Association between serum uric acid and relative handgrip strength compared using metabolic syndrome components

Abstract

Background: This study investigated the association between serum uric acid (UA) and relative handgrip strength (HGS) using metabolic syndrome components.

Methods: We analyzed the data of 5,579 Korean adults aged ≥20 years (2,486 men and 3,093 women) who participated in the Korea National Health and Nutrition Examination Survey VII (2018).

Results: Among women, relative HGS was significantly lower in participants with hyperuricemia (1.61 ± 0.03) than in those without (1.92 ± 0.01) and was significantly decreased in the highest quartile (4Q:1.74 ± 0.02) of serum UA compared with that in the lowest quartile (1Q:1.96 ± 0.02). Among men, relative HGS was lower in participants with hyperuricemia (3.09 ± 0.03 vs. 3.15 ± 0.02) and decreased in the highest quartiles (4Q:3.08 ± 0.03) of serum UA compared with that in the lowest quartile (1Q:3.14 ± 0.03); however, these results were not statistically significant. In age- and multivariate-adjusted analyses in men, relative HGS was significantly lower in 4Q compared with that in 1Q in model 1 (adjusted for age), but there were no significant differences in model 2 (adjusted for age, body mass index, and waist circumference) and model 3 (adjusted for age, body mass index, waist circumference, systolic and diastolic blood pressure, fasting blood glucose, triglycerides and high-density lipoprotein cholesterol). Meanwhile in women, relative HGS was significantly decreased in 4Q compared with that in 1Q in all models.

Conclusions: An inverse correlation was observed between serum UA levels and relative HGS. These results were particularly significant in women, and their significance was maintained even after adjusting for age and metabolic syndrome components. 

1. Introduction

Uric acid (UA) is produced during the purine metabolism [1]. Although UA is a powerful antioxidant [2], it can also induce systemic inflammation [3] by acting as a pro-oxidant [4]. Furthermore, elevated serum UA levels are associated with hypertension [5], impaired fasting glucose [6], increased cardiovascular disease mortality [7, 8], and metabolic syndrome (MetS), which is a cluster of cardiometabolic risks [9].

Sarcopenia is defined as a decrease in muscle mass and strength [10]. Handgrip strength (HGS), a measure of the maximum voluntary force of the hands, is a convenient and direct method for assessing total muscle strength [10, 11]. Generally, HGS is accepted as a recommended tool in diagnostic algorithms for sarcopenia [12, 13]. Although there is no standardized method yet, various methods for assessing HGS, such as dominant HGS (maximal HGS of the dominant hand), absolute HGS (summation of maximal HGS of each hand), and relative HGS (absolute HGS divided by body mass index), have been used in previous studies. Among these, relative HGS shows a stronger correlation with cardiovascular biomarkers [14, 15]. However, few studies have examined the relationship between serum UA levels and relative HGS.

We aimed to investigate the association between serum UA levels and relative HGS through MetS components using representative data of Korean adults who participated in the Korea National Health and Nutrition Examination Survey (KNHANES) VII 2018.

2. Methods

2.1. Study population

We analyzed data from the third year (2018) of the KNHANES VII. The KNHANES is a nationwide, population-based, cross-sectional health examination and survey that has been conducted annually since 1998 by the Division of Chronic Disease Surveillance of the Korea Centers for Disease Control and Prevention in the Ministry of Health and Welfare to monitor the general health and nutritional status of the non-institutionalized civilian population of South Korea.

In 2018, the surveys were completed by 7,992 participants. Of these, those aged ≥20 years (n = 6,424) were selected for analysis. We excluded those who were pregnant (n = 23) and had missing data on measurements, including HGS (n = 565), serum UA (n = 159), body mass index (BMI) (n = 29), waist circumference (WC) (n = 3), blood pressure (n = 24), high-density lipoprotein cholesterol (HDL-C) (n = 3), and creatinine ≥1.5 mg/dL (n = 39). Finally, a total of 5.579 participants (2,486 men and 3,093 women), with a weighted total of 38,423,027 participants (19,557,503 men and 18,865,524 women), were included in the analysis (Figure 1). All the KNHANES participants provided written informed consent for the data to be used in the study. This study was approved by the Institutional Review Board of the Korea Centers for Disease Control and Prevention (2018-01-03-P-A) and the Institutional Review Board of Pusan National University Yangsan Hospital, which waived the requirement for approval (IRB No. 05-2022-100).

KNHANES, Korea National Health and Nutrition Examination Survey; HGS, handgrip strength; UA, uric acid; BMI, body mass index; WC, waist circumference; BP, blood pressure; HDL-C, high-density lipoprotein cholesterol.

2.2. Data collection

Health examinations included medical history taking, physical examination, administration of a questionnaire on health-related behaviors, and anthropometric and biochemical measurements. All individuals over the age of 20 were subjected to a physical examination and blood sampling by trained medical personnel who followed standardized procedures. Participants were asked about their health-related behaviors, including cigarette smoking, alcohol consumption, and regular exercise. Smoking status was indicated as “yes” when the participants had smoked more than five packs of cigarettes (100 cigarettes) during their lifetime and were smoking at the time of the survey. A standard drink was defined as a single glass of beer, wine, liquor, or traditional Korean distilled liquor, Soju. One beer bottle (355 mL) was counted as 1.6 standard drinks. The amount of alcohol per standard drink was calculated to be 10 g. Heavy alcohol consumption was indicated as “yes” when the participant had at least seven drinks at one time for men (at least five drinks for women) more than twice a week. Regular exercise was indicated as “yes” when the participant regularly performed moderate (>2 hours and 30 minutes/week, causing slightly increased respiration and heart rate) or strenuous (>1 hour and 15 minutes/week, causing rapid respiration and a substantial increase in heart rate) exercise, regardless of indoor or outdoor activity; or when the participant walked for a minimum of 30 minutes each day for 5 days/week. The completed questionnaires were reviewed by trained staff, and the records were entered into a database.

2.3. Anthropometric and biochemical data

The height and weight were measured to the nearest 0.1 cm and 0.1 kg, respectively, with participants wearing light clothing and barefooted. BMI was calculated as weight in kilograms divided by the square of height in meters. Blood pressure was measured in the right arm using a standard mercury sphygmomanometer (Baumanometer Wall Unit 33 (0850), W.A. Baum Co. Inc., Copiague, NY, USA), with the participant in a sitting position. Systolic and diastolic blood pressure (SBP and DBP, respectively) readings were recorded twice at five-minute intervals and averaged for analysis. WC was measured at the midpoint between the lower margin of the last palpable rib and the top of the iliac crest at the end of normal expiration with the arms relaxed at the sides. 

Blood samples were collected from the antecubital vein of each participant in the morning following an overnight fast of at least 8 hours. The samples were processed, transferred to cold storage (2–8 °C) at the central laboratory of Neodin Medical Institute (Seoul, Korea), and analyzed within 24 hours. Measurements of serum UA, fasting blood glucose (FBG), triglyceride (TG), HDL-C, and creatinine levels were performed using a Hitachi automatic analyzer 7600-210 (Hitachi Ltd., Tokyo, Japan). 

Hyperuricemia was defined as a serum UA level ≥7.0 mg/dL in men and ≥6.0 mg/dL in women [16, 17]. Serum UA levels were classified into the following quartiles according to their distribution: first quartile (1Q); 2.0–5.0, second quartile (2Q); 5.1–5.9, third quartile (3Q); 6.0–6.8, and fourth quartile (4Q); 6.9–11.2 mg/dL and 1Q; 1.7–3.8, 2Q; 3.9–4.4, 3Q; 4.5–5.1, and 4Q: 5.2–10.1 mg/dL in men and women, respectively.

2.4. HGS measurement

The HGS was measured using a digital hand dynamometer (Digital Grip Dynamometer, TKK 5401, Takei Scientific Instruments Co., Ltd., Tokyo, Japan). Grip strength was measured with the participant in a standing position, with the arms fully extended at the sides without touching the body. The participants were asked to squeeze the dynamometer with as much force as possible for <3 seconds, three times with each hand alternately. A rest interval of at least 30 seconds was allowed between the trials. Absolute HGS was calculated as the summation of the maximal reading from each hand and was expressed in kilograms. Relative HGS was defined as the absolute HGS divided by BMI.

2.5. Statistical analysis

Statistical analyses were performed using SPSS Statistics for Windows, version 18.0 (SPSS Inc., Chicago, IIL., USA), using sampling weights from the KNHANES to acquire nationally representative estimates. In this study, the data were presented as weighted means with standard errors for continuous variables and percentages for categorical. Data for men and women were separated for further analysis owing to significant differences in serum UA and HGS by sex. In the general linear model, the t-test and analysis of variance (ANOVA) were used for continuous variables, and the chi-square test was used for categorical variables. ANOVA was performed using a general linear model approach to determine the association between serum UA levels and relative HGS with progressive levels of adjustment for age and MetS components. The primary independent variable was the serum UA level (categorized into sex-specific quartiles) in each model, and the dependent variable was relative HGS. Model 1 was corrected for age; model 2 was corrected for age, BMI, and WC; and model 3 was corrected for age, BMI, WC, SBP, DBP, FBG, TG, and HDL-C. All statistical tests were two-tailed, and statistical significance was defined as p <0.05.

3. Results

3.1. Clinical characteristics of the participants by sex

The characteristics of the 5,579 individuals (2, 486 men and 3,093 women) included in the study are shown in Table 1. The mean age was 46.3 ± 0.4 years in men and 48.5 ± 0.4 years in women. Serum UA was 6.0 ± 0.0 mg/dL in men and 4.5 ± 0.0 mg/dL in women. The absolute HGS was 76.35 ± 0.43 kg in men and 43.41 ± 0.28 kg in women. The relative HGS was 3.14 ± 0.02 in men and 1.90 ± 0.01 in women. Mean BMI, WC, SBP, DBP, FBG, and TG levels were significantly higher in men than in women. In contrast, the mean HDL-C levels were significantly lower. The proportions of current smoking (71.1% vs. 73.4%), heavy alcohol consumption (51.5% vs. 26.4%), and regular exercise (33.8% vs. 22.5%) were significantly higher in men.

3.2. Differences in clinical characteristics between participants with and without hyperuricemia by sex

The differences in clinical characteristics between participants with and without hyperuricemia according to sex are shown in Table 2. The mean age was significantly lower in participants with hyperuricemia in men (41.5 ± 0.8 years vs. 47.7 ± 0.5 years) but higher in participants with hyperuricemia in women (53.2 ± 1.3 years vs. 48.2 ± 0.5 years). The mean BMI, WC, SBP, DBP, and TG levels were significantly higher in participants with hyperuricemia, whereas the mean HDL-C level was significantly lower in both sexes. The mean FBG level was significantly lower in participants with hyperuricemia but higher in women. The proportion of heavy alcohol consumption was significantly higher in men with hyperuricemia than in men without hyperuricemia (56.5% vs. 49.8%). There were no specific differences in the proportions of current smoking, heavy alcohol consumption, or regular exercise in women. Absolute HGS was significantly higher in participants with hyperuricemia in men (78.82 ± 0.81 vs. 75.64 ± 0.46) but lower in women (41.21 ± 0.76 vs. 43.59 ± 0.26). Relative HGS was significantly lower in participants with hyperuricemia in women (1.61 ± 0.03 vs. 1.92 ± 0.01). In men, relative HGS was lower in participants with hyperuricemia (3.09 ± 0.03 vs. 3.15 ± 0.02, p = 0.076) but not significantly.

3.3. Comparisons among quartiles of serum UA

The participants were classified according to quartiles of serum UA levels, and their clinical characteristics were compared by sex (Tables 3 and 4). In men, the mean age decreased significantly with increasing quartiles of serum UA level. The mean BMI, WC, DBP, and TG were significantly higher in the 4Q group than in the 1Q group. Mean FBG and HDL-C levels were significantly lower in the 4Q group than in the 1Q group. The proportion of heavy alcohol consumption was significantly higher in 4Q (56.4%) than in 1Q (45.5%). The absolute HGS increased significantly with increasing quartiles of serum UA levels. Relative HGS decreased in 4Q (3.08 ± 0.03) compared with that in 1Q (3.14 ± 0.03), but the difference was not statistically significant (Table 3). In women, the mean age showed no significant difference between the 1Q and 4Q. Mean BMI, WC, SBP, DBP, FBG, and TG levels were significantly higher in 4Q than in 1Q. The mean HDL-C level was significantly lower in the 4Q group than in the 1Q group. The proportion of heavy alcohol consumption was significantly higher in 4Q (29.2%) than in 1Q (19.4%). Absolute HGS decreased in 4Q (42.23 ± 0.50 kg) compared with that in 1Q (43.25 ± 0.45 kg), but the difference was not statistically significant. Relative HGS significantly decreased in 4Q (1.74 ± 0.02) compared with that in 1Q (1.96 ± 0.02) (Table 4).

3.4. Sex-specific regression coefficients for relative HGS and clinical characteristics 

The regression coefficients between the relative HGS and clinical variables are shown in Table 5. Age, BMI, and SBP showed a significant negative correlation with relative HGS, while DBP showed a positive correlation with relative HGS in both sexes. HDL-C levels were positively correlated in women.

3.5. Age and multivariate-adjusted relative HGS of participants categorized by sex and quartiles of serum UA

Table 6 shows the age and multivariate-adjusted relative HGS of men and women categorized by serum UA quartile. In men, the relative HGS was significantly decreased in 4Q compared with that in 1Q in model 1 (adjusted for age), but there were no significant differences in models 2 (adjusted for age, BMI, and WC) and 3 (adjusted for age, BMI, WC, SBP, DBP, FBG, TG, and HDL-C). However, relative HGS significantly decreased in women in 4Q compared with that in 1Q in models 1, 2, and 3.

4. Discussion

The principal finding of this study was an inverse correlation between serum UA levels and relative HGS. These results were particularly significant in women, and their significance was maintained even after adjusting for age and MetS components. Our study mainly focuses on relative HGS because it can minimize the confounding effect of body size and has been known to reflect cardiovascular risk better than other HGS indices [14, 15].

Several previous studies have shown that an increase in serum UA level is associated with increased HGS, mainly in older adults [18-20]. However, few studies have investigated the relationship between serum UA levels and HGS in adults over 20 years of age. One study of 3,595 participants in the NHANES study reported that a negative association was observed between serum UA and dominant HGS in adults aged 20–40 years, and this association was reversed after the age of 60 years, suggesting that the association between UA and muscle strength differed depending on age [21]. Another study showed that a high serum UA level is independently associated with increased dominant HGS in the older Korean population, but no significant relationship was found in young people [22]. In our study, which analyzed patients aged ≥20 years, the relative HGS decreased with an increase in serum UA levels, and the relative HGS was also lower in the hyperuricemia group. This negative association between serum UA levels and relative HGS was more significant in women than in men. On the other hand, in absolute HGS, a significant positive association was observed between an increased absolute HGS and an increase in serum UA levels, and absolute HGS was higher in the hyperuricemia group in men. This finding is consistent with that of Lee et al. [22]. They showed that low serum UA levels were a risk facto`r for low HGS only in the older male population. A possible explanation for this result could be the following. First, the higher the serum UA levels, the lower was the mean age, in the comparison among serum uric acid quartiles, and the mean age was also lower in the hyperuricemia group in men. Second, the differences in the proportion of heavy alcohol consumption and current smoking according to serum UA levels and the natural differences in hormones between the sexes may have affected the results. 

Huang et al. [23] reported that HGS was much lower in participants with hyperuricemia than in those without hyperuricemia, and HGS showed a higher value in the second serum UA quartile than in the first quartile and decreased with an increase in serum UA quartiles after the second quartile, similar to an inverted J-shaped curve. Our findings in relative HGS, an adjusted HGS by body size, are consistent with this study when comparing with and without hyperuricemia (men: 3.15 vs. 3.09; women: 1.92 vs. 1.61), as well as serum UA quartiles (men:1Q 3.14, 2Q 3.18, 3Q 3.15, 4Q 3.08; women: 1Q 1.96, 2Q 1.97, 3Q 1.92, 4Q 1.74). These results were also similar to those of previous epidemiological studies, which showed a J-shaped association between serum UA levels and cardiovascular events [24] and all-cause mortality [25], suggesting that both low and high UA levels may be related to higher cardiovascular risks. Higher-than-normal serum UA levels are associated with high levels of inflammatory cytokines [23, 26], which could contribute to poor muscle strength and having UA as a pro-oxidant. This is also consistent with the findings of our previous study, which demonstrated that relative HGS has an inverse relationship with MetS [27]. Meanwhile, in the case of lower-than-normal serum UA levels, the antioxidant capacity of UA could be decreased, which could be a possible reason for lower muscle strength [23]. Therefore, it could be assumed that the best muscle strength may be maintained at optimal serum UA levels. 

In our study, the negative associations between serum UA levels and relative HGS were more prominent, and these significances were maintained after adjusting for age and MetS components in women. Kawamoto et al. [19] also reported that serum UA levels were independently associated with HGS only in women. We also suggest that the combined effects of the differences in hormones, alcohol consumption rate, mean serum UA levels, and smoking habits between sexes might explain these findings, as previously described by Lee et al. [22].

The main limitation of this study is that it is difficult to determine causal relationships because of its cross-sectional design. In addition, since the KNHANES did not include a muscle mass evaluation tool such as dual-energy X-ray absorptiometry, it was impossible to measure the muscle mass required to diagnose sarcopenia directly.

5. Conclusions

There was an inverse correlation between the serum UA levels and relative HGS. These results were particularly significant in women, and their significance was maintained even after adjusting for age and MetS components. In addition, relative HGS could be a better indicator of muscle strength than the other HGS indices.

Abbreviations

1Q, first quartile

2Q, second quartile

3Q, third quartile

4Q, fourth quartile

AHGS, absolute handgrip strength

BMI, body mass index

DBP, diastolic blood pressure

FBG, fasting blood glucose

HDL-C, high-density lipoprotein cholesterol

HGS, handgrip strength

KNHANES, Korea National Health and Nutrition Examination Survey

MetS, metabolic syndrome

N, number

RHGS, relative handgrip strength

SBP, systolic blood pressure 

TG, triglyceride

UA, uric acid

WC, waist circumference

Declarations

Ethics approval and consent to participate

All the KNHANES participants provided written informed consent for the data to be used in the study. This study was approved by the Institutional Review Board of the Korea Centers for Disease Control and Prevention (2018-01-03-P-A) and the Institutional Review Board of Pusan National University Yangsan Hospital, which waived the requirement for approval (IRB No. 05-2022-100).

Consent for publication

Not applicable

Availability of data and materials

The dataset can be downloaded from the Korea National Health and Nutrition Examination Survey website (https://knhanes.kdca.go.kr/knhanes/eng/index.do).

Competing interests

The authors declare that they have no competing interests.

Funding

None

Authors’ contributions

DY contributed to data analysis and wrote the main manuscript text. MJL and ARK contributed to discussions about the study, and to the reviewing and editing the manuscript. YHK is the guarantor of this work and takes responsibility for the integrity of the data and accuracy of the data analysis. All authors read and approved the final manuscript.

Acknowledgments

This work was supported by a 2-year Research Grant of the Pusan National University (No. 202014270002). 

Authors’ information

ORCID 

Dongwon Yi: 0000-0003-3574-036X; Min Jin Lee: 0000-0002-4351-789X; Ah Reum Khang: 0000-0002-9154-6468; Yang Ho Kang: 0000-0002-1215-7975.

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Tables

Table 1 

Clinical characteristics between the sexes.

N, number; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; UA, uric acid; AHGS, absolute handgrip strength; RHGS, relative handgrip strength. 

Table 2 

Comparisons between participants with and without hyperuricemia in each sex.

N, number; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; UA, uric acid; AHGS, absolute handgrip strength; RHGS, relative handgrip strength.

Table 3

Comparisons between the quartiles of serum uric acid in men.

*; P < 0.05 vs. 1Q

N: number, 1Q: first quartile. 2Q, second quartile; 3Q, third quartile; 4Q, fourth quartile; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; UA, uric acid; AHGS, absolute handgrip strength; RHGS, relative handgrip strength.

Table 4

 Comparisons between the quartiles of serum uric acid in women.

*; P < 0.05 vs. 1Q

N: number, 1Q: first quartile. 2Q, second quartile; 3Q, third quartile; 4Q, fourth quartile; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; UA, uric acid; AHGS, absolute handgrip strength; RHGS, relative handgrip strength.

Table 5

Regression coefficients for relative handgrip strength and various characteristics by sex.

N, number; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol.

Table 6

Comparisons of adjusted relative HGS among the quartiles of serum uric acid in each sex.

Model 1: adjusted for age

Model 2: adjusted for age, BMI, and WC

Model 3: adjusted for age, BMI, WC, SBP, DBP, FBG, TG, and HDL-C levels.

*; P < 0.05 vs. 1Q

1Q, first quartile; 2Q, second quartile; 3Q, third quartile; 4Q, fourth quartile; BMI, body mass index; WC, waist circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; FBG, fasting blood glucose; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol.