Taurine's health influence on Japanese high school girls
- 2.9k Downloads
The prevalence of metabolic syndrome (MS) in children and adolescents has been increasing at an alarming rate. MS risks during childhood and adolescence adversely affect health conditions in later life. Thus, the characterization of their MS risks is a critical research field. The aims of this study are to survey the health status of Japanese adolescent females, a poorly characterized population, and to investigate the potential relationship between their MS risks and dietary factors like potassium (K) and taurine.
Anthropometric characteristics of 243 healthy school girls aged 13 to 18 years were measured. Serum levels of triglycerides, total cholesterol and high-density lipoprotein (HDL), and plasma levels of glucose and insulin were analyzed in fasting blood samples. We assessed overweight, disturbed lipid prolife, higher blood pressure (hBP) and higher plasma glucose (hGlc) levels as indicators of MS risks. The relationships between MS risks and urinary K or taurine excretion were investigated by dividing into higher and lower groups at medians of their urinary excretions.
Half of junior high school (JHS) and one-quarter of senior high school (SHS) girls had at least one MS risk. The quite common risk was hGlc, the rates being 21% in JHS girls and 14% in SHS. The prevalence of being overweight and obesity were only small portions, the rate being 0% and 0% in JHS girls, and 10% and 1% in SHS, respectively. Substantial differences in the prevalence of hBP were observed between JHS (22%) and SHS (4%) girls. Furthermore, higher urinary K excretion group showed a significant decrease in triglyceride level (P = 0.03) and increase in HDL level (P = 0.003) compared with the lower. Also, the higher urinary taurine excretion group exhibited a significant reduction in triglyceride level (P = 0.04) compared with the lower.
These results indicate that control of plasma glucose level rather than body weight is a crucial task in Japanese pubertal girls, and that a dietary habit rich in K and taurine could improve their lipid profile. Nutritional education based on these findings would help to prevent the future development of MS in Japanese female adolescents.
KeywordsTaurine Dietary Habit Junior High School Senior High School Abdominal Circumference
List of abbreviations used
body mass index
- CARDIAC study
cardiovascular diseases and alimentary comparison study
diastolic blood pressure
disturbed lipid profile
higher plasma glucose
higher blood pressure
homeostasis and assessment of insulin resistance
high performance liquid chromatography
junior high school
senior high school
systolic blood pressure.
Metabolic syndrome (MS) is a cluster of risk factors for type 2 diabetes mellitus (T2DM) and cardiovascular diseases (CVDs), which includes obesity, insulin resistance, hypertension and dyslipidemia. A recent large cohort study on school children revealed the significant association of higher MS risks during childhood with increased risks for CVDs in adulthood . This implies not only that the origins of T2DM and CVDs begin in childhood and adolescence, but also that MS risks in childhood and adolescence adversely affect health conditions in later life. Given that the prevalence of MS in children and adolescents has been increasing at an alarming rate [2, 3], the worldwide epidemic of MS could further accelerate in the near future. To prevent such a public health crisis, it is critically important to understand MS risks in children and adolescents as well as adults. However, little is known about health status and MS risks of Asian young population, although those in European and American children and adolescents have been reported [1, 2, 4].
Our world-wide epidemiological study collaborating with WHO was designated Cardiovascular Diseases and Alimentary Comparison (CARDIAC) study, and has been carried out over the past 25 years in 61 populations in 25 countries to determine the relationship between their MS risks and dietary habits [5, 6, 7, 8]. In each population, about 100 males and 100 females aged 48 to 56 years were randomly selected, with the number of participants being over 14,000 in all. The CARDIAC study yielded interesting findings. Namely, the populations with higher sodium (Na) excretion in 24-h urine, correlated with high salt intake, had increased risk for stroke compared with those with lower, whereas the populations with higher taurine excretion, correlated with high seafood intake, had decreased risk for coronary heart disease compared with those with lower [7, 9, 10]. Also, increased excretion of urinary potassium (K), an indicator for vegetables and fruits intakes, was reported to inversely correlate with body mass index (BMI) and blood pressure (BP) . These findings indicate that dietary habit beneficially or adversely affect health status and MS risks. Thus, the characterization of dietary habits may provide a clue to properly control MS risks. Considering that the recording of accurate dietary history is difficult for participants, 24-h urine analysis would be a practical and reliable tool for the characterization of dietary habits. In this study, we conducted a health survey of 243 healthy school girls aged 13-18 years at Mukogawa High School in Nishinomiya, Japan, to obtain baseline data on the health status of Japanese adolescent females, and then investigated the potential relationship between their MS risks and dietary habits by 24-h urine analysis in combination with anthropometric measurements and blood chemical analysis.
A total of 243 healthy school girls aged 13 to 18 years participated in this health survey held at Mukogawa junior and senior high school in Nishinomiya, Japan, from 2007 to 2008. The participants were composed of 67 junior high school (JHS) girls and 176 senior high school (SHS) ones. The study design was approved by the research ethics committee of the Mukogawa Women's University.
Anthropometric characteristics, including height, weight and abdominal circumference (AC), were measured. BMI was calculated as (body weight [kg])/(height [m])2. BP was measured twice with an automated sphygmomanometer (HEM-970; OMRON, Kyoto, Japan) in sitting position after over 10 minutes rest and the average was used in this study. According to the criteria of MS risks in JHS and SHS students established by the Ministry of Health, Labour and Welfare in Japan, higher BP (hBP), overweight, obesity and increased AC were defined as follows: hBP, systolic BP (SBP) ≧ 125 mmHg and/or diastolic BP (DBP) ≧ 70 mmHg for JHS students and SBP ≧ 130 mmHg and/or DBP ≧ 80 mmHg for SHS ones; overweight, BMI ≧ 25; obesity, BMI ≧ 30; increased AC, AC (cm)/height (cm) ≧ 0.5 or AC ≧ 80 cm for JHS students and AC ≧ 90 cm for SHS ones. Also, the rate of thinness (BMI < 18.5) in the participants was determined according to the criterion set by the Japan Society for the Study of Obesity.
Blood chemical analysis
Blood samples were obtained after a more than 3-h fasting. Serum levels of triglycerides, total cholesterol and high-density lipoprotein (HDL), and plasma levels of insulin and glucose were determined by SRL, Inc (Tokyo, Japan). According to the criteria of MS risks in JHS and SHS students established by the Ministry of Health, Labour and Welfare in Japan, higher plasma glucose (hGlc) and disturbed lipid profile (dLP) were defined as follows: hGlc, fasting plasma glucose ≧ 110 g/ml; dLP, serum triglycerides ≧ 120 mg/dl and/or serum HDL < 40 mg/dl for JHS students and serum triglycerides ≧ 150 mg/dl and/or serum HDL < 40 mg/dl for SHS ones. Insulin resistance (homeostasis model assessment of insulin resistance: HOMA-IR) was calculated using the following formula: HOMA-IR = fasting plasma insulin (μIU/ml) × fasting plasma glucose (mg/dl)/405.
Twenty-four-hour urine analysis
A 24-h urine specimen was collected using a standard aliquot cup that allowed the participants to repeatedly collect an exact portion of voided urine . Taurine concentration (μmol/ml) in the 24-h urine sample was measured by high performance liquid chromatography (HPLC) (GL Sciences, Tokyo, Japan). The concentrations of K (mEq/l) and Na (mEq/l) were determined by ion selective electrodes at SRL, Inc (Tokyo, Japan). Creatinine concentration (mg/l) in the 24-h urine sample was measured by an enzyme method at SRL, Inc. Urinary excretions per day of taurine (μmol/day), K (g/day), Na (g/day) and creatinine (mg/day) were estimated from their urinary concentrations and daily urine volume. Daily intake of NaCl (g/day) was determined from urinary Na excretion. Subjects who had failed to appropriately collect 24-h urine samples were determined by calculating creatinine coefficient (creatinine/body weight) and excluded from this urinary analysis. Two hundred twelve students successfully collected 24-h urine samples. The participants were divided into two (higher or lower) groups at a median of each urinary taurine or K excretion. The differences in the MS risks of their groups were analyzed and compared.
Differences between the two groups were evaluated by student t-test. P values less than 0.05 were considered as significant for every statistical analysis.
MS risks in Japanese JHS and SHS girls
Anthropometric and blood chemical profiles of junior and senior high school girls
Junior high school girls (n = 67)
Senior high school girls (n = 67)
14.3 ± 0.7
17.1 ± 0.7*
19.4 ± 2.1
21.1 ± 2.7*
107.6 ± 9.8
107.9 ± 10.5
64.2 ± 7.3
63.8 ± 7.6
78.3 ± 47.0
70.2 ± 37.2
171.4 ± 22.5
181.0 ± 31.4
60.3 ± 10.6
63.5 ± 12.7
92.9 ± 8.6
92.2 ± 8.0
14.9 ± 12.2
12.5 ± 11.0
3.5 ± 3.2
2.9 ± 2.8
Inverse correlations between urinary K excretion and dyslipidemic risk in Japanese adolescent girls
Daily intake of NaCl and Urinary profiles in junior and senior high school girls
Junior high school girls (n = 54)
Senior high school girls (n = 158)
8.3 ± 3.0
7.9 ± 3.2
1.4 ± 0.5
1.4 ± 0.5
4.5 ± 2.6
4.0 ± 1.7
957.1 ± 717.9
920.7 ± 651.1
Inverse correlations between urinary taurine excretion and dyslipidemic risk in Japanese adolescent girls
Recent studies demonstrate that the prevalence of MS in children and adolescents living in Europe and North America has dramatically increased in parallel with that in adults [2, 3]. There is only limited information available on the prevalence of MS in the Asian young generation, including Japanese, who differs from European and American ones in the component and pathologic mechanisms of MS. These prompted us to survey health status of Japanese school girls and to investigate how their dietary habits affect MS risks.
Anthropometric and blood chemical analyses showed that half of JHS girls and one-quarter of SHS girls had at least one MS risk. The quite common MS risk among JHS and SHS girls was hGlc. These features may reflect excess consumption of sugar-sweetened soft drinks and snacks, decreased physical activity or both. With respect to BMI, the rate of overweight (10%) in SHS girls was found to be nearly equal to the rates of Hong Kong's (9.8%) and British (11.7%) girls, and much lower than those of American (24.0%) and Brazilian ones (15.2%) [13, 14], although it seems hard to directly compare their overweight rates because of some differences in age and study period. Given the rate of obesity in JHS and SHS groups were as small as 0% and 1%, respectively, overweight and obesity are likely to be minor risk factors in Japanese female adolescents compared with American and Brazilian ones with a high prevalence of obesity. Also, the substantial difference in the rates of hBP between JHS (22%) and SHS (4%) girls might be attributed to the application of different criterion for hBP established by the Japanese government. Alternatively, such a difference could be accounted for by a higher intake of salty foods in JHS group, because their daily intake of NaCl and Na/K ratio were larger than those of SHS.
Thinness during adolescence and young adulthood is associated with adverse health consequences in later life, such as osteoporosis and unfavorable pregnancy outcomes, which is regarded as another important health concern different from MS [15, 16]. Thus, we also investigated the prevalence of thinness and confirmed the non-negligible proportion in Japanese school girls. Other groups also demonstrated the increasing trend of thinness particularly in young Japanese women aged 15-29 years . Because such a national trend is attributed mainly to an excess desire for slim body shape , nutritional education on risks of unhealthy weight loss as well as on benefits of healthy diets would serve to prevent the unfavorable epidemic.
Our group and other groups reveal that urinary excretions of particular minerals and food factors are associated with dietary habit. For instance, increased urinary excretions of Na, K, and taurine significantly correlate with intakes of salty foods, vegetables and fruits, and seafood, respectively [7, 8, 10, 19]. Thus, 24-h urine analysis, in combination with anthropometric and blood chemical analyses, enables us to link between MS risks and dietary habit. Indeed, a significant reduction in serum triglyceride level and increase in serum HDL level were observed in higher urinary K excreters, indicating that the higher group had a lower risk for dyslipidemia. Such an improvement on serum triglyceride level was shown in the higher urinary taurine excretion group. Intakes of vegetables and fruits rich in K, and seafood rich in taurine are likely useful for getting a better lipid profile of Japanese pubertal girls. Furthermore, we confirmed a decreased tendency in insulin level and HOMA-IR in higher urinary taurine excreters, although the differences did not reach statistical significance possibly due to a small studied population. It points out the possibility that taurine could prevent the future development of insulin resistance, a major cause of T2DM and CVDs.
It is widely accepted that the increased intakes of vegetables and fruits or seafood lead to improvement in anthropometric parameters, particularly BP, in adults [20, 21]. Hence, one might ask why a significant decrease in anthropometric parameters, such as BP and BMI, was not observed in higher K and taurine excretion groups. Although the reason remains unclear, it could be explained by a small studied population, high rates of non-obese and normotensive participants, or both. Further studies are needed to clarify the correlations between dietary habit and each MS risk in Japanese female adolescents.
We here demonstrate that hGlc is quite a common MS risk in Japanese JHS and SHS girls aged 13-18 years, whereas overweight and obesity are minor risk factors. These findings indicate that control of plasma glucose level rather than body weight is a crucial task in Japanese pubertal girls. We also confirm that dietary habit rich in K and taurine, namely adequate intakes of vegetables, fruits and seafood, can improve their lipid profile. Given that vegetables, fruits and seafood abundantly contain multifunctional dietary factors other than K and taurine, such as folate and n-3 fatty acids, nutritional education promoting healthy dietary habit would help to improve health status and to prevent the future development of MS in Japanese female adolescents.
Written consent was obtained from all participants for publication of this study. We thank all participants for their invaluable cooperation. This work has been implemented in part by Yamada Bee Farm Grant for Honeybee Research (to MM).
This article has been published as part of Journal of Biomedical Science Volume 17 Supplement 1, 2010: Proceedings of the 17th International Meeting of Taurine. The full contents of the supplement are available online at http://www.jbiomedsci.com/supplements/17/S1.
- 3.Zimmet P, Alberti G, Kaufman F, Tajima N, Silink M, Arslanian S, Wong G, Bennett P, Shaw J, Caprio S, International Diabetes Federation Task Force on Epidemiology and Prevention of Diabetes: The metabolic syndrome in children and adolescents. Lancet. 2007, 369: 2059-2061. 10.1016/S0140-6736(07)60958-1.CrossRefPubMedGoogle Scholar
- 4.Steinberger J, Daniels SR, American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee (Council on Cardiovascular Disease in the Young); American Heart Association Diabetes Committee (Council on Nutrition, Physical Activity, and Metabolism): Obesity, insulin resistance, diabetes, and cardiovascular risk in children: an American Heart Association scientific statement from the Atherosclerosis, Hypertension, and Obesity in the Young Committee (Council on Cardiovascular Disease in the Young) and the Diabetes Committee (Council on Nutrition, Physical Activity, and Metabolism). Circulation. 2003, 107: 1448-1453. 10.1161/01.CIR.0000060923.07573.F2.CrossRefPubMedGoogle Scholar
- 5.WHO and WHO Collaborating Center: CARDIAC (Cardiovascular Diseases and Alimentary Comparison) study protocol. Shimane, Geneva. 1986Google Scholar
- 6.Yamori Y: Hypertension and biological dietary markers in urine and blood: a progress report from the CARDIAC study group. New horizons in preventing cardiovascular diseases. Edited by: Yamori Y, Strasser T. 1989, Amsterdam: Elsevier, 111-126.Google Scholar
- 7.Yamori Y, Nara Y, Mizushima S, Mano M, Sawamura M, Kihara M, Horie R: International cooperative study on the relationship between dietary factors and blood pressure: a report from the Cardiovascular Diseases and Alimentary Comparison (CARDIAC) Study. J Cardiovasc Pharmacol. 1990, 16 (Suppl 8): S43-47.CrossRefPubMedGoogle Scholar
- 8.Yamori Y, Liu L, Ikeda K, Miura A, Mizushima S, Miki T, Nara Y, WHO-Cardiovascular Disease and Alimentary Comparison (CARDIAC) Study Group: Distribution of twenty-four hour urinary taurine excretion and association with ischemic heart disease mortality in 24 populations of 16 countries: results from the WHO-CARDIAC study. Hypertens Res. 2001, 24: 453-457. 10.1291/hypres.24.453.CrossRefPubMedGoogle Scholar
- 20.Appel LJ, Moore TJ, Obarzanek E, Vollmer WM, Svetkey LP, Sacks FM, Bray GA, Vogt TM, Cutler JA, Windhauser MM, Lin PH, Karanja N: A clinical trial of the effects of dietary patterns on blood pressure. DASH Collaborative Research Group. N Engl J Med. 1997, 336: 1117-1124. 10.1056/NEJM199704173361601.CrossRefPubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.