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Introduction
Hemodialysis (HD) is the most widely used dialysis modality in patients with end-stage renal disease (ESRD). The number of HD patients has been increasing rapidly worldwide including Korea: the total number of HD patients has been increased 18 times from 1986 to 2006 in Korea (ESRD Registry Committee, 2006). The prognosis for ESRD patients remains poor although our understanding of the uremic state and the science and technology of HD has been improved (Caglar et al., 2002).
Malnutrition is prevalent in patients with HD and strongly associated with increased morbidity and mortality in these patients (Fleischman et al., 1999; Kopple et al., 1999; Leavey et al., 1998; Pifer et al., 2002). Factors contributing to malnutrition in HD patients may include low food intake and food intake characteristics (Aguilera et al., 2004), loss of appetite (Lopes et al., 2007), HD adequacy (Teixeira Nunes et al., 2008), comorbidity (Miskulin et al., 2004; van Manen et al., 2002), and socioeconomic status such as income and education (Byrne et al., 1994; Perneger et al., 1995a; Perneger et al., 1995b; Young et al., 1994). Among the causes of malnutrition in HD patients, inadequate dietary intake seems to be the most frequent and important. Although it has been hypothesized that inadequate intake might be secondary to underlying illness, psychosocial conditions, aging, or chronic inflammation, definite data on the etiology of inadequate intake in HD patients are still lacking (Bergstrom, 1995). Assessment of the nutritional status in HD patients is of critical importance because poor nutritional status is associated with a poor prognosis in ESRD patients. To prevent malnutrition among HD patients, it is important to identify the patient characteristics associated with inadequate nutrition (Aguilera et al., 2004).
Several studies have shown that family history of ESRD is strongly associated with increased risk of ESRD (Ferguson et al., 1988; Freedman et al., 1993; Freedman et al., 1995; Lei et al., 1998; Spray et al., 1995; Steenland et al., 1990). An individual's family history of ESRD is a better predictor of the future risk for CRF than blood glucose concentration or blood pressure (Freedman et al., 1997; Seaquist et al., 1989), indicating genetic susceptibility increased the risk of developing the commonly reported etiologies of ESRD. One population-based study found that the familial component of ESRD plays a significantly independent role in both ESRD and non-ESRD chronic kidney disease mortality (Goldfarb-Rumyantzev et al., 2006), suggesting a direct association between family history and ESRD mortality. It is possible that a family history of CRF is related to a poor prognosis for ESRD, including malnutrition.
Although a few studies have reported inadequate nutritional status and its correlates in Korean HD patients (Kim et al., 1990; Kim et al., 2000; Kim et al., 2001), to our knowledge, no study has investigated the factors related to malnutrition after controlling for other factors and the relationship between malnutrition and family history of CRF. We investigated the nutritional status and factors influencing malnutrition including a family history of CRF in ESRD patients in South Korea.
Subjects and Methods
Subjects
All subjects were ESRD outpatients from general hospitals or HD centers in Seoul who had been referred to our dialysis center in Seoul, Korea, for maintenance of HD care. To be eligible for inclusion in the study, a patient had to have been undergoing maintenance HD three times a week for more than 3 months, to have signed a consent form, and not to have advanced senility or dementia. Among the 144 patients recruited from June 2007 through March 2008, 110 (46 men and 64 women) agreed to participate and were enrolled in this study. The median age of these patients was 58.6 y (range, 28-81 y). All patients were interviewed individually to obtain information about their general characteristics and health behaviors. Patients were asked about a family history of CRF and the family history was considered positive if a patient reported having either a first-degree (parent, sibling, or child) or second-degree (grandparent, aunt, uncle, grandchild, or half sibling) relative with CRF. The primary cause of ESRD was reported and documented by the treating nephrologist. For information about comorbidity, patients were asked to report whether they had ever been diagnosed previously as having diabetes mellitus, bone diseases, hypertension, heart diseases, gastrointestinal diseases, or other diseases.
Measurements
For anthropometrics, height and postdialysis weight were measured with light clothes and without shoes using an automatic height/weight measuring instrument. Percentage of ideal body weight (%IBW) was calculated as (actual body weight / IBW)×100, and body mass index (BMI) was calculated as kg/m2. Triceps skinfold thickness (TSF) was measured using a Lange skinfold caliper (Cambridge Scientific Inc., Cambridge, MD, USA). Mid-arm circumference (MAC) was measured with a plastic measuring tape using standardized techniques. Mid-arm muscle circumference (MAMC) was calculated as MAC-(0.314×TSF) (Blumenkrantz et al., 1980). We defined malnutrition as a TSF or MAMC less than the fifth percentile for age and sex for Korean adults (Wicks et al., 1995).
Food intake was recorded using a 24-hour recall method for two consecutive days including one dialysis day and one nondialysis day. The average intake of the two days was considered the daily food intake. The portion size picture booklet was used to help the patients estimate portion size. Food intake data were analyzed using CAN-Pro 3.0 software (The Korean Nutrition Society, 2006) and compared with the Dietary Reference Intake (The Korean Nutrition Society, 2005) for Koreans. Energy and protein intake data were compared with the National Kidney Foundation Kidney Dialysis Outcome Quality Initiative (National Kidney Foundation, 2000) recommended intake for HD patients. The percentage of calories from carbohydrate, fat, and protein was also calculated. Other methods of the study have been described elsewhere (Cho et al., 2008).
Statistical analysis
Data were expressed as mean and standard error (continuous variables) or number and percentage (categorical variables). Differences between diabetic and nondiabetic ESRD patients were evaluated using Student's t test or the chi-square test, as appropriate. Because serum ferritin and triglyceride concentrations had a skewed distribution, these variables were log-transformed before analysis. Multivariable-adjusted logistic regression analysis was conducted to examine the odds ratio (OR) for malnutrition between patients with and without a family history of ESRD. All analyses were performed using SAS 9.1 software (SAS Inc., Cary, NC, USA). Significance was defined as P < 0.05.
Results
Prevalence of malnutrition and characteristics of Korean HD patients
The clinical characteristics of these Korean HD patients are shown in Table 1. The mean age and duration of HD were 58.6 years and 5.8 years, respectively. Forty-seven of the 110 patients were malnourished. Diabetes mellitus was the main primary cause of ESRD. About 17% of patients had a positive family history of CRF, 85% had hypertension, 49% had diabetes, and 93% anemia, defined as a hemoglobin level <13 g/dL for men and <12 g/dL for women. As expected, the mean BMI and %IBW were greater in patients without malnutrition (both P < 0.0001). Malnutrition was more prevalent in women (P=0.0014), nondiabetic patients (P=0.0113), those with an adequate HD (P=0.0178), patients with a family history of CRF (P=0.0255) or bone diseases (P=0.0427). Fewer patients who had ever smoked were malnourished than those who had never smoked (P=0.0007). For hematological variables, hematocrit was slightly higher in malnourished HD patients (P=0.0416), whereas serum iron concentration (P=0.0151) and TIBC (P=0.0471) were higher in HD patients without malnutrition. Serum concentrations of creatinine (P=0.0099) and uric acid (P=0.0444) were higher in HD patients without malnutrition. Serum HDL-C concentration was higher in HD patients with malnutrition (P=0.0419), and serum TG concentration was higher in HD patients without malnutrition (P=0.0339).
Inadequacy of nutrient intake of Korean HD patients
The inadequacy of daily nutrient intake of patients is shown in Table 2. More than 60% of patients consumed less than the intake of energy (30-35 kcal/kg IBW) and protein (1.2 g/kg IBW) recommended by the National Kidney Foundation Kidney Dialysis Outcome Quality Initiative. The percentages of patients consuming less than the Korean estimated average requirements (EAR) was 81.8% for calcium, 60.0% for vitamin B1, 80.9% for vitamin B2, 60.0% for vitamin C, and 95.5% for folate. The percentage of patients consuming less than the energy/IBW and protein/IBW levels recommended by the Korean EAR did not differ significantly between HD patients with and without malnutrition.
OR and 95% confidence intervals for malnutrition
The relationships between various factors and the risk of malnutrition are shown in Table 3. After adjusting for age, sex, duration of HD, having diabetes, having bone diseases, smoking, and HD adequacy, the OR for malnutrition was higher in HD patients with a family history of CRF (OR, 3.290; 95% confidence interval (CI), 1.003-10.793).
Discussion
Nutritional assessment and management are considered as an important therapeutic approach for HD patients for better prognosis. We found that 43% of Korean HD patients were malnourished, as defined by TSF or MAMC values below the fifth percentile for age and sex for Korean adults. Previous studies of Korean HD patients have used different indicators to assess the prevalence of malnutrition; for example, 76% of patients were classified as being mildly malnourished based on the weight and serum albumin concentration (Kim et al., 2000), and 21% were classified as underweight (Kim et al., 2001). Malnourished HD patients often have low fat mass and lean body mass (Kim & Kim, 2001; Kim et al., 2001; Oksa et al., 1991). Thus, the assessment of fat mass by TSF and lean body mass by MAMC is an important part of the nutritional assessment of HD patients. HD patients' daily nutrient intakes are also inadequate. More than 60% of our patients had dietary intakes below the levels of energy and protein recommended by the National Kidney Foundation Kidney Dialysis Outcome Quality Initiative (2000); our data are consistent with those of another study (Kim et al., 1990) showing HD patients were in protein and energy malnutrition. The percentage of patients consuming less than the EAR was 81.8% for calcium, 60.0% for vitamin B1, 80.9% for vitamin B2, 60.0% for vitamin C, and 95.5% for folate. In previous studies in Korea, Kim et al. (1990) reported inadequate intake of protein, energy, and vitamins A, B1, B2, and C in HD patients, and Chun (2001) reported insufficient intakes of vitamins A, B1, and B2, and niacin.
Unexpectedly, the means of energy/IBW and protein/IBW did not differ significantly between HD patients with and without malnutrition. The proportions of people consuming less than the Korean EAR also did not differ significantly between the two groups. That is, in our patients, the inadequacy of dietary intake did not differ significantly between the two groups. After adjusting for other variables related to malnutrition, only a family history of CRF remained significant. After adjusting for age, sex, duration of HD, having diabetes, having bone diseases, smoking, and HD adequacy, the OR for malnutrition was 3.3 times greater in HD patients with a family history of CRF (OR, 3.290; 95% CI, 1.003-10.793), indicating that a family history of CRF may be an independent risk factor for malnutrition in HD Korean patients. In HD patients, malnutrition is known to be related to case mix and comorbid conditions (Qureshi et al., 1998), which may be associated with a family history of CRF. Our results showed that nutritional intake of HD patients was inadequate but no difference in inadequacy existed between patients with and without malnutrition. Thus, malnutrition may not be mainly due to inadequate nutritional intake but be due to secondary effects such as chronic inflammation from comorbid conditions and a poor prognosis related to familiar history of CRF in our study subjects, although we were not able to determine the causality of relation due to the nature of cross-sectional study. Family history of ESRD is strongly associated with an increased risk of ESRD (Ferguson et al., 1988; Freedman et al., 1993; Freedman et al., 1995; Lei et al., 1998; Spray et al., 1995; Steenland et al., 1990). A population-based study showed that a familial component of ESRD plays a significantly independent role in both ESRD and non-ESRD chronic kidney disease mortality (Goldfarb-Rumyantzev et al., 2006). This suggests a direct association between family history and ESRD mortality, and it is possible that a family history of CRF is related to a poor prognosis for ESRD including malnutrition.
Family history shares both environmental and genetic factors including underlying diseases among family members. Environmental risk factors for ESRD can be shared among family members. For example, families of low socioeconomic status might not be able to afford treatment for diabetes, hypertension, or early symptoms of kidney damage because of limited access to health care (Byrne et al., 1994; Perneger et al., 1995a; Perneger et al., 1995b; Young et al., 1994). To account for differences in socioeconomic status, we compared income and education levels between patients with and without malnutrition but found no significant differences. To study the role of underlying diseases, Lei et al. (1998) showed that familial clustering of ESRD is independent of diabetes and hypertension. We also controlled for comorbidities, but family history of CRF remained significant. It has been suggested that patients with CRF relating to a genetic predisposition might have more rapid progression of disease and reach ESRD earlier (Goldfarb-Rumyantzev et al., 2006). It is possible that HD patients with a family history of CRF are more likely to be malnourished because of the rapid progression to ESRD and prolonged duration of ESRD.
Malnutrition is prevalent and is strongly associated with increased morbidity and mortality in patients on HD (Fleischman et al., 1999; Kopple et al., 1999; Leavey et al., 1998; Pifer et al., 2002). Our findings suggest that HD patients with a family history of CRF should be monitored and targeted to prevent malnutrition. Given that a family history of CRF is a strong risk factor for malnutrition, individuals with a family history should be targeted for periodic routine nutritional intervention. Adequate dietary intake seems to be one of the top priorities for them. To prevent malnutrition among HD patients, it is also important to identify patient characteristics (Aguilera et al., 2004) such as socioeconomic status that would predispose them to inadequate dietary intake.
Our study had several limitations that should be addressed in future studies. We observed an association in a cross-sectional setting, but we were unable to compare the relative impact of a family history of CRF and malnutrition on morbidity and mortality in HD patients. The information about a family history of CRF relies on the ability of patients to identify correctly a positive family history. One study of African-Americans found that 88% of those who reported a positive family history of ESRD correctly identified their family history (Freedman et al., 1997). Although we have no comparable data for Koreans and some of our study subjects aged over 65 years, the effect of any potential recall error is likely to be small. Our study also has several advantages. It is the first study to test whether there is a direct association between a family history of CRF and malnutrition in HD patients in Korea. We included in our analyses most of the putative risk factors for malnutrition, such as socioeconomic factors, behavioral factors, appetite, comorbidity, dietary intake, and HD adequacy. We also employed a combination of anthropometric and biochemical indicators to assess nutritional status rather than a single measure.
In conclusion, our study showed that the nutritional status of Korean HD patients is inadequate. Active nutrition monitoring is needed to improve the nutritional status of HD patients in Korea. Individuals on HD with a family history of CRF should be targeted for dietary intervention to prevent malnutrition. Our results also suggest that a family history of CRF is an independent risk factor for malnutrition in Korean HD patients. A follow-up study is needed to investigate whether there is a causal relation between a family history of CRF and malnutrition, and the underlying mechanism in Korean ESRD patients.
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