ORIGINAL RESEARCH

Association Between the Hemodialysis Eating Index and Risk Factors of Cardiovascular Disease in Hemodialysis Patients Yi-Fang Chiu, LD,* Yi-Chun Chen, PhD,* Pei-Yu Wu, MS,* Chun-Kuang Shih, PhD,* Hsin-Hung Chen, PhD,† Hsi-Hsien Chen, MD,‡ Tso-Hsiao Chen, PhD,§ and Shwu-Huey Yang, PhD*,{ Objective: In this study, a Hemodialysis Eating Index (HDEI) suitable for hemodialysis (HD) patients in Taiwan was developed based on the dietary recommendations of the U.S. National Kidney Foundation for HD patients and the Taiwanese 2011 Daily Food Guide. The HDEI was used to explore HD-associated cardiovascular disease (CVD) risk factors. Methods: In this prospective study, 108 HD patients from 2 HD centers in Taiwan were recruited as participants in 2010. All participants were older than 20 years. Patient CVD risk factor and 3-day dietary data were collected, and their HDEI scores were calculated. The HDEI scores comprise 12 food-related factors: the consumption of vegetables, fruits, total grains, whole grains, high-protein foods, high biological values, red and white meat, fish, oils, saturated fatty acids or trans fatty acids, nuts, and the duration of multivitamin use. The scores ranged from 5 to 100, and SAS software version 9.3 was used to perform statistical analyses. A P value less than .05 was considered statistically significant. Results: The HDEI scores and serum albumin (Alb) levels were significantly and positively correlated. The participants were divided into 2 groups on the basis of the median HDEI score of 72.2. Two months after HDEI evaluation, the high-HDEI scoring group exhibited significantly decreased levels of serum total cholesterol and increased hemoglobin (Hb) levels. Conclusion: The HDEI can be used to reflect selected nutritional status markers, such as Alb and Hb levels and CVD risk factors, for HD patients. The HDEI can also serve as an eating index for HD patients in Taiwan to facilitate CVD prevention. Ó 2014 by the National Kidney Foundation, Inc. All rights reserved.

Introduction

C

ARDIOVASCULAR DISEASE (CVD) is a major complication and the leading cause of death among hemodialysis (HD) patients. The CVD mortality rate for HD patients is 15 times greater compared with that of the general population.1,2 The risk factors of CVD can be divided into ‘‘traditional’’ and HD patient-specific ‘‘nontraditional’’ risk factors.3 Implementing a healthy diet can ameliorate the traditional risk factors of CVD, such as hypertension, diabetes, dyslipidemia, and cardiac hypertrophy, as well as nontraditional risk factors such as * School of Nutrition and Health Sciences, Taipei Medical University, Taipei, Taiwan. † Department of Nutrition and Health Sciences, Chang Jung Christian University, Tainan, Taiwan. ‡ Department of Internal Medicine, Taipei Medical University Hospital, Taipei, Taiwan. § Department of Internal Medicine, Wan Fang Hospital, Taipei, Taiwan. { Nutrition Research Center, Taipei Medical University Hospital, Taipei, Taiwan. Financial Disclosure: The authors declare that they have no relevant financial interests. Address correspondence to Shwu-Huey Yang, Taipei Medical University, School of Nutrition and Health Sciences, No. 250, Wu-Xin Street, Taipei City, Taiwan. E-mail: [email protected] Ó 2014 by the National Kidney Foundation, Inc. All rights reserved. 1051-2276/$36.00 http://dx.doi.org/10.1053/j.jrn.2013.12.006

Journal of Renal Nutrition, Vol 24, No 3 (May), 2014: pp 163-171

inflammation, malnutrition, calcium (Ca) and phosphorus (P) imbalances, and hyperkalemia.3 The U.S. National Kidney Foundation (NKF) provides dietary recommendations for HD patients to reduce the risks of CVD.4,5 An eating index is a tool that combines nutritional and food-related concepts to quantify and score the quality of dietary patterns or assess overall diet. Nearly 20 eating indices have been developed.6 An improved diet quality correlates with a reduced mortality rate.7 Nevertheless, current eating indices are primarily designed for healthy adults and are unsuitable for use among HD patients. For example, eating nuts reduces the risks of coronary heart disease and myocardial infarction among healthy populations8; however, nuts contain large amounts of P and potassium (K) and may increase serum P concentrations, causing Ca-phosphate products to accumulate among HD patients.9 The NKF indicated that HD patients should avoid eating nuts and seeds to reduce their dietary intake of P and K and reduce the risk of CVD.4,5 Waijers and colleagues contended that a dietary eating index should be established based on national dietary recommendations.6 Moreover, dietary recommendations for HD patients should be adjusted from the recommendations of a typical diet.10 Therefore, in this study, an HDpatient-specific Hemodialysis Eating Index (HDEI) was established based on the HD patient dietary recommendations of the 2011 Daily Food Guide in Taiwan (Ministry of 163

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Health and Welfare, Executive Yuan, 2011)11 and the NKF.4 We also analyzed the correlations between the HDEI and nutritional status and between the HDEI and CVD risk factors.

Patients and Methods Patients The patients were recruited from the HD centers of Taipei Medical University Hospital (TMUH) and Wan Fang Hospital (WFH) in 2010. This study was approved by the Taipei Medical University–Joint Human Review Board (no. 201005004 and 99053). The recruitment criteria required participants be 20 years or older and undergo regular HD treatments in the previous 3 months. Patients who were tube fed, exhibited hepatic failure or cancer, or were scheduled for surgery were excluded. The patients were enrolled in this study after signing an informed consent form. Research Design The patient demographics, blood pressures, anthropometric measurement values, blood biochemical values, and cardiothoracic ratios (CTRs) were recorded at baseline. In addition, the HDEI score was evaluated using 3-day dietary data, and the correlation between the HDEI scores and CVD risk factors was analyzed. After 2 months, the blood pressure measurements and blood values were recollected to serve as the follow-up data. The anthropometric measurements, blood biochemical values, and dietary information were collected in the same week. Demographics, Anthropometry, Blood Pressure, and CTRs The patient medical records were reviewed to obtain demographic information, such as age, sex, and dialysis and medical history (for diabetes, hypertension, and CVD), as well as anthropometric information, including height, body weight before and after dialysis, the weight gained between 2 dialysis sessions, and body mass index (BMI). The blood pressure data included systolic and diastolic pressure before dialysis was performed. The average values of the patient anthropometric measurements and blood pressure were obtained within 1 week. The CTR values (maximum heart and thorax diameters derived from X-ray photography) and patient comorbidity scores12 were determined by reviewing their medical records. Blood Biochemical Values In this study, 8-hour preprandial and predialysis blood samples were collected and were subsequently analyzed in the clinical laboratories of TMUH or WFH. The analysis items included traditional CVD risk factors, total cholesterol (TC), triglycerides, preprandial blood glucose, nontraditional CVD risk factors, white blood cell (WBC) count, albumin (Alb), creatinine (Cr), hemoglobin (Hb),

Ca, P, and K. The Alb, Cr, and Hb levels were considered representative of nutritional status.

Dietary Data The patients or their family members recorded patient diets during 3 days: 1 day of dialysis, 1 nondialysis day, and 1 weekend day. The recorded dietary items comprised meal time, meal location, food name, brand names, ingredients, portion or weight of food, and the cooking methods and oils used. A dietitian conducted face-to-face or phone interviews with the patients, performing a 24-hour dietary recall to confirm the dietary data. We interviewed patients and confirmed their medical records regarding the consumption of multivitamins. If a participant consumed multivitamins, then they were asked whether the duration of their consumption exceeded 5 years. Nutrient analysis software (Nutritionist Edition, Enhancement plus 3, version 2009, Taichung, Taiwan) was used to analyze the food data. This software references the Taiwanese food composition table to calculate the serving sizes of the 6 major food groups, the total calories consumed, and intakes of the 3 major nutrients; cholesterol; saturated fatty acids (SFAs), monounsaturated and polyunsaturated fatty acids; dietary fiber; vitamins B6 and B12; folic acid; and P. We also analyzed the following dietary factors: the red-to-white meat consumption ratio, and servings of vegetables, fruits, soy products, white meat (poultry, fish, seafood), red meat (pork, beef, mutton, or processed meat products), whole eggs, refined and unrefined grains, oils, nuts, and seeds. HDEI The HDEI was established based on the recommendations of the Daily Food Guide in Taiwan and the NKF. Table 1 shows the content of the HDEI. The Daily Food Guide provides recommended intakes of11 (1) vegetables, (2) fruits, (3) total grains, (4) high-protein foods, and (5) oils. When the recommended intake was met, the maximum score was achieved. According to the NKF, HD patients should refrain from consuming dairy products that contain high P levels, and 1 serving of low-fat dairy should be replaced with 1 portion of total grains and 1 serving of high-protein food. Regarding the qualitative dietary portion, on the basis of the NKF recommendations for HD patients, (6) people should refrain from consuming high-P whole grains; those who consumed whole grains achieved the maximum score. (7) In addition, a high biological value (HBV) protein ratio greater than 50% was recommended, and the maximum score is achieved for this suggested amount. (8) The intake of iron-rich red meat, not including processed meat, was also recommended to prevent anemia. The ratio concept was used to consider the balance between red meat and white meat and establish the red-to-white meat ratio. The mean value was 4.3 6 14.4. A red-to-white meat ratio of greater than 4 was set as the maximum score.13 A score of 0 was awarded

165

HEMODIALYSIS EATING INDEX AND CARDIOVASCULAR DISEASE Table 1. HDEI: Components and Scoring Criteria Component

Daily Intake

Score

Daily Intake Criteria for Minimum Score of 0

Daily Intake Criteria for Maximum Score of 10

Vegetables (serving) Fruits (serving) Total grains (serving) Whole grains High-protein foods (serving) ‡ HBV (%) Red/white meat§ Fish (serving) Oil (serving)k Foods rich in SFAs or TFAs{ Nuts Duration of multivitamin use (y)**

1.8 6 1.5 0.8 6 0.9 9.1 6 4.1 N 5 19† 4.9 6 3.0 57.4 6 15.8 4.3 6 14.4 0.7 6 0.9 5.3 6 3.8 N 5 49† N 5 10† ,5, n 5 32 S 5, n 5 76

5.1 6 2.8 3.6 6 3.4 3.1 6 1.2 4.1 6 1.9 7.5 6 2.7 9.3 6 1.7 3.8 6 3.8 5.7 6 4.8 1.6 6 2.4 2.6 6 2.5 9.1 6 2.4 8.5 6 2.5

0 0 0 .0 0 0 0 0 0 or . 4-8 .0 .0 ,5

3-5 2-4 8-18* 0* 4.5-10 .50% .4 2 serving/wk 4-8* 0* 0 $5

HDEI

72.5 6 10.5

5-100

HBV, high biological value; HDEI, Hemodialysis Eating Index; SFA, saturated fatty acid; TFA, trans fatty acid. Values are mean 6 standard deviation. Intermediate intakes were scored proportionately between 0 and 10. *The minimum score was 0 and the maximum score was 5. †Number of category of food intake. ‡Includes soy products, meats (pork, beef, lamb, poultry, fish, seafood), and eggs. §HDEI-T: ratio of serving. Red meat does not include processed meats. Score 5 0 if no white meat consumed. k Includes oil, nuts, and seeds. {Rich SFA or TFA food included high-fat meats, animal oil, and baked products. **For multivitamins, the minimum score was 5 and the maximum score was 10.

if no white meat was consumed. (9) The NFK also recommended that 2 servings of fish per week should be consumed to obtain the maximum score. (10) Those who eliminate or reduce their intake of SFAs and trans fatty acids (TFAs), such as high-fat meats, animal fats, and baked goods, can achieve a maximum score. (11) Consuming nuts that are high in P and K should be avoided to achieve a maximum score. (12) Moderate water-soluble vitamin intake was also recommended. Patients who consumed water-soluble vitamins for 5 years or more were awarded a maximum score of 10 points, and those who consumed water-soluble vitamins for less than 5 years were awarded 5 points. Twelve HDEI items were adopted: vegetables, fruits, total grains, whole grains, high-protein foods, HBV protein, red and white meat, fish, oils, food lacking large amounts of SFAs and TFAs, nuts, and the duration of multivitamin use. Guenther and colleagues indicated that the weights of the dietary scores can be set based on the research direction.14 Ten points were allocated to those who consumed foods in the same categories as foods that exhibited a significant linear correlation to CVD risk factors. Vegetables, fruits, high-protein foods, HBV protein, red and white meat, fish, and nuts scored 0 to 10 points. Total grains, whole grains, oils, and food that lacked large amounts of SFA and TFA scored 0 to 5 points. Thus, the total scores ranged between 5 and 100 (Table 1).

Statistical Methods Values are represented as the mean 6 standard deviation, percentage, or correlation coefficients. SAS software version

9.3 was adopted for the statistical analyses; the Shapiro-Wilk test was used to assess normality, the Wilcoxon rank sum test was used to compare the high-scoring and low-scoring groups, the Wilcoxon signed-rank test was used to compare the baseline and follow-up periods, and Spearman rank and partial Spearman rank correlations were applied for correlation analysis. The correlation analysis was adjusted according to sex and age, and a value of P less than .05 indicated statistical significance.

Results Of the 108 HD patients who participated in this study, 68 were from TMUH and 40 were from WFH. Of these, 54 were men (50%) and 54 were women (50%), the average age was 63.5 6 14.6 years, average BMI was 23.2 6 3.9 kg/m2, and the average ratio of weight gain between dialyses was 4.0 6 1.6%. Regarding complications, 44% of patients were diagnosed with diabetes, 54.6% were diagnosed with hypertension, and 47.2% exhibited a history of CVD. The comorbidity scores were 17.6% Grade 0 (n 5 19), 6.9% Grade 1 (n 5 68), and 19.5% Grade 2 (n 5 21). Furthermore, 91.7% of patients consumed vitamin B complex supplements and 89.8% consumed folic acid supplements. The median HDEI score was 72.5 6 10.5 points. Considering the average scores for each item and the percentage of patients who scored the maximum, the nuts item demonstrated the highest average score (9.1 6 2.5 points), and 90.7% of the patients obtained the maximum score for this item. In addition, 82.4% of patients obtained a maximum whole grains score and 78.5% exhibited a daily

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Table 2. Correlation Between HDEI Components and Traditional Cardiovascular Disease Risk Factor Data Component HDEI Adjusted Vegetables Adjusted Fruits Adjusted Total grains Adjusted Whole grains Adjusted High-protein foods Adjusted HBV Adjusted Red/white meat Adjusted Fish Adjusted Oil Adjusted Foods rich in SFAs or TFAs Adjusted Nuts Adjusted Duration of multivitamin use Adjusted

SBP (mmHg)

DBP (mmHg)

TG (mg/dL)

TC (mg/dL)

AC-Sugar (mg/dL)

CTR

0.051 0.050 0.038 20.006 20.028 20.044 20.013 20.025 20.059 20.041 20.126 20.118 20.045 20.029 0.032 0.051 0.008 20.001 20.033 0.010 0.164 0.107 0.222* 0.228* 20.061 20.059

0.076 0.057 0.124 0.075 20.070 20.082 0.039 0.024 20.136 20.130 0.052 0.052 0.063 0.079 20.129 20.125 0.034 0.025 20.101 20.070 0.169 0.105 0.263* 0.249* 20.057 20.052

0.069 0.029 0.033 0.053 20.035 20.031 20.014 20.031 0.044 0.001 0.022 0.038 20.087 20.098 0.073 0.076 0.142 0.130 0.016 20.009 20.114 20.110 20.014 20.079 20.048 20.062

0.114 0.167 0.071 0.158 20.045 20.049 20.113 20.103 0.128 0.079 0.051 0.037 20.011 20.034 0.067 0.079 0.144 0.205* 0.042 20.020 20.202* 20.107 0.031 0.007 0.056 0.051

0.141 0.164 0.047 0.002 0.046 0.022 20.058 20.046 0.138 0.184 0.057 0.054 0.114 0.117 0.241* 0.236* 0.229* 0.233* 20.203* 20.166 20.167 20.186 20.064 20.015 20.134 20.100

20.062 20.081 20.129 20.215* 20.001 20.047 0.094 0.091 20.142 20.136 20.105 20.023 0.032 0.082 0.000 0.050 0.047 0.000 20.182 20.118 0.132 0.051 20.012 0.015 20.150 20.182

AC-Sugar, preprandial blood glucose; CTR, cardiothoracic ratio; DBP, diastolic blood pressure; HBV, high biological value; HDEI, Hemodialysis Eating Index; SBP, systolic blood pressure; SFA, saturated fatty acids; TC, total cholesterol; TFA, trans fatty acids; TG, triglycerides. Values are correlation coefficients. Statistical analysis by Spearman rank correlation. Adjusted for gender and age. *P , .05.

intake of at least 50% of the recommended HBV protein amount. However, none of the patients consumed sufficient total grains, and only 6.5% demonstrated an adequate oil intake (Table 1). No significant correlation was observed between the HDEI score and interdialytic weight gain, but HDEI was significantly and positively correlated with calorie intake (P ,.05). Tables 2 and 3 show the total HDEI score as well as scores for various items and their correlations with various CVD risk factors. After adjusting for age and sex, the vegetable item score exhibited a significant negative correlation with CTR. The scores of the fruit and total grain items were significantly and negatively correlated with the serum P concentrations and Ca-P levels, respectively. The scores of the high-protein food and HBV protein items exhibited a significant positive correlation with the serum K levels. In addition, the scores of the red-to-white meat ratio and fish items were significantly and positively correlated with blood glucose. The fish item score was significantly correlated with TC and WBC levels. The SFA- and TFA-rich food item scores were negatively correlated with TC levels. In addition, the total HDEI, fruit, and duration of multivitamin use item scores were significantly and positively correlated with Alb levels (Tables 2 and 3). No significant correlation existed between the HDEI score and normal-

ized protein nitrogen appearance (NPNA) or daily protein intake. The participants were divided into high- and lowscoring HDEI groups; the median scores and the Alb concentrations of the high-scoring group members were significantly higher than were those of the low-scoring group members (4.1 6 0.4 g/dL vs. 3.8 6 0.4 g/dL, P , .05; Table 4). Regarding the high-scoring group, the TC values significantly declined (P 5 .048) and Hb values significantly increased (P 5.034) 2 months after the beginning of the experiment. The values for the CVD risk factors did not significantly change for the low-scoring group during the study period (P . .05) (Table 5).

Discussion The results of this study revealed that the total HDEI score was significantly and positively correlated with Alb levels, indicating that HDEI can be used as a tool to monitor malnutrition risks. Among the HDEI items, the vegetable, fruit, total grain, whole grain, high-protein food, HBV protein, and duration of multivitamin use scores were associated with decreased CVD risk factors. Therefore, the HDEI score reflects the nutritional statuses of HD patients and a positive CVD prognosis. No correlation existed between the HDEI score and NPNA or daily protein intake, suggesting that

167

HEMODIALYSIS EATING INDEX AND CARDIOVASCULAR DISEASE Table 3. Correlation Between HDEI Components and Nontraditional Cardiovascular Disease Risk Factor Data Component HDEI Adjusted Vegetables Adjusted Fruits Adjusted Total grains Adjusted Whole grains Adjusted High-protein foods Adjusted HBV protein Adjusted Red/white meat Adjusted Fish Adjusted Oils Adjusted Foods rich in SFAs or TFAs Adjusted Nuts Adjusted Duration of multivitamin use Adjusted

WBC (103/mL)

Alb (g/dL)

Cr (mg/dL)

Hb (g/dL)

Ca (mg/dL)

P (mg/dL)

Ca 3 PO4

K (mEq/L)

0.050 0.032 20.126 20.145 20.057 20.063 20.063 20.065 0.060 0.055 0.049 0.048 0.075 0.064 0.047 0.029 0.259* 0.254* 20.093 20.092 20.108 20.092 20.070 20.084 20.086 20.069

0.239* 0.248* 0.046 0.083 0.206* 0.247* 20.169 20.181 0.148 0.114 20.035 20.080 0.029 0.014 0.096 0.089 20.001 0.019 0.210* 0.169 20.105 20.071 20.010 20.067 0.370* 0.388*

0.125 0.094 20.061 20.062 20.160 20.168 20.008 20.001 20.022 20.077 0.143 0.071 0.015 20.053 0.079 20.018 0.115 0.165 0.129 0.076 20.229* 20.141 0.057 0.024 0.050 0.137

0.031 20.006 0.016 20.002 0.042 0.057 20.034 20.053 0.054 0.032 20.052 20.080 20.079 20.090 20.115 20.135 0.151 0.159 20.118 20.139 0.060 0.047 0.117 0.065 0.099 0.113

0.138 0.185 0.112 0.122 0.095 0.084 0.018 0.030 0.062 0.055 20.077 20.093 20.136 20.133 20.064 20.038 20.012 0.019 0.049 0.055 0.146 20.161 20.030 20.046 0.331* 0.335*

20.029 20.082 20.090 20.065 20.245* 20.239* 20.186 20.206* 0.052 0.029 0.118 0.063 0.127 0.095 0.052 20.021 0.059 0.073 0.026 20.051 20.192* 20.104 0.015 20.012 20.037 20.008

0.006 20.027 20.088 20.058 20.221* 20.213* 20.176 20.195* 0.065 0.041 0.083 0.025 0.110 0.079 0.042 20.023 0.034 0.056 0.078 0.008 20.140 20.048 0.005 20.026 0.063 0.097

20.024 20.021 20.020 20.047 20.027 20.013 20.151 20.144 20.100 20.081 0.299* 0.297* 0.226* 0.217* 0.102 0.077 20.055 20.059 0.095 0.084 20.101 20.057 0.005 0.058 20.174 20.170

Alb, albumin; Ca, calcium; Cr, creatinine; Hb, hemoglobin; HBV, high biological value; HDEI, Hemodialysis Eating Index; K, potassium; P, phosphorus; PO4, phosphate; SFA, saturated fatty acids; TFA, trans fatty acids; WBC, white blood cell. Values are correlation coefficients. Statistical analysis by Spearman rank correlation. Adjusted for gender and age. *P , .05.

the NPNA could reflect the daily protein intake in HD patients15; however, this must be confirmed in future studies. The results also indicated that increased vegetable scores corresponded to a decreased CTR; thus, the CTR can serve as an index for cardiac hypertrophy16 and is associated with heart disease and dilated cardiomyopathy.17,18 Vegetables intake exhibited a significant negative correlation with coronary artery disease; thus, it can improve blood pressure levels.19 The folic acid in vegetables also reduces homocysteine levels.20 Furthermore, vitamins C and E and carotenoids can improve endothelial function and prevent lipid peroxidation.21 These factors all contribute to reducing the risk of CVD. The findings indicated that an increased fruit score was correlated with increased Alb concentrations. Bermejo contended that a high fruit intake is conducive to vitamin ingestion and can reduce homocysteine levels, which are inflammation markers. Reducing inflammation may ameliorate Alb levels,22 which are an indicator of nutritional status. In this study, an increased fruit score corresponded with low levels of serum P and Ca-P. Fruits are rich in dietary fiber, and previous research has demonstrated that dietary fibers can bind with dietary P and increase the level of P excreted in feces,23 reducing P absorption in the intestine, serum P concentrations, and Ca-P. Hyperphosphatemia is a common CVD risk factor

among HD patients; thus, fruit scores can be used to reflect nutritional status and serum P concentrations. Regarding the participants, refined grains accounted for 98.9% of total grain intake. According to the NKF, refined grains should be the primary source of carbohydrates for HD patients. An adequate intake of refined grains presumably provides sufficient calories24 and can reduce the intake of foods that contain high P levels, thereby reducing the serum P and Ca-P levels. The HDEI emphasizes consuming an adequate amount of total grains, but avoiding whole grains to obtain sufficient calories and reduce the risk of malnutrition. No participant who consumed whole-grain products achieved a maximum score (10 points) on the basis of the HDEI scoring standard. The HDEI scores of high-protein foods and HBV protein ratios can be used to assist in maintaining serum K concentrations. Given sufficient calories, HBV proteins can prevent protein-energy malnutrition, thereby reducing mortality rates.25,26 Noori and colleagues indicated that dietary protein intake is positively correlated with dietary K intake because consuming dietary protein increases serum K levels.27 The results of this study are consistent with those of Noori. In addition, Kovesdy and colleagues investigated 81,013 HD patients, determining that maintaining serum K levels at 4.6 and 5.3 mEq/L ensures a

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Table 4. Comparison of Cardiovascular Disease Risk Factor Data Between Low and High HDEI Score at Baseline HDEI and Clinical Parameters n HDEI score Range Blood pressure SBP (mmHg) DBP (mmHg) Lipid profile TG (mg/dL) TC (mg/dL) Glycemic AC-sugar (mg/dL) CTR Inflammatory marker WBC (103/mL) Nutrition status Alb (g/dL) Cr (mg/dL) Hb (g/dL) Electrolyte Ca (mg/dL) P (mg/dL) Ca 3 PO4 K (mEq/L)

HDEI Score Low

High

54 64.1 6 6.6 33.3-69.2

54 80.8 6 6.2 69.3-93.8

143.1 6 21.2 74.9 6 11.7

145.3 6 23.9 76.0 6 12.9

P for Group*

.281 .167

174.4 6 114.9 189.9 6 138.1 171.6 6 46.5 178.2 6 45.3

.500 .151

115.3 6 49.8 0.5 6 0.1

132.9 6 77.1 0.5 6 0.1

.349 .280

6.5 6 2.3

6.3 6 1.8

.145

3.8 6 0.4 10.1 6 2.8 10.5 6 1.0

4.1 6 0.4 10.7 6 3.1 10.5 6 1.2

.004 .167 .474

9.3 6 0.8 5.1 6 1.6 47.1 6 15.3 4.5 6 0.8

9.5 6 0.9 4.9 6 1.2 46.6 6 12.7 4.4 6 0.8

.160 .222 .125 .281

AC-sugar, preprandial blood glucose; Alb, albumin; Ca, calcium; Cr, creatinine; CTR, cardiothoracic ratio; DBP, diastolic blood pressure; Hb, hemoglobin; HDEI, Hemodialysis Eating Index; K, potassium; P, phosphorus; PO4, phosphate; SBP, systolic blood pressure; TC, total cholesterol; TG, triglycerides; WBC, white blood cell. Values are mean 6 SD. *Statistical analysis by Wilcoxon rank sum test.

superior survival rate whereas a serum K level of less than 4.0 mEq/L increases the mortality rate; thus, serum K levels should be maintained within an acceptable range.28 The NKF recommends that HD patients maintain serum K levels of 3.5 to 5.0 mEq/L. In this study, approximately 70% of participants reached this standard. The red-to-white meat ratio score exhibited a significant positive correlation with serum glucose levels. This finding was based on the observation that the 20 participants who exhibited a red-to-white meat ratio score of 4 or greater accounted for more than 50% of the diabetics. Therefore, the positive correlation between the red-to-white meat score and serum glucose levels may be related to disease history. The NKF recommends that HD patients consume red meat because it is rich in iron, zinc, and vitamin B12, which help to prevent anemia. According to Lou and colleagues, HD patients who consume high amounts of red meat exhibit a superior nutritional status and appetite.29 We recommend further investigating how consuming red meat affects HD patients. In this study, fish consumption and TC levels were significantly and positively correlated, and fewer patients attained

the recommended TC levels compared with the 93 endstage chronic renal failure patients in the study of Arslan and Kiziltan,30 in which 66 patients who consumed a moderate amount of fish exhibited an average TC of 179.3 mg/ dL (104-388 mg/dL), and more than 70% of the patients attained TC levels within the NKF-recommended range (151-199 mg/dL).31 Burr and colleagues examined 2,033 men who exhibited a history of myocardial infarction, determining that a moderate fish intake can reduce TC concentrations by 3 to 4%.32 In the study presented here, the fish score was significantly and positively correlated with glucose levels. This presumably resulted because of the 66 (n 5 108) patients who habitually consumed fish, more than 50% exhibited a history of diabetes. Regardless of diabetes, the fish scores were positively correlated with glucose levels, and the members of the high-scoring group exhibited no increased blood glucose concentrations after 2 months. This contradicts numerous studies in which a moderate intake of fish was suggested to improve blood sugar levels. Consequently, the causality between fish intake and blood glucose concentrations remains to be confirmed in future studies. Freskens and colleagues discovered that 175 healthy participants who consumed large amounts of fish exhibited lower levels of preprandial blood glucose than did those who consumed small amounts of fish.33 Mori and colleagues investigated 63 hypertensive patients, determining that consuming fish can improve glucose and insulin metabolism levels.34 This suggested that patients who consumed large amounts of fish would exhibit higher blood sugar levels compared with those who consumed small amounts of fish. Fish is rich in zinc, and previous studies have indicated that zinc improves the nausea and abnormal tastes caused by urinary toxins35,36; thus, consuming fish can increase appetite, caloric intake, and blood glucose concentrations. The current findings indicated that most patients exhibited no inflammation. Basu and colleagues asserted that fish rich in n-3 polyunsaturated fatty acids yielded antiinflammatory effects, reducing the risk of coronary heart disease.37,38 In the study presented here, the fish item score was significantly and positively correlated with WBC levels, 72.9% of patients achieved the WBC standard, and 6 patients demonstrated a WBC greater than 10.8 3 103/mL. These results indicated that neither oil intake nor consuming SFA- and TFA-rich foods is significantly correlated with the risk factors of CVD. The NFK recommends that HD patients reduce their consumption of SFAs and TFAs to decrease the risk of CVD. Oils are a vital source of calories, facilitating the digestion, absorption, and transportation of fat-soluble vitamins.39 However, excessively consuming oils may increase the risk of CVD.40 The Daily Food Guide recommends a daily intake of 1,200 kcal and 4 servings of oils. Similar to the current results, previous findings have indicated that consuming multivitamin supplements contributes to maintaining a positive nutritional status. Among

High HDEI Score (HDEI $ 72.2) Clinical Parameters Blood pressure SBP (mmHg) DBP (mmHg) Lipid profile TG (mg/dL) TC (mg/dL) Glycemic AC-sugar (mg/dL) Inflammatory marker WBC (103/mL) Nutrition status Alb (g/dL) Cr (mg/dL) Hb (g/dL) Serum electrolyte Ca (mg/dL) P (mg/dL) Ca 3 PO4 K (mEq/L)

Low HDEI Score (HDEI , 72.2)

Baseline

Month 2

Difference

P for Time†

Baseline

Month 2

Difference

P for Time†

P for Group Difference*

145.3 6 23.9 76.0 6 12.9

145.7 6 25.8 74.9 6 11.1

0.6 6 33.7 20.6 6 17.8

.369 .841

143.1 6 21.2 74.9 6 11.7

141.9 6 20.4 76.1 6 13.4

20.3 6 26.6 25.7 6 15.3

.836 .864

.385 .423

189.9 6 138.1 178.2 6 45.3*

163.8 6 108.4 171.4 6 49.1

226.1 6 100.4 26.8 6 22.9*

.108 .048

174.4 6 114.9 171.6 6 46.5

160.7 6 102.9 170.6 6 44.1

211.9 6 102.6 21.6 6 35.7

.072 .946

.448 .014

132.9 6 77.1

117.0 6 55.9

215.9 6 87.3

.358

115.3 6 49.8

112.2 6 52.2

224.5 6 82.8

.802

.350

6.3 6 1.8

6.4 6 1.6

0.1 6 1.2

.899

6.5 6 2.3

6.5 6 2.2

20.6 6 2.4

.954

.191

4.1 6 0.4 10.7 6 3.1 10.5 6 1.2

4.0 6 0.3 10.9 6 3.0 10.8 6 1.2*

20.1 6 0.2 0.2 6 1.3 0.3 6 0.9

.073 .598 .034

3.8 6 0.4 10.1 6 2.8 10.5 6 1.0

3.8 6 0.4 10.3 6 2.5 10.5 6 1.1

0.1 6 0.2 0.7 6 1.9 20.4 6 1.1

.662 .612 .580

.119 .150 .050

9.5 6 0.9 4.9 6 1.2 46.6 6 12.7 4.4 6 0.8

9.5 6 0.8 4.8 6 1.4 45.7 6 13.8 4.3 6 0.9

0.0 6 0.7 20.1 6 1.4 20.9 6 11.6 20.1 6 0.5

.485 .842 .604 .374

9.3 6 0.8 5.1 6 1.6 47.1 6 15.3 4.5 6 0.8

9.3 6 0.8 4.9 6 1.4 46.1 6 14.7 4.4 6 0.8

0.2 6 0.7 0.1 6 1.9 1.6 6 19.4 20.2 6 0.9

.554 .460 .479 .271

.149 .102 .105 .429

AC-sugar, preprandial blood glucose; Alb, albumin; Ca, calcium; Cr, creatinine; DBP, diastolic blood pressure; Hb, hemoglobin; HDEI, Hemodialysis Eating Index; K, potassium; P, phosphorus; PO4, phosphate; SBP, systolic blood pressure; TC, total cholesterol; TG, triglycerides; WBC, white blood cell. Values are mean 6 SD. *P , .05. *Statistical analysis by Wilcoxon rank sum test. †Statistical analysis by Wilcoxon sign rank test.

HEMODIALYSIS EATING INDEX AND CARDIOVASCULAR DISEASE

Table 5. Comparisons of High and Low HDEI Score Group in Cardiovascular Disease Risk Factors Between Baseline and Month 2

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healthy populations, nuts can reduce the risks of coronary heart disease and myocardial infarction.8 However, nuts contain high P and K levels, and long-term consumption may enhance serum P and Ca-P concentrations, potentially increasing the risk of CVD among HD patients. The NKF indicated that HD patients should avoid eating nuts and seeds to lower their dietary intake of P and K, reducing the risk of CVD.41 In addition, WhaYoung and colleagues provided multivitamin supplements to 123 patients (ages .60 years), observing that they maintained normal Alb levels.42 The Alb concentration levels of the high-scoring HDEI group were significantly higher than those of the lowscoring group. Among the HDEI items, high-protein food and HBV protein could represent the quantity and quality of food protein sources. Suitable protein sources can increase Alb concentrations. In addition, the fruit, oil, and duration of multivitamin use item scores exhibited a significant positive correlation with the Alb levels, indicating that patients who adhered to the HDEI standard possessed higher Alb concentrations compared with those who did not. The high-scoring group exhibited reduced TC levels after the 2-month follow-up period, indicating that patients who comply with the HDEI standards can reduce their TC concentrations. Among the HDEI items, oils and food lacking large amounts of SFAs or TFAs could represent the quantity and quality of oil sources. After 2 months, the Hb concentrations of the high-scoring group were more favorable than were those of the low-scoring group, indicating that the patients who complied with the HDEI item standards maintained their Hb levels. Among the HDEI items, if the red-to-white meat ratio score was greater than 4, the participant received 10 points toward their total score. According to the NKF recommendations, HD patients should consume red meat to supplement their iron and increase their Hb concentration levels, reducing the risk of anemia.43 Therefore, the HDEI score can reflect the Hb concentrations, and therefore the nutritional statuses and lipid levels, of HD patients. At present, few dietary quality scores have been designed for HD patients. This study is the first in which an HDEI suitable for HD patients was designed based on national dietary guidelines and recommendations for HD patients. A limitation of this study is that only 108 HD patients were recruited for analysis, decreasing the likelihood that the statistical analyses could show significant differences. In addition, the patients were only monitored for 2 months; several CVD risk factors may not cause significant changes during this period, requiring an extended evaluation and observation period. However, the TC levels decreased and Hb levels increased among the high-scoring HDEI group members in this study. In future studies, additional items, such as glycated Hb, insulin, low- and high-density lipoprotein cholesterol, C-reactive protein, folic acid, and vitamin B12 concentrations should be explored to elucidate

the CVD risk factors and dietary patterns of HD patients. To explore the relation between HDEI and NPNA, additional participants should be recruited in future studies.

Conclusion The total HDEI score was significantly and positively correlated with serum Alb levels. After a 2-month follow-up period, the high-scoring HDEI group exhibited reduced TC levels and increased Hb concentrations. Therefore, the HDEI score can reflect the nutritional status and CVD outcomes of HD patients. We recommend that the HDEI be used as an eating index for HD patients in Taiwan to facilitate CVD prevention; however, it should not be extrapolated to other populations.

Practical Application Nutrition therapy is a critical component of medical care, and diet and health are closely related, even in HD patients. Clinical dietitians typically use 24-hour dietary recalls to assess the nutritional statuses of patients before consultations. It is difficult to provide patients with a clear numerical description of their diet and nutritional implementation status. During clinical nutrition care, providing HD patients with a dynamic diet index can facilitate monitoring and modifying the dietary statuses and promote the health of patients. Therefore, the proposed HDEI can be used to identify the qualitative and quantitative diet factors among HD patients and identify potential CVD risk factors.

Acknowledgments The authors thank all of those who made this study possible, including the Hemodialysis Centers of Taipei Medical Hospital and Wan Fang Hospital. The authors are also extremely grateful to the patients who participated in this study.

References 1. Foley RN, Parfrey PS, Sarnak MJ. Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis. 1998;32:S112-S119. 2. Herzog CA, Ma JZ, Collins AJ. Poor long-term survival after acute myocardial infarction among patients on long-term dialysis. N Engl J Med. 1998;339:799-805. 3. Sarnak MJ. Cardiovascular complications in chronic kidney disease. Am J Kidney Dis. 2003;41:S11-S17. 4. National Kidney Foundation. K/DOQI Clinical Practice Guidelines for cardiovascular disease in dialysis patients. Am J Kidney Dis. 2005;45:S1-S153. 5. National Kidney Foundation. Dietary Guidelines for Adults Starting on Hemodialysis. http://www.kidney.org/atoz/content/dietary_hemodialysis. cfm. Accessed May 7, 2013. 6. Waijers PM, Feskens EJ, Ocke MC. A critical review of predefined diet quality scores. Br J Nutr. 2007;97:219-231. 7. McCullough ML, Willett WC. Evaluating adherence to recommended diets in adults: the Alternate Healthy Eating Index. Public Health Nutr. 2006;9:152-157. 8. Hu FB, Stampfer MJ, Manson JE, et al. Frequent nut consumption and risk of coronary heart disease in women: prospective cohort study. BMJ. 1998;317:1341-1345. 9. Block GA, Port FK. Re-evaluation of risk associated with hyperphosphatemia and hyperparathyroidism in dialysis patients: recommendations for a change in management. Am J Kidney Dis. 2000;35:1226-1237.

HEMODIALYSIS EATING INDEX AND CARDIOVASCULAR DISEASE 10. Tabakian A, Juillard L, Laville M, Joly MO, Laville M, Fouque D. Effects of recombinant growth factors on energy expenditure in maintenance hemodialysis patients. Miner Electrolyte Metab. 1998;24: 273-278. 11. Department of Health, Executive Yuan, Taiwan. Daily Food Guide; 2011. 1. Available at http://health99.doh.gov.tw/media/public/pdf/21733.pdf. Accessed January 22, 2014. 12. Davies SJ, Phillips L, Naish PF, Russell GI. Quantifying comorbidity in peritoneal dialysis patients and its relationship to other predictor of survival. Nephrol Dial Transplant. 2002;17:1085-1092. 13. Freedman LS, Guenther PM, Krebs-Smith SM, Kott PS. A population’s mean Healthy Eating Index-2005 scores are best estimated by the score of the population ratio when one 24-hour recall is available. J Nutr. 2008;138: 1725-1729. 14. Guenther PM, Casavale KO, Reedy J, et al. Update of the Healthy Eating Index: HEI-2010. J Acad Nutr Diet. 2013;113:569-580. 15. Kalantar-Zadeh K, Supasyndh OS, Lehn R, et al. Normalized protein nitrogen appearance is correlated with hospitalization and mortality in hemodialysis patients with Kt/V greater than 1.20. J Ren Nutr. 2003;13: 15-25. 16. Giamouzis G, Sui X, Love TE, Butler J, Young JB, Ahmed A. A propensity-matched study of the association of cardiothoracic ratio with morbidity and mortality in chronic heart failure. Am J Cardiol. 2008;101: 343-347. 17. Komajda M, Jais JP, Reeves F, et al. Factors predicting mortality in idiopathic dilated cardiomyopathy. Eur Heart J. 1990;11:824-831. 18. Spinar J, Vitovec J, Blaha M, et al. Radiologic changes in chronic heart failure. Cor Vasa. 1992;34:88-99. 19. Bellow A, Epstein JF, Parikh-Patel A. Lifestyle behaviors associated with secondary prevention of coronary heart disease among California adults. Prev Chronic Dis. 2011;8:A31. 20. Rimm EB, Willett WC, Hu FB, et al. Folate and vitamin B6 from diet and supplements in relation to risk of coronary heart disease among women. JAMA. 1998;279:359-364. 21. Galleano M, Pechanova O, Fraga CG. Hypertension, nitric oxide, oxidants, and dietary plant polyphenols. Curr Pharm Biotechnol. 2010;11: 837-848. 22. Bermejo L, Aparicio A, Andr
es P, L
opez-Sobaler AM, Ortega RM. The influence of fruits and vegetables intake on the nutritional status and plasma homocysteine levels of institutionalised elderly people. Public Health Nutr. 2007;10:266-272. 23. Reinhold JG, Faradji B, Abadi P, Ismail-Beigi F. The Journal of Nutrition, Volume 106, 1976: decreased absorption of calcium, magnesium, zinc and phosphorus by humans due to increased fiber and phosphorus consumption as wheat bread. Nutr Rev. 1991;49:204-206. 24. Slavin J. Why whole grains are protective: biological mechanisms. Proc Nutr Soc. 2003;62:129-134. 25. Avram MM, Goldwasser P, Erroa M, Fein PA. Predictors of survival in continuous ambulatory peritoneal dialysis patients: the importance of prealbumin and other nutritional and metabolic markers. Am J Kidney Dis. 1994;23:91-98.

171

26. Borovnicar DJ, Wong KC, Kerr PG, et al. Total body protein status assessed by different estimates of fat-free mass in adult peritoneal dialysis patients. Eur J Clin Nutr. 1996;50:607-616. 27. Noori N, Kalantar-Zadeh K, Kovesdy CP, et al. Dietary potassium intake and mortality in long-term hemodialysis patients. Am J Kidney Dis. 2010;56:338-347. 28. Kovesdy CP, Regidor DL, Mehrotra R, et al. Serum and dialysate potassium concentrations and survival in hemodialysis patients. Clin J Am Soc Nephrol. 2007;2:999-1007. 29. Lou LM, Campos B, Gimeno JA, Cavern
ı A, Boned B. Nutrient intake and eating habits in hemodialysis patients: comparison with a model based on Mediterranean diet. Nefrologia. 2007;27:38-45. 30. Arslan Y, Kiziltan G. Nutrition-related cardiovascular risk factors in hemodialysis patients. J Ren Nutr. 2010;20:185-192. 31. National Kidney Foundation. K/DOQI Clinical Practice Guidelines for managing dyslipidemias in chronic kidney disease. Am J Kidney Dis. 2003;41:S1-S60. 32. Burr M, Fehily A, Gilbert J, et al. Effects of changes in fat, fish, and fibre intakes on death and myocardial reinfarction: diet and reinfarction trial (DART). Lancet. 1989;2:757. 33. Feskens EJ, Bowles CH, Kromhout D. Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care. 1991;14:935-941. 34. Mori TA, Bao DQ, Burke V, Puddey IB, Watts GF, Beilin LJ. Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr. 1999;70:817-825. 35. G€ unes¸ FE. Medical nutrition therapy for hemodialysis patients. In: Suzuki H, ed. Hemodialysis. Lancashire, UK: InTech; 2013:21-43. 36. Rucker D, Thadhani R, Tonelli M. Trace element status in hemodialysis patients. Semin Dial. 2010;23:389-395. 37. Basu A, Devaraj S, Jialal I. Dietary factors that promote or retard inflammation. Arterioscler Thromb Vasc Biol. 2006;26:995-1001. 38. LaFleur-Brooks M. Exploring medical language. In: A Student-Directed Approach. 7th ed. St. Louis, MO: Mosby Elsevier; 2008:398. 39. Gallagher ML. Intake: the nutrients and their metabolism. In: Mahan LK, Sylvia Escott-Stump S, Janice L, Raymond J, eds. Krause’s Food & the Nutrition Care Process. 13th ed. Saunders; 2012:40-94. 40. Yu-Poth S, Zhao G, Etherton T, Naglak M, Jonnalagadda S, KrisEtherton PM. Effects of the National Cholesterol Education Program’s Step I and Step II dietary intervention programs on cardiovascular disease risk factors: a meta-analysis. Am J Clin Nutr. 1999;69:632-646. 41. National Kidney Foundation. K/DOQI Clinical Practice Guidelines for nutrition in chronic renal failure. Am J Kidney Dis. 2000;35(suppl): S1-S140. 42. WhaYoung K, ShoYoung A, YoSuk S. The nutritional status and intervention effects of multivitamin-mineral supplementation in nursing-home residents in Korea. Korean J Comm Nutr. 2000;5:201-207. 43. National Kidney Foundation. K/DOQI Clinical Practice Guidelines and Clinical Practice Recommendation for anemia in chronic kidney disease. Am J Kidney Dis. 2006;48(suppl):S11-S145.