Journal List > Korean J Community Nutr > v.16(1) > 1038314

Kim, Kim, Bae, Kim, Lee, Na, and Sohn: Relationship between Nutrients Intakes, Dietary Quality, and Serum Concentrations of Inflammatory Markers in Metabolic Syndrome Patients

Abstract

Elevated serum concentration of inflammation markers is known as an independent risk factor of metabolic syndrome (MS) and dietary intake is an important factor to control MS. The purpose of this study was to investigated the hypothesis that inflammatory indices are associated with dietary intake and diet quality index-international (DQI-I) in subjects with MS. A cross-sectional study was conducted on 156 men and 73 postmenopausal women with MS, defined by three or more risk factors of the modified Adult Treatment Panel III criteria. Serum levels of high sensitive C-reactive protein (hs-CRP), adiponectin were examined and nutrients intake and DQI-I were assessed using a semiquantitative food frequency questionnaire. The total DQI-I score was significantly higher in female subjects (65.87 ± 9.86) than in male subjects (62.60 ± 8.95). There was a positive association between hs-CRP and polyunsaturated fatty acid intake (p < 0.05) and a negative association between adiponectin and lipid (p < 0.05), total sugar (p < 0.01), and total fatty acids (p < 0.05). When the subjects were divided into 5 groups by quintile according to serum adiponectin and hs-CRP level, there was no association between DQI-I score and hs-CRP levels. Moderation score of DQI-I was significantly higher in highest quintile group than the lower quintile groups. Therefore, our results provide some evidence that dietary intake and diet quality are associated with inflammation markers and dietary modification might be a predictor to decrease risk for metabolic syndrome complications. However further research is needed to develop the dietary quality index reflecting the inflammatory change by considering the dietary habit and pattern of Koreans. (Korean J Community Nutr 16(1) : 51~61, 2011)

REFERENCES

Ahn Y., Lee JE., Cho NH., Shin C., Park C., Oh BS., Kimm K. 2004. Validation and calibration of semi-quantitative food frequency questionnaire. Korean J Community Nutr. 9(2):173–182.
Arita Y., Kihara S., Ouchi N., Takahashi M., Maeda K., Miyagawa J., Hotta K., Shimomura I., Nakamura T., Miyaoka K., Kuriyama H., Nishida M., Yamashita S., Okubo K., Matsubara K., Muraguchi M., Ohmoto Y., Funahashi T., Matsuzawa Y. 1999. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 257:79–83.
crossref
Bae SJ., Son HY., Pyun DK., Nah SS., Koh JM., Kim GS. 2004. Higher circulating hs-CRP levels are associated with lower bone mineral density in healthy premenopausal and postmenopausal women: evidence for link between systemic inflammation and osteoporosis. Korean J Bone Metab. 11:147–157.
Choi EY., Park EH., Cheong YS., Rheem I., Park SG., Yoo S. 2006. Association of C-reactive protein with the metabolic risk factors among young and middle-aged Koreans. Metabolism. 55:415–422.
crossref
Choi MK., Jun YS., Bae YJ., Sung CJ. 2007. A study on nutrient intakes and blood parameters of adult men and women with metabolic syndrome. J Korean Soc Food Sci Nutr. 36(3):311–317.
crossref
Esmaillzadeh A., Kimiagar M., Mehrabi Y., Asadbakht L., Hu FB., Willett WC. 2006. Fruit and vegetable intakes, C-reactive protein, and the metabolic syndrome. Am J Clin Nutr. 84(6):1489–1497.
crossref
Esposito K., Nappo F., giugliano F., DiPalo C., Ciotola M., Barbieri M., Paolisso G., Giugliano D. 2003. Meal modulation of circulating interleukin 18 and adiponectin concentrations in healthy subjects and in patients with type 2 diabetes mellitus. Am J Clin Nutr. 78(6):1135–1140.
crossref
Esteve E., Ricart W., Fernández-Real JM. 2009. Adipocytokines and insulin resistance: the possible role of lipocalin-2, retinol binding protein-4, and adiponectin. Diabetes Care 32(Suppl 2): S362-367.
Feingold KR., Grunfeld C. 1992. Role of cytokines in inducing hyperlipidemia. Diabetes. 41(2):97–101.
crossref
Fredrikson GN., Hedblad B., Nilsson JA., Alm R., Berglund G., Nilsson J. 2004. Association between diet, lifestyle, metabolic cardiovascular risk factors, and plasma C-reactive protein levels. Metabolism. 53(11):1436–1442.
crossref
Fung TT., McCullough ML., Newby PK., Manson JE., Meigs JB., Rifai N., Willett WC., Hu FB. 2005. Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr. 82(1):163–173.
crossref
Gabay C., Kushner I. 1999. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 340:448–454.
crossref
Ghayour-Mobarhan M., Yaghootkar H., Lanham-New SA., Lamb DJ., Ferns GA. 2007. Association between serum CRP concentrations with dietary intake in healthy and dyslipidaemic patients. Asia Pac J Clin Nutr. 16(2):262–268.
Giugliano D., Ceriello A., Esposito K. 2006. The effects of diet on inflammation: Emphasis on the metabolic syndrome. J Am Coll Cardiol. 48(4):677–685.
International Obesity Task Force (1999): Asia-Pacific regional obesity guideline. International Association for the Study of Obesity. Sydney Isomaa B., Almgren P., Tuomi T., Forsen B., Lahti K., Lissen M., Taskinen MR., Groop L. 2001. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 24(4):683–689.
Jang M. 2010. . Repeated nutrition education has positive effect on health improvement at workplace. MS thesis, Kyunghee University Kasim-Karakas SE, Tsodikov A, Singh U, Jialal I (2006): Responses of inflammatory markers to a low-fat, high-carbohydrate diet; effects of energy intake. Am J Clin Nutr. 83(4):774–779.
Kim BJ., Kim WG., Jung CH., Byun SW., Koh JM., Kim GS. 2006. Relationship between bone turnover rate and a systemic inflammatory marker in Korean women. Korean J Bone Metab. 13:129–138.
Kim S., Haines PS., Siega-Riz AM., Popkin BM. 2003. The diet quality index-international (DQI-I) provides an effective tool for cross-national comparison of diet quality as illustrated by China and the United States. J Nutr. 133(11):3476–3484.
crossref
Koenig W., Sund M., Frohlich M., Fischer HG., Lowel H., Doring A., Hutchinson WL., Pepys MB. 1999. C-Reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation. 99:237–242.
Krakoff J., Funahashi T., Stehouwer CD., Schalkwijk CG., Tanaka S., Matsuzawa Y., Kobes S., Tataranni PA., Hanson RL., Knowler WE., Lindsay RS. 2003. Inflammatory markers, adiponectin, and risk of type 2 diabetes in the Pima Indian. Diabetes Care. 26(6):1745–1751.
crossref
Kumada M., Kihara S., Sumitsuji S., Kawamoto T., Matsumoto S., Ouchi N., Arita Y., Okamoto Y., Shimomura I., HIraoka H., Nakamura T., Funahashi T., Matsuzawa Y. for the Osaka CAD study group. 2003. Association of hypoadiponectinemia with coronary artery disease in men. Arterioscler Thromb Vasc Biol. 23:85–89.
crossref
Lakka HM., Laaksonen DE., Lakka TA., Niskanen LK., Kumpusalo E., Tuomilehto J., Salonen JT. 2002. The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA. 288:2709–2716.
crossref
Lara-Castro C., Fu Y., Chung BH., Garvey WT. 2007. Adiponectin and the metabolic syndrome: mechanisms mediating risk for metabolic and cardiovascular disease. Curr Opin Lipidol. 18(3):263–267.
crossref
Lee MY., Kim JH. 2010. Association of serum lipids and dietary intakes with serum adiponectin level in overweight and obese Korean women. Korean J Community Nutr. 15(1):27–35.
Mckeown NM., Liu E., Meigs JB., Rogers G., D'Agostino R., Jacques P. 2009. Carbohydrate-related dietary factors and plasma adiponectin levels in healthy adults in the Framingham Offspring Cohort. FASEB J 23 (Meeting abstract supplement) 229.5.
Ministry of Health and Welfare (MOHW). 2005. Korea national health and nutrition examination survey report (KNHANES III).
Mohamed-Ali V., Goodrick S., Rawesh A., Katz DR., Miles JM., Yudkin JS. 1997. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-a, in vivo. J Clin Endocrinol Metab. 82(12):4196–4200.
Mottillo S., Filion KB., Genest J., Joseph L., Pilote L., Poirier P., Rinfret S., Schiffrin EL., Eisenberg MJ. 2010. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol. 56(14):1113–1132.
National Cholesterol Education Program(NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. 2002. Third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 106:3143–3421.
Palmieri VO., Grattagliano I., Portincasa P., Palasciano G. 2006. Systemic oxidative alterations are associated with visceral adiposity and liversteatosis in patients with metabolic syndrome. J Nutr. 136(12):3022–3326.
Park JY., Kim JW., Kim JM., Han Y., Park SK., Mok JY., Park MK., Lee HJ., Kim DK. 2008. Adiponectin concentrations in type 2 diabetic patients with or without metabolic syndrome. Korean Diabetes J. 32:224–235.
crossref
Ridker PM. 2001. High-sensitivity C-reactive protein; potential adjunct for global risk assessment in the primary prevention of cardiovascular disease. Circulation. 103(13):1813–1818.
crossref
Ridker PM. 2003. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation. 107:363–369.
crossref
Ridker PM., Buring JE., Cook NR., Rifai N. 2003. C-reactive protein, the metabolic syndrome and risk of incident cardiovascular events: an 8-year follow-up of 14719 initially healthy American women. Circulation. 107(3):391–397.
crossref
Salmeron J., Manson JE., Stampfer MJ., Colditz GA., Wing AL., Willett WC. 1997. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women. JAMA. 277(6):472–477.
crossref
Seddon JM., Gensler G., Klein ML., Milton RC. 2006. C-reactive protein and homocysteine are associated with dietary and behavioral risk factors for age-related macular degeneration. Nutrition. 22(4):441–443.
crossref
Tamakoshi K., Yatsuya H., Kondo T., Hori Y., Ishikawa M., Zhang H., Murata C., Otsuka R., Zhu S., Toyoshima H. 2003. The metabolic syndrome is associated with elevated circulating C-reactive protein in healthy reference range, a systemic low-grade inflammatory state. Int J Obes Relat Metab Disord. 27(4):443–449.
crossref
The Korean Nutrition Society (2010): Dietary reference intakes for Koreans. Hanareum. Seoul Timar O., Sestier F., Levy E. 2000. Metabolic syndrome X: a review. Can J Cardiol. 16(6):779–789.
Tracy RP., Lemaitre RN., Psaty BM., Ives DG., Evans RW., Cushman M., Meilahn EN., Kuller LH. 1997. Relationship of C-reactive protein to risk of cardiovascular disease in the elderly. Results from the cardiovascular health study and the rural health promotion project. Arterioscler Thromb Vasc Biol. 17:1121–1127.
Tur JA., Romaguera D., Pons A. 2005. The diet quality index-internaitonal (DQI-I): is it a useful tool to evaluate the quality of the mediterranean diet? Br J Nutr. 93(3):369–376.
Yun HK., Kim H., Chang N. 2009. Diet quality index-international score is correlated with weight loss in female college students on a weight management program. Korean J Nutr. 42(5):453–463.
crossref

Fig. 1.
Comparison of nutrient intakes of the two groups with KDRIs1)(%) DRI for reference : Energy EER2), Protein EAR3), Fiber AI4), Calcium EAR, Phosphorus EAR, Iron EAR, Sodium AI, Zinc EAR, Vitamin A EAR, Vitamin B1 EAR, Vitamin B2 EAR, Vitamin B6 EAR, Niacin EAR, Vitamin C EAR, Folate EAR, Vitamin E AI 1) KDRIs : Dietary Reference Intakes for Koreans 2) EER : Estimated energy requirement 3) EAR : Estimated average requirement 4) RNI : Recommended nutrient intake Significantly different between men and women groups by student's t test at ∗: P < 0.05, ∗∗: P < 0.01 and ∗∗∗: P < 0.001
kjcn-16-51f1.tif
Table 1.
Comparison of anthropometric measurements, blood pressure and biochemical indices in men and women groups
  Men (n = 156) Women (n = 73) t-score
Age (years) 49.39 ± 10.101) 48.72 ± 81.02 0.542
Height (cm) 172.86 ± 6.37 157.13 ± 5.16 18.454∗∗∗
BMI (kg/m2)2) 26.66 ± 2.85 26.00 ± 3.80 1.315
Weight (kg) 79.79 ± 10.85 64.17 ± 9.82 10.450∗∗∗
WC (cm)3) 93.48 ± 7.11 88.05 ± 7.56 5.274∗∗∗
SBP (mmHg)4) 128.14 ± 13.94 129.75 ± 14.40 0.807
DBP (mmHg)5) 81.03 ± 10.68 77.41 ± 9.06 2.505∗
GGT (IU/L)6) 56.60 ± 31.52 42.33 ± 43.98 2.644∗∗
Glucose (mg/dL) 106.44 ± 22.33 99.16 ± 17.52 2.453∗
Cholesterol (mg/dL) 196.72 ± 36.16 212.01 ± 36.14 2.983∗∗
Triglyceride (mg/dL) 175.92 ± 74.40 159.71 ± 58.22 1.790
HDL-C (mg/dL)7) 43.64 ± 9.22 46.18 ± 9.70 1.911
LDL-C (mg/dL)8) 109.37 ± 29.77 121.90 ± 32.23 2.888∗∗
hs-CRP (µg/mL)9) 1.82 ± 2.55 1.97 ± 2.78 0.406
Adiponectin (µg/mL) 8.10 ± 2.75 12.10 ± 4.79 6.663∗∗∗

1) Values are Mean ± SD, 2) BMI: Body Mass Index, 3) WC: Waist Circumference, 4) SBP: Systolic Blood Pressure, 5) DBP: Diastolic Blood Pressure, 6) GGT: Gamma Glutamyl Transferase, 7) HDL-C: high-density lipoprotein cholesterol, 8) LDL-C: low-density lipoprotein cholesterol, 9) hs-CRP: High-sensitivity C-reactive protein, Significantly different between men and women groups by student's t test at ∗: P < 0.05, ∗∗: P < 0.01 and ∗∗∗: P < 0.001

Table 2.
Correlation of inflammatory markers and metabolic syndrome factors
Factors log hs-CRP log Adiponectin
WC −0.184∗∗ −0.165∗
Glucose −0.056 −0.147∗
Triglyceride −0.078 −0.193∗∗
HDL-C −0.028 −0.222∗∗
SBP −0.037 −0.110
DBP −0.091 −0.020

Significantly different at ∗: P < 0.05 and ∗∗: P < 0.01 Serum hs-CRP and Adiponectin concentrations were logarithmically transformed because of their right-skewed deviation.

Table 3.
Comparison of daily nutrients intake in men and women groups
  Men (n = 156) Women (n = 73) Total (N = 229) t-score
Energy (kcal)1) 1859.28 ± 7613.14 1721.94 ± 7731.72 1815.50 ± 7654.80 1.483
Protein (g) 7769.97 ± 7734.85 7763.95 ± 7732.02 7768.05 ± 7734.02 1.250
Fiber (g) 7717.73 ± 7779.26 7719.44 ± 7710.85 7718.28 ± 7779.80 1.228
Calcium (mg) 7471.56 ± 7311.86 7528.36 ± 7338.89 7489.67 ± 7321.07 1.249
Phosphorus (mg) 7977.00 ± 7451.78 7956.00 ± 7457.85 7970.31 ± 7452.82 0.326
Iron (mg) 7711.27 ± 7776.33 7711.19 ± 7776.28 7711.25 ± 7776.30 0.088
Sodium (mg) 2845.75 ± 1827.75 2639.56 ± 1699.65 2780.02 ± 1786.78 0.813
Zinc (mg) 7779.73 ±777 5.93 7778.59 ± 7774.50 7779.36 ± 7775.53 1.455
Vitamin A (µgRE) 7533.74 ± 7403.36 7579.57 ± 7441.79 7548.35 ± 7415.58 0.777
Vitamin B1 (mg) 7771.16 ± 7770.60 7771.05 ± 7770.55 7771.12 ± 7770.59 1.345
Vitamin B2 (mg) 7771.06 ±777 0.57 7771.01 ± 7770.58 7771.04 ± 7770.57 0.539
Vitamin B6 (mg) 7771.73 ±777 0.85 7771.70 ± 7770.92 7771.72 ± 7770.87 0.228
Niacin (mg) 7716.47 ± 7778.32 7714.84 ± 7777.56 7715.95 ± 7778.11 1.418
Vitamin C (mg) 7101.81 ± 7773.44 7119.30 ± 789.40 7107.38 ± 779.10 1.564
Folate (µg) 7232.05 ± 7137.35 7249.42 ± 7155.88 7237.59 ± 7143.40 0.853
Vitamin E (mg) 7778.57 ± 7774.43 7779.38 ± 7776.89 7778.83 ± 7775.34 1.067

1) Values are Mean ± SD All values are not significantly different between the two groups by student's t-test

Table 4.
Correlation of inflammatory markers and nutrients Intake
Factors log hs-CRP1) log Adiponectin2)
Lipid 0.071 0.125∗
Total sugar 0.025 0.167∗∗
Fiber 0.023 0.076
β-carotene 0.015 0.101
Vitamin C 0.011 0.049
Cholesterol 0.105 0.082
Total fatty acid 0.082 0.128∗
Saturated fatty acids s −0.067 0.099
Monounsaturated fa tty acids −0.073 0.116∗
Polyunsaturated fatty y acids −0.122∗ 0.194∗∗

1) Adjustment for waist circumference

2) Adjustment for waist circumference, glucose, triglyceride, and HDL-cholesterol

Significantly different at ∗: P < 0.05 and ∗∗: P < 0.01

Table 5.
Comparison of Diet Quality index-international(DQI-I) in men and women groups
  Score ranges (points) Men (n = 156) Women (n = 73) t-score
Overall food group variety 0 − 15 10.48 ± 2.221) 10.89 ± 2.37 1.272
Within-group variety for protein source 0 − 5 83.00 ± 1.93 82.68 ± 2.05 1.127
Variety 0 − 20 13.48 ± 3.26 13.58 ± 3.66 0.197
Vegetable group 0 − 5 82.68 ± 1.41 82.97 ± 1.55 1.422
Fruits group 0 − 5 81.90 ± 1.71 82.52 ± 1.94 2.347∗
Grain group 0 − 5 84.29 ± 1.01 84.21 ± 1.04 0.618
Fiber 0 − 5 83.28 ± 1.27 83.60 ± 1.28 1.774
Protein 0 − 5 84.95 ± 0.32 84.97 ± 0.23 0.574
Iron 0 − 5 83.88 ± 1.16 83.85 ± 1.29 0.207
Calcium 0 − 5 82.44 ± 1.43 82.56 ± 1.38 0.625
Vitamin C 0 − 5 83.37 ± 1.50 83.68 ± 1.38 1.506
Adequacy 0 − 40 26.79 ± 5.94 28.37 ± 6.14 1.850
Total fat 0 − 6 85.02 ± 1.64 85.10 ± 1.63 0.330
Saturated fat 0 − 6 85.63 ± 1.10 85.42 ± 1.38 1.140
Cholesterol 0 − 6 83.85 ± 2.48 84.44 ± 2.07 1.893
Sodium 0 − 6 82.68 ± 0.61 82.44 ± 0.72 2.582∗∗
Empty calorie foods 0 − 6 82.23 ± 2.52 84.44 ± 2.07 7.001∗∗∗
Moderation 0 − 30 19.46 ± 4.95 21.73 ± 4.00 3.378∗∗∗
Macronutrient ratio (Carbohydrate : Protein : Fat) 0 − 6 82.13 ± 2.10 81.89 ± 2.31 0.773
Fatty acid ratio (PUFA : MUFA : SFA) 0 − 4 80.41 ± 0.96 80.30 ± 0.86 0.828
Overall balance 0 − 10 82.54 ± 2.09 82.19 ± 2.31 1.131
Total 100 62.60 ± 8.95 65.87 ± 9.86 2.525∗

1) Values are Mean ± SD

Significantly different between men and women groups by student's t test at ∗: P < 0.05, ∗∗: P < 0.01 and ∗∗∗: P < 0.001

Table 6.
Comparison of DQI-I in the subjects according to serum hs-CRP and Adiponectin level
  hs-CRP (µg/mL)
Q 1 (n = 47) Q 2 (n = 44) Q 3 (n = 47) Q 4 (n = 45) Q 5 (n = 46) Total (N = 229)
Variety 13.51 ± 83.8721) 13.27 ± 3.252 13.26 ± 82.952 13.64 ± 3.524 13.87 ± 3.344 13.51 ± 3.382
Adequacy 27.68 ± 86.058 27.23 ± 5.665 27.00 ± 85.912 26.22 ± 6.153 28.33 ± 6.415 27.30 ± 6.036
Moderation 21.34 ± 84.620 20.43 ± 4.133 19.23 ± 85.230 19.69 ± 4.709 20.27 ± 4.901 20.18 ± 4.757
Balance 82.34 ± 81.970 82.82 ± 2.414 82.64 ± 81.961 82.67 ± 2.132 82.70 ± 1.942 82.63 ± 2.075
Total 64.84 ± 10.163 64.38 ± 8.307 62.12 ± 89.504 62.22 ± 8.468 65.45 ± 9.959 63.77 ± 9.338
  Adiponectin (µg/mL)
Q 1 (n = 45) Q 2 (n = 46) Q 3 (n = 46) Q 4 (n = 46) Q 5 (n = 46) Total (N = 229)
Variety 13.67 ± 83.268 13.26 ± 3.587 13.65 ± 83.261 13.17 ± 3.440 13.80 ± 3.442 13.51 ± 3.382
Adequacy 28.73 ± 85.561 26.70 ± 6.397 26.48 ± 86.257 26.24 ± 6.201 28.37 ± 5.511 27.30 ± 6.036
Moderation 19.71 ± 84.883a 19.96 ± 4.871ab 19.47 ± 85.459a 19.93 ± 4.590ab 21.93 ± 3.502b 20.18 ± 4.757
Balance 82.98 ± 81.840 82.35 ± 1.946 82.83 ± 82.407 82.57 ± 2.051 82.43 ± 2.105 82.63 ± 2.075
Total 65.08 ± 89.253ab 62.57 ± 8.457a 62.68 ± 10.394a 61.82 ± 9.504a 66.88 ± 8.349b 63.77 ± 9.338

1) Values are Mean ± SD

a, b values with different letters within the same line are significantly different from each other by Duncan's test at P = 0.05

TOOLS
Similar articles