1. Introduction
Obesity is a severe health problem and a key risk factor for other diseases, including type 2 diabetes, hypertension, dyslipidemia, and coronary heart disease [
1]. Metabolic syndrome (MS) is a cluster of symptoms, including abdominal obesity, dyslipidemia, hypertension, and glucose intolerance [
2]. Improving nutrient intake is a key factor in reducing the risk of MS. Dietary fiber is one of the candidates for improving nutrient intake: epidemiological evidence has shown a negative relationship between dietary fiber intake and the incidence of type 2 diabetes [
3,
4], hypertension, dyslipidemia [
5], and coronary heart disease [
6]. However, the average daily fiber intake in the Japanese population has been low for many years (<15 g/d) [
7].
Seaweed, especially kelp (
Laminaria), is a good source of dietary fiber; the soluble fibers consist of alginates, laminarin (β1–3, β1-6-glucan), and fucoidan, whereas the insoluble fiber is essentially cellulose [
8,
9]. Seaweed is an important dietary component for people in Japan: it is served in approximately 21% of meals [
10]; however, the daily median consumption per person was reported to be 1.2 g/d, and the contribution of dietary fiber intake from seaweed to total dietary fiber intake was only 0.4 g/d [
7]. These results suggest that the consumption of dietary fiber-rich seaweed could be increased in the Japanese diet. The major seaweeds consumed include Wakame (
Undaria), Nori (
Porphyra), Konbu (
Laminaria), and Hijiki (
Hizikia).
The consumption of seaweeds has been reported to affect both health status and chronic disease: several studies have reported a relationship between seaweed intake and risk reduction in cardiovascular disease [
11], metabolic syndrome [
12], and type 2 diabetes [
13]. In addition, effects of seaweed and seaweed extract intake on digestive tract health [
14], bone health [
15], and cancer prevention [
11], as well as antiviral properties [
16], have been reported; however, there are few reliable human studies.
Seaweed also contains bioactive compounds with high antioxidant capacity, such as carotenoids and polyphenols [
17,
18]. Reports have shown that fucoxanthin, from different types of algae, has anti-inflammatory and anti-obesity effects [
19,
20].
The effects of whole seaweed meals and seaweed extract on obesity have been widely studied in both animal and human intervention studies. In diet-induced obese mice, feeding Wakame (
Undaria) produced positive effects on body weight gain and glucose metabolism [
21]. Another investigation reported body weight reduction and reduced serum total cholesterol and triacylglycerol levels in mice fed a high-fat diet containing extracts from red seaweed (
Gelidium amansii) [
22].
There are very few reports on the effects of kelp intake on body weight loss: only one report showed a significant reduction in serum cholesterol using Japanese subjects given 5 g of seaweed powder daily [
23]; however, the control and subject information were not completely described.
Many species of red, green, and brown algae (seaweed) are used in Japanese meals [
24]. One of the three most popular seaweed products in Japan is kelp, which contains 2353 μg/g of iodine [
25,
26]. Since several grams of kelp powder supplementation exceeds the tolerable upper intake level (3000 μg/d in adults) of iodine [
27], it is difficult to conduct intervention studies on body weight loss using kelp powder. Approximately 80% of the iodine in kelp is released after boiling [
28]; therefore, we conducted an intervention study using iodine-reduced kelp powder produced through a boiling process.
The purpose of this study was to confirm whether supplementation with boiled kelp powder causes body weight and body fat loss in overweight Japanese subjects (BMI 25–30 kg/m2). Blood lipids and thyroid hormone levels were also examined. To our knowledge, this is the first randomized, double-blind, placebo-controlled trial to evaluate the effects of iodine-reduced kelp in Japanese participants.
3. Discussion
In a parallel, double-blind, placebo-controlled study, we randomly assigned 48 overweight (BMI 25–30 kg/m2) subjects to either a placebo supplement or a kelp supplement (6 g kelp powder/d, 3.3 g alginate/d) group. No differences in the changes in body fat percentage and visceral fat area (VFA) between groups were shown in the per-protocol (PP) analysis; however, in the male subjects, there was a significant body fat percentage loss within the test group compared with the placebo group. In the PP analysis, serum concentrations of total, LDL, and HDL cholesterol and triglyceride concentrations did not differ between the groups; however, after sub-analysis in non-hyperlipidemic subjects, serum LDL cholesterol concentration was significantly different at 8 weeks between the test and placebo groups.
We hypothesized that supplementation with a boiled kelp powder rich in alginate could enhance body fat loss and improve body composition in overweight Japanese subjects. A large reduction in body fat percentage was previously reported after alginate supplementation (45 g/d for 12 weeks) [
29]; however, other alginate supplementation studies have reported conflicting results [
30]. To our knowledge, this is the first randomized, double-blind, placebo-controlled trial to evaluate the effects of boiled kelp powder in overweight Japanese subjects (BMI 25–30 kg/m
2).
In this study, body fat loss after kelp intake was observed only in male subjects. Men and women exhibit significant differences in obesity and cardiovascular disease [
31]. Men generally have a greater incidence of obesity due to increased visceral adipose tissue; women tend to have increased fat mass proportional to their body weight due to increased subcutaneous adipose tissue. Generally, Japanese women have much lower rates of MS (14.3% in women, 25% in men) [
32]. A previous study used a higher dose of seaweed in female subjects but did not report any changes in weight; however, a decreased waist circumference among female subjects treated with the higher dose of seaweed was observed and was suggested to be modulated by estrogen metabolism [
33]. Our previous study on cereal fiber intake showed a reduction in visceral fat weight when the visceral fat area was more than 100 cm
2 [
34]. In this study, there were seven subjects (5 male and 2 female) in the test group and only three (2 male and 1 female) in the placebo group with a visceral fat area more than 100 cm
2, and this is suggested to be the reason why we did not observe a reduction in visceral fat in all subjects and body fat loss in female subjects. Further studies are needed to elucidate the effect of kelp intake on visceral fat reduction in abdominal obesity subjects.
Dietary fiber has been reported to prolong gastric emptying time, thereby enhancing satiety and resulting in a reduction in food intake [
35]. Seaweed is a good source of dietary fiber, and it is reported that alginate isolated from seaweed may attenuate appetite and associated markers [
36]. In our study, the daily energy intake at 0 and 8 weeks did not differ between the groups, suggesting that the reduction in body fat percentage in men was not due to prolonged gastric emptying time.
Alginate is a typical viscous soluble fiber, which can inhibit the absorption of carbohydrate and lipid from the gut [
37]. Repeated reductions in carbohydrate and lipid absorption rate by alginate consumption might protect against body fat accumulation. We hypothesized that this could be one possible explanation for the reduced body fat percentage observed in the kelp group compared with the placebo group.
We also investigated whether the intake of alginate from kelp would lead to improvements in cholesterol metabolism, which have been proposed with similar viscous soluble fibers [
38]. The hypocholesterolemic effect of dietary fiber has been attributed to its ability to inhibit the intestinal absorption of bile acids and neutral steroids, resulting in increased fecal bile acids and neutral steroid excretions [
39]. It is speculated that alginate in kelp increases the excretion of bile acids and neutral steroids, suggesting a causative role in the lowering of serum cholesterol concentrations.
It has been estimated that the average Japanese iodine intake is 1–3 mg/d [
40]. Kelp contains iodine, and the additional iodine supplementation in our study was 1 mg/d, which did not increase serum TSH levels. It is unlikely that the results observed in our study could be attributed to the iodine supplementation since a previous study reported that intake of 0.5 mg/d iodine from seaweed produced only minor transient changes in serum TSH [
41]. A previous study reported that seven weeks of 5 g/d seaweed supplementation in American women was associated with a small but statistically significant increase in TSH [
41]. Therefore, our result may be a phenomenon peculiar to Japanese subjects with relatively high intake of iodine from seaweed. Further studies are needed to clarify the influence of iodine intake from kelp.
Ethnic differences in lipid and glucose metabolism are mainly caused by frequency differences in genetic polymorphism. This difference results in the rapid increase in obesity and type 2 diabetes among mongoloids exposed to a westernized diet. In addition, the results of intervention studies may also differ. Some Asian countries, such as Korea, Japan, and parts of China, consume the greatest proportion of seaweed; therefore, the results of seaweed intervention studies may differ from those in Western countries due to differences in iodine tolerance and microbiota fermentation, as well as genetic differences. Kelp intervention studies are rarely reported in African and European countries; therefore, it is difficult to extrapolate our data for other races. Further studies are needed to elucidate the effect of kelp intake on the anti-obesity effect in all races.
A major limitation of the study was the small sample size: a larger study is planned for the future. A second limitation was the study design: there were quite a few subjects with abdominal obesity in spite of the BMI inclusion criteria of 25–30 kg/m2. Future studies are needed to elucidate the effect of kelp on visceral fat area loss in subjects with a VFA larger than 100 cm2.