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European Journal of Heart Failure 2008 10(4):428-434; doi:10.1016/j.ejheart.2008.02.016
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© 2008 European Society of Cardiology

Nutrient intake and serum cytokine pattern in elderly people with heart failure

Girolamo Catapanoa, Claudio Pedoneb,*, Eleonora Nunziatab, Alessandro Zizzoa, Andrea Passantinoc and Raffaele Antonelli Incalzia,b

a Fondazione San Raffaele—Cittadella della Carità Taranto, Italy
b Area di Geriatria, Università Campus Biomedico Roma, Italy
c Divisione di Cardiologia e Riabilitazione Cardiaca, Istituto di Ricovero e Cura a Carattere Scientifico "Fondazione Salvatore Maugeri" Cassano Murge (BA), Italy

* Corresponding author. Area di Geriatria, Università Campus Biomedico, Via dei Compositori 130, 00128 Roma, Italy. Tel.: +39 06 22541654; fax: +39 06 22541602. E-mail address: claudio_pedone{at}virgilio.it (C. Pedone).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Background: Heart failure (HF) is frequently complicated by malnutrition. We estimated nutrient intake in HF patients and evaluated the correlation between serum cytokines and dietary pattern.

Methods: We studied 124 elderly (≥ 60 years) patients with severe HF (N = 62) or without HF (controls, N = 62), matched for age and sex. Nutritional data were obtained from the European Prospective Investigation into Cancer and Nutrition (EPIC) questionnaire. We compared the intake of macro- and micronutrients in the two groups; in the HF group nutritional intake was correlated with serum cytokines.

Results: HF patients had a lower energy intake (26.8 Kcal/Kg of ideal weight vs. 37.3 Kcal /Kg ideal weight in controls, P < 0.001) due to a lower intake of all macronutrients. The energy intake was lower than the recommended (30 Kcal/Kg of ideal body weight) in 72% of HF and 34% of the controls. The intake of several minerals and vitamins was inferior to the recommended dietary allowance (RDA) in most participants. Those HF patients with a caloric intake below the median (22.6 Kcal/Kg ideal weight) did not differ substantially from those with higher caloric intake with regard to age, functional characteristics, and lean body mass as expressed by the mid-arm muscle circumference, however, they had a higher concentration of IL4 (61.5 pg/ml vs. 37.7 pg/ml, P = 0.075) and of IL10 (6.32 pg/ml vs. 2.06 pg/ml, P = 0.046).

Conclusions: Nutritional intake is frequently inadequate in patients with severe HF. Our results suggest that some interleukins might affect caloric intake in patients with HF.

Key Words: Heart failure • Nutrition • Elderly

Received June 14, 2007; Revised December 20, 2007; Accepted February 26, 2008


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 
A proportion of patients with heart failure (HF), especially those with advanced disease, have malnutrition with loss of muscle mass, which may be due to both a systemic inflammatory status driving hypercatabolism and to inadequate nutrient intake [1,2]. Patients with systolic HF have an increased concentration of serum proinflammatory cytokines [3], these have a catabolic effect [4] and could in part explain the anorexia which frequently complicates HF [5]. Medical (anorectic effects of drugs, slowed digestion, renal failure, depression) and social factors (inability to go shopping and to prepare meals due to reduced personal independence) are also likely to contribute to decreased nutrient intake, especially in older patients. To our knowledge, the relationship between serum cytokines and nutrient intake has never been investigated, while there is only one study of nutrient intake in a sample of 57 HF patients with a mean age of 52 years showing a nutritional intake that was generally inadequate [6]. However, this observation may not apply to the HF population in general because the majority of patients with severe HF are older [7] and are liable to the concurrent effects of comorbidity and social factors on nutrient intake. The only available observation in a geriatric population shows that the intake of several macronutrients and micronutrients was below the recommended dietary allowances (RDA) in both HF and non-HF subjects [8]. This observation is of interest because some micronutrients, such as thiamine and magnesium, have cardiovascular and metabolic effects and are frequently depleted in patients taking diuretics [9,10].

Clarifying the relationship between cytokine levels and nutritional intake might help to improve selection of HF patients who may benefit from nutritional supplementation or anticytokine therapy, which are presently considered of no or uncertain usefulness [11,12].

This study had two objectives. First, to compare the nutrient intake of a population of patients with HF and depressed LVEF aged over 60 years, with that of control subjects of comparable age free from any major medical problems. Only patients with HF of ischaemic origin were included because aetiology can affect serum cytokine levels [13]. Second, to analyze the relationship between the plasma concentration of proinflammatory and anti-inflammatory cytokines and caloric and macronutrient intake.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1. Sample selection
Subjects with and without HF, aged 60 years or older, were enrolled. This age threshold was selected because it was considered that younger HF patients would not be representative of the overall HF population.

All 62 systolic HF patients were in patients at the Cardiac Rehabilitation Unit of the San Raffaele—Cittadella della Carità foundation (Taranto, Italy). This is a private, non-profit foundation administratively linked to the HSR San Raffaele in Milan which provides universal medical coverage and is funded by the Italian Health Care System. The patients were attending a three week program of cardiac rehabilitation. All patients had stable, severe (NYHA class 3 or 4) HF, secondary to ischaemic heart disease with or without coexisting hypertension and an LVEF of <40%. HF was considered stable if the patient was free from oedema and pleural effusion, rated his/her level of personal independence as "the usual" and had not needed any change in therapy in the month preceding the study. Ischaemic heart disease was diagnosed by angiography in 12 patients and by non-invasive studies (201Thallium myocardial scintigraphy or stress echocardiography with dobutamine) in the remaining 50. LVEF was obtained by the modified Simpson equation [14]. All echocardiograms were recorded by the same operator (GC) using a Vivid 7 GE instrument.

The most common disorders known to increase serum cytokine levels were excluded on the basis of history, physical examination, review of usual pharmacological therapy and previous medical records, and extensive blood and urine analysis including arterial blood gas analysis. Briefly, exclusion criteria were: 1) medical conditions affecting the nutritional status or the appetite or requiring special diets, such as hypoxaemic chronic obstructive pulmonary disease, chronic renal failure, or diabetes mellitus; 2) use of non-cardiovascular drugs which could affect the appetite, nutritional needs or body composition, such as steroids, methotrexate, thyroid hormones, antidepressants; 3) hospital admission for any reason in the 3 months prior to the study; 4) myocardial infarction or unstable angina or revascularization in the last 6 months or decompensated HF in the last 3 months; 5) any acute non-cardiac event likely to affect the nutritional status in the last 3 months, e. g. pneumonia or a surgical procedure; 6) cardiac cachexia, i.e. severe malnutrition defined by body mass index (BMI) <20 Kg/cm2 or serum albumin <3.0 g/dl. We excluded cachectic patients, because a preliminary analysis of pertinent records showed a very high frequency of HF decompensations and hospitalisations in these patients, thus limiting their clinical stability and therefore the assessment of relevant nutrient intake.

As a control group, we selected age and sex matched subjects without HF attending the geriatric outpatient facility of a privately owned, non-profit tertiary care teaching hospital funded by the Italian Health Service System (Centro di Medicina dell’Invecchiamento of the Catholic University in Rome) for minor medical problems such as dyspepsia or mild hypertension. All control subjects had normal laboratory analyses and 12-lead EKG.

2.2. Assessment of nutritional intake and anthropometric measurements
Dietary intake was estimated using the questionnaire developed by the European Prospective Investigation into Cancer and Nutrition (EPIC) [15]. The EPIC questionnaire is divided into two parts: the first investigates the general dietary pattern and the frequency of meals consumed away from home, the second the intake frequency of 236 specific foods, along with the average size of the serving selected from a range as shown in photographs. The information derived from the questionnaire was automatically converted into data on energy, micro- and macronutrient intake, by software specifically designed for the EPIC study. The EPIC nutritional assessment has been successfully validated in the population being studied, by comparing the dietary intake estimated by this method with the dietary intake estimated by a direct method of measuring, weighing and recording of seven day food consumption [16].

The EPIC questionnaire was administered by a registered dietician experienced at interviewing elderly and frail patients. Given that EPIC assesses the usual food intake in the year prior to the interview, the study group had the interview administered on the first day of their hospital stay. Subjects in the control group completed the questionnaire during their outpatient visit after informed consent had been obtained. Thus, the reported nutrient intake of both study and control groups reflects their usual intake at home.

Weight was measured to the nearest kilogram using a standard office scale with individuals in lightweight clothing with shoes removed; height was measured to the nearest centimetre using a metallic tape with the patients head in the Frankfurt plane.

To obtain an index of body composition, we measured the mid-arm circumference and the triceps skin fold [17], then calculated the mid-arm muscular circumference (MAMC), which is an indicator of lean body mass [18].

2.3. Clinical assessment
Physical performance was evaluated using the six minute walking test, performed according to ATS recommendations [19] to measure the 6' walked distance (6' WD), which was also expressed as a percentage of the predicted [20]. Briefly, patients were instructed to walk back and forth along a 30 m hospital corridor to cover as much ground as they could during the 6', without running. An assistant gave encouragement every minute. Patients were allowed to stop and rest, but they were encouraged to resume walking as soon as possible. No supplemental oxygen was given during the test. Transcutaneous oxygen saturation and heart rate were continuously recorded throughout the test using a finger pulse oximeter.

Mood status was evaluated using the 15-item Geriatric Depression Scale (GDS), scores range from 0 to 15, with a score of 5 or more indicating depression [21].

Cognitive function was evaluated using the Mini-Mental State Examination, scores range from 0 to 30, with a score below 24 indicating cognitive impairment [22].

2.4. Serum cytokine measurements
A fasting blood sample was collected after a supine rest of 20 min. The blood was transferred to a pre-refrigerated tube containing EDTA (1 mg/ml) and aprotinin (500 U/ml), and then centrifuged at 3000 rpm for 15' at 4 °C. Plasma concentrations of interleukins 2, 4, 5, 8, and 10, Tumour Necrosis Factor (TNF), and {gamma}-interferon were measured by ELISA (Immunotech Beckman Coulter Company). The coefficient of variation was less than 10% for all assays. We chose these cytokines on the basis of the available information on cytokine pattern in HF and with the additional aim of testing both Th1-derived (IL2, IL8, {gamma}-interferon) and Th2-derived (IL4, IL5, IL10) molecules [12,23]. Thus, we aimed to assess the balance between T Lymphocyte populations in CHF instead of merely focusing the study on well recognized inflammatory cytokines. We did not measure IL6, a well known marker of HF severity, because it is released in direct response to TNF [23]. Thus, we judged that IL6 would have not added to the information provided by TNF.

2.5. Analytical approach
We compared HF and non-HF participants with respect to demographic and anthropometric characteristics, and to energy and nutrient intake. Macronutrient intake was compared both in absolute values and in relation to actual and ideal body weight estimated using the Lorenz formula (see Appendix A). We also compared the basal metabolic rate (BMR) calculated using the HarrisonvrectoBenedict formula (see Appendix A) and the total energy intake (TEI) / BMR ratio in the two groups.

For micronutrients (minerals, vitamins and fatty acids), we reported the absolute intake and, where available, the intake expressed as a percentage of the RDA [24] and the proportion of participants with an intake below the RDA.

In the HF group only, we sought to identify the clinical and functional characteristics associated with a lower caloric intake, and also whether lower caloric intake was associated with a distinctive serum cytokine pattern. Therefore, we grouped the HF patients according to their caloric intake, using the median of the distribution (22.6 Kcal/day) as the cut-off, and compared the characteristics of the two groups using a t-test to evaluate the probability of a false positive result.

All analyses were performed using SAS version 9.0 (SAS Institute, Cary NC).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 Appendix A
 References
 
We analyzed data from 62 HF patients (66% men, mean age 73.8±8.9 years), in NYHA class 3 (N=44) or 4 (N=18), with an average ejection fraction of 32.4% (SD: 6.8), and 62 controls (men 66 %, mean age 75.5±5.5 years).There was no difference in the sex-specific mean age of the subjects with and without HF. All HF patients reported having a care-giver and none reported any financial problems in buying food. The diagnoses with the highest prevalence among the HF patients were ischaemic heart disease, hypertension, chronic obstructive pulmonary disease, and chronic renal insufficiency. Among the control subjects, the most common diagnoses were hypertension and degenerative joint disease. HF patients and controls had a similar mean number of coexisting diseases (4.4 and 4.1, respectively), but patients with HF received more medications (mean number of drugs: 7.6 vs. 2.6 in the controls).

The two groups had comparable average BMI (Table 1), although the group with HF tended to have a lower weight. Mean energy intake was lower in HF patients (1511 Kcal vs. 2264 Kcal in the control subjects without HF), as was energy intake expressed as a function of actual weight (22.3 Kcal/Kg vs. 29.2 Kcal /Kg) or ideal weight (26.8 Kcal/Kg vs. 37.3 Kcal/Kg). The two groups had a similar estimated basal metabolic rate, and the group with HF had a lower TEI/BMR ratio. The proportion of calories coming from lipids and carbohydrates was similar in the two groups. The caloric intake from non-protein nutrients was lower in the group with HF (1291.9 Kcal vs. 1921.7 in the control group without HF), as was the protein intake/body weight (1.0 vs. 1.4 in the control group). About one-third (32.2%) of the patients with HF had a protein intake lower than 0.8 g/Kg, compared with only 8% of the controls. The proportion of subjects with a caloric intake lower than the recommended (30 Kcal/Kg of ideal body weight/day) was 72% and 24% for those with and without HF, respectively.


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  		Table 1 Intake of macronutrients

 
The intake of minerals, vitamins and fatty acids is shown in Tables 2 and 3. Reflecting the lower intake of macronutrients, patients with HF had on average a lower intake of micronutrients. The intake of thiamine, colecalciferol, and linolenic acid was similar in the two groups. Most subjects in both groups had an inadequate intake of sodium, potassium and calcium; the intake of iron was on average adequate, but about 1/3 of the HF patients had an intake below the RDA. Compared to the RDA, folate intake was on average largely inadequate (48% of the RDA in the group with HF and 69% of the RDA in the control group). The intake of other hydrosoluble vitamins was on average good in the control group, but most patients with HF did not meet the RDA for these vitamins.


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  		Table 2 Intake of micronutrients

 


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  		Table 3 Intake of micronutrients compared to daily allowances (20)

 
The intake of liposoluble vitamins (retinol, colecalciferol, tocoferol) met the RDA in a small minority of both HF patients and controls. In particular, we observed a very low intake of tocoferol (34% and 53% of the RDA in people with and without HF, respectively) and colecalciferol (40% and 47% of the RDA in people with and without HF, respectively).

As expected in this Italian population, the intake of oleic acid was comparable to that observed in other populations consuming a Mediterranean diet; patients with HF, however, had a lower intake (25.5 g/day vs. 38.9 g/day in patients without HF). The intake of PUFA, especially of linoleic acid, was low in both groups.

Table 4 compares HF patients with or without a low caloric intake, defined as a ratio Kcal/Kg of ideal weight above or below the median, with regard to clinical and anthropometric characteristics, and concentration of circulating cytokines. We found no differences between the groups, except for a higher concentration of IL4 and IL10 in the group with lower caloric intake (61.5 pg/ml vs. 37.7 pg/ml in the higher caloric intake group, P=0.07 for IL4, and 6.32 pg/ml vs. 2.06 pg/ml in the higher caloric intake group, P=0.05 for IL 10).


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  		Table 4 Characteristics of HF patients with and without low caloric intake

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
Appendix A
 References
 
We found that caloric intake was significantly lower in HF patients than in a control population of comparable age with various chronic diseases, but free from HF. The proportion of calories derived from each of the three categories of macronutrients was not different between the groups, indicating that patients with HF have a homogenous reduction in nutrient intake rather than a distinctive nutritional pattern. The intake of micronutrients was also lower than recommended in most of the HF patients, but the same was true also for selected micronutrients in the control group. Finally, nutritional intake was related to serum levels of IL4 and IL10 in the group with HF.

4.1. Population
We studied HF patients with a mean age of over 70 years with a heavy burden of comorbidity and an important impairment of health status. Such a demographic and health status profile was expected in this group of patients with advanced age and depressed LVEF. However, the studied population may not be completely representative of the average HF population because we excluded cachectic patients and those with comorbidities likely to affect serum cytokine levels, such as hypoxemic chronic obstructive pulmonary disease and renal failure. Furthermore, patients with diastolic HF, which is reported in up to 45% of elderly patients with hypertension [25], were excluded from our study because serum cytokines have been reported to increase in the context of depressed LVEF [23].

4.2. Methods
Nutrient intake in a HF-free population of comparable age, with minor medical problems was used as reference. While not reflecting the nutrient needs of HF patients, these reference data allow the evaluation of nutrient intake of HF patients in a real life situation: the lack of a control population would make it impossible to tell whether the intake of individual nutrients is generically age-related in our country or is typical of patients with HF. We used a high quality nutritional questionnaire administered by skilled personnel and collected data in a framework free from the major confounders. Thus, the information from the comparison between the groups should be interpreted in the context of assessing whether HF patients had a distinctive nutrient intake and not whether this intake is adequate to their needs. Accordingly, the computation of the ratios between actual intake and RDA for micronutrients is provided to improve the comparison between HF and non-HF patients and not to assess the adequacy of intake in HF patients.

4.3. Results
The main finding was that HF patients had an average nutrient intake only 14% greater than the BMR and 30% less than that of controls, with a daily intake of 26.8 Kcal/Kg ideal weight and 1 g of proteins per Kg of ideal body weight. However, their nutritional status, as reflected by both BMI and MAMC, was fair, which is consistent with the intake meeting nutrient requirements, likely because of reduced physical activity. Thus, our findings show that nutritional status can be preserved even if the nutrient intake is slightly low compared to the most conservative estimate of the average requirement (about 1700 Kcal/day in non-cachectic HF patients) [26].

Interestingly, Aquilani et al. found a comparable average intake in a younger (mean age 52.3±3 years) HF population with poorer nutritional status, as expressed by a mean BMI of 22.4±3 [6], and similar findings were also obtained by Gorelik et al. in an older HF population [8]. Thus, nutrient intake seems to be reduced to a comparable extent in HF populations with different ages and nutritional status.

We found a low TEI/BMR ratio in patients with HF. However, since we did not directly estimate the physical activity level, the explanation of this finding can only be speculative. Given the relatively high average 6' walked distance (60% of predicted) and the good reliability of the EPIC questionnaire, we believe that the most likely explanation is that patients with HF are losing weight. Follow up of these HF patients would be required to test this hypothesis.

The fact that protein intake was lower than 0.8 g/Kg ideal weight in 30% of patients in the absence of conditions such as renal failure, in which such a reduction is advisable, might impact on the evolution of health status. Low protein intake has been shown to be associated with incident osteoporosis and sarcopenia [27,28], conditions which are highly prevalent in HF populations and associated with frailty and mortality in the general elderly population [29,30].

We found that IL4 and IL10 serum concentrations were higher in HF patients with lower caloric intake. This finding deserves consideration because both IL4 and IL10 are Th2-derived cytokines promoting humoral mediated immunity [31]. Thus, it cannot be excluded that the balance between selected Th1-derived and Th2-derived cytokines is a marker of the catabolic status complicating HF. However, the biological effect of cytokines stems from their competitive or cooperative interaction. Thus, the relationships between serum levels of individual cytokines and nutrient intake may not capture the full spectrum of cytokine effects on nutrient intake.

4.4. Limitations
We used a very accurate diagnostic instrument which guarantees the quality of the recorded nutrient intake, although it does not take into account vitamin and mineral supplements; however, we did not measure caloric requirements which were derived from studies providing partly discordant results. Indeed, Obisesan et al. found that resting metabolic rate increased with worsening symptoms in HF [32], but other studies have reported a lower energy expenditure in HF patients compared to normal subjects of similar age [33]. Differences in studied populations might explain these discrepancies: it is possible that the dramatic decline in physical activity with HF progression results in decreased energy expenditure [26]. Because of this uncertainty, we referred to the RDA developed for the elderly general population and not for elderly HF patients.

For selected nutrients, differences in RDA between the most recent and previous dietary recommendations cast some doubt in this area, and thus prevents us from drawing unequivocal conclusions, for example as to whether the intake of potassium was or was not in the recommended range.

No information is available on the presence of a care-giver in the control group. The tight family ties which account for the fact that none of the HF patient had problems with preparing meals are also likely to be true for control subjects. At any rate, the potential bias introduced is a conservative one: the proportion of patients with problems in food supply/preparation can only be either the same or higher in the control group. Furthermore, we studied patients who were carefully selected at unique geriatric and cardiac centres, and this might limit the generalizability of our findings. For instance, the adherence to a strictly low sodium diet, which is recommended to HF patients, might not be so common in the average HF population.

Finally, we could not calculate the intake of magnesium, a mineral which has important cardiovascular effects.

4.5. Conclusions
Elderly HF patients have a lower caloric intake than home-dwelling elderly subjects free from HF and any other major medical problems. The intake of almost all micronutrients was largely inferior to recommended levels in the vast majority of HF patients, but this was also true in a proportion of the non-HF controls. The relationship between cytokines and reduced calorie intake suggests that either selected cytokines might affect nutrient intake; or that the given cytokine profile and the corresponding pattern of nutrient intake reflect the severity of HF. Further work is required to clarify whether a given alimentary pattern heralds weight loss and ultimately malnutrition in currently well nourished HF patients; as well as whether nutritional supplementation and, possibly, targeted anticytokine therapy could improve the nutritional status of selected patients.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
References
 
Lorenz formula:

Ideal Weight (males)=height–100–(height–150)/4.
Ideal Weight (women)=height–100–(height–150)/2.

Harrison-Benedict formula:

Basal metabolic rate (males)=66+(13.7*weight)+(5*height)–(6.8*age).
Basal metabolic rate (females)=655+(9.6*weight)+(1.8*height)–(4.7*age).


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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