Association Between Serum Concentration of Carotenoid and Visceral Fat

<a href="/goto?url=https://www.mdpi.com/journal/nutrients" target="_blank">nutrients </a>Article Association between Serum Concentration of Carotenoid and Visceral Fat Mai Matsumoto 1,*, Hiroyuki Suganuma 1 , Naoki Ozato 2,3 , Sunao Shimizu 1,4,5 , Mitsuhiro Katashima 2,3 Yoshihisa Katsuragi 2,3, Tatsuya Mikami 5, Ken Itoh 4,6 and Shigeyuki Nakaji 5,7 ,1Innovation Division, KAGOME CO. LTD., 17 Nishitomiyama, Nasushiobara, Tochigi 329-2762, Japan; [email protected] (H.S.); [email protected] (S.S.) Department of Active Life Promotion Sciences, Graduate School of Medicine, Hirosaki University, 25 Zaifu-cho, Hirosaki, Aomori 036-8562, Japan; [email protected] (N.O.); [email protected] (M.K.); [email protected] (Y.K.) Health & Wellness Products Research Laboratories, Kao Corporation, Tokyo 131-8501, Japan 34Department of Vegetable Life Science, Graduate School of Medicine, Hirosaki University, 5 Zaifu-cho, Hirosaki, Aomori 036-8562, Japan; [email protected] 5Innovation Center for Health Promotion, Graduate School of Medicine, Hirosaki University, 5 Zaifu-cho, Hirosaki, Aomori 036-8562, Japan; [email protected] (T.M.); [email protected] (S.N.) Department of Stress Response Science, Center for Advanced Medical Research, Graduate School of Medicine, Hirosaki University, 5 Zaifu-cho, Hirosaki, Aomori 036-8562, Japan Department of Social Medicine, Graduate School of Medicine, Hirosaki University, 5 Zaifu-cho, Hirosaki, Aomori 036-8562, Japan 67*Correspondence: [email protected]; Tel.: +81-80-1581-1874 Abstract: Consumption of fruits and vegetables rich in carotenoids has been widely reported to prevent cardiovascular diseases. However, the relationship between serum carotenoid concentrations and visceral fat area (VFA), which is considered a better predictor of cardiovascular diseases than the body-mass index (BMI) and waist circumference, remains unclear. Therefore, we examined the relationship in healthy individuals in their 20s or older, stratified by sex and age, to compare the relationship between serum carotenoid concentrations and VFA and BMI. The study was conducted on 805 people, the residents in Hirosaki city, Aomori prefecture, who underwent a health checkup. An inverse relationship between serum carotenoid concentrations and VFA and BMI was observed only in women. In addition, the results were independent of the intake of dietary fiber, which is mainly supplied from vegetables as well as carotenoids. This suggests that consumption of a diet rich in carotenoids (especially lutein and beta-carotene) is associated with lower VFA, which is a good predictor of cardiovascular disease, especially in women. This study is the first to comprehensively evaluate the association between serum carotenoid levels and VFA in healthy individuals. <a href="/goto?url=https://www.mdpi.com/2072-6643/13/3/912?type=check_update&version=1" target="_blank">ꢀꢁꢂꢀꢃꢄꢅꢆꢇ </a><a href="/goto?url=https://www.mdpi.com/2072-6643/13/3/912?type=check_update&version=1" target="_blank">ꢀꢁꢂꢃꢄꢅꢆ </a>Citation: Matsumoto, M.; Suganuma, H.; Ozato, N.; Shimizu, S.; Katashima, M.; Katsuragi, Y.; Mikami, T.; Itoh, K.; Nakaji, S. Association between Serum Concentration of Carotenoid and Visceral Fat. Nutrients 2021, 13, 912. <a href="/goto?url=https://doi.org/10.3390/nu13030912" target="_blank">https://doi.org/10.3390/nu13030912 </a>Academic Editor: Antonio Pérez-Gálvez Received: 29 January 2021 Accepted: 8 March 2021 Published: 11 March 2021 Keywords: carotenoid; visceral fat; metabolic syndrome; vegetable intake; resident-based cross- sectional study; healthy subjects Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. 1. Introduction Carotenoids are red, orange, and yellow pigments widely distributed among plants, animals, and microorganisms. Because carotenoids have a strong ability to quench singlet oxygen, their ingestion is expected to prevent and improve various diseases in which reactive oxygen species (ROS) are involved in the onset or exacerbation of symptoms. Many studies have been conducted in this regard. Several epidemiological studies have shown that ingestion of carotenoids and carotenoid-rich vegetables and fruits leads to the amelioration of arteriosclerosis and hypertension and reduces the risk of chronic Copyright: <ul style="display: flex;"><li style="flex:1">©</li><li style="flex:1">2021 by the authors. </li></ul>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// <a href="/goto?url=https://creativecommons.org/licenses/by/4.0/" target="_blank">creativecommons.org/licenses/by/ </a>4.0/). cardiovascular diseases, such as ischemic heart disease and cerebrovascular disease [ We also found that the higher the levels of carotenoids in the blood and skin, the healthier are many predictive markers of chronic cardiovascular disease in healthy individuals [ ], 1–7]. 8,9 <ul style="display: flex;"><li style="flex:1">Nutrients 2021, 13, 912. <a href="/goto?url=https://doi.org/10.3390/nu13030912" target="_blank">https://doi.org/10.3390/nu13030912 </a></li><li style="flex:1"><a href="/goto?url=https://www.mdpi.com/journal/nutrients" target="_blank">https://ww</a><a href="/goto?url=https://www.mdpi.com/journal/nutrients" target="_blank">w</a><a href="/goto?url=https://www.mdpi.com/journal/nutrients" target="_blank">.</a><a href="/goto?url=https://www.mdpi.com/journal/nutrients" target="_blank">mdpi.com/journal/nutrients </a></li></ul>Nutrients 2021, 13, 912 2 of 16 suggesting that vegetable intake may be preventive against diseases in healthy as well as ill individuals. In addition to their role in reducing oxidative stress, some carotenoids have an inhibitory effect on the differentiation and hypertrophy of adipocytes [10], and some affect lipid and glucose metabolism [11,12]. Thus, copious intake of carotenoid-rich vegetables is also expected to inhibit metabolic syndrome (visceral fat syndrome), which is a crucial trigger of chronic cardiovascular disease and is thought to be important for its prevention [13]. Visceral fat area (VFA) is commonly measured by computed tomography (CT). How- ever, because of the involvement of X-ray radiation, this measurement is not readily feasible. Therefore, the relationship between carotenoids and obesity was limited to the body-mass index (BMI) or waist circumference-based assessments. For example, in our previous study [8], high BMI was associated with low serum concentration of total carotenoid, whereas Suzuki et al. have reported an association between high waist circumference and low serum β-carotene levels in females [14]. Carotenoid concentrations in adipose tissue have also been measured, which have been shown to be related to waist circumference [15]. Sato et al. reported that there were misjudgments of more than 20% when they judged whether the VFA was equal to or larger than 100 cm2 using the criteria of waist circumference [16], so measuring VFA itself rather than waist circumference is considered preferable for subsequent disease prevention. However, as mentioned earlier, due to the difficulties in the measurement of VFA, the relationship between carotenoids and VFA has been evaluated only in a few previous studies [17]. The relationship between carotenoid intake, calculated from the food frequency questionnaire (FFQ), and VFA was evaluated in a few studies, wherein it was found that the higher the intake of β-carotene and lycopene, the lower the VFA in middle-aged and older men [17]. However, there has been no comprehensive assessment of the relationship between VFAs and levels of different carotenoids in the blood. To our knowledge, the age group for which the evaluations have been performed are also limited, and the studies evaluating a wide range of age groups, including younger age groups, are lacking. Ryo et al. developed a noninvasive, easy-to-measure method for VFA, the results of which highly correlate with the measurements by CT [18]. They evaluated the relationship between VFA levels measured using the device developed by them and various biomarkers and environmental factors relevant to the field of medical examination and found a negative relationship between VFA and intake of dietary fiber (total and water-soluble), mainly taken through vegetables, as well as carotenoids [19]. However, the relationship between carotenoids and VFA has remained unclear. In this study, we evaluated the relationship between serum carotenoid levels and VFA, including dietary habits, such as dietary fiber intake, in healthy individuals who participated in the Iwaki Health Promotion Project, a health examination project for a wide range of age groups. 2. Materials and Methods 2.1. Study Design and Subjects This cross-sectional study was based on an annual health examination (the Iwaki Health Promotion Project) for the residents of the rural area of Hirosaki city, Aomori prefecture, Japan, conducted by Hirosaki University in May and June 2015. Of all participants (n = 1113), 805 (310 males and 495 females) were included as healthy subjects (Figure 1). Complete clinical data were available for these subjects, and they were not on any medication for dyslipidemia and had no history of serious diseases, such as cancer, stroke, cardiovascular diseases, liver diseases, kidney diseases, or diabetes. All proce- dures, including subject recruitments, were conducted in accordance with the Declaration of Helsinki and were approved by the ethics boards of Hirosaki University School of Medicine (2014-377, 2016-028) and KAGOME CO., LTD. (2015-R04). Written informed consent was provided by all subjects. This work has also been registered in the public in- Nutrients 2021, 13, 912 3 of 16 formation database UMIN-CTR by Hirosaki University and Kao Corporation (registration number: UMIN000030351). Figure 1. Flowchart for the recruitment of participants. 2.2. Body Measurements We measured VFA using the EW-FA90 (Panasonic Corporation, Osaka, Japan) based on an abdominal bioimpedance method developed at the Kao Corporation. BMI was calculated from the body weight and height, which were obtained by anthropometric measurements. 2.3. Self-Administered Questionnaire On the day of the health examination, we collected the self-developed questionnaires that the participants had filled out in advance. The questionnaire contained information about sex, age, current smoking habits, exercise habits, medical history, and medications. We defined an exerciser as a person who habitually exercised at least 30 min a day and at least twice a week throughout the year. The volume of food consumed (g/day), including alcohol intake, was estimated using a brief-type self-administered diet history questionnaire (BDHQ) [20]. The daily intake for key food groups is calculated using BDHQ based on the past month’s dietary surveys. 2.4. Blood Sampling and Testing Blood was collected from the median cubital vein after overnight fasting. The serum carotenoids were quantified at KAGOME CO., LTD. (Nagoya, Japan). Carotenoids (lutein, zeax- <ul style="display: flex;"><li style="flex:1">anthin, </li><li style="flex:1">β-cryptoxanthin, </li><li style="flex:1">α-carotene, </li><li style="flex:1">β-carotene, and lycopene) were extracted and measured </li></ul>in accordance with the methods described previously [21,22]. We used a high-performance liquid chromatograph with a photodiode array detector (Prominence LC-30AD/Nexera X2 SPPD-M30A, SHIMADZU CORPORATION, Kyoto, Japan) for the measurements. 2.5. Statistical Analyses As described in our previous report [8], the mean value of each measurement was stratified by sex (male and female) and compared using Student’s t-test. It was also Nutrients 2021, 13, 912 4 of 16 stratified by age category (young, 20–39 years; middle-aged, 40–59 years; old ≥60 years) and compared using one-way ANOVA (post hoc: Bonferroni). Because previous studies have shown that carotenoid concentrations do not follow normality [8], Mann–Whitney U test and Kruskal–Wallis test (post hoc: Bonferroni) were used for the carotenoids. Correlation analysis between serum concentrations of carotenoids and other factors (VFA, BMI, and foods) stratified by sex was performed using Pearson’s correlation coefficient. Multiple regression analysis stratified by sex and age was conducted to evaluate the relationships between the serum concentrations of carotenoids and VFA or BMI. VFA and BMI were adopted as objective variables, whereas carotenoids were adopted as explana- tory variables. Age, use of medication for some diseases (hypertension, hyperlipidemia, diabetes, dementia, rheumatism, and steroids), alcohol intake, current smoking habits, exercise habits, and total dietary fiber intake were adopted as adjustment factors according to the analysis. Analyses were performed using the R statistical package (version 3.5.1, R Foundation for Statistical Computing, Vienna, Austria) and EZR (version 1.4) [23], and a p-value < 0.05 was considered statistically significant. 3. Results 3.1. Characteristics of the Study Subjects The mean values of all measurements stratified by sex and age categories are shown in Table 1. Both smoking habit and exercise habit rates were higher in males than in females in total. VFA and BMI were significantly higher in males in total. In males, VFA in the young individuals was lower than that in the middle-aged and old individuals, and it increased by age in females. BMI was significantly higher in old individuals compared with that in young ones only in females. Serum concentrations of carotenoids were higher in females except for zeaxanthin and lycopene. Concentrations of serum lycopene were significantly lower in the old in both males and females. For most of the other carotenoids, the serum levels were higher in middle-aged and old individuals than in the young ones. Dietary fiber intake was higher in older age groups. The intake of carrots and pumpkin, and root vegetables was higher in females than in males. For both males and females, the intake of “radish/turnip” and “pickles” was higher in the old than in the other age groups. 3.2. Relationship between Serum Carotenoid Concentrations and VFA/BMI Table 2 shows simple correlation coefficients between serum concentrations of carotenoids and VFA or BMI. The correlation coefficient between α-carotene and β-carotene was found to be high in previous studies [ a representative for the assessment. 8], and the β-carotene concentration was used as In males, neither VFA nor BMI showed significant correlations with either total carotenoids or individual carotenoids. In contrast, both VFA and BMI were negatively <ul style="display: flex;"><li style="flex:1">correlated with total carotenoids, lutein, </li><li style="flex:1">β-carotene, and lycopene in females. BMI also had </li></ul>a negative correlation with zeaxanthin in females. Nutrients 2021, 13, 912 5 of 16 Table 1. Characteristics of the study subjects. <ul style="display: flex;"><li style="flex:1">Male </li><li style="flex:1">Female </li></ul><ul style="display: flex;"><li style="flex:1">Measurement Item </li><li style="flex:1">All </li></ul>Young (20–39 Years) Middle-Aged (40–59 Years) Young (20–39 Years) Middle-Aged (40–59 Years) <ul style="display: flex;"><li style="flex:1">All </li><li style="flex:1">Old (≥60 Years) </li><li style="flex:1">All </li><li style="flex:1">Old (≥60 Years) </li></ul>N Age, year <ul style="display: flex;"><li style="flex:1">805 </li><li style="flex:1">310 </li></ul>49.1 ± 14.8 21.8 ± 24.2 32.6 <ul style="display: flex;"><li style="flex:1">103 </li><li style="flex:1">118 </li></ul>49.6 ± 5.5 25.8 ± 24.8 37.3 89 67.7 ± 5.8 19 ± 20.8 20.2 <ul style="display: flex;"><li style="flex:1">495 </li><li style="flex:1">120 </li></ul>32.5 ± 5.1 4.3 ± 9.9 11.7 <ul style="display: flex;"><li style="flex:1">188 </li><li style="flex:1">187 </li></ul>51.1 ± 14.8 11 ± 19 32.5 ± 4.6 19.8 ± 25.6 37.9 52.3 ± 14.6 ** 4.2 ± 10.1 *** 11.3 50 ± 5.8 6.2 ± 12.4 17.6 67.3 ± 5.8 2.3 ± 6.9 b 4.8 Alcohol intake, g/day <ul style="display: flex;"><li style="flex:1">Smoking, % </li><li style="flex:1">19.5 </li></ul>Habitual exercise, % Medication, % <ul style="display: flex;"><li style="flex:1">9.2 </li><li style="flex:1">11.3 </li><li style="flex:1">12.6 </li><li style="flex:1">11.9 </li><li style="flex:1">9</li><li style="flex:1">7.9 </li><li style="flex:1">9.2 </li><li style="flex:1">6.9 </li><li style="flex:1">8</li></ul><ul style="display: flex;"><li style="flex:1">19.3 </li><li style="flex:1">16.5 </li><li style="flex:1">2.9 </li><li style="flex:1">13.6 </li><li style="flex:1">36 </li><li style="flex:1">21 </li><li style="flex:1">0.8 </li><li style="flex:1">11.2 </li><li style="flex:1">43.9 </li></ul><ul style="display: flex;"><li style="flex:1">VFA, cm2 </li><li style="flex:1">72.4 ± 32.49 ab </li></ul>22.58 ± 3.28 a 1.84 ± 0.84 ab 0.41 ± 0.16 ab 0.06 ± 0.02 0.21 ± 0.12 ab 0.21 ± 0.17 0.74 ± 0.52 ab 0.21 ± 0.12 ab 79.11 ± 42.28 22.58 ± 3.46 1.47 ± 0.72 0.34 ± 0.14 0.06 ± 0.02 0.15 ± 0.1 0.17 ± 0.16 0.5 ± 0.42 0.25 ± 0.13 102.81 ± 44.96 23.61 ± 3.23 1.15 ± 0.53 0.3 ± 0.13 0.06 ± 0.02 0.11 ± 0.06 0.13 ± 0.14 0.3 ± 0.28 0.24 ± 0.13 92.2 ± 47.62 23.14 ± 3.86 1.07 ± 0.5 0.25 ± 0.1 0.06 ± 0.02 0.1 ± 0.05 0.13 ± 0.15 0.25 ± 0.25 0.28 ± 0.14 108.1 ± 41.09 a 24.13 ± 2.87 1.13 ± 0.53 0.31 ± 0.12 a 0.06 ± 0.02 0.1 ± 0.05 0.13 ± 0.13 0.28 ± 0.28 0.24 ± 0.12 108.07 ± 45.03 a 23.47 ± 2.8 1.28 ± 0.56 a 0.35 ± 0.15 a 0.06 ± 0.02 0.14 ± 0.08 ab 0.14 ± 0.14 0.39 ± 0.28 ab 0.19 ± 0.13 ab 64.27 ± 32.74 *** 21.94 ± 3.45 *** 1.67 ± 0.75 *** 0.36 ± 0.15 *** 0.06 ± 0.02 0.17 ± 0.11 *** 0.2 ± 0.16 *** 0.62 ± 0.44 *** 0.26 ± 0.14 53.13 ± 32.36 21.22 ± 3.95 1.5 ± 0.68 0.3 ± 0.11 0.06 ± 0.02 0.13 ± 0.06 0.21 ± 0.19 0.5 ± 0.36 0.3 ± 0.13 63.31 ± 31.13 a 21.76 ± 3.16 1.61 ± 0.68 0.35 ± 0.15 a 0.06 ± 0.02 0.17 ± 0.11 a 0.19 ± 0.12 0.57 ± 0.36 a 0.27 ± 0.13 BMI, kg/m2 Total carotenoid, µg/mL Lutein, µg/mL Zeaxanthin, µg/mL β-Cryptoxanthin, µg/mL α-Carotene, µg/mL β-Carotene, µg/mL Lycopene, µg/mL BDHQ Total dietary fiber, g/day Soluble dietary fiber, g/day Insoluble dietary fiber, g/day Fresh vegetables, g/day Green leafy vegetables, g/day Carrot and pumpkin, g/day Tomato, g/day 10.74 ± 4.40 2.66 ± 1.20 7.73 ± 3.05 11.11 ± 4.74 2.72 ± 1.32 8.04 ± 3.24 9.55 ± 3.52 2.33 ± 0.99 6.95 ± 2.50 10.58 ± 4.23 2.57 ± 1.18 7.67 ± 2.90 10.51 ± 4.16 2.62 ± 1.13 8.98 ± 3.75 2.26 ± 1.01 6.46 ± 2.61 10.36 ± 3.93 a 2.60 ± 1.08 a 7.42 ± 2.71 a 26.33 ± 19.04 31.95 ± 31.01 17.33 ± 14.01 20.25 ± 23.81 27.5 ± 23.32 13.47 ± 14.28 31.42 ± 24.36 4.15 ± 6.81 13.63 ± 5.56 ab 3.38 ± 1.56 ab 9.79 ± 3.72 ab 25.24 ± 21.89 29.4 ± 28.5 16.28 ± 13.39 0.58 ± 21.01 34.12 ± 33.34 20.4 ± 24.45 ab 32.83 ± 33.55 10.42 ± 12.67 ab 11.63 ± 4.33 ab 2.86 ± 1.19 a 8.37 ± 3.04 ab 24.25 ± 19.91 30.21 ± 28.89 20.22 ± 17.11 21.45 ± 24.79 32.1 ± 29.23 7.54 ± 2.90 * 24.8 ± 19.32 30.25 ± 29.04 18.36 ± 15.78 *** 19.95 ± 22.76 28.71 ± 25.76 15.31 ± 16.49 31.36 ± 24.18 * 5.6 ± 8.88 <ul style="display: flex;"><li style="flex:1">25 ± 19.88 </li><li style="flex:1">25.31 ± 20.77 </li></ul>26.73 ± 27.81 14.23 ± 13.52 18.49 ± 19.96 30.27 ± 27.24 15.3 ± 18.84 27.52 ± 26.27 6.84 ± 9.05 23.94 ± 20.38 26.09 ± 24.93 12.9 ± 12.13 17.35 ± 19.82 26.29 ± 22.66 12.86 ± 13.64 24.74 ± 20.37 4.59 ± 5.33 26.56 ± 20.33 25.28 ± 29.7 13.84 ± 14.64 17.9 ± 19.31 30.84 ± 25.52 13.57 ± 17.25 25.95 ± 24.16 6.1 ± 7.5 23.26 ± 18.81 27.64 ± 25.94 17.08 ± 16.07 17.14 ± 16.98 25.34 ± 23.09 13.12 ± 14.23 30.29 ± 23.55 3.36 ± 6.37 28.89 ± 28.61 16.77 ± 15.07 19.39 ± 21.72 29.31 ± 26.34 15.31 ± 17.42 29.88 ± 25.06 6.08 ± 8.96 Cabbage, g/day 18.57 ± 19.25 ab 31.99 ± 24.49 8.5 ± 11.08 ab Radish and turnip, g/day Root vegetables, g/day Pickled green leafy vegetables, g/day

Association Between Serum Concentration of Carotenoid and Visceral Fat

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