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INTRODUCTION
Osteoporosis is characterized by low bone mass and reduced bone structure, in which bone becomes brittle and fragile from loss of bone tissues, thus making it more vulnerable to fracture [1]. Osteoporosis is particularly associated with age and thus impose a heavy burden on global public health for aging population [23]. Among Korea, the prevalence of osteoporosis was 7.3% in male and 38.0% in female adults ≥ 50 years old in 2011 and it has continuously increased [4]. This trend is thought to be a result of a westernized dietary lifestyle in Korea, along with demographic and sociological factors [5].
Diet is a crucial modifiable factor that causes or contributes to osteoporosis and fractures [6]. Even though diet play an important role in bone health, most studies has concentrated on single nutrients including calcium and vitamin D, or supplements containing these nutrients [78]. Recently, population-based observational studies have been identified beneficial effects of dietary potassium and fruit and vegetables on bone health [2910]. The most facilitated hypothesis regarding to benefit of dietary potassium on bone health is through its effect on acid-base balance, even though the role of the skeleton in pH regulation is controversial [1112]. The western diet including high meats and cereal grains produces a low-grade metabolic acidosis [11]. The continual release of alkaline salts from bone for acid-base balance would cause bone loss and osteoporosis [13]. Fruit and vegetable intake could balance this excess acidity by providing alkaline salts of potassium [14]. Thus, the alkaline potassium salt is thought to prevent bone resorption for pH homeostasis [15]. In addition, increasing potassium intake increases urinary retention, reducing loss of calcium and thus creating a more positive calcium balance and inhibiting bone resorption [1617]. The potassium bicarbonate, but not sodium bicarbonate, reduced urinary calcium excretion in healthy men [18], and the potassium citrate reduced urinary calcium excretion in men with uric acid nephrolithiasis [19]. It suggests that the positive effect of potassium could be through either suppressing calcium resorption or bone mineral dissolution or both [20].
Hence, the current study aimed to identify the link between dietary potassium and the prevalence of osteoporosis and osteopenia in at-risk Koreans, using national survey data. We also analyzed the correlation of potassium intake with bone mineral density (BMD).
SUBJECTS AND METHODS
Study design
The KNHANES was conducted to investigate the health and nutritional status of Koreans from 1998 onwards. These were cross-sectional and nationally representative surveys performed by the Division of Chronic Disease Surveillance, and the Korea Centers for Disease Control and Prevention. The current study was based on data from the KNHANES IV-V (2008-2011), which conducted bone mineral density examinations. Data were collected from the cross-sectional KNHANES study database, including from health interviews, health examinations, and nutrition surveys, as well as BMD examinations.
A total of 21,303 participants were examined in KNHANES from 2008 to 2011. The International Society for Clinical Densitometry recommends that osteoporosis be diagnosed in postmenopausal women, and in men aged 50 and older, if the T-score of the lumbar spine, total hip or femoral neck is −2.5 or less [21]. According to this guideline, we selected postmenopausal women (n = 5,624) and men aged 50 years old and older (n = 4,053). Among 9,677 subjects, we additionally excluded subject (n = 5) without BMD data in current study. We defined postmenopausal status as not experiencing menstruation for > 12 months, and included surgical menopause. An additional 940 participants with implausible energy intake based on dietary surveys (< 500 or > 5,000 kcal/d) were also excluded. Finally, the current study included 8,732 subjects (3,590 men and 5,142 women) for analysis.
The protocols for KNHANES IV-V were approved by the Institutional Review Board (IRB) of the Korea Centers for Disease Control and Prevention (2010-02CON21-C, 2011-02CON-06-C) and the research was performed in compliance with the guidelines laid down in the Declaration of Helsinki. Informed consent was obtained from all participants.
Nutrition assessment
Assessment of dietary consumption was conducted using a single-day 24-hour dietary recall method [22]. Highly qualified dietitians conducted a nutrition survey. Total energy and nutrient intake including protein, carbohydrate, fat, and calcium were estimated using the food composition table from the Korean National Rural Development Institute [23]. The residual method was applied to nutrient intake to adjust the total energy intake as demonstrated by Willett and Stampfer [24].
BMD measurement and definition of osteoporosis
The BMD (g/cm2) was measured at the lumbar spine (L1-L4 spine) and five regions of the femur (total femur, trochanter, intertrochanter, femoral neck, and Ward's triangle) using dual-energy X-ray absorptiometry (DEXA, Discovery QDR 4500; Hologic, Inc., Waltham, MA, USA) at the health examination site. The BMD measurements were conducted via a standardized protocol from the International Society for Clinical Densitometry [21]. The BMD at the lumbar spine (L1–L4) and femoral neck were used for diagnosis of osteoporosis and osteopenia. We defined osteoporosis as a T-score < −2.5 and osteopenia as a T-score between −2.5 and −1.0; a T-score > −1.0 was considered normal bone mass [25].
Covariates
Physical examinations included body weight, height and body mass index (BMI) measurements. Demographic characteristics were obtained from a structured questionnaire. Educational levels were divided into four groups: ≤ elementary school, middle school, high school, and ≥ college. The household income was grouped into four levels by quartile. Lifestyle factors included smoking, alcohol drinking, and physical activity. Physical activity was estimated from the International Physical Activity Questionnaire (IPAQ) Korean version [26]. The minutes of Physical activity were then transformed into metabolic equivalents (METs) [27] and then we classified our subjects into 3 groups: “Health promoting active”, “Minimally active” or “Inactive” in accordance with the IPAQ guidelines [28]. Serum 25-hydroxyvitamin D (25(OH)D) level was measured by a radioimmunoassay (DiaSorin Inc, Stillwater, MN, USA) using a gamma counter (1470 Wizard; PerkinElmer, Turku, Finland). Calcium intake was accessed by nutritional survey using 24 h-recall.
Statistical analysis
Categorical and continuous parameters were indicated as percentages and standard error, and as means and standard error, respectively. We applied the sampling weight value via the SAS survey procedure to consider the complex sampling design in all statistical analyses. Survey regression for comparisons of continuous variable and chi-square analysis for comparisons of categorical parameter were applied according to potassium intake categories.
To identify the association between dietary potassium intake and bone health, including osteoporosis, osteopenia, and BMD, we categorized subjects into tertile groups according to sex (men and women) and age (under 39, 40 to 49, 50 to 59, 60 to 69 and over 70) using proc rank analysis. The range of potassium intake for each tertile was as follows: for men, 386.7-2,726.5 mg/day in T1, 1,994.6–3,950.9 mg/day in T2, and 2,935.6–18,573.0 mg/day in T3; for women, 142.8–2,242.4 mg/day in T1, 1,450.8–3,441.6 mg/day in T2, and 2,223.0–13,303.9 mg/day in T3.
Multinomial logistic regression was performed to identify the link of potassium intake with the risk of osteoporosis and osteopenia, used as ordered outcomes adjusting for putative covariates of bone health. Potential confounders are either known or suspected risk factors for osteoporosis from previous studies [2930]. Multivariate analyses of the multinomial logistic regression were conducted in three models. Model 1 was controlled for age, BMI (continuous), and energy consumption (continuous). Model 2 also included quartile household income, four educational levels, alcohol consumption status (non-current and current), smoking status (never, past, and current), physical activity (inactive, minimally active, health promoting active). Finally, Model 3 was adjusted for serum vitamin D concentration (continuous) and residual energy-adjusted calcium intake (continuous). Missing values of continuous variables were replaced by the median and the missing statement of categorical variables was defined as the ‘missing’ group. All statistical analyses were performed using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA).
RESULTS
General characteristics of participants according to potassium intake
Mean ages were 61.9 ± 0.2 years in men and 62.3 ± 0.2 years in women. Mean potassium intakes were 3,258 ± 38 mg/d in men and 2,620 ± 29 mg/d in women. The general characteristics of subjects based on potassium tertile levels are described in Table 1. Data were similar for men and women. Subjects in group T3 (highest potassium consumption) were more likely to be younger and at a high level of household income and education, and less likely to be current smokers, compared with those in group T1 (lowest potassium intake). Men in group T3 had a higher BMI and were more health promotingly active than those in group T1. Furthermore, women in the T3 group had greater serum vitamin D levels compared to those in the T1 group. Furthermore, the level of energy and calcium consumption, and energy percentage from protein and fat, was positively associated with potassium intake. In contrast, energy from carbohydrate intake was inversely related to potassium intake among both males and females.
BMD and prevalence of osteoporosis according to potassium intake
The BMD value from six bone measurement sites and the distribution of osteopenia and osteoporosis based on potassium intake are presented in Table 2. BMD values of the total femur (P = 0.031) and Ward's triangle (P = 0.010) were statistically different according to the potassium intake among men. Women in the T3 group had greater BMD at all measurement points (total femur P = 0.013, trochanter P = 0.033, intertrochanter P = 0.041, femoral neck P = 0.025, Ward's triangle P = 0.019, and lumbar spine P = 0.009) than women in the T1 group. The osteoporosis prevalence in men was 8.1% and in women was 25.5%. In the T3 group, the prevalence of osteoporosis at the femoral neck and lumbar spine was significantly lower compared to the T1 group, among both males and females (all P < 0.001).
The association of potassium intake with osteopenia and osteoporosis
The odd ratios (ORs) and 95% confidence intervals (CIs) for osteopenia and osteoporosis according to potassium intake are presented in Table 3. Using group T1 as the reference group, men in T3 were associated with decreased odds for osteoporosis at the lumbar spine in model 1, controlled for age, BMI, and energy intake (OR: 0.63, 95% CI: 0.42-0.96, P trend = 0.044). However, this association was attenuated in model 3, which also adjusted for smoking status, alcohol consumption, physical activity, education, household income, serum vitamin D, and energy-adjusted calcium intake (OR: 0.82, 95% CI: 0.51–1.33, P trend = 0.476). The women in the T3 group showed a decreased OR for osteoporosis in the lumbar spine (OR: 0.68, 95% CI: 0.48–0.96, P trend = 0.030) in fully adjusted model 3. However, potassium intake level was not statistically associated with the odds for osteoporosis among men.
DISCUSSION
The crucial finding in this study is the positive link of dietary potassium with bone health among Korean older adults, particularly in females. After adjusting for the putative confounders, the osteoporosis prevalence at the lumbar spine was 32% lower in women with a higher potassium intake than in those with a lower intake. However, this association was not significant among men.
Our findings are further supported by the evidence from previous epidemiological studies [103031323334]. The EPIC-Norfolk cohort study reported positive association of dietary potassium intake with a quantitative ultrasound measurement of bone density status and reduced fracture risk of a population in the United Kingdom [30]. Another study in a similar age group identified that higher dietary potassium is associated with an increase in total hip and femur neck BMD in both males and females [10]. Furthermore, dietary potassium level was significantly correlated with an increased BMD in total body and lumbar spine among men aged 39 to 42 years [33]. It has been reported that greater baseline potassium intake is closely linked to preventing bone mass loss of the femoral neck and trochanter at a 4-year follow-up survey among men [34].
The putative theoretical mechanism of the favorable impact of dietary potassium on bone mechanism is based on the acid-base balance hypothesis [34]. In 1968, Wachman and Bernstein [13] suggested that bone mineral functions as a buffer base, and that lifetime buffering of the acid load from ingestion of mixed diets leads to gradual and accumulated bone loss. They suggested that “The therapy of osteoporosis may lie in its prevention… it might be worthwhile to consider decreasing the rate of bone attrition by the use of a diet favoring ‘alkaline ash’. This type of diet would emphasize the ingestion of fruit, vegetables, vegetable protein, and moderate amount of milk.” Two nutrients that may have such buffering effects are potassium and magnesium, which are found in a variety of whole, unrefined foods, including fruit and vegetables [3536]. Diets high in fruit and vegetables produce more alkaline urine by contributing a variety of compounds which, during their metabolism, accept hydrogen ions [1336]. In summary, potassium or alkaline potassium salts from fruits and vegetables might protect against bone resorption via pH homeostasis. Furthermore, potassium treatment raises calcium retention in renal tissue, while a low dietary potassium level increases calcium secretion in the kidneys [37]. A further study of 18 postmenopausal women showed that supplementation with potassium bicarbonate neutralized the status of endogenous acid loads. Additionally, potassium bicarbonate improved calcium equilibrium and blood osteocalcin levels, and reduced hydroxyproline secretion in the urine [38].
In our study, we did not find any significant link between potassium intake and the odds for osteoporosis in men. This disparity may be due to the differing degree of completion of a single day 24-hour dietary recall between men and women. Generally, women in Korea prepare the meals and are more knowledgeable about the dietary contents of food, which may lead to more reliable data collection from women. Furthermore, it is possible that residual confounding effects such as smoking and drinking may have had a greater influence on the null associations in men compared to women.
The current study had some limitations. Firstly, the results cannot be used to determine causality between potassium level and osteoporosis owing to the cross-sectional nature of the study. Hence, longitudinal studies are required to establish causality. Secondly, dietary potassium intake was evaluated via a one day 24-hour recall method, which might not correspond to participant's usual intake. Generally, the Food Frequency Questionnaire (FFQ) or multiple-day 24-hour dietary recall is used to assess usual intake. However, the FFQ had not been validated in the 2008-2011 KNHANES study, so the one-day 24-hour dietary recall method was used. Lastly, we could not exclude the possibility of potential confounding variables (e.g., calcium or vitamin D supplementation, biochemical markers regarding bone metabolism), even if we carefully adjusted for the relevant confounders. Despite these limitations, this is the first study to identify the association of dietary potassium intake with the prevalence of osteopenia and osteoporosis in the older adult Korean population.
In conclusion, our results, based on a representative population in Korea demonstrate that a higher dietary potassium level is positively associated with increased BMD and a decreased risk for osteoporosis in older Korean women. The current study highlights the potential benefits of potassium consumption on bone health among Korean adults. Importantly, we suggest that further prospective studies with a more exact dietary assessment method are needed to verify the link between dietary potassium consumption level and bone health.
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