A low-calorie diet improves the rate of nutrient oxidation, lowers body fat, and maintains lean mass in morbidly obese Brazilian women

Nutrition Researc

Research Articles

A low-calorie diet improves the rate of nutrient oxidation, lowers body fat,

and maintains lean mass in morbidly obese Brazilian women

Carla B. Nonino-Borges4, Isolda P.N.N. Maduro, Marinella Bavaresco,

Ricardo M. Borges, Vivian M.M. Suen, Julio S. MarchiniDivision of Nutrology, Department of Internal Medicine, University Hospital, Faculty of Medicine of Ribeirao Preto,

University of Sao Paulo, Ribeirao Preto, SP 14049-900, Brazil

Received 23 March 2006; revised 6 July 2006; accepted 10 July 2006

www.elsevier.com/locate/nutres

Abstract

To assess the effect of a low calorie diet on the resting metabolic rate (RMR), substrate oxidation,

0271-5317/$ – see fro

doi:10.1016/j.nutres.2

4 Corresponding

Ribeirao Preto, Sao P

E-mail address: c

body composition, and to compare measured and calculated RMR of obese Brazilian women, we

selected 19 patients aged 31 F 9 years, with a body mass index of 51 F 8 kg/m2, for admission to

the Metabolic Unit of the University Hospital for 8 weeks, who were then submitted to a 3.3 to

4.2 MJ/d (800-1000 kcal/d) diet. Weight, height, and circumferences were measured on the first and

last days of the study. Body composition was assessed by bioelectrical impedance, and RMR and

substrate oxidation rate by indirect calorimetry. A decrease in body weight (134 F 23 kg vs 121 F21 kg, P b .05), waist (136F 17 cm vs 123F 17 cm, P b .05), and hip circumference (149F 14 cm

vs 137 F 16 cm, P b .05) occurred during the study. Mean RMR measured by indirect calorimetry

(10.6 F 1.7 MJ/d; 2540 F 420 kcal/d) was 16% higher (P b .05) than that calculated by Harris-

Benedict and World Health Organization equations (8.7 F 0.9 MJ/d; 2070 F 210 kcal/d and 9.0 F1.4 MJ/d; 2161 F 344 kcal/d, respectively) at the beginning, but not at the end of the study. Lipid

oxidation rate was 45% of RMR at the beginning of the study, reaching 59% at the end (P N .05).

Present data suggest that equations to estimate RMR of obese females are reliable after a low-calorie

diet and weight loss. Resting metabolic rate was correlated with fat-free mass and body fat. A low-

calorie diet with balanced macronutrients is effective for weight loss, leading to a maintenance of

lipid oxidation rate and to a reduction of carbohydrate and protein oxidation rates. The low-calorie

diet reduced body fat and maintained lean mass.

D 2006 Elsevier Inc. All rights reserved.

Keywords: Low-calorie diet; Obesity; Body composition; Harris-Benedict equation; Indirect calorimetry; Substrate

oxidation; Women

1. Introduction

The etiology of obesity involves various mechanisms.

The imbalance between calorie ingestion and energy

expenditure is the final result of the sum of variables to

influence body mass [1]. Energy restriction is always

considered, directly or indirectly, to be part of the treatment

nt matter D 2006 Elsevier Inc. All rights reserved.

006.07.005

author. Departamento de Clinica Medica (68 andar),

aulo 14049-900, Brazil.

[email protected] (C.B. Nonino-Borges).

of obesity. A low-calorie or restricted diet is usually defined

as a diet providing 3.3 to 4.2 MJ/d (800-1000 kcal/d) [2];

however, during the weight-loss process, the body compart-

ments of obese subjects are not reduced in a uniform manner

[3]. Thus, the oxidation of macronutrient substrates differs

according to their availability in food, the body, and the

energy expenditure of the individual. During the process of

weight loss, there is oxidation of energy reserves and this

oxidation may influence the body composition resulting

from weight loss.

h 26 (2006) 437–442

C.B. Nonino-Borges et al. / Nutrition Research 26 (2006) 437–442438

The curve for the real weight loss does not always follow

the curve for the predicted (theoretical) loss [4]. This

difference has been suggested to occur mainly because of a

decrease in resting metabolic rate (RMR) [5,6]. Thus, a

greater weight loss would be expected to occur in the

presence of an elevated RMR, or weight loss would not

occur in a similar pattern to the decrease in basal energy

expenditure.

Because a low-calorie diet is part of the clinical treatment

of obesity, the objective of the present study was to

determine the effect of such diet on weight loss, the rate

of substrate oxidation, and body composition of morbidly

obese women. Thus, we (1) analyzed the RMR of obese

women with a body mass index (BMI) of 40 kg/m2 or

higher submitted to a low-calorie diet (3.3 to 4.2 MJ/d [800-

1000 kcal/d]) for a period of 8 weeks; (2) compared the

RMR calculated by the Harris-Benedict (HB) equation [7]

and by the World Health Organization (WHO) equation [8]

to that obtained by indirect calorimetry (IC); (3) calculated

the correlation between RMR measured by IC and body

composition determined by bioimpedance (BIA); and (4)

compared the oxidation rate of energy substrates before and

after weight loss.

2. Methods and procedures

2.1. Subjects

Nineteen adult morbidly obese women (BMI, z40 kg/m2)

were selected for the protocol. The exclusion criteria were

associated comorbidities such as diabetes mellitus, high

blood pressure, dyslipidemia, pulmonary disorder, and

pregnancy. The study was approved by the Ethics Commit-

tee of the University Hospital, Faculty of Medicine of

Ribeirao Preto, University of Sao Paulo, and the selected

patients gave informed consent to participate.

2.2. Experimental design

The patients were admitted to a Metabolic Unit of the

University Hospital for a period of 8 weeks. A clinical and

feeding history was obtained from each patient before

admission, and each subject was submitted to physical,

laboratorial, and anthropometric examination.

Before the initial measurements, the volunteers main-

tained their usual energy intake. They did not practice

any kind of physical activity. On the first (day 1) and last

day (day 56) of hospitalization, a feeding history was

obtained, and the following procedures were performed:

nutritional evaluation, BIA, calculation of RMR using the

HB equation [7], the equation proposed by the WHO [8],

and IC.

The first measurements were made while the patients

were still following their usual dietary habits. The final

measurements were made while the patients were on the

low-calorie diets, and weight loss was still occurring, with

each patient serving as her own control.

2.3. Diet

The patients were submitted to a low-calorie diet of 3.3

to 4.2 MJ/d (800-1000 kcal/d) (15% protein, 55% carbohy-

drate, and 30% fat) throughout the study period (8 weeks).

The foods were selected according to the patients’ dietary

habits. The Nutrition Division of the Hospital das Clinicas,

Ribeirao Preto School of Medicine, prepared the meals. The

meals were divided into portions in the Metabolic Unit of

the University Hospital.

2.4. Clinical-nutritional evaluation

Before starting the protocol, the patients were submitted

to a detailed medical history, including duration of obesity

and practice of physical activity, as well as the presence of

complaints that might indicate associated diseases. A diet

history was also obtained to calculate food ingestion before

admission.

2.5. Anthropometry

Data concerning weight, height, calculation of BMI,

waist circumference (WC), hip circumference (HC), and

waist/hip ratio (WHR) were obtained, as well as analysis of

fat-free mass (FFM) and body fat (BF) by bioelectric

impedance. The patients were weighed on a Filizola (Sao

Paulo, SP, Brazil) digital platform type scale with 300-kg

capacity and 0.2-kg precision. Height was measured with a

nonextensible vertical rod with 0.5-cm graduations. Body

mass index was obtained by the following formula: BMI =

W/H2, where W is weight in kilograms and H is height in

meters. Waist circumference was measured above the

umbilical scar considering the smallest circumference

between the inferolateral portion of the rib cage and the

hip. Height circumference was measured in the largest

circumference between the waist and the knee. A nonexten-

sible metric tape with 0.1-mm graduations was used. Waist/

hip ratio was obtained by the formula: WHR = WC/HC [9].

All measurements were made by a single investigator.

2.6. Bioimpedance

Body composition was assessed by BIA measurement

using a Quantum BIA 101Q apparatus (RJL Systems,

Clinton Township, Mich). Fat-free mass and BF were

calculated using mathematical equations specific for obese

women validated against underwater weighing [10].

The phase of the menstrual cycle was the same for all

volunteers, and the hydration status was also controlled. A

neutral water balance was observed in all the volunteers.

There was no clinically detected edema, and the subjects

had no history of cardiac, renal, or hepatic failure.

2.7. Indirect calorimetry and substrate oxidation rates

Energy expenditure and substrate oxidation rates were

measured by bedside IC after an overnight fast, in the

morning, with the patient awaken, at room temperature. At

this time of the day and under these conditions, energy

Table 1

Effects of low-calorie diet in anthropometry, body composition, and energy

expenditure

Day 1 (n = 19) Day 56 (n = 19)

Weight (kg) 134 F 23 121 F 214

BMI (kg/m2) 51 F 8 46 F 74

WC (cm) 136 F 17 123 F 174

HC (cm) 149 F 14 137 F 164

WHR 0.9 F 0.1 0.9 F 0.1

FFFM (kg) 56 F 7 52 F 6.2

BF (kg) 78 F 17 69 F 164

RMR indirect

calorimetry

(MJ/d) (kcal/d)

10.6 F 1.7

(2540 F 420)

8.0 F 1.1

(1920 F 280)4

RMR HB equation

(MJ/d) (kcal/d)

8.7 F 0.9

(2070 F 210)

8.1 F 0.8

(1940 F 190)4

RMR WHO equation

(MJ/d) (kcal/d)

9.0 F 1.4

(2161 F 344)

8.5 F 1.3

(2019 F 302)4

Values are shown as mean F SD.

Anthropometric evaluation and determination of body composition and

RMR on obese females at baseline (day 1) and after 8 weeks (day 56) of

low-calorie diet intervention.

4 P b .05.

Fig. 1. Predicted values of resting metabolic rate compared to the values

obtained from obese females at baseline (filled square, day 1) and after

8 weeks (hollow square, day 56) of low-calorie diet intervention. Filled

square, Initial RMR = (1091.834 + 1.197 * W � 0.765 * HC + 0.231 * H)/

1000 (r = 0.71 and P b .05). Hollow square, Final RMR = (�13118.715 +1.069 * WC + 0.475 * H + 0.266 * A � 0.498 * HC)/1000 (r = 0.89 and

P b .05).

C.B. Nonino-Borges et al. / Nutrition Research 26 (2006) 437–442 439

expenditure best reflects RMR [11]. The measurements

were made using a Sensor Medics Vmax 29 calorimeter

(Sensor Medics Corporation, Yorba Linda, Calif) for a

period of 30 minutes. The instrument was calibrated against

2 gas mixtures: gas 1, 16% O2 and 3.8% CO2; gas 2, 26%

O2 and 0% CO2. Twenty-four–hour urine was collected for

the determination of urinary nitrogen (g/d).

Substrate oxidation was calculated by the following

formulas based on oxygen consumption (Vo2), carbon

dioxide production (Vco2), and urinary nitrogen excretion

(Nu): lipid oxidized (g/d) = 1.67� (Vo2� Vco2)� 1.92�Nu; glucose oxidized (g/d) = 4.09 � Vco2 � 2.88 � Vo2

� 2.59 � Nu; protein oxidized (g/d) = 6.25 � Nu [12].

Resting metabolic rate was calculated by the Weir formula

using Vo2 and Vco2 as follows: 3.94 � Vo2 + 1.106 �Vco2 [13].

2.8. Estimate of RMR

Resting metabolic rate was estimated by the HB equation

[7]: RMR = 655.1 + (9.59 �W) + (1.85 � H) � (4.67 � I),

where W is current weight in kilograms, H is height in

centimeters, and A is age in years, and by the equation

proposed by the WHO [8] for women aged 18 to 30 years:

RMR = 14.7 � W + 496; and for women aged 30 to

60 years: RMR = 8.7 � W + 829, where W is current

weight in kilograms.

2.9. Statistical analysis

The results are reported as mean F SD. The Wilcoxon

test was used to compare the rate of substrate oxidation

before and after the low-calorie diet. The Friedman test was

used to compare the RMR by 3 different methods, that is,

IC, HB equation, and WHO equation. The correlation

between the RMR and body composition and anthropomet-

ric data was calculated by the Spearman coefficient and

multiple regression analysis. The level of significance was

set at P b .05 [14].

3. Results

More than 100 patients were first interviewed for

admission to the study and those who presented with

associated comorbidities such as endocrine disease, moder-

ate or severe systemic arterial hypertension, severe chronic

obstructive pulmonary disease, or cardiac, renal, or hepatic

insufficiency were excluded. Nineteen female patients aged

31 F 9 years (mean F SD) were included in the study,

which lasted 8 weeks.

Clinical evaluation of the patients revealed that all

of them presented a history of weight gain for more than

10 years. In addition, 79% had a family history of obesity.

None of the patients reported participating in any formal

program of physical activity over a minimum period of

1 year before study admission.

Analysis of feeding history before admission revealed a

daily ingestion of 9.5F 2.9 MJ (2270F 700 kcal) consisting

of 17% F 5% proteins, 38% F 8% lipids, and 44% F11% carbohydrates. Thus, nonprotein calorie ingestion was

7.9 F 2.7 MJ/d (1898 F 650 kcal/d) and protein ingestion

was 0.7 F 0.2 g/kg per day (actual body weight).

Table 1 shows the data on anthropometry, body

composition, and RMR measured by IC and predicted

by the HB and WHO equations before and after weight

loss. The data demonstrate a significant reduction in

Table 2

Substrate oxidation rate

Day 1 (n = 19) Day 56 (n = 19)

Oxygen consumed

(Vo2) (mL/min)

360.5 F 59.7 221.3 F 29.24

Carbon dioxide

produced (Vco2)

(mL/min)

318.3 F 69.7 221.3 F 29.24

Respiratory quotient 0.88 F 0.14 0.80 F 0.06

Carbohydrate

oxidation rate (g/d)

120.5 F 200.3 94.9 F 56.34

Lipid oxidation

rate (g/d)

52.9 F 80.9 83.5 F 34.9

Protein oxidation

rate (g/d)

57.6 F 12.2 31 F 5.74

Values are shown as mean F SD.

Substrate oxidation rate on obese females at baseline (day 1) and after

8 weeks (day 56) of low-calorie diet intervention.

4 P b .05.

C.B. Nonino-Borges et al. / Nutrition Research 26 (2006) 437–442440

weight, BMI, WC, HC, and BF, but not in WHR or FFM.

At the end of the study, after weight loss, there was a

reduction in RMR measured by IC and estimated by the

HB and WHO equations.

Fig. 2. Lipid (hollow square) and carbohydrate oxidation rate (filled square) in obes

day 56) with a low-calorie diet.

Comparison of the methods for the determination of

RMR showed that RMR measured by IC was 16% higher,

on average, than RMR calculated by the HB and WHO

equations at the beginning of the study, with this value

being reduced to 1% at the end of the study. Thus,

comparison of RMR measured by IC and calculated by

the HB and WHO equations showed a significant difference

at the beginning of the study (P b .05) which was no longer

detected at the end of the study (P N .05). When the

correlation between RMR and body composition was

calculated, a positive correlation was observed between

RMR and weight, and FFM and BF at the beginning and at

the end of the study. Multiple regression analysis using

RMR as the dependent variable before and after weight loss

yielded significant results when the following parameters

were included in the predictive equations: weight, height,

age, WC, and HC (Fig. 1).

The substrate oxidation rate is shown in Table 2. Lipid

oxidation rate was 52.9 F 80.9 g/d at the beginning of the

study, before the hypocaloric diet. At the end of the study,

the lipid oxidation rate increased to 83.5 F 34.9 g/d

(mean F SD) g/min. Fig. 2 shows the lipid and carbohy-

e females at baseline (A, day 1) and after 8 weeks of dietary intervention (B,

C.B. Nonino-Borges et al. / Nutrition Research 26 (2006) 437–442 441

drate oxidation rate at the beginning and at the end of the

study in the subjects.

4. Discussion

All the patients studied here had a long history of weight

gain. According to the Food and Nutrition Board [15], the

daily energy requirements for nonobese women in the 25- to

50-year age range for weight maintenance are obtained by

multiplying the RMR by 1.55. This corresponds to 0.013 to

0.015 MJ/kg per day (30-35 kcal/kg per day). In the present

group, the energy balance would be kept at the energy needs

of 16.4 F 2.7 MJ/d (3940 F 650 kcal/d), corresponding to

0.126 F 0.021 MJ/kg per day (30 F 5 kcal/kg per day)

considering the current weight. However, an analysis of the

24-hour food recall before admission showed that the mean

reported daily energy intake was 9.5 F 2.9 MJ/d (2270 F700 kcal/d), corresponding to 0.08 F 0.013 MJ/kg per day

(20 F 3 kcal/kg per day). This evidences underreporting of

the energy intake. It has been shown that obese subjects

often, consciously or not, omit data about their food

ingestion [16]. If the calorie ingestion were the one

reported, a weight loss rather than weight maintenance or

gain would be expected to occur. Another factor to be

considered is the low physical activity level, which might

explain the weight gain.

Because the Harris Benedict equation was developed

based on data from the American people, this might explain

the difference evidenced in the present study. However, the

decrease in RMR after weight loss observed here confirms

the findings from Das et al [17]. The high RMR found in

morbidly obese subjects explains the fact that a high-energy

intake is required to maintain the excess weight. After

weight loss, the energy needs to maintain the energy balance

might decrease.

In the present study, during hospitalization, when the

patients ingested a low-calorie diet corresponding to

approximately 8 kcal/kg per day, there was a significant

weight loss resulting in a significant reduction in BMI,

although the value of the latter continued to be much higher

than desired [18]. The WHR indicated that the patients were

at high risk for morbidity and mortality both at the

beginning and at the end of the study because, despite the

significant reduction in both WC and HC, there was no

change in the WHR, suggesting the need for a continued

weight loss.

Analysis of body composition after the period of

hospitalization showed a significant BF loss, a fact that

was not observed for FFM. Because the patients were in

negative energy balance, there was probably a utilization of

energy reserves (adipose tissue) to meet their requirements,

as demonstrated by the reduction in carbohydrate oxidation

and the maintenance of lipid oxidation. We suggest that

the maintenance of FFM and the reduction of BF were the

consequence of the change in the substrate oxidation

pattern due to the low-calorie diet. We also suggest that

the proportion of macronutrients in the diet can be

responsible for this substrate oxidation, a fact that confirms

the need for a balanced diet even when the number of

calories is reduced.

Predictive equations for the estimate of RMR in obese

persons are widely used in clinical practice, probably

because of the scarce availability of adequate instruments

for the real measurement. Multiple regression analysis of the

variables, considered in the present study for the determi-

nation of RMR, showed that the most important ones were

weight, height, age, HC, and WC. When we compared the

predicted vs the measured values, we detected a correlation

both at the beginning and at the end of the study, suggesting

the existence of various parameters that affect the RMR of

these patients. These results show the influence of BF

distribution determined by WC and HC on the RMR.

When we compared the RMR obtained by IC and by

the HB equation, we did not find a correlation between the

methods at the beginning of the study. Because the

predictive HB equations have been developed using a

population with weight, and probably body composition,

within normal limits [7], we may suggest that great excess

of weight or deviations such as the disproportion between

visceral and/or peripheral fat implicated in body composi-

tion lead to estimate errors, tending to underestimate RMR.

In the present study, the HB equation underpredicted the

RMR by 16% F 11% and the WHO equation under-

predicted the RMR by 13% F 15% before the weight loss.

This finding is different from that of Das et al [17] who

showed that the difference between measured and predicted

RMR was 3%. Thus, the RMR of obese females with a BMI

of 40 kg/m2 or higher not recently submitted to restrictive

diets should be interpreted with caution when estimated by

the HB and WHO equations. Several investigators have

shown the correlation between FFM and RMR [19,20]. In

the present study, we observed a positive correlation

between RMR, FFM, and BF before and after the weight

loss. This finding suggests that BF might play a role in

RMR in obese females with BMI of 40 kg/m2 or higher, as a

decrease in BF was accompanied by a decrease in RMR.

The present data do not permit us to state that the use of the

HB equation can estimate RMR in a reliable manner in

obese Brazilian females with a BMI of 40 kg/m2 or higher.

However, the data suggest that, after these individuals were

submitted to a restrictive diet with a consequent weight loss

(about 10% of the initial weight), the HB equation became

reliable for the estimation of RMR, mostly because there is a

reduction in it, as shown in this study and in another [21].

The present results support the need to perform studies

with a larger number of morbidly obese Brazilian patients to

establish the validity of using 1 or more body components to

estimate RMR in obese females with BMI of 40 kg/m2 or

higher. The data also suggest that the RMR of obese females

with a BMI of 40 kg/m2 or higher is not only related to

anthropometrical variables and to body composition. There

are probably nonanthropometric factors associated with

C.B. Nonino-Borges et al. / Nutrition Research 26 (2006) 437–442442

anthropometric ones that affect RMR in this group of

individuals, such as genetic factors [22].

Although FFM was well correlated with RMR measured

by IC in this group of individuals, before and after weight

loss because of a restrictive diet, this correlation did not

seem to differ from the correlation between fat mass and

RMR and between weight and RMR. The use of FFM to

estimate RMR still needs better validation by means of more

expanded studies. It is important to point out that the

decrease in BF occurred when a low-calorie diet was used,

with a reduction in the rate of carbohydrate oxidation and an

increase in the rate of fat oxidation.

The most important findings of the present study were

that the HB equation was shown to underpredict the RMR in

morbidly obese women and the treatment with a low-calorie

diet with balanced macronutrients was shown to be effective

for weight loss, leading to the maintenance of the rate of

lipid oxidation and to a reduction of the rate of carbohydrate

and protein oxidation, which permitted a reduction of BF

and maintenance of lean mass.

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