Association between dietary intake and nutritional status in Eastern Mediterranean patients receiving hemodialysis

Abstract

BACKGROUND:

Studies on hemodialysis (HD) patients reveal suboptimal dietary intakes, which have been linked to protein-energy wasting and its detrimental consequences.

OBJECTIVE:

Given the paucity of data regarding nutrient intakes of Eastern Mediterranean HD patients, we conducted a pilot study on HD patients at Heraklion, Crete, Greece to assess adequacy of dietary intakes and to determine their relationship with nutritional status.

METHODS:

Nutritional status of 36 patients aged 61.8±15.0 years was evaluated by three 24-hour dietary recalls, anthropometry and blood biochemical markers.

RESULTS:

The mean dietary energy and protein intakes were 34.4±2.1 kcal/kg and 1.25±0.067 g/kg, respectively. The anthropometric results were indicative of a well-maintained somatic status. 30.6% of the patients had adequate weight (BMI 18.5–24.9 kg/m²) and 69.4% were overweight or obese (BMI≥25 kg/m²). Patients had arm anthropometrics higher than the 25th percentile. Mean predialysis serum levels of urea and creatinine, were within the expected range, phosphorus was borderline high, while albumin and cholesterol were at the optimum level for HD patients. In univariate linear regression, a positive relation was observed between ideal weight-adjusted energy (wEI) and protein (wPI) intakes with anthropometric and biochemical indices. However, in the multivariate model, only the associations between dietary intakes of energy and protein with anthropometric indices remained significant.

CONCLUSIONS:

24-hour derived-dietary intakes reached recommended targets and adequately reflected the nutritional status of the patients, according to anthropometric and biochemical indices. Additionally, the 24-hour recall method should be part of the routine care for HD patients, in order to identify patients at nutritional risk before objective parameters of wasting are documented.

Keywords

Nutritional assessment nutritional status hemodialysis wasting

1 Introduction

End-stage renal disease patients receiving hemodialysis (HD) are at substantial risk for protein-energy wasting, which is a strong predictor of morbidity and mortality [1, 2]. Protein-energy wasting is characterized by deterioration of body composition with depleted energy (fat tissue) stores, loss of somatic protein (low muscle mass) and low levels of serum albumin, and other visceral proteins [3]. Factors contributing to wasting include poor appetite, suboptimal nutrient intake, hormonal imbalances, metabolic derangements, systemic inflammation, increased catabolism, dialysis-related nutrient losses, uremic toxin accumulation, and psychosocial conditions.

Therefore, regular evaluation of HD patients’ nutritional status is required for prevention or early detection of wasting. To date, there is no single ideal method for this purpose and the National Kidney Foundation (NKF) Clinical Practice Guidelines for nutrition in Chronic Kidney Disease (CKD) recommend the coordinated use of several methods, including dietary records, anthropometric and biochemical measurements that correlate with nutritional status [4]. These guidelines suggest a daily energy intake of 25–35 Kcal/Kg ideal body weight and a daily protein intake of 1.0–1.2 g/Kg ideal body weight. However, numerous studies report that these recommendations are far from being fully obtained [5].

Given that there is no published data on diet adequacy and only a few published studies on the nutritional status of Eastern Mediterranean renal patients, a pilot study was undertaken in a small sample of HD patients from a dialysis center in Heraklion Crete [6 –8]. The objectives of the study were: a) to assess the adequacy of their dietary intakes, including energy, protein, sodium, calcium and phosphorus, by three 24hour recalls, since this method provides valid estimates in a relatively simple, cost-effective, and time-efficient manner [9], and b) to determine whether anthropometric and biochemical indices, which are more objective nutritional status indicators, would confirm and corroborate yielded intakes.

2 Materials and methods

2.1 Sample

The study involved 36 hemodialysis (HD) patients, 29 men and 7 women of Caucasian origin, from a single dialysis center, in Heraklion Crete, Greece. The dialysis center is a private ISO certified dialysis clinic, which contracts with all insurance providers. The clinic has a capacity of 160 patients. It is equipped with 40 Fresenius Medical Care 5008S online hemodiafiltration machines and it cooperates with the University Hospital. HD patients were enrolled in the study if they were between 25 to 85 years old and were under HD for at least 3 months. Exclusion criteria included ages over 85 years, having active infections or other catabolic diseases (i.e. cancer, heart failure, cirrhosis etc.) and dementia. All eligible patients were invited to participate in the study. Informed consent was obtained from 39 individual participants, while 3 of them did not complete the study. Dialysis treatment consisted of 3 weekly-sessions, using bicarbonate-buffered dialysate and polysulfone dialyzer-membranes. Dialysis duration was 3–5 hours, in daytime, depending on the individual patient’s prescription and the decisions of the Center’s nephrologists. All procedures performed in the present study were in accordance with the ethical standards of the institutional research committee of the Mesogeios Dialysis Center (prot. n. 7348-C, 2018-08-19) and with the 1964 Helsinki declaration and its later amendments.

2.2 Data collection

Dietary intake was assessed by use of 24-hour food recall. For each patient three 24-hour recall interviews were conducted, by an experienced dietitian. Two weekdays (a dialysis day and a non-dialysis day) and a weekend day (not on dialysis) were included, and daily data were averaged. Prior to the first recall, an interview was conducted but not studied further, in order to avoid significant underreporting, associated with the first recall, as suggested by Ma [10]. The dietetic software “DietSpeak” (Release 2.0212 Copyright 12.11.20011, http://www.dietspeak.gr) was used to calculate the mean dietary intakes. Diet Speak is based on the USDA National Nutrient Database for Standard Reference, Release 28, in combination with a Greek food composition database (http://www.fao.org/infoods/infoods/tables-and-databases/europe/en/), which includes approximately 200 Greek foods. Protein and energy intakes were expressed in kg of ideal bodyweight per day.

Anthropometric measurements included height (cm), body dry weight (in kg), and body mass index (BMI, dry weight/height², in kilograms per square meter), and were carried out using a Seca digital scale and a Seca stadiometer [11]. The assessment and achievement of the optimal dry weight was achieved for each patient through ambulatory blood pressure monitoring and interventions of qualified nephrologists of the Center. Underweight was defined as a BMI below 18.5 kg/m², overweight was defined as a BMI in the range of 25–29.9 kg/m² and obesity was defined as a BMI equal or above 30 kg/m², according to the definition of World Health Organization [12]. Triceps skin fold thickness (TSF) was measured using a conventional Harpenden skin fold caliper. Mid-arm circumference (MAC) was measured with an inextensible measure tape. These measurements were taken, by an experienced single observer after dialysis, on the right arm. In some cases, measurements were taken on the left arm because the right arm was functionally impaired, due to an arteriovenous fistula. Each measurement was repeated three times, and the average result was registered [13]. Mid-arm muscle circumference (MAMC) was calculated using the formula: MAMC (mm) = MAC (mm) – (3.14×TSF) (mm) [14]. Percentiles of TSF, MAC and MAMC for every patient were evaluated according to Frisancho [15]. Percentiles were considered as normal when they were in the 15th to 85th range.

Biochemical markers associated with nutritional status included predialysis albumin, urea, creatinine, cholesterol and phosphorus. Samples were collected just before the start of hemodialysis and all markers were measured via automated and standardized methods [16]. For albumin measurements, the bromocresol green (BCG) assay utilized [17]. Average values were calculated from results obtained during a 2-month period.

2.3 Data analysis

We assessed the normal distribution of our data using the Shapiro-Wilk test. Mean and standard deviation were reported for normally distributed data, otherwise median and interquartile range were presented. For the evaluation of the association between energy and protein intake with anthropometric and biochemical indices, Pearson and Spearman correlation coefficient were calculated for normally and non-normally distributed data, respectively. For comparing the data obtained from male and female patients, the independent sample Student t test was used, while the homogeneity of distribution was assessed with the Levene’s test. The inclusion of independent variables in the multivariate model, was assessed univariately, where variables with a p < 0.2 were entered in the multivariate model. When a p value > 0.2 was observed in the univariate model but the variable was of clinical interest, it was also entered in the multivariate model. The multivariate model was adjusted for age, sex, and time on dialysis. The presence of multicollinearity in the multivariate model was evaluated with the variance inflation factor (VIF), while the assessment of the autocorrelation in residuals were performed with the Durbin – Watson test. Statistical significance was set at p < 0.05. All analyses were performed with SPSS version 25.0 (SPSS, Chicago, IL, USA).

3 Results

The study enrolled 36 patients, with 80.6% being men. The mean age of the participants was 61.8±15.0 years, range of 25 to 85 years. Patients were on dialysis for 5.3±2.8 years. Anthropometric and biochemical characteristics classified by gender are summarised in Table 1. Table 2 presents the mean ideal weight-adjusted dietary intakes based on three 24-hour recalls. The distribution of patients according to anthropometric characteristics is shown in Table 3. The corresponding percentiles of the arm anthropometric values, as evaluated according to Frisancho [15] ranked all patients above the 25% of the reference population. More specifically, both MAC and MAMC values were ≥25th percentile and TSF values were ≥50th percentile.

Table 1
Anthropometric and biochemical characteristics of Hemodialysis patients

All patients (n = 36) Male (n = 29) Female (n = 7) p value

Height (m)^b 1.66 (1.59–1.70) 1.68 (1.63–1.70) 1.50 (1.49–1.56) <0.001

Dry weight (kg)^a 75.34±14.52 78.14±13.93 63.71±11.35 0.016

BMI (kg/m²)^a 27.88±5.04 28.01±5.00 27.35±5.70 0.762

TSF (mm)^b 18.40 (15.00–19.95) 17.60 (12.80–19.00) 28.40 (25.5–30.90) 0.001

MAC (cm)^b 31.77 (30.03–34.00) 32.00 (30.90–34.00) 30.00 (29.00–33.50) 0.345

MAMC (cm)^b 26.73 (25.11–27.54) 26.90 (26.00–27.91) 23.35 (21.09–23.80) 0.001

Albumin (g/dl)^b 4.37 (4.09–4.54) 4.45 (4.15–4.55) 4.20 (3.91–4.33) 0.065

Creatinine (mg/dl)^a 8.97±2.05 9.33±1.97 7.47±1.76 0.029

Urea (mg/dl)^a 145.08±28.04 150.87±27.39 121.10±15.88 0.010

Cholesterol (mg/dl)^b 163.83 (139.42–183.75) 168.00 (138.67–184.67) 159.50 (145.83–164.58) 0.460

Phosphorus (mg/dl)^b 5.32 (4.25–6.62) 5.30 (4.27–6.37) 6.37 (4.69–6.81) 0.401

	All patients (n = 36)	Male (n = 29)	Female (n = 7)	p value
Height (m)^b	1.66 (1.59–1.70)	1.68 (1.63–1.70)	1.50 (1.49–1.56)	<0.001
Dry weight (kg)^a	75.34±14.52	78.14±13.93	63.71±11.35	0.016
BMI (kg/m²)^a	27.88±5.04	28.01±5.00	27.35±5.70	0.762
TSF (mm)^b	18.40 (15.00–19.95)	17.60 (12.80–19.00)	28.40 (25.5–30.90)	0.001
MAC (cm)^b	31.77 (30.03–34.00)	32.00 (30.90–34.00)	30.00 (29.00–33.50)	0.345
MAMC (cm)^b	26.73 (25.11–27.54)	26.90 (26.00–27.91)	23.35 (21.09–23.80)	0.001
Albumin (g/dl)^b	4.37 (4.09–4.54)	4.45 (4.15–4.55)	4.20 (3.91–4.33)	0.065
Creatinine (mg/dl)^a	8.97±2.05	9.33±1.97	7.47±1.76	0.029
Urea (mg/dl)^a	145.08±28.04	150.87±27.39	121.10±15.88	0.010
Cholesterol (mg/dl)^b	163.83 (139.42–183.75)	168.00 (138.67–184.67)	159.50 (145.83–164.58)	0.460
Phosphorus (mg/dl)^b	5.32 (4.25–6.62)	5.30 (4.27–6.37)	6.37 (4.69–6.81)	0.401

BMI: Body mass index; MAC: Mid-arm circumference; MAMC: Mid-arm muscle circumference; TSF: Triceps skinfold. ^avalues are expressed as mean±standard deviation. ^bvalues are expressed as median and interquartile ranges.

Table 2

24 hour-derived dietary intakes of Hemodialysis patients

	All patients (n = 36)	Male (n = 29)	Female (n = 7)	p value
Energy (kcal/kg/d)^a	34.53 (33.25–35.22)	34.14 (33.24–35.03)	35.00 (33.40–35.79)	0.717
Protein (g/kg/d)^a	1.25 (1.20–1.28)	1.25 (1.20–1.28)	1.20 (1.20–1.26)	0.526
Potassium (mg/d)^a	1698.50 (1433.25–2286.75)	1709.00 (1454.00–2424.00)	1514.00 (1454.00–1706.50)	0.145
Sodium (mg/d)^a	1329.00 (886.50 –1868.50)	1406.00 (1049.00–1881.00)	857.00 (674.00–1183.00)	0.058
Calcium (mg/d)^b	662.14±340.83	694.97±330.68	526.14±374.88	0.245
Phosphorus (mg/d)^b	1049.64±452.10	1132.24±448.52	707.43±109.47	0.023

^avalues are expressed as median and interquartile ranges. ^bvalues are expressed as mean±standard deviation.

Table 3

Distribution of HD patients according to anthropometric characteristics

Anthropometric measurements	Below average		Healthy (average) range		Above average
	Male	Female	Male	Female	Male		Female
TSF	0	0	16	6	13		1
MAC	0	0	24	6	5		1
MAMC	0	0	26	6	3		1
					Overweight	Obese	Overweight	Obese
BMI	0	0	8	3	14	7	3	1

HD: Hemodialysis; BMI: Body mass index; MAC: Mid-arm circumference; MAMC: Mid-arm muscle circumference; TSF: Triceps skin fold. Underweight was defined as a BMI below 18.5 kg/m², adequate weight as a BMI in the 18.5–24.9 9 kg/m² range, overweight as a BMI in the range of 25–29.9 kg/m², and obesity as a BMI equal or above 30 kg/m². Percentiles of TSF, MAC, and MAMC were considered as healthy, when they were in the 15th to 85th range.

Ideal weight-adjusted energy intakes (wEI) positively correlated with ideal weight-adjusted protein intakes (wPI) (r = 0.666; p = 0.000), and negatively with patient’s age (r = –0.342; p = 0.041) (data not shown). In univariate linear regression, wEI was positively related to BMI, MAC, MAMC, and creatinine (Table 4). However, in the multivariate model, adjusted for age, sex, and time on dialysis, only the association between wEI and anthropometric indices remained significant. Of note, in the multivariate model, the relation between wEI and TSF was significant, even though there was not a statistically significant relation in the unadjusted model.

Table 4

Univariate and multivariate regression between ideal weight-adjusted energy intake and anthropometric and biochemical indices

	Univariate Model			Multivariate Model
Anthropometric Measurements	Unadjusted β coefficient	95% CI	p value	Adjusted β coefficient	95% CI	p value
BMI (kg/m²)	0.292	0.186 to 0.399	<0.001	0.390	0.317 to 0.464	<0.001
TSF (mm)	0.097	–0.002 to 0.195	0.054	0.319	0.193 to 0.445	<0.001
MAC (cm)	0.381	0.218 to 0.545	<0.001	0.507	0.370 to 0.644	<0.001
MAMC (cm)	0.341	0.129 to 0.553	0.003	0.597	0.374 to 0.819	<0.001
Albumin (g/dl)	0.582	–1.456 to 2.619	0.580	1.233	–0.938 to 3.405	0.256
Creatinine (mg/dl)	0.390	0.055 to 0.725	0.024	0.398	–0.027 to 0.824	0.066
Urea (mg/dl)	0.021	–0.004 to 0.046	0.102	0.023	–0.001 to 0.052	0.111

BMI: Body mass index; MAC: Mid-arm circumference; MAMC: Mid-arm muscle circumference; TSF: Triceps skinfold. Multivariate model was adjusted for age, sex, and time on dialysis.

As far as wPI is concerned, a positive relationship was found with variables BMI, TSF, and MAC in the univariate and multivariate (adjusted for age, sex, time on dialysis and total energy intake) model (Table 5). A positive relationship between wPI and MAMC (β= 0.014, 95% CI = 0.008 to 0.020) and albumin (β= 0.072, 95% CI = 0.008 to 0.020) was observed only in the univariate model.

Table 5

Univariate and multivariate regression between ideal weight-adjusted protein intake and anthropometric and biochemical indices

	Univariate Model			Multivariate Model
Anthropometric Measurements	Unadjusted β coefficient	95% CI	p value	Adjusted β coefficient	95% CI	p value
BMI (kg/m²)	0.013	0.012 to 0.014	<0.001	0.012	0.010 to 0.014	<0.001
TSF (mm)	0.004	0.002 to 0.007	0.003	0.003	0.000 to 0.006	0.029
MAC (cm)	0.016	0.013 to 0.020	<0.001	0.007	0.002 to 0.011	0.006
MAMC (cm)	0.014	0.008 to 0.020	<0.001	0.005	–0.001 to 0.011	0.086
Albumin (g/dl)	0.072	0.013 to 0.131	0.018	0.022	0.000 to 0.000	0.332
Creatinine (mg/dl)	0.004	–0.007 to 0.015	0.457	–0.002	–0.009 to 0.004	0.489
Urea (mg/dl)	0.000	–0.001 to 0.001	0.752	0.000	–0.001 to 0.000	0.063

BMI: Body mass index; MAC: Mid-arm circumference; MAMC: Mid-arm muscle circumference; TSF: Triceps skin fold. Multivariate model was adjusted for age, sex, time on dialysis, and total energy intake.

4 Discussion

The present study is one of the few attempts to report the nutritional status of end-stage renal disease patients in an Eastern Mediterranean region [6 –8]. The assessment involved a small group of patients (36 participants) treated at a single dialysis center at Crete, Greece. In contrast to most previous studies [5], patients’ dietary intakes of energy, protein, calcium, sodium, and potassium, as estimated by three 24-hour dietary recalls, reached target values suggested by Kalantar-Zadeh & Fouque (2017) and the most recent NKF guidelines (2019) [4, 17].

The results of the anthropometric measurements were indicative of a well-maintained somatic status. All patients had a BMI higher than 20 kg/m² and most of them (69.4%, male and female) were overweight or obese. High BMI values are generally associated with a lower mortality risk in HD patients, while a BMI below 18 kg/m² is considered an index of wasting [4]. Additionally, patients had MAC and MAMC values ≥25th percentile, which reflect adequate maintenance of somatic mass and body protein reserves, respectively [14]. The TSF values (≥50th percentile) were representative of a healthy to above the average proportion of subcutaneous fat deposits.

Regarding the biochemical markers, pre-dialysis serum values were generally within target ranges. More specifically, serum cholesterol levels were within the recommended range for HD patients (<200 mg/dl) and far beyond the cut off value of 100 mg/dl, which is indicator of protein-energy wasting [3]. The mean urea level was within the expected range, as seen by other reports [18]. Serum creatinine, which is considered a surrogate of muscle mass, was within the common range for HD patients (8–20 mg/dl) [19]. Serum albumin, which is considered an index of nutritional status, was at the optimum level for HD patients (>4 g/dl) [4].

Male patients had significantly higher phosphorus intakes than female patients, which is in line with gender-associated trends in nutritional habits and nutrient intakes of the general population, although the percentage of female patients enrolled in our study was very low (only 19.4%) [20, 21]. Dietary phosphorus intakes were higher than the values suggested by Kalantar-Zadeh & Fouque [17]. Although dietary phosphorus intake influences serum phosphate in HD patients, factors other than intestinal phosphorus absorption (namely exchange with bone and excretion by the kidneys in patients with residual renal function) may be major determinants of serum phosphate levels. For this reason, the most recent NFK guidelines prefer not to suggest specific dietary phosphorus intake ranges, and instead emphasize on the need to individualize treatments based on patient needs and clinical judgment [4]. In our case, serum phosphate levels were only borderline high and generally within the target range suggested.

According to the 24-hour dietary recalls, weight-adjusted dietary energy and protein intakes reached the recommended values. Few studies have reported adequate energy or protein intakes among HD patients e.g. Arslan and Kiziltan reported a daily energy intake of 34.2±8.89 kcal/kg/day, Moreira and colleagues reported a mean protein intake of 1.27 g/kg/day [22, 23]. Most investigations exploring dietary intakes among HD patients report insufficient energy and protein intakes and underreporting has been suggested as a possible explanation for the contradiction of stable body mass in HD patients, despite reported insufficient intakes [24].

A recent study by Lopes et al. demonstrated that the frequency of underreporting was lower for energy intakes estimated with the 24h recall than that estimated with food records [25]. Also, dietary intake among patients is significantly different on HD and non-HD treatment days [26]. In our study three 24-hour diet recalls were conducted on non-consecutive days, including a dialysis day, a non-dialysis day and a weekend day (not on dialysis), in order to obtain the best approximation of the patients’ usual intake during their weekly cycle [10]. The estimated dietary intakes were the average of three recalls.

In multivariate regression analysis, after controlling for confounding variables (age, gender and time on dialysis), the positive association of wEI with BMI, MAC, and MAMC remained significant, while TSF emerged as a major determinant, indicating that patients who reported higher energy intakes were those who had higher somatic mass, subcutaneous fat deposits and muscle mass. Concerning wPI, a positive relationship was also found with variables BMI, TSF, and MAC in the univariate and multivariate model, thereby highlighting the link between protein intake and well-preserved body composition, as reflected by anthropometric indices. Interestingly, the correlations between the dietary intakes, wEI and wPI, with biochemical indices did not persist after adjustment, which underlines their limited value as predictors of nutritional status among these patients.

Patients’ dietary intakes reached recommended target values by following a more plant-based diet with plenty of fresh low-potassium fruits and vegetables, whole grains, legumes, olive oil and less processed food. Meat, poultry, fish, and eggs were less frequently consumed. This dietary approach offers a low phosphorus to protein ratio, since processed foods contain a high content of inorganic phosphorus, which is highly bioavailable, whereas natural foods from animal or plant origin contain mostly organic phosphorus, which is less bioavailable [27]. Especially plant foods contain organic phosphorus mostly in the form of phytic acid, which is the least bioavailable form.

Given the pilot nature of this study, there are several limitations that should be acknowledged. Firstly, the sample size was small with a predominance of male patients, attenuating the ability of robust statistical results. Moreover, we did not assess appetite or patients’ adherence to the traditional Mediterranean diet. Clearly, further research is required to determine the dietary intake and nutritional status of this patient population. However, a multicentre study is currently in progress to assess adherence of Greek HD patients to the Mediterranean diet.

Nevertheless, our study highlights that 24-hour derived-dietary intakes reached recommended targets and adequately reflected the nutritional status of the patients according to anthropometric and biochemical indices. Furthermore, the 24-hour recall method should be part of the routine care for HD patients, in order to identify patients at nutritional risk before objective parameters of wasting are documented.

Funding

The authors report no funding.

Conflict of interest

The authors have no conflict of interest to report.

Footnotes

Acknowledgments

The authors wish to thank all the patients participating in the study, the nephrologist and the staff of the dialysis center.

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