Clinical Nutrition xxx (2014) 1e6
Contents lists available at ScienceDirect
Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu
Original article
Energy expenditure and balance among long term liver recipients Helem S. Ribeiro a, Lucilene R. Anastácio b, Lívia G. Ferreira c, Agnaldo S. Lima d, Maria Isabel T.D. Correia d, * a
Food Science Post Graduation Program, Pharmacy School, Universidade Federal de Minas Gerais, Brazil Adult Health Post Graduation Program, Medical School, Universidade Federal de Minas Gerais, Brazil c Surgery Post Graduation Program, Medical School, Universidade Federal de Minas Gerais, Brazil d Alfa Institute of Gastroenterology, Hospital of Clinics, Medical School, Universidade Federal de Minas Gerais, Brazil b
a r t i c l e i n f o
s u m m a r y
Article history: Received 15 April 2013 Accepted 27 December 2013
Background: Excessive weight gain in patients undergoing liver transplantation has been well documented. The etiology for this complication is not well defined, although it has a high prevalence in posttransplant patients. Reduced energy expenditure may be related to excessive weight gain. Thus, the assessment of the resting energy expenditure (REE) in this patient population is of utmost importance. Methods: Therefore, patients who underwent liver transplantation had their REEs measured by indirect calorimetry (IC). These results were compared with the demographic, socioeconomic, clinical, anthropometric, dietary and lifestyle variables assessed by uni- and multivariate statistical analyses. The REEs were also compared to estimates using the HarriseBenedict formula, and the patients were classified as hypo-, normo- and hypermetabolic. Results: We evaluated 42 patients with an average of 6.5 years post-transplant and an REE of 1449.7 kcal/ day (measured by IC) or 1404.5 kcal/day (predicted by the HB formula). There was great correlation between the methods, and the best predictors of REE were age, weight, amount of lean mass and amount of total body water. Excessive weight was observed in 57% of patients, and obesity was observed in 26.2%. Underreporting of energy intake was observed in 65.8% of patients, and most patients (92.7%) were classified as sedentary or less active. No patient was classified as hypometabolic. Conclusions: These results indicate that hypometabolism should be discarded as cause of the high prevalence of overweight and obese patients in the population undergoing LT. However, energy consumption and low levels of physical activity may be risk factors. Ó 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism.
Keywords: Liver transplantation Resting energy expenditure Excessive weight
1. Introduction Transplantation is the only effective treatment method for endstage and acute liver failure. A combination of advances in surgical technique, patient selection, improved perioperative care, and availability of adequate immunosuppressive agents has resulted in significant improvements in the overall patient survival after liver transplantation (LT).1 Long-term survival has also increased the
Abreviations: LT, liver transplantation; REE, resting energy expenditure; IC, indirect calorimetry; TEE, total energy expenditure; MET, metabolic equivalent; WC, waist circumference; BMI, body mass index; WHO, World Health Organization. * Corresponding author. Alfa Institute of Gastroenterology, Medical School, Hospital of Clinics Universidade Federal de Minas Gerais, Avenida Prof. Alfredo Balena, 110, Sala 208, Belo Horizonte, Minas Gerais 31270-901, Brazil. Tel.: þ55 31 91688239. E-mail addresses: [email protected] (H.S. Ribeiro), [email protected]. br (M.I.T.D. Correia).
incidence of long-term complications. One of the most prevalent complications is being overweight.2e4 Weight gain can result in the onset of metabolic syndrome and its individual components.5,6 However, few studies have demonstrated an association between energy intake and weight gain7e9 or metabolic syndrome.5 The hypothesis that these patients can be hypometabolic, however, has been raised in the literature8 but not yet confirmed. To understand the nutritional status changes and clinical outcomes of these patients, it is of paramount importance to understand the changes in energy expenditure that occur in the post-transplant period. Potential reduced metabolism, combined with higher food intake and physical inactivity, could justify the excessive weight gain in these patients. Furthermore, the study of resting energy expenditure (REE) can assist in confirming the data obtained from dietary surveys. There are few published data measuring REE in patients undergoing LT. Moreover, these data have usually been collected in patients assessed after a short post LT time period.8,10e12
0261-5614/$ e see front matter Ó 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. http://dx.doi.org/10.1016/j.clnu.2013.12.015
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
2
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
The aim of this study was to measure the REE by indirect calorimetry (IC) and to identify the associated predictive factors as well as compare the measured REE with the predicted REE using the HarriseBenedict (HB) equation and examine the presence of hypoor hypermetabolism to assess total energy expenditure (TEE) versus total caloric intake. 2. Methods 2.1. Study design and patients This was a cross-sectional study. The data were collected from March to October 2011. The study was conducted at a single center. Post-liver transplant patients were followed at the Alfa Institute of Gastroenterology e Transplant Outpatient Clinic, Universidade Federal de Minas Gerais, Brazil. The minimum patient age was 18 years and only patients who had at least 1 year posttransplantation were included. Pregnant women, patients with recurrent liver failure with ascites (according to a physical examination at the time of the current assessment) and patients with a history of thyroid dysfunction or kidney disease were excluded. The patients were interviewed once to assess their demographic, socioeconomic, lifestyle, clinical, anthropometric, metabolic and dietetic characteristics. Retrospective variables were collected from the medical records. Informed written consent was collected from all patients and the study was approved by the Ethics Committee of Universidade Federal de Minas Gerais (protocol number ETIC 44/08). 2.2. Methods Demographic and socioeconomic data were age, sex, marital status (married versus single), paid professional activity, education, and income. The lifestyle data were based on hours of sleep per night, smoking, past smoking, and physical activity levels. The patients were asked about their daily activities, and their responses were transformed into corresponding Metabolic Equivalent (MET).13 The daily activities that were transformed into MET were multiplied by the respective time spent on these activities, and the results were added and divided by 24 h. This value was categorized according to the level of activity performed into 1.9 e very active).14 The following clinical data were assessed: the time since LT, tacrolimus or cyclosporine use; hypertension and diabetes mellitus at the time of assessment (current medication as described in the medical records, registered arterial hypertension and diabetes mellitus prior to LT), the family history of diabetes, hypertension, overweight and cardiovascular disease. The measured anthropometric data were waist circumference (WC) (two fingers above the umbilicus), body mass index (BMI) and BMI classification (prior to liver dysfunction and on the day of the interview), and weight gain after the transplantation. Each patient’s weight prior to the liver dysfunction was self-reported, and the current weight was measured. Abdominal obesity and BMI were classified according to the World Health Organization (WHO)(1998).14 A multi-frequency bioelectrical impedance analysis (Quantum X e RJL Systems, Inc., Clinton Township, Michigan) was used to determine the body composition. Obesity was defined if the body fat percentage was >25% in men and 32% in women.15 Energy intake was assessed with a 3-day food record (intake on 2 weekdays and 1 weekend day). The quantification of the foods and drinks was estimated using household measures (such as cups or spoons). The assessed food intake was converted into calories; carbohydrates; proteins; total fat; saturated fat; monounsaturated fat; polyunsaturated fat; cholesterol; total fiber; vitamins A, C, D, and E;
thiamin; riboflavin; niacin; pantothenic acid; vitamin B6; folic acid; vitamin B12; calcium; iron; magnesium; potassium; sodium; and zinc with the aid of Microsoft Excel (Microsoft Corp., Redmond, WA, USA) software and the Philippi et al. table of food composition.16 To assess each patient’s reliability on energy intake, the total assessed consumption was divided by measuring REE, and a Goldberg cut-off point of 1.2 for sedentary people was considered.17 The REE was measured using open-circuit IC (Teem 100 e Aerosport Inc., Ann Arbor, Michigan, EUA), validated by previous studies.18 The device was calibrated before each measurement according to the manufacturer’s recommendation. After an overnight fast of at least 8 h, the patients were placed in a recumbent position and were motionless and awake during the test. Oxygen consumption (VO2) and carbon dioxide production (VCO2) were measured for 30 min, and the first 5 min were discarded. The energy expenditure was calculated using the Weir formula.19 The predicted energy expenditure was derived from Harris Benedict’s formula.20 Patients were classified as hypermetabolic if the ratio REE measured by IC:REE provided by the equation was >120%, and as hypometabolic if the ratio REE measured by IC:REE provided by the equation was 25 kg/m2 (excessive weight) before hepatic dysfunction was present in 31.0% of patients and present in 59.5% at the time of evaluation. And BMIs >30 kg/m2 (obesity) was observed in 4.8% of the patients before and in 26.2% after the transplantation. There were statistically significant differences between the groups when assessing BMI before transplantation >30.0 kg/m2 versus current BMI >30.0 kg/ m2 (MC Nemar test, p < 0.05). The mean WC was 86.7 13.2 cm in
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
women and 94.5 13.7 cm in men. According to the World Health Organization WHO criteria (1998), abdominal obesity level 1 was present in 53.7% of the patients (57.9% of women and 50.0% of men) and abdominal obesity level 2 in 36.7% of patients (52.6% in women and 22.7% in men). The bioelectrical impedance analysis was performed in 40 patients. Approximately half of the female population (45.2%) had an elevated fat percentage (>32%), and 28.6% of the men also had high body fat (>25%). The current phase angle average was 6.2 1.1. Detailed descriptions of food intake are shown in Table 2, 29.0% of the patients had total energy intakes >90% of TEE; 36.8% had an optimal energy consumption (90% and 110% of TEE) and 34.2% (n ¼ 13) had an energy consumption < 90% of the TEE. Sub notification of diet reports was observed in most of the patients (65.8%). The median of TEE/energy intake was 0,77 and no association was found with this ratio and weight gain (Pearson’s test; p ¼ 0,72; r ¼ 0,06). The average REE measured by IC was 1449.7 226.7 kcal/d. It was 1404.5 166.1 kcal/d when estimated with the HB formula. No patient was classified as hypo- or hypermetabolic. Pearson’s correlation between the methods showed a coefficient of 0.97 (p < 0.01). Subsequently, the linear regression of the methods resulted in R2 ¼ 0.91 (Figure 1). The absolute values of REE obtained by IC were analyzed with the numerical and categorical variables. The variables with p < 0.2 entered in the multiple linear regression model are shown in Table 3. The final multiple linear regression model to predict the REE was p < 0.01, R2 ¼ 0.970 and adjusted R2 ¼ 0.967. In the final Table 1 Characteristics of patients undergoing liver transplantation (n ¼ 42), Brazil, 2012. Categorical parameters
Table 2 Consumption of total calories, macronutrients and micronutrients of patients undergoing liver transplantation (n ¼ 38), Brazil, 2012. Nutrient
Average SD/Median (MineMax)
Calories (kcal) Carbohydrates (%) Protein (%) Lipids (%) Fiber (g) Vitamin A (mcg) Vitamin D (mcg) Vitamin E (mg) Vitamin C (mg) Thiamine (mg) Riboflavin (mg) Niacin (mg) Pyridoxine (mg) Vitamin B12 (mcg) Folate (mcg) Iron (mg) Calcium (mg) Magnesium (mg) Zinc (mg) Potassium (mg) Phosphorus (mg)
1620.9 457.0 53.8 6.0 15.9 3.4 29.1 5.2 17.3 7.1 629.3 624.4 2.0 1.3 15.4 5.2 96.8 (40.3e888.7) 1.16 0.34 1.0 (0.4e2.1) 16.2 5.2 1.5 0.6 1.6 (0.3e5.9) 109.7 51.3 10.4 3.1 538.5 262.4 169.9 57.6 7.1 2.4 1803.1 596.9 631.8 192.3
model, age (p < 0.001), current weight (p < 0.001), lean body mass (p < 0.004) and total body water (p < 0.022) remained as the highest predictors of resting energy expenditure. These variables were used to develop the equation that predicted up to 97% of the REEs of the assessed patients: REE (kcal/day) ¼ 6905 age (years) þ 10.3 current weight (kg) þ 26.7 lean mass (kg)28.1 total body water (liters)
% (n)
Gender e male Married/Lives with partner Housewife/unemployed/retired Smokers Former smokers Level activity Sedentary Low activity Active Tacrolimus use Arterial hypertension prior to LT Arterial hypertension after LT Diabetes mellitus prior to LT Diabetes mellitus after LT Family history Arterial hypertension Diabetes mellitus Excessive weight Cardiovascular diseases Other parameters
3
52.4 76.2 62.8 2.4 40.5
(22) (32) (27) (1) (17)
48.8 43.9 7.3 88.1 21.4 33.3 7.1 21.4
(20) (18) (3) (37) (9) (14) (3) (9)
69.0 33.3 42.9 50.09
(29) (14) (18) (21)
4. Discussion Indirect calorimetry is considered the standard method for measuring REE.22 Few studies have reported the REE in patients undergoing LT. In the Brazilian population, there are no data related to the topic. This study evaluated 42 patients who underwent LT. The mean REE measured by IC was 1449.7 226.7 kcal, a value that aligned with other studies (Table 4). However, 3 of these 4 studies
Average standard deviation
Sleep per night (h) 7.8 Weight prior LT (kg) 65.3 Weight at the moment of assessment (kg) 71.3 BMI prior LT (kg/m2) 24.5 2 BMI at the moment of assessment (kg/m ) 26.8 Waist circumference (cm) 90.8 Total body water (%) 50.0 Intracellular body water (%) 55.2 Extracellular body water (%) 44.8 Lean mass (%) 66.9 Body fat (%) 32.5 REE measured by IC (kcal/d) 1449.7 REE predict by HB (kcal/d) 1404.5
1.1 16.1 15.5 4.6 4.8 13.9 8.0 3.8 3.8 10.4 9.6 226.7 166.1
LT: liver transplantation, BMI: body mass index, REE: resting energy expenditure.
Fig. 1. Linear regression between resting energy expenditure by indirect calorimetry and the Harris and Benedict formula in patients undergoing liver transplantation (n ¼ 42), Brazil, 2012.
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
4
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
Table 3 Variables associated/correlated with resting energy expenditure by indirect calorimetry in patients undergoing liver transplantation inserted in the multiple linear regression model (n ¼ 42). Brazil, 2012. Variables
p value
Gender Weight (kg) Height (m) Waist circumference (cm) Lean mass (kg) Total body water (L) Systolic blood pressure (mmHg) Carbohydrate intake (%) Protein consumption (g) Monounsaturated fatty acid intake (g) Dietary cholesterol (mg) Consumption of calcium (mg) Phosphorus intake (mg) Adequate intake or more of vitamin E (mg) Adequate intake or more of vitamin B1 (mg) Adequate intake or less of sodium (mg)
0.04
Contents lists available at ScienceDirect
Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu
Original article
Energy expenditure and balance among long term liver recipients Helem S. Ribeiro a, Lucilene R. Anastácio b, Lívia G. Ferreira c, Agnaldo S. Lima d, Maria Isabel T.D. Correia d, * a
Food Science Post Graduation Program, Pharmacy School, Universidade Federal de Minas Gerais, Brazil Adult Health Post Graduation Program, Medical School, Universidade Federal de Minas Gerais, Brazil c Surgery Post Graduation Program, Medical School, Universidade Federal de Minas Gerais, Brazil d Alfa Institute of Gastroenterology, Hospital of Clinics, Medical School, Universidade Federal de Minas Gerais, Brazil b
a r t i c l e i n f o
s u m m a r y
Article history: Received 15 April 2013 Accepted 27 December 2013
Background: Excessive weight gain in patients undergoing liver transplantation has been well documented. The etiology for this complication is not well defined, although it has a high prevalence in posttransplant patients. Reduced energy expenditure may be related to excessive weight gain. Thus, the assessment of the resting energy expenditure (REE) in this patient population is of utmost importance. Methods: Therefore, patients who underwent liver transplantation had their REEs measured by indirect calorimetry (IC). These results were compared with the demographic, socioeconomic, clinical, anthropometric, dietary and lifestyle variables assessed by uni- and multivariate statistical analyses. The REEs were also compared to estimates using the HarriseBenedict formula, and the patients were classified as hypo-, normo- and hypermetabolic. Results: We evaluated 42 patients with an average of 6.5 years post-transplant and an REE of 1449.7 kcal/ day (measured by IC) or 1404.5 kcal/day (predicted by the HB formula). There was great correlation between the methods, and the best predictors of REE were age, weight, amount of lean mass and amount of total body water. Excessive weight was observed in 57% of patients, and obesity was observed in 26.2%. Underreporting of energy intake was observed in 65.8% of patients, and most patients (92.7%) were classified as sedentary or less active. No patient was classified as hypometabolic. Conclusions: These results indicate that hypometabolism should be discarded as cause of the high prevalence of overweight and obese patients in the population undergoing LT. However, energy consumption and low levels of physical activity may be risk factors. Ó 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism.
Keywords: Liver transplantation Resting energy expenditure Excessive weight
1. Introduction Transplantation is the only effective treatment method for endstage and acute liver failure. A combination of advances in surgical technique, patient selection, improved perioperative care, and availability of adequate immunosuppressive agents has resulted in significant improvements in the overall patient survival after liver transplantation (LT).1 Long-term survival has also increased the
Abreviations: LT, liver transplantation; REE, resting energy expenditure; IC, indirect calorimetry; TEE, total energy expenditure; MET, metabolic equivalent; WC, waist circumference; BMI, body mass index; WHO, World Health Organization. * Corresponding author. Alfa Institute of Gastroenterology, Medical School, Hospital of Clinics Universidade Federal de Minas Gerais, Avenida Prof. Alfredo Balena, 110, Sala 208, Belo Horizonte, Minas Gerais 31270-901, Brazil. Tel.: þ55 31 91688239. E-mail addresses: [email protected] (H.S. Ribeiro), [email protected]. br (M.I.T.D. Correia).
incidence of long-term complications. One of the most prevalent complications is being overweight.2e4 Weight gain can result in the onset of metabolic syndrome and its individual components.5,6 However, few studies have demonstrated an association between energy intake and weight gain7e9 or metabolic syndrome.5 The hypothesis that these patients can be hypometabolic, however, has been raised in the literature8 but not yet confirmed. To understand the nutritional status changes and clinical outcomes of these patients, it is of paramount importance to understand the changes in energy expenditure that occur in the post-transplant period. Potential reduced metabolism, combined with higher food intake and physical inactivity, could justify the excessive weight gain in these patients. Furthermore, the study of resting energy expenditure (REE) can assist in confirming the data obtained from dietary surveys. There are few published data measuring REE in patients undergoing LT. Moreover, these data have usually been collected in patients assessed after a short post LT time period.8,10e12
0261-5614/$ e see front matter Ó 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. http://dx.doi.org/10.1016/j.clnu.2013.12.015
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
2
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
The aim of this study was to measure the REE by indirect calorimetry (IC) and to identify the associated predictive factors as well as compare the measured REE with the predicted REE using the HarriseBenedict (HB) equation and examine the presence of hypoor hypermetabolism to assess total energy expenditure (TEE) versus total caloric intake. 2. Methods 2.1. Study design and patients This was a cross-sectional study. The data were collected from March to October 2011. The study was conducted at a single center. Post-liver transplant patients were followed at the Alfa Institute of Gastroenterology e Transplant Outpatient Clinic, Universidade Federal de Minas Gerais, Brazil. The minimum patient age was 18 years and only patients who had at least 1 year posttransplantation were included. Pregnant women, patients with recurrent liver failure with ascites (according to a physical examination at the time of the current assessment) and patients with a history of thyroid dysfunction or kidney disease were excluded. The patients were interviewed once to assess their demographic, socioeconomic, lifestyle, clinical, anthropometric, metabolic and dietetic characteristics. Retrospective variables were collected from the medical records. Informed written consent was collected from all patients and the study was approved by the Ethics Committee of Universidade Federal de Minas Gerais (protocol number ETIC 44/08). 2.2. Methods Demographic and socioeconomic data were age, sex, marital status (married versus single), paid professional activity, education, and income. The lifestyle data were based on hours of sleep per night, smoking, past smoking, and physical activity levels. The patients were asked about their daily activities, and their responses were transformed into corresponding Metabolic Equivalent (MET).13 The daily activities that were transformed into MET were multiplied by the respective time spent on these activities, and the results were added and divided by 24 h. This value was categorized according to the level of activity performed into 1.9 e very active).14 The following clinical data were assessed: the time since LT, tacrolimus or cyclosporine use; hypertension and diabetes mellitus at the time of assessment (current medication as described in the medical records, registered arterial hypertension and diabetes mellitus prior to LT), the family history of diabetes, hypertension, overweight and cardiovascular disease. The measured anthropometric data were waist circumference (WC) (two fingers above the umbilicus), body mass index (BMI) and BMI classification (prior to liver dysfunction and on the day of the interview), and weight gain after the transplantation. Each patient’s weight prior to the liver dysfunction was self-reported, and the current weight was measured. Abdominal obesity and BMI were classified according to the World Health Organization (WHO)(1998).14 A multi-frequency bioelectrical impedance analysis (Quantum X e RJL Systems, Inc., Clinton Township, Michigan) was used to determine the body composition. Obesity was defined if the body fat percentage was >25% in men and 32% in women.15 Energy intake was assessed with a 3-day food record (intake on 2 weekdays and 1 weekend day). The quantification of the foods and drinks was estimated using household measures (such as cups or spoons). The assessed food intake was converted into calories; carbohydrates; proteins; total fat; saturated fat; monounsaturated fat; polyunsaturated fat; cholesterol; total fiber; vitamins A, C, D, and E;
thiamin; riboflavin; niacin; pantothenic acid; vitamin B6; folic acid; vitamin B12; calcium; iron; magnesium; potassium; sodium; and zinc with the aid of Microsoft Excel (Microsoft Corp., Redmond, WA, USA) software and the Philippi et al. table of food composition.16 To assess each patient’s reliability on energy intake, the total assessed consumption was divided by measuring REE, and a Goldberg cut-off point of 1.2 for sedentary people was considered.17 The REE was measured using open-circuit IC (Teem 100 e Aerosport Inc., Ann Arbor, Michigan, EUA), validated by previous studies.18 The device was calibrated before each measurement according to the manufacturer’s recommendation. After an overnight fast of at least 8 h, the patients were placed in a recumbent position and were motionless and awake during the test. Oxygen consumption (VO2) and carbon dioxide production (VCO2) were measured for 30 min, and the first 5 min were discarded. The energy expenditure was calculated using the Weir formula.19 The predicted energy expenditure was derived from Harris Benedict’s formula.20 Patients were classified as hypermetabolic if the ratio REE measured by IC:REE provided by the equation was >120%, and as hypometabolic if the ratio REE measured by IC:REE provided by the equation was 25 kg/m2 (excessive weight) before hepatic dysfunction was present in 31.0% of patients and present in 59.5% at the time of evaluation. And BMIs >30 kg/m2 (obesity) was observed in 4.8% of the patients before and in 26.2% after the transplantation. There were statistically significant differences between the groups when assessing BMI before transplantation >30.0 kg/m2 versus current BMI >30.0 kg/ m2 (MC Nemar test, p < 0.05). The mean WC was 86.7 13.2 cm in
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
women and 94.5 13.7 cm in men. According to the World Health Organization WHO criteria (1998), abdominal obesity level 1 was present in 53.7% of the patients (57.9% of women and 50.0% of men) and abdominal obesity level 2 in 36.7% of patients (52.6% in women and 22.7% in men). The bioelectrical impedance analysis was performed in 40 patients. Approximately half of the female population (45.2%) had an elevated fat percentage (>32%), and 28.6% of the men also had high body fat (>25%). The current phase angle average was 6.2 1.1. Detailed descriptions of food intake are shown in Table 2, 29.0% of the patients had total energy intakes >90% of TEE; 36.8% had an optimal energy consumption (90% and 110% of TEE) and 34.2% (n ¼ 13) had an energy consumption < 90% of the TEE. Sub notification of diet reports was observed in most of the patients (65.8%). The median of TEE/energy intake was 0,77 and no association was found with this ratio and weight gain (Pearson’s test; p ¼ 0,72; r ¼ 0,06). The average REE measured by IC was 1449.7 226.7 kcal/d. It was 1404.5 166.1 kcal/d when estimated with the HB formula. No patient was classified as hypo- or hypermetabolic. Pearson’s correlation between the methods showed a coefficient of 0.97 (p < 0.01). Subsequently, the linear regression of the methods resulted in R2 ¼ 0.91 (Figure 1). The absolute values of REE obtained by IC were analyzed with the numerical and categorical variables. The variables with p < 0.2 entered in the multiple linear regression model are shown in Table 3. The final multiple linear regression model to predict the REE was p < 0.01, R2 ¼ 0.970 and adjusted R2 ¼ 0.967. In the final Table 1 Characteristics of patients undergoing liver transplantation (n ¼ 42), Brazil, 2012. Categorical parameters
Table 2 Consumption of total calories, macronutrients and micronutrients of patients undergoing liver transplantation (n ¼ 38), Brazil, 2012. Nutrient
Average SD/Median (MineMax)
Calories (kcal) Carbohydrates (%) Protein (%) Lipids (%) Fiber (g) Vitamin A (mcg) Vitamin D (mcg) Vitamin E (mg) Vitamin C (mg) Thiamine (mg) Riboflavin (mg) Niacin (mg) Pyridoxine (mg) Vitamin B12 (mcg) Folate (mcg) Iron (mg) Calcium (mg) Magnesium (mg) Zinc (mg) Potassium (mg) Phosphorus (mg)
1620.9 457.0 53.8 6.0 15.9 3.4 29.1 5.2 17.3 7.1 629.3 624.4 2.0 1.3 15.4 5.2 96.8 (40.3e888.7) 1.16 0.34 1.0 (0.4e2.1) 16.2 5.2 1.5 0.6 1.6 (0.3e5.9) 109.7 51.3 10.4 3.1 538.5 262.4 169.9 57.6 7.1 2.4 1803.1 596.9 631.8 192.3
model, age (p < 0.001), current weight (p < 0.001), lean body mass (p < 0.004) and total body water (p < 0.022) remained as the highest predictors of resting energy expenditure. These variables were used to develop the equation that predicted up to 97% of the REEs of the assessed patients: REE (kcal/day) ¼ 6905 age (years) þ 10.3 current weight (kg) þ 26.7 lean mass (kg)28.1 total body water (liters)
% (n)
Gender e male Married/Lives with partner Housewife/unemployed/retired Smokers Former smokers Level activity Sedentary Low activity Active Tacrolimus use Arterial hypertension prior to LT Arterial hypertension after LT Diabetes mellitus prior to LT Diabetes mellitus after LT Family history Arterial hypertension Diabetes mellitus Excessive weight Cardiovascular diseases Other parameters
3
52.4 76.2 62.8 2.4 40.5
(22) (32) (27) (1) (17)
48.8 43.9 7.3 88.1 21.4 33.3 7.1 21.4
(20) (18) (3) (37) (9) (14) (3) (9)
69.0 33.3 42.9 50.09
(29) (14) (18) (21)
4. Discussion Indirect calorimetry is considered the standard method for measuring REE.22 Few studies have reported the REE in patients undergoing LT. In the Brazilian population, there are no data related to the topic. This study evaluated 42 patients who underwent LT. The mean REE measured by IC was 1449.7 226.7 kcal, a value that aligned with other studies (Table 4). However, 3 of these 4 studies
Average standard deviation
Sleep per night (h) 7.8 Weight prior LT (kg) 65.3 Weight at the moment of assessment (kg) 71.3 BMI prior LT (kg/m2) 24.5 2 BMI at the moment of assessment (kg/m ) 26.8 Waist circumference (cm) 90.8 Total body water (%) 50.0 Intracellular body water (%) 55.2 Extracellular body water (%) 44.8 Lean mass (%) 66.9 Body fat (%) 32.5 REE measured by IC (kcal/d) 1449.7 REE predict by HB (kcal/d) 1404.5
1.1 16.1 15.5 4.6 4.8 13.9 8.0 3.8 3.8 10.4 9.6 226.7 166.1
LT: liver transplantation, BMI: body mass index, REE: resting energy expenditure.
Fig. 1. Linear regression between resting energy expenditure by indirect calorimetry and the Harris and Benedict formula in patients undergoing liver transplantation (n ¼ 42), Brazil, 2012.
Please cite this article in press as: Ribeiro HS, et al., Energy expenditure and balance among long term liver recipients, Clinical Nutrition (2014), http://dx.doi.org/10.1016/j.clnu.2013.12.015
4
H.S. Ribeiro et al. / Clinical Nutrition xxx (2014) 1e6
Table 3 Variables associated/correlated with resting energy expenditure by indirect calorimetry in patients undergoing liver transplantation inserted in the multiple linear regression model (n ¼ 42). Brazil, 2012. Variables
p value
Gender Weight (kg) Height (m) Waist circumference (cm) Lean mass (kg) Total body water (L) Systolic blood pressure (mmHg) Carbohydrate intake (%) Protein consumption (g) Monounsaturated fatty acid intake (g) Dietary cholesterol (mg) Consumption of calcium (mg) Phosphorus intake (mg) Adequate intake or more of vitamin E (mg) Adequate intake or more of vitamin B1 (mg) Adequate intake or less of sodium (mg)
0.04
