary fiber intakes from the two 24 h
2011–2012 and 2013–2014) were combined for analyses. The recalls were used if an individual completed both 24 h recalls.
response rates were 79.4%, 72.6% and 71.0% for the interviewed Otherwise, we used the single dietary recall data.34 Among all
sample and 77.3%, 69.5% and 68.5% for the examined sample participants, 99.68% completed both the 24 h recalls. Different
for 2009–2010, 2011–2012 and 2013–2014, respectively. The sources of dietary fiber intake were identified by food codes.
2009–2014 NHANES included 30 468 participants, and our ana-
lyses were limited to 17 547 participants aged 20 years or older. Study covariates
We excluded pregnant women (n = 149) and individuals who did Based on the previous literature, factors that had been proved
not provide dietary fiber intake information and those with to be correlated with hyperuricemia and intake of dietary fiber
missing uric acid information (n = 2762). Participants with unreli- were included in regression models to control for potential
able or incomplete dietary recall data (n = 1629) were also confoundings. Demographic characteristics included age
excluded. In addition, individuals whose total daily energy (20–44 y, 45–59 y, 60–74 y, and ≥75 y), sex, race (Mexican
intakes > mean + 3SD (4630 kcal) or <mean − 3SD (0 kcal) were American, other Hispanic, non-Hispanic White, non-Hispanic
excluded (n = 138). Finally, 12 869 individuals (6158 men and Black, and other race), and educational level (lower than high
6711 women) were included in our analysis (Fig. 1). school, high school diploma, and higher than high school).
Other covariates included body mass index (BMI), total energy
Serum uric acid measurement intake, smoking status (smoking at least 100 cigarettes in life
The key outcome of interest was the serum uric acid concen- or not), alcohol consumption status (having at least 12 alcohol
tration which was detected on a Beckman Synchron LX20 or drinks per year or not), vigorous recreational activity, diabetes
Beckman UniCel® DxC800 Synchron after oxidization with the status (yes or no), and hypertension status (yes or no).
specific enzyme uricase to form allantoin and H2O2. Diabetes was defined as the fasting plasma glucose level
Hyperuricemia was defined by the cut-off values of 7.0 mg dL−1 ≥7.0 mmol L−1, or the 2 h plasma glucose level (OGTT)
for men and 6.0 mg dL−1 for women.32 ≥11.1 mmol L−1, or the glycohemoglobin level ≥6.5%, or
taking diabetes pills or insulin, or self-report diabetes
Dietary fiber intake diagnosis.20,35 Hypertension was defined as the mean systolic
The data of dietary fiber intakes were obtained through two blood pressure ≥130 mm Hg, or the mean diastolic blood
24 h dietary recall interviews. The first dietary recall interview pressure ≥80 mm Hg, or self-report hypertension diagnosis.36
was conducted in person in the mobile examination center, and
the second interview was conducted via telephone 3 to 10 days Statistical analysis
later. Dietary fiber intakes were calculated according to the US Statistical analyses were conducted using Stata 15.0 to account
Department of Agriculture (USDA) Food and Nutrient Database for the complex sampling design. To perform a nationally
Table 1 Baseline characteristics of the participants by hyperuricemia, U.S. adults aged ≥20 years, NHANES 2009–2014
Number of participants (%) 10 257 (80.65%) 2612 (19.35%) 4761 (77.68%) 1397 (22.32%) 5496 (83.33%) 1215 (16.67%)
Age group (n, %) <0.001 0.044 <0.001
20–44 years 4514 (83.8%) 832 (16.20%) 1971 (76.25%) 584 (23.75%) 2543 (83.89%) 248 (8.92%)
45–59 years 2669 (81.86%) 616 (18.14%) 1221 (79.57%) 318 (20.43%) 1448 (83.89%) 298 (16.11%)
60–74 years 2196 (76.04%) 743 (23.96%) 1098 (79.09%) 315 (20.91%) 1098 (73.39%) 428 (26.61%)
≥75 years 878 (69.53%) 421 (30.47%) 471 (75.04%) 180 (24.96%) 407 (65.34%) 241 (34.66%)
Race (n, %) <0.001 0.006 <0.001
Mexican American 1545 (86.75%) 244 (13.25%) 724 (82.28%) 155 (17.72%) 821 (91.59%) 89 (8.41%)
Other Hispanic 1054 (86.25%) 183 (13.75%) 442 (81.72%) 102 (18.28%) 612 (90.18%) 81 (9.82%)
Non-Hispanic White 4607 (79.97%) 1265 (20.03%) 2166 (77.15%) 673 (22.85%) 2441 (82.55%) 592 (17.45%)
Non-Hispanic Black 1949 (77.26%) 648 (22.74%) 909 (76.31%) 305 (23.69%) 1040 (77.96%) 343 (22.04%)
Other race 1102 (80.89%) 272 (19.11%) 520 (75.75%) 162 (24.25%) 582 (85.71%) 110 (14.29%)
BMI, body mass index; TC, total cholesterol; HDL, high density lipoprotein cholesterol. Data are presented as mean ± standard deviation (SD) for continuous variables or participants
(percentage) for categorical variables.
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representative estimate, appropriate sampling weights, and 95% confidence interval (CI) were calculated from logistic
primary sampling unit, and strata information were con- regression models. Dose–response relationship was evaluated by
sidered in our analyses. Following the NHANES analytical using restricted cubic spline functions with three knots located
guidelines,37 2-year sample weights for NHANES 2009–2010, at the 5th, 50th, and 95th percentiles of the exposure distribution
2011–2012 and 2013–2014 are provided on public-use files. To in the multivariate-adjusted model 2. All p-values were two-sided,
combine these cycles to produce 6-year estimates, a new 6-year and p ≤ 0.05 indicated statistical significance.
weights can be calculated by dividing the 2-year weights by
3 (the number of 2-year cycles). The detailed command to
create new weights is available in https://wwwn.cdc.gov/nchs/ Results
nhanes/tutorials/module3.aspx. The approach to get weighted
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Table 2 Weighted ORs and 95% CIs for hyperuricemia according to the quartiles of dietary fiber intake
CI, confidence interval; OR, odds ratio. Model 1 adjusted for age and gender. Model 2 adjusted for age, gender, race, BMI, educational level,
smoking status, alcohol consumption, daily total energy intake, hypertension, diabetes, physical activity, TC and HDL. The lowest quartile of
dietary fiber intake was used as the reference group. Results are survey-weighted. * p < 0.05; ** p < 0.01.
the results were similar to the crude ORs (95% CIs). Further the highest vs. lowest quartile, the OR of hyperuricemia was
adjustment for race, BMI, educational level, smoking status, 0.52 (0.38–0.72) for total fiber intake and 0.52 (0.41–0.67) for
alcohol consumption, recreational activity, daily total energy cereal fiber intake in multivariate analysis (model 2) for men.
intake, hypertension, diabetes, TC and HDL (model 2), total and For women, after adjustment for multiple covariates, com-
cereal fiber intakes were inversely associated with the risk of pared with quartile 1, the ORs of hyperuricemia for quartile 2,
hyperuricemia, whereas the association of fruit fiber intake with quartile 3 and quartile 4 of total fiber intake were 0.82
hyperuricemia was no longer statistically significant. The corres- (0.67–1.01), 0.73 (0.59–0.91) and 0.77 (0.55–1.07), respectively.
ponding ORs (95% CI) of hyperuricemia for quartile 4 of total, However, no significant association was found between cereal
cereal and fruit fiber intake were 0.58 (0.46–0.74), 0.61 (0.52–0.74), fiber intake across quartiles 2 to 4 compared with quartile 1.
0.94 (0.76–1.16), respectively. However, no significant association In the stratified analyses by age, for participants younger than
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was observed between vegetable fiber intake and the risk of hyper- 45 years old, the OR (95% CI) of hyperuricemia was 0.53
uricemia with or without adjustment for confounders. (0.35–0.79) for total fiber intake and 0.45 (0.33–0.62) for cereal
We also conducted analyses for relationship between fiber intake for the highest quartile versus lowest quartile in
dietary fiber intake and hyperuricemia risk stratified by sex multivariate analysis, and the corresponding results were 0.68
(Table 3) and age (Table 4). In the stratified analyses by sex, for (0.48–0.97) and 0.78 (0.61–1.00) for subjects aged 45+ years.
Table 3 Weighted ORs and 95% CIs for hyperuricemia according to the quartiles of dietary fiber intake, stratified by gender
Male
Total fiber (g d−1)
<11.65 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
11.65 to <16.80 0.76 (0.60–0.97)* 0.76 (0.60–0.97)* 0.73 (0.55–0.97)*
16.80 to <23.71 0.62 (0.50–0.76)** 0.63 (0.51–0.77)** 0.63 (0.48–0.83)**
≥23.71 0.48 (0.39–0.60)** 0.49 (0.39–0.61)** 0.52 (0.38–0.72)**
Cereal fiber (g d−1)
<4.35 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
4.35 to <7.40 0.74 (0.59–0.91)** 0.74 (0.60–0.92)** 0.71 (0.55–0.91)**
7.40 to <11.45 0.74 (0.61–0.91)** 0.75 (0.61–0.91)** 0.78 (0.62–0.98)*
≥11.45 0.51 (0.40–0.65)** 0.50 (0.39–0.65)** 0.52 (0.41–0.67)**
Fruit fiber (g d−1)
<1.05 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
1.05 to <2.43 1.11 (0.84–1.47) 1.11 (0.83–1.47) 1.08 (0.80–1.45)
2.43 to <4.65 0.78 (0.63–0.98) * 0.79 (0.63–0.98)* 0.85 (0.66–1.11)
≥4.65 0.91 (0.70–1.18) 0.92 (0.71–1.19) 1.09 (0.83–1.43)
Vegetable fiber (g d−1)
<1.45 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
1.45 to <2.95 0.91 (0.70–1.18) 0.91 (0.70–1.18) 0.90 (0.68–1.19)
2.95 to <4.95 1.02 (0.80–1.30) 1.03 (0.81–1.31) 1.03 (0.79–1.34)
≥4.95 0.93 (0.74–1.17) 0.94 (0.75–1.19) 0.93 (0.71–1.21)
Female
Total fiber (g d−1)
<10.10 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
10.10 to <14.15 0.81 (0.68–0.96) 0.74 (0.62–0.88) 0.82 (0.67–1.01)
14.15 to <19.50 0.63 (0.52–0.76) 0.58 (0.47–0.70) 0.73 (0.59–0.91)*
≥19.50 0.56 (0.42–0.75) 0.51 (0.37–0.69) 0.77 (0.55–1.07)
Cereal fiber (g d−1)
<3.60 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
3.60 to <5.75 0.91 (0.72–1.15) 0.89 (0.70–1.15) 0.96 (0.74–1.26)
5.75 to <8.75 0.78 (0.61–0.99)* 0.77 (0.60–0.98)* 0.90 (0.68–1.19)
≥8.75 0.56 (0.43–0.72)** 0.59 (0.45–0.77)** 0.80 (0.60–1.07)
Fruit fiber (g d−1)
<1.10 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
1.10 to <2.35 1.03 (0.81–1.32) 0.94 (0.73–1.22) 0.98 (0.76–1.26)
2.35 to <4.29 0.99 (0.75–1.29) 0.84 (0.64–1.10) 0.89 (0.67–1.17)
≥4.29 0.70 (0.51–0.97)* 0.58 (0.41–0.83)** 0.79 (0.54–1.15)
Vegetable fiber (g d−1)
<1.40
1.40 to <2.70 1.16 (0.91–1.47) 1.10 (0.85–1.44) 0.99 (0.74–1.33)
2.70 to <4.50 1.18 (0.92–1.50) 1.08 (0.84–1.39) 1.08 (0.80–1.44)
≥4.50 1.04 (0.84–1.28) 0.91 (0.74–1.12) 1.03 (0.77–1.36)
CI, confidence interval; OR, odds ratio. Model 1 adjusted for age. Model 2 adjusted for age, race, BMI, educational level, smoking status, alcohol
consumption, daily total energy intake, hypertension, diabetes, physical activity, TC and HDL. The lowest quartile of dietary fiber intake was
used as the reference group. Results are survey-weighted. * p < 0.05; ** p < 0.01.
Table 4 Weighted ORs and 95% CIs for hyperuricemia according to the quartiles of dietary fiber intake, stratified by age
<45 years
Total fiber (g d−1)
<10.75 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
10.75 to <15.30 0.90 (0.71–1.13) 0.81 (0.64–1.03) 0.79 (0.61–1.03)
15.30 to <21.50 0.68 (0.52–0.90)** 0.60 (0.45–0.80)** 0.61 (0.44–0.85)**
≥21.50 0.68 (0.51–0.92)* 0.50 (0.37–0.69)** 0.53 (0.35–0.79)**
Cereal fiber (g d−1)
<3.90 1.00 (ref.) 1.00 (ref.) 1.00 (ref.)
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CI, confidence interval; OR, odds ratio. Model 1 adjusted for gender. Model 2 adjusted for gender, race, BMI, educational level, smoking status,
alcohol consumption, daily total energy intake, hypertension, diabetes, physical activity, TC and HDL. The lowest quartile of dietary fiber intake
was used as the reference group. Results are survey-weighted. * p < 0.05; ** p < 0.01.
In the restricted cubic spline model, a nonlinear inverse hyperuricemia, we did not analyse the dose–response relation-
association ( pfor nonlinearity < 0.01) between total dietary fiber ship between fruit and vegetable fiber and the risk of
intake and hyperuricemia was detected (Fig. 2). The risk of hyperuricemia.
hyperuricemia dropped with an increasing intake of total fiber
and reached a plateau approximately at 27 g d−1 (OR: 0.4; 95%
CI: 0.29–0.56). Discussion
The dose–response relationship between cereal fiber intake
and hyperuricemia is shown in Fig. 3. Cereal fiber intake was In the large sample, nationally representative cross-sectional
inversely associated with the risk of hyperuricemia in a linear study, we explored the relationship between dietary fiber
manner ( pfor nonlinearity = 0.71). The OR of hyperuricemia intake and the risk of hyperuricemia. After adjustment for
decreased as cereal fiber intake increased. Cereal fiber showed multiple potential confounders (age, sex, BMI, race, edu-
significantly protective effects on hyperuricemia when intake cational level, smoking status, alcohol consumption, total
of cereal fiber reached 8 g d−1 (OR: 0.78; 95% CI: 0.61–0.99). energy intake, physical activity, hypertension, diabetes, TC and
Because no significant associations were observed among HDL), total dietary fiber intake was inversely associated with
dietary intakes of fruit and vegetable fiber and the risk of the risk of hyperuricemia in general U.S. adults. When strati-
different sources of fiber and the risk of hyperuricemia. Examination Survey, J. Am. Med. Assoc., 2000, 283, 2404–
Moreover, the association between various sources of dietary 2410.
fiber intake and hyperuricemia was examined for the first time. 7 T. Mehta, E. Nuccio, K. McFann, M. Madero, M. J. Sarnak
However, our study has some limitations to acknowledge. and D. Jalal, Association of Uric Acid With Vascular
First, this is a cross-sectional study which is difficult to make Stiffness in the Framingham Heart Study, Am. J. Hypertens.,
causal inference, and prospective longitudinal studies and 2015, 28, 877–883.
trials are needed to establish a causal association between 8 M. E. Kleber, G. Delgado, T. B. Grammer, G. Silbernagel,
dietary fiber intake and hyperuricemia. Second, dietary data J. Huang, B. K. Kramer, E. Ritz and W. Marz, Uric Acid and
were calculated by the average of two 24 h recalls. Although Cardiovascular Events: A Mendelian Randomization Study,
the data of the two dietary recalls were significantly correlated, J. Am. Soc. Nephrol., 2015, 26, 2831–2838.
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they might be influenced by recall bias and cannot represent 9 D. H. Kang, T. Nakagawa, L. Feng, S. Watanabe, L. Han,
an individual’s usual intake. In addition, there may be residual M. Mazzali, L. Truong, R. Harris and R. J. Johnson, A role
confusion caused by incomplete adjustment for dietary for uric acid in the progression of renal disease, J. Am. Soc.
factors. Nephrol., 2002, 13, 2888–2897.
10 C. Borghi, E. A. Rosei, T. Bardin, J. Dawson, A. Dominiczak,
J. T. Kielstein, A. J. Manolis, F. Perez-Ruiz and G. Mancia,
Conclusions Serum uric acid and the risk of cardiovascular and renal
disease, J. Hypertens., 2015, 33, 1729–1741; discussion
In conclusion, intakes of total and cereal fiber were inversely 1741.
associated with the risk of hyperuricemia in the U.S. general 11 Y. Zhu, B. J. Pandya and H. K. Choi, Prevalence of gout and
adult population. hyperuricemia in the US general population: the National
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Conflicts of interest 12 G. Trifiro, P. Morabito, L. Cavagna, C. Ferrajolo,
S. Pecchioli, M. Simonetti, E. Bianchini, G. Medea,
The authors declare no conflicts of interest.
C. Cricelli, A. P. Caputi and G. Mazzaglia, Epidemiology of
gout and hyperuricaemia in Italy during the years
2005–2009: a nationwide population-based study, Ann.
Acknowledgements Rheum. Dis., 2013, 72, 694–700.
This work was supported by the grant from the Natural 13 S. Guan, Z. Tang, X. Fang, X. Wu, H. Liu, C. Wang and
Science Foundation of China [No. 81703206] and China C. Hou, Prevalence of hyperuricemia among Beijing post-
Postdoctoral Science Foundation [No. 2017M622146]. menopausal women in 10 years, Arch. Gerontol. Geriatr.,
2016, 64, 162–166.
14 J. G. Puig, M. A. Martinez, M. Mora, J. M. Fraile,
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