Abstract
Introduction. This study was conducted to examine the relationship between dietary intake and the risk of chronic kidney disease (CKD), treated hyperuricemia (or gout) without CKD, and untreated hyperuricemia without CKD in elderly men.
Methods. The study population comprised 752 men aged 65 or older who had been included in the Elderly Nutrition and Health Survey (1999–2000) (Elderly NAHSIT).
Results. Statistical analysis using a polychotomous logistic regression model revealed that compared with the individuals in the normouricemic group, the individuals in the other groups exhibited a significant association between a higher prevalence of CKD and the following factors: advanced age, drug use for hypertension, egg and shellfish consumption and consumption of poultry with the skin and meat with fat. The significant risk factors for the patients who did not have CKD and were undergoing treatment for hyperuricemia were as follows: BMI ≥ 25 kg/m2; drug use for hypertension; intake of poultry with skin; increased daily consumption of shellfish, fried food, sugar and juice.
Conclusions. Men who use anti-hypertensive drugs and who consume fewer soy products and more shellfish may be at a higher risk of developing hyperuricemia or CKD.
Introduction
Chronic kidney disease (CKD) and associated comorbidities are progressive conditions with increasing incidences and prevalence rates [Citation1–5], and CKD has been identified as an early warning sign for end-stage renal disease [Citation6], cardiovascular events [Citation7–10] and death [Citation9–11]. The relationship between CKD and serum uric acid (SUA) has been investigated, including the effect of hyperuricemia on the estimated glomerular filtration rate (eGFR) and incident CKD [Citation12–20]. Researchers have conducted studies on hyperuricemic patients who had CKD and were receiving treatment for hyperuricemia and found that treatment did indeed reduce the proportion of requirement for renal dialysis and played a role in the management of CKD [Citation21–23]. These researchers considered that hyperuricemia could play a pathogenic role in kidney disease progression rather than merely being a marker for incident CKD. Many studies have been conducted on the influence of a multi-factorial diet on SUA, hyperuricemia and gout [Citation24–30]. With regard to CKD, many authors have focused on the effect of energy/protein and specific foods rather than a multi-factorial diet; fewer studies have addressed the influence of a multi-factorial diet on hyperuricemia, gout and CKD.
The purpose of this study was to demonstrate the differences between the dietary and clinical characteristics of elderly Taiwanese men with CKD, treated hyperuricemia or gout, untreated hyperuricemia, or normouricemia. Instead of taking the energy/protein approach, we examined the effect of diet in four groups that had been formed on the basis of SUA-related conditions. In the present work, the role of the protein source, purine-rich food, vegetables, preserved vegetables, drinks, snacks, sugar, fried/fermented foods, and special dietary intake in relation to the risk of hyperuricemia (with or without treatment), gout and CKD was examined. Moreover, possible changes in diet were discussed by comparing the self-reported intake of certain foods by subjects in the four groups formed on the basis of SUA-related conditions.
Methods
Study population
The Elderly Nutrition and Health Survey (1999–2000) (Elderly NAHSIT) [Citation31], a cross-sectional study, targeted persons aged 65 and older and was conducted to investigate the diet, nutrition and health status of eligible subjects in this age group, who had registered for 6 months or more in Taiwan as of January 1, 1999. Detailed household data were obtained from the 1998 Ministry of the Interior's Household Data Registry. A multistage stratified sampling design with probability proportional to sizes (PPS) was adopted to randomly select the sampling units at each stage. With regard to the ethnicity, locality, and population density, the main strata were defined as the first-stage sampling units and included the ‘Hakka areas’, ‘Mountain areas’, ‘Eastern areas’, ‘PengHu Island’, ‘Northern areas’, ‘Central areas’ and ‘Southern areas’. The last three strata were further divided into three substrata as the second-stage sampling units. Among the total 13 strata, the PPS method was applied again to sample of total 39 townships/districts. On the basis of the same principle, two villages (street blocks) were selected from each selected township or district. After the first household was selected, the houses and the apartments located nearby were included in the target list. The household interviews were not limited to the registered residents; persons who did not qualify for this selected stratum but had been residing for 6 months or more in Taiwan also were likely to be selected. The interview process was terminated when the target of 26 elderly persons from each of the 78 selected villages was achieved.
A total of 1937 elderly individuals from 78 villages completed the questionnaires, and 2432 participants underwent physical examination. After adjusting for age and gender strata, the overall response rates for household interviews and physical examination were 55.2% and 52.8%, respectively. A total of 1473 subjects, including 752 men and 721 women, completed both the questionnaire survey and the physical examination. For the purpose of the present study, the men were selected for further analysis.
Outcomes
In order of increasing severity, four groups were defined on the basis of SUA-related conditions, (1) normouricemic group, (2) untreated hyperuricemic subjects without CKD (untreated hyperuricemic group), (3) treated hyperuricemic subjects without CKD and (4) the CKD group. The CKD group included individuals whose eGFR was <60 ml/min/1.73 m2 or who were taking prescription medicines for kidney disease at the time of the study. The eGFR calculation was based on the modification of diet in renal disease study equation [Citation32,Citation33]
where SCr is the serum creatinine concentration (mg/dl) and the age has been represented in years. The CKD stage classification was defined by the eGFR levels: individuals with high eGFR values were assigned to the advanced stages. The eGFR levels of the subjects at Stages I, II, III, IV and V were >90, 60–89, 30–59, 15–29 and <15 ml/min/1.73 m2, respectively. The treated hyperuricemic group comprised participants who did not have CKD but who were undergoing treatment for hyperuricemia at the time of the study (SUA level >7 mg/dl) or had taken drugs for gout within the previous month [Citation24,Citation34–37]. The untreated hyperuricemic group included participants who did not have CKD but had hyperuricemia for which they had not been treated within the previous month. The normouricemic group comprised subjects who had neither CKD nor hyperuricemia.
Measurements
The Elderly NAHSIT included physical examination and a structured interview questionnaire. In this study, the physical and the laboratory examination data, which included that for body measurements, blood pressure and blood samples, were assessed [Citation31]. The interview questionnaire contained several sections: personal information; dietary habits; history of underlying disease; nutrition-related knowledge, attitudes and behaviours.
Physical examination included blood pressure measurement and body measurements, i.e. height (HT), body weight (BW) and waist circumference (WC) measurement. After the subjects had rested for at least 5 min, the arterial blood pressure was measured thrice. Each measurement was separated by a 30-s interval. If the difference between the second and the third measurements of systolic blood pressure (SBP) or diastolic blood pressure (DBP) was ≥ 10 mm Hg, a fourth measurement was recorded. The mean value of these measurements was used for further statistical analysis. After the subjects had fasted for at least 8 h, venous blood samples were collected, processed and transported to a laboratory at Academia Sinica, a national academic institution in Taiwan, and then stored at –70°C for downstream analysis. The blood samples were analysed for fasting plasma glucose (FPG), triglyceride (TG), total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), SUA and serum creatinine levels. History of hypertension and drug use within the previous month was recorded.
In the Elderly NAHSIT, dietary intake was quantified by the frequency of consumption of each food during the previous month in quantitative units of day, week or month. This included fish (freshwater, saltwater fish or canned fish), poultry (chicken, duck or goose), lean meat, semi-fatty meat (streaky pork, ground meat, pork trotters or semi-fatty beef), processed meat products (sausage), shellfish, shrimp, soy products (soy milk, tofu, tofu pudding or other soybean products), poultry, seafood, eggs, milk (or yogurt), low-fat milk/yogurt, reduced-fat milk/yogurt, vegetables, mushrooms, fruit, fresh juice, fries, coffee, tea, snacks, sugar drinks, sugar, raw meat, preserved vegetables and fermented food. Alcohol consumption was assessed by the following parameters: the time point at which the individuals started their drinking habit, their history of quitting, the frequency of alcohol consumption (in days, weeks or months) and the type of alcohol consumed. The average weekly alcohol consumption (in grams) was determined. Smoking habits were assessed by the following parameters: the time point at which the individuals started their smoking habit; whether they had continuously maintained the smoking habit for more than 6 months; average amount of smoking in the previous month (in terms of cigarettes, packs, cigars or social smoking); the maximum number of cigarettes smoked, together with the corresponding period. The habit of betel-nut chewing was assessed according to the following parameters: frequency of betel-nut chewing, amount of betel used and the type of material chewed (piper betel with or without chemical supplements like slaked lime, betel leaf of Piper Linn or unripe fruit of Piper Linn). Questions about nutrition-related knowledge, attitudes and behaviours were adopted in this paper partly to evaluate whether a subject followed or decreased intake of a diet item, and the information was quantified and categorised on the basis of frequency of consumption.
Statistical analysis
All data were processed and analysed using the SAS program (version 9.1, SAS Institute, Cary, NC). A significant level α = 0.05 was set to implement the following statistical analysis. Stratified by the four SUA-related conditions, the mean and the standard deviation (SD) values of continuous variables were compared by analysis of variance (ANOVA). The distribution of categorical variables was assessed for the existence of a linear trend in proportions by the chi-square test for trend. A polychotomous logical regression model was applied, and the multinomial responses were the four groups on the basis of SUA-related conditions. The odds ratios (ORs) and their 95% confidence intervals (CI) were estimated. Compared with the reference (normouricemic) group, the estimated ORs and 95% confidence intervals are listed for risk factors associated with the SUA-related conditions.
Results
The clinical characteristics for the four SUA-related conditions have shown in . Since the distribution of TGs was skewed, the median and interquartile range values of TG have been shown, and a log-transformed function was used to calculate the logged TG values for ANOVA. When compared to the individuals in all the other groups, the individuals in the CKD group were older and had higher levels of SBP, TG, SUA and creatinine; a lower level of HDL-C; the lowest eGFR. Patients being treated for hyperuricemia were more likely to be overweight (body mass index [BMI] ≥ 25 kg/m2) and have a lower TC level. The mean SUA in the treated hyperuricemic group was 7.9 mg/dl and had larger SD (2.5 mg/dl) than that seen in the untreated hyperuricemic group and CKD group, both of which had a mean SUA value of 8.2 mg/dl with SD of 1.1 and 2.2, respectively. At least 70% of the treated hyperuricemic patients and 76% of the CKD patients had an SUA value greater than 7 mg/dl (data not shown). The age and BMI for the groups increased in the order of SUA-related conditions. In contrast, the HDL-C (52.9, 51.3, 49.7 and 47.6 mg/dl, respectively) and eGFR (85.5, 82.7, 76.2 and 47.6 ml/min/1.73 m2) values exhibited an inverse trend across four groups in the order of SUA-related conditions. No significant differences were observed between the four groups with respect to the FPG, TC and LDL-C levels.
Table I. Clinical characteristics of 752 elderly men, stratified by serum uric acid-related conditions in Elderly NAHSIT, Taiwan, 1999–2000.§
On comparing the four groups with regard to consumption of animal protein (), it was observed that 35.6% of the individuals in the CKD group were likely to always consume poultry with the skin and meat with the fat; these characteristics were observed in 15.9% of the individuals in the treated hyperuricemic group. It was found that 15.9% of the treated hyperuricemic individuals always consumed poultry with skin but did not consume meat with fat. As compared to the individuals in the other groups, the individuals in the treated hyperuricemic group had significantly higher BMI values (≥25 kg/m2) and more frequent drug use for hypertension, and a significantly lower percentage of egg consumption (≥3 times/wk) and soy product consumption (≥4 times/wk). The data revealed that 34.1% of these individuals frequently consumed reduced-fat milk (≥7 times/wk). Across the four groups formed on the basis of SUA-related conditions, the prevalence of drug use for hypertension and of shellfish consumption (≥1 time/wk) exhibited significantly positive trends, while that of soy product consumption (≥4 times/wk) and alcohol consumption (≥60 g/wk) showed significantly decreasing patterns. Weak reverse trends were observed in the case of preserved vegetable consumption (≥4 times/wk), coffee consumption (≥1 time/mo) and snack consumption (≥4 times/wk). Variables such as the consumption of viscera, fish and sugar; betel-nut chewing; education level; current smoking status, were not linearly related with the ordinal order of the four SUA-related conditions.
Table II. Demographic, clinical and dietary characteristics of 752 elderly men, stratified by serum uric acid-related conditions in Elderly NAHSIT, Taiwan, 1999–2000.
The results of the polychotomous logical regression model are shown in . Significant differences were observed between the four groups with regard to age; BMI (≥25 kg/m2); drug use for hypertension; types of poultry and meat consumed; consumption of shellfish (≥1 time/wk), eggs (≥3 times/wk), soy products (≥4 times/wk), fried food (≥1 time/wk) and juice (≥4 times/wk). The untreated and treated hyperuricemic patients differed with regard to the intake of fried food; the patients who were undergoing treatment for hyperuricemia tended to consume fried food more frequently (≥1 time/wk) than did the patients with untreated hyperuricemia. The patients undergoing treatment for hyperuricemia and the patients with CKD differed with regard to the type of poultry and meat consumed; the hyperuricemic patients preferred to consume poultry with the skin, while the patients with CKD preferred to consume both poultry with skin and meat with fat. Except for the individuals in the normouricemic group, the shellfish consumption, i.e. ≥1 time/wk, was similar in the other three groups.
Table III. Risk factors associated with serum uric acid-related conditions among 752 elderly men in Elderly NAHSIT, Taiwan, 1999–2000.
Discussion
Three objectives have been addressed in this study. The main objective was to explore the heterogeneity of dietary intake between the patients in the four groups that were formed on the basis of SUA-related conditions rather than solely emphasising on the role of SUA. Since SUA is the product of purine degradation and acts as a mediator between dietary and metabolic mechanisms, an overwhelming SUA effect would mask the real relationship between dietary intake and renal function. Second, this study has explored the association between CKD and dietary intake instead of the energy/protein intake. The third objective was to determine the differences between treated and untreated hyperuricemic patients.
This study presents many new findings. First, heterogeneity was observed in drug use for hypertension between the four groups [Citation38,Citation39]. In this study, the blood pressures were present in each SUA-related condition by combining subjects with and without undertaking hypertensive therapy. Future studies should examine the effect of uric acid-lowering therapy on blood pressures in hypertensive patients with hyperuricemia or gout.
Second, although most papers have strongly stated that consumption of purine-rich seafood would increase SUA levels, only a few papers have clarified which class of seafood predisposes individuals to the risk of hyperuricemia or CKD [Citation24,Citation27,Citation29,Citation40]. The present study confirmed that shellfish consumption indeed acted as a significant predictor in the untreated hyperuricemic, treated hyperuricemic and CKD groups, and that fish and crustacean consumption did not act as predictors. These results were similar to those of a matched case–control study that categorised seafood into 3 classes – fish, shrimp and shellfish [Citation27].
Third, the present article has addressed the benefits of soy products for hyperuricemic and CKD patients [Citation41] to counter the erroneous nutritional belief held by the Asian population that patients with hyperuricemia should reduce their intake of soy products [Citation42,Citation43]. This is because most of the purine content is lost in the tofu and soymilk manufacturing processes [Citation43,Citation44]. Moreover, the amino acid composition and relative proportion in soy and animal proteins vary [Citation28,Citation45], and the purines in both types of proteins belong to different categories. Mushroom consumption did not differ between the four groups. Lyu et al. [Citation26] reported that the increase in the intake of purine-rich plant foods did not increase the risk of gout and that intake of dietary fibre had a protective effect against gout.
Fourth, the main difference between the treated hyperuricemic and CKD groups was poultry or meat consumption with skin or fat, respectively. This finding strongly supports the claim that the high purine content of poultry skin would contribute to an increase in the SUA level and the risk of hyperuricemia and gout [Citation25,Citation46]. Especially, the role of the type of dietary intake in causing CKD has rarely been studied. An important issue that arises and needs to be further investigated is whether elderly Taiwanese individuals are aware that the excessive intake of non-dairy animal proteins is harmful; however, their healthy behaviours may be limited by food customs, such as saving chicken/duck skin, meat fat and egg yolks for use in other preparations rather than discarding them.
Our study has several potential limitations. One is the possibility of bias due to the measurement in the food consumption frequency questionnaire, for example, measurement of the sugar and dairy product intake. The interviewers were trained to calculate the total frequency of sugar intake, including that of sugar drinks, green tea, coffee, tofu pudding and other food. This would amount to collinearity between sugar, sugar drinks, juice and other sources of sugar intake in the model. In addition, this analysis hardly clarifies the effect of the ingestion of dairy products mixed with other foods, i.e. the effect of dairy products added in various foods and drinks such as tea, coffee, juice, fruit, cookies and candies as well as in cooking preparations such as sauces, creams, ice cream and fruit creams.
In conclusion, our study reveals the heterogeneity in the dietary intake in Taiwanese men aged 65 and older who were segregated into four groups according to their SUA-related conditions. Men who use anti-hypertensive drugs and who consume fewer soy products and more shellfish may be at a higher risk of hyperuricemia or CKD. Further studies are needed to confirm these findings with respect to different gender and age strata.
Acknowledgements
Data analysed in this article were collected by the research project “Elderly Nutrition and Health Survey in Taiwan 1999–2000” sponsored by the Department of Health, Executive Yuan, Taiwan. This research project was carried out by Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan, and directed by Dr. Wen-Harn Pan. The Center for Survey Research of Academia Sinica is responsible for the data distribution. The author appreciates the assistance in providing data by the institutes and individuals aforementioned. The views expressed herein are the authors' own. For this study, the author Dr. Chang has conceptualised the study, performed the literature review and statistical analysis, written the first draft of the manuscript and approval of the final manuscript. The author has no conflict of interest.
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