YCLNU3294_proof ■ 16 November 2017 ■ 1/8

Clinical Nutrition xxx (2017) 1e8

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Contents lists available at ScienceDirect 56
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Clinical Nutrition 59
60
journal homepage: http://www.elsevier.com/locate/clnu 61
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Original article 64
65
1 Development and validation of new predictive equation for resting 66
2 67
3 Q7 energy expenditure in adults with overweight and obesity 68
4 69
5 Q6 Ximena Orozco-Ruiz a, Edgar Pichardo-Ontiveros a, Armando R. Tovar a, Nimbe Torres a, 70
6
Isabel Medina-Vera a, Federica Prinelli c, Claudio L. Lafortuna b, Martha Guevara-Cruz a, * 71
7 72
8
a
Departmento de Fisiología de Nutricio n, Instituto Nacional de Ciencias M
edicas y Nutricio n, M
n, Salvador Zubira exico D.F., Mexico
b 73
Q1 Istituto di Bioimmagini e Fisiologia Molecolare, 20090 Segrate, Milano, Italy
9 c 74
Istituto di Tecnologie Biomediche del Consiglio Nazionale delle Ricerche, 20090 Segrate, Milano, Italy
10 75
11 76
12 77
13
a r t i c l e i n f o s u m m a r y
78
14 79
Article history: Background & aims: Accurate predictive equations of resting energy expenditure (REE) are crucial in
15 Received 19 January 2017 devising nutritional strategies to manage overweight/obesity, especially in countries where these are 80
16 Accepted 27 October 2017 highly prevalent. REE is the most common measurement used to estimate energy requirements in the 81
17 nutritional context; the most accurate method of measuring REE is indirect calorimetry (IC). However, 82
18 Keywords: this method is costly and often rarely feasible in many clinical settings. The objective of the present study 83
19 Energy expenditure
was to develop and validate a new equation for predicting REE in adults with overweight and obesity. 84
Predicted equation
20 Overweight
Methods: This was a cross-sectional study including 410 men and women with overweight and obesity 85
21 (20e60 y). Participants were randomly assigned; the development group included 200 subjects and the
Obesity 86
22 validation group 210 subjects. The new predictive equation was derived using stepwise multiple linear
87
23 regression analysis. The accuracy of the new equation was compared to several existing predictive
equations (PEs). The accuracy rate was calculated as the percentage of subjects whose REE-PE was within
88
24 89
±10% of the REE-IC. REE was measured by IC and anthropometric measurements.
25 90
Results: One predictive equation was developed (NEQ) in which weight was the strongest predictor of
26 REE. Compared with others predicted equations already using, the new designed equation showed the 91
27 less mean bias (Kj/day): NEQ: 25.7, Valencia:129, WHO/FAO/United Nations University: 270, Mifflin-St 92
28 Jeor: 308, Owen:
808, Carrasco:
1097, Korth:
36.4, Johnstone:
375, Livingstone:
315, De 93
29 Lorenzo:
28.3, Lazzer:
123, Muller:
145, Huang:
399 and Bernstein:
1335. 94
30 Conclusions: The present equation had the highest predictive accuracy in subjects with overweight or 95
31 obesity compared with the previous equations derived from different populations. Thus, these new 96
32 equation can be used to assist the nutritional management of these subjects.
97
33 © 2017 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
98
34 99
35 100
36 101
37 102
38 103
1. Introduction world, the prevalence of overweight and obesity have been
39 104
considerably increased. So that, in 2014 WHO reported a prevalence
40 105
Overweight and obesity are defined by The World Health Or- of overweight and obesity of 39% and 13% respectively in adult
41 106
ganization (WHO) as an excessive fat accumulation that could population [1].
42 107
causes injuries in health [1], therefore obesity is considered one of Mexico is one of the countries with the highest prevalence of
43 108
the major causes of mortality and metabolic diseases [2]. Over the obesity in adults [3]. In 2012, the prevalence of overweight and
44 109
obesity in adults aged over 20 years in Mexico was 71.3% [4].
45 110
Consequently, Mexico was ranked as having the second highest
46 Abbreviations: BIA, bioelectrical impedance analysis; FFM, Fat free mass; FM, Fat 111
mass; HC, hip circumference; HT, height; IC, Indirect calorimetry; PEs, Predictive
prevalence of obesity worldwide by the Organization for Economic
47 112
equations; REE, Resting energy expenditure; REE-IC, Resting energy expenditure by Co-operation and Development (OECD) [5].
48 113
indirect calorimetry; REE-PE, Resting energy expenditure by prediction equations; Obesity is the result of an energy imbalance, with energy intake
49 VO2, Oxygen consumption volume; VCO2, Carbon dioxide consumption volume; 114
exceeding energy expenditure (EE) over a considerable period of
50 WC, waist circumference; WRC, wrist circumference; WT, weight. 115
time. Even a small consistent deviation over a long period is
51 * Corresponding author. Av. Vasco de Quiroga, No. 15, 14080. Me xico City, Mexico.
considered capable of producing large increases in body weight [6]. 116
E-mail address: marthaguevara8@yahoo.com.mx (M. Guevara-Cruz).
52 117
53 118
https://doi.org/10.1016/j.clnu.2017.10.022
54 0261-5614/© 2017 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved. 119

Please cite this article in press as: Orozco-Ruiz X, et al., Development and validation of new predictive equation for resting energy expenditure in
adults with overweight and obesity, Clinical Nutrition (2017), https://doi.org/10.1016/j.clnu.2017.10.022
 YCLNU3294_proof ■ 16 November 2017 ■ 2/8

2 X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8

1 Although the composition of the ideal or healthiest diet is unclear, (REF 1456). All participants were informed about the scope and 66
2 there is considerable evidence of the importance of diets with an procedures of the study, and prior to any study procedures, written 67
3 energy deficit in enhancing short-term weight loss and helping informed consent was formally obtained. 68
4 maintain reduced body weight [7]. For effective interventions to 69
5 occur, health care practitioners need to be equipped with both 2.1. Procedures 70
6 knowledge and appropriate tools [8]. Based on the evidence 71
7 regarding nutritional approach, the clinical guidelines for over- Participants completed demographic and health-related ques- 72
8 weight and obesity recommend personalized management of tionnaires under the supervision of a nutritionist, who also ob- 73
9 weight loss, which involves an individual assessment of energy tained their anthropometric measurements including body weight 74
10 requirement using estimates of EE [9]. (WT), height (HT), waist circumference (WC), hip circumference 75
11 Resting Energy Expenditure (REE) represents approximately (HC) and wrist circumference (WRC), as well as the body compo- 76
12 60e80% of EE [10], and it is the most common measurement used sition (fat free mass (FFM) and fat mass (FM)). Subjects REE's was 77
13 to estimate energy requirements in the nutritional context; the measured by IC (REE-IC), while body composition was assessed by 78
14 most accurate method of measuring REE is indirect calorimetry (IC) bioelectrical impedance analysis (BIA). 79
15 [11]. However, this method is costly and often rarely feasible in 80
16 many clinical settings [12]. Therefore, Predictive Equations (PEs) 2.1.1. Measurement of REE 81
17 that provide estimates of REE using easily obtained variables such REE-IC was measured using the Quark PFT device (Cosmed, 82
18 as height, weight, age and sex have thought to have large clinical Roma, Italy) [11]. Measurements were obtained in a thermoneutral 83
19 utility. Also, several other important anthropometric variables have (20e25  C), humidity-controlled (45e55%), quiet environment. The 84
20 being analyzed in relation with REE, like fat free mass, fat mass, hip, O2 and CO2 flows were directly measured with a mask and flow- 85
21 waist and wrist circumference [13e17]. Over time, numerous meter of 18 mm diameter. The calibration of the flowmeter was 86
22 equations that predict EE have been developed. However, when performed every day using a certified 3L calibration syringe, the 87
23 these PEs are applied to individuals who do not share important ventilation range of flowmeter is from 0 to 80 L/min with an ac- 88
24 characteristics with the group of people from whom the equation curacy of 3%. The calorimeter was calibrated prior to each testing 89
25 was developed, the possibility of significant errors can easily occur, session using gas mixtures with concentrations of 16% O2 and 1% 90
26 limiting the efficacy of the intervention. CO2, according to the manufacturer's prescriptions. The O2 analyzer 91
27 An Expert Panel from The American Dietetic Association (ADA) is a paramagnetic sensor and the CO2 analyzer is an infrared digital 92
28 recently systematically reviewed the validity of predictive equa- sensor, both have an accuracy of 0.02%, it has been shown with a 93
29 tions for REE applied to the general public [14] to address the issue comparable equipment, the Quark PFT, that the measurement of 94
30 of divergence between the groups of people used to generate the energy expenditure has a difference of 2% in comparison with the 95
31 equations and those in whom the equations are used. The Panel measurements made with the calorimeter Deltratrac [11,18]. We 96
32 concluded by cautioning clinicians to use predictive methods with determined the intradevice coefficient variation measuring a REE 97
33 suspicion in groups of people who are underrepresented in studies during five consecutive days in the same subject, and it was less 98
34 validating equations. Thus, it appears that an individual's race/ than 4%. Energy expenditure was calculated using the abbreviated 99
35 ethnicity is a central issue that, as evidenced by several studies, has Weir's equation [17]. 100
36 been shown to play an important role in the variation in EE [14,15]. All the measures were performed in the morning (between 101
37 Therefore, the purpose of the present study is to develop and 07:00 and 09:30) with 8e12 h of fasting conditions. Participants 102
38 validate a new equation to estimate REE in adults with overweight were instructed to refrain from exercise for at least 12 h (vigorous 103
39 and obesity and to compare the accuracy of this equation with resistance exercise for 24 h before the test) prior to their laboratory 104
40 those of previous equations developed in different populations to visit and to abstain from drinking alcohol or consuming caffeine at 105
41 assess its utility in clinical population with excess body mass. least while fasting. Upon arriving at the laboratory, participants sat 106
42 for a period of approximately 20e30 min while the informed 107
43 2. Subjects and methods consent letter was reviewed and signed. Participants were tested at 108
44 rest in a supine position for a period of at least 35 min with minimal 109
45 This cross-sectional study was conducted at the Instituto movement, ensuring that each individual was physically comfort- 110
46 Nacional de Ciencias Me dicas y Nutricio n Salvador Zubira n able and in the proper position for measurements. The REE mea- 111
47 (INCMNSZ) located in Mexico City from January 2015 to March surements were taking after the steady state was achieved, for that, 112
48 2016. the first 5 min of measurement or those resulting in a coefficient of 113
49 Overall, in order to develop a REE predictive equation for over- variation 10% of VO2 and VCO2 volumes were discarded [19]. REE 114
50 weight and obese subjects, a total of 410 mestizo subjects of both was determined according to Weir's equation, without using uri- 115
51 sexes from different areas of the country with a BMI 25 kg/m2 nary urea nitrogen level: REE (kcal/min) ¼ 3.9 [VO2 (l/min)] þ 1.1 116
52 who were between 20 and 60 y were included in the study. Addi- [VCO2 (l/min)]  1.440 min [17]. 117
53 tionally, 200 subjects with normal BMI (18.5e24.9 kg/m2) were 118
54 studied in order to assess differences in REE compared to over- 2.1.2. Body composition and anthropometric measures 119
55 weight and obese subjects. Subjects receiving treatment for pre- Body weight and body composition (FFM and FM) were deter- 120
56 viously diagnosed chronic diseases (such as hypertension, diabetes, mined prior to the REE measurement by a trained nutritionist using 121
57 dyslipidaemia and thyroid diseases), weight loss >3 kg in the last 3 a standard calibrated electronic scale and multi-frequency BIA 122
58 months or with any disease that could affect the measurement of (InBody 720, Biospace, Seoul, Korea), in which impedance was 123
59 gas exchange, as well as smokers, those using medications that measured using a tetrapolar 8-point tactileelectrode system at 1, 5, 124
60 could alter EE, and women who were pregnant, had breastfed in the 50, 250, 500 and 1000 kHz. The system measured the impedance of 125
61 previous 6 months, or had used hormonal drugs and/or oral con- the participant's right arm, left arm, trunk, right leg and left leg. 126
62 traceptives were not enrolled in the study. Total body impedance value was calculated by summing the 127
63 This study was conducted according to the guidelines laid down segmental impedance values. Participants were positioned on the 128
64 in the Declaration of Helsinki and all procedures involving human scale platform of the instrument holding the handles of the device, 129
65 subjects were approved by the Ethics Committee of the INCMNSZ to provide contact with a total of eight electrodes (two for each foot 130

Please cite this article in press as: Orozco-Ruiz X, et al., Development and validation of new predictive equation for resting energy expenditure in
adults with overweight and obesity, Clinical Nutrition (2017), https://doi.org/10.1016/j.clnu.2017.10.022
 YCLNU3294_proof ■ 16 November 2017 ■ 3/8

X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8 3

1 and for each hand). Body composition was estimated using a were applied to the corresponding validation group to obtain a 66
2 manufacturer's equations [20]. All the measurements were taken REE-PE for each subject. Pearson's correlation coefficients and the 67
3 with subjects in light clothing and without shoes. WT and HT were coefficients of determination (R2) between the REE-IC and REE-PEs 68
4 recorded in duplicate according to the method of Lohman [21] HT were calculated. BlandeAltman's method [39] was used to evaluate 69
5 was measured in centimeters using the stadiometer BSM 370 the agreement between the REE-IC and the REE-PE estimated by 70
6 (Biospace Co. Seoul, Korea) to the nearest mm. the new equation by plotting the distribution of the differences 71
7 WC and HC were assessed according to the recommendations of between the REE-PE and REE-IC (Mean bias) against their respec- 72
8 the Report of the World Health Organization (WHO) expert tive average values. The same procedure was performed with the 73
9 consultation [22]. WRC was measured according to a previous study other PEs from the literature. 74
10 [23]. All circumferences were obtained with a Seca measuring tape, The accuracy rate was calculated as the percentage of subjects 75
11 Model 201. whose REE-PE was within ±10% of the REE-IC [40], a level 76
12 commonly used to determine the accuracy of a PE. 77
13 2.1.3. REE predictive equations All p values were two-tailed, and we considered a p < 0.05 to be 78
14 The predictive equations evaluated in this study were selected statistically significant. All statistical analyses were performed us- 79
15 due to those were developed including a comparable sample of our ing SPSS (version 22, SPSS Inc, Chicago, IL) and GraphPad Prism 80
16 population (overweight/obesity subjects): (version 5.0, GraphPad Software, Inc. San Diego CA) software. 81
17 Valencia [24] FAO/WHO/UNU [25] Mifflin [26], Owen [27], Car- 82
18 rasco [28] Korth [29], Johnstone [30], Livingston [31], De Lorenzo 3. Results 83
19 [32], Lazzer [33], Muller [34], Huang [35] and Bernstein [36]. In 84
20 addition, the NEQ was also compared with the HarriseBenedict The recruited overweight and obese subjects were from different 85
21 equation, since it is the most commonly equation used, despite it areas of the country: 72.7% were from Mexico City, 11.5% from the 86
22 was obtained from a population with normal body weight [37]. central region, 1.2% from the northern region and 12.2% from the 87
23 southern region. The anthropometric characteristics and REE of the 88
24 2.2. Statistical analysis overall of overweight and obese subjects and of the development 89
25 and validation groups are shown in Table 1, separated by sex in 90
26 Several statistical procedures were performed to a) develop a Supplementary Table 1 and were shown to be comparable. The 91
27 new PE to estimate REE (REE-PE); b) validate the new equation anthropometric characteristics and REE of the group of subjects with 92
28 against actually measured REE-IC; and c) compare the accuracy of normal-BMI are shown in Supplementary Table 2. The correlations 93
29 the new equation with those of different PEs for predict REE in between all of the anthropometric variables and REE for the over- 94
30 subjects with overweight and obesity. Valencia, WHO/FAO/UNU, weight and obese groups were analyzed in the development of the 95
31 Mifflin/St-Jeor, Owen, Korth, Johnstone, Livingston, De Lorenzo, models and are shown in Table 2. WT showed a significantly cor- 96
32 Carrasco, Lazzer, Muller, Huang, Bernstein and the REE-PE of Har- relation (R ¼ 0.632, R2 ¼ 0.400), as depicted in Supplementary Fig. 1. 97
33 riseBenedict obtained in subjects with normal body weight. 98
34 Continuous variables were expressed as the means and standard 3.1. Equation development for overweight and obese subjects 99
35 deviations, and categorical variables as frequencies and percent- 100
36 ages. When variables were not normally distributed, appropriate The NEQ was derived by including WT, Age and Sex to provide a 101
37 logarithmic transformation procedures were performed. simple and easily usable equation for the clinical context even 102
38 Sample size was calculated with a coefficient correlation equa- without the need of the assessment of body composition. The new 103
39 tion [38] to obtain an optimal number of subjects to develop a new equation is presented in Table 3, along with the parameters 104
40 model of predicting EE. Ten variables were considered for the describing its ability to predict REE-IC. 105
41 sample size assessment: WT, HT, BMI, Age, Sex, WC, HC, WRC, FM 106
42 and FFM. The size of the sample required to develop the equation 3.2. Equation validation in overweight and obese subjects 107
43 was 200 subjects (100 with obesity and 100 with overweight). The 108
44 relationships between REE and the ten variables were assessed us- The predictability of the NEQ was tested in the validation group 109
45 ing Pearson's or Spearman correlation coefficient when appropriate. by calculating the average difference between the REE-IC and REE- 110
46 To develop the new equation for the prediction of REE, the PE. No significantly difference was observed between the REE-PE by 111
47 whole sample was randomly separated into development and NEQ and the REE-IC (REE-IC: 6820 kJ/day ± 1475 SD; REE-PE NEQ: 112
48 validation groups. The mean value of the clinical, demographic and 6844 kJ/day ± 950; P ¼ 0.192). NEQ resulted in a coefficient of 113
49 anthropometric parameters and REE-IC were compared between determination value of R2 ¼ 0.59 (P ¼ 0.001), with a prediction 114
50 the development and validation groups using Student's t-test for mean bias of 25.7 kJ/day. 115
51 independent samples. A stepwise multiple linear regression was Limit-of-agreement analysis - The accuracy of the REE-PE over 116
52 performed to develop the new REE-PE in the development group, the range of REE (concordance) was evaluated by BlandeAltman 117
53 using REE-IC as the dependent variable and the ten anthropometric plots [39], in which the reference lines represent the mean bias and 118
54 variables as the independent variables. Variables that were signif- the subjects within ±10% of accuracy. The agreement between the 119
55 icant and stronger predictors were selected to develop the new PE. REE-PE and REE-IC resulting from NEQ is shown in Fig. 1. 120
56 Then, an Enter multiple linear regression models were performed, A comparison of the results obtained in the validation group 121
57 obtaining a model that complied all the assumptions of the mul- with the NEQ and the other equations for subjects with overweight 122
58 tiple regression analysis. In order to assess the REE in subjects with and obesity is reported in Table 4, which also presents the limit-of- 123
59 normal BMI, we conducted a similar study analyzing 100 subjects agreement analysis for each different equation in terms of: a) the 124
60 with the aim to design a new model for these individuals. This agreement between REE-IC and REE-PE; b) the accuracy, as deter- 125
61 model was validated in a group in another group of 100 subjects mined by the percentage of predicted values within ±10% of the 126
62 with normal BMI. REE-IC; and c) the under- and over-estimations, as determined by 127
63 Student's paired t-test was used to assess the difference be- the percentage of predicted values outside of the ±10% range of 128
64 tween REE-IC and REE-PE. The regression equations derived from REE-IC. It appears from Table 4 that the REE-PE obtained from NEQ, 129
65 the development groups (with BMI > 25 kg/m2 or normal BMI) has the highest accuracy of 60%. For the validation group, the REE 130

Please cite this article in press as: Orozco-Ruiz X, et al., Development and validation of new predictive equation for resting energy expenditure in
adults with overweight and obesity, Clinical Nutrition (2017), https://doi.org/10.1016/j.clnu.2017.10.022
 YCLNU3294_proof ■ 16 November 2017 ■ 4/8

4 X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8

1 Table 1 66
2 Characteristics of all the subjects and comparison between design and validation group. 67
3 All subjects Design group Validation group P** 68
4 n ¼ 410 n ¼ 200 n ¼ 210 69
5 W ¼ 303 (73.9%) W ¼ 151 (75.5%) W ¼ 152 (72.4%) 70
6 M ¼ 107 (26.1%) M ¼ 49 (24.5%) M ¼ 58 (27.6%) 71
7 Age (years) 39.1 ± 10.9 39.1 ± 11.2 39.3 ± 10.8 0.76 72
8 Weight (kg) 81.4 ± 14.4 80.8 ± 16.5 81.4 ± 13.2 0.44 73
9 Height (cm) 160 ± 8.61 160 ± 8.35 159.5 ± 8.76 0.82 74
10 BMI (kg/m2) 31.4 ± 4.34 31.6 ± 5.35 31.9 ± 4.17 0.26 75
Overweight (%) 174 (42.4) 100 (50) 74 (35.2)
11 Obeisty I (%) 144 (35.1) 55 (27.5) 89 (42.4)
76
12 ObesityII (%) 64 (15.6) 27 (13.5) 37 (17.6) 77
13 Obesity III (%) 28 (6.8) 18 (9) 10 (4.8) 78
14 Waist circumference (cm) 95.9 ± 11.6 95.5 ± 12.3 96.2 ± 10.8 0.49 79
Hip circumference (cm) 109 ± 8.72 109 ± 9.17 110 ± 8.97 0.13
15 80
Fat Mass (%) 41.6 ± 7.14 41.5 ± 7.07 41.7 ± 7.22 0.75
16 Fat Mass (kg) 33.4 ± 9.08 33.9 ± 10.8 34.0 ± 9.23 0.51 81
17 Fat free mass (%) 58.3 ± 7.14 58.5 ± 7.08 58.2 ± 7.22 0.70 82
18 Fat free mass (kg) 46.9 ± 9.34 46.9 ± 9.45 46.9 ± 9.26 0.99 83
19 Indirect Calorimetry 84
REE (kJ/day) 6803 ± 1565 6792 ± 1657 6812 ± 1475 0.79
20 REE/FFM (kJ/day) 145 ± 29.4 145 ± 26.3 145 ± 23.9 0.82
85
21 kJ/kg weight (kJ/day) 84.3 ± 15.1 84.6 ± 16.1 84.1 ± 14.1 0.55 86
22 VO2 consumption, 230 ± 58.7 236 ± 60.2 236 ± 54.4 0.99 87
23 (ml/min) 88
VCO2 consumption, (ml/min) 193 ± 54.7 192 ± 52.5 197 ± 51.8 0.34
24 89
RQ 0.77 ± 0.05 0.76 ± 0.051 0.77 ± 0.053 0.10
25 90
26 The values show the means ± SD; ** the data were analyzed using Independent Student's t test and Chi-square test (design and validation group).; 91
Abbreviations: W, women; M, men; BMI, Body mass index; REE, Resting energy expenditure; FFM; Fat free mass, kJ, KiloJoules (1 kcal ¼ 4.186 kJ); VO2,
27 Volume of oxygen; VCO2, Volume of carbon dioxide and RQ, Respiratory Quotient.
92
28 93
29 94
30 Table 2 95
31 Correlation coefficients for resting energy expenditure by indirect calorimetry with 96
32 each anthropometric variable. 97
33 Anthropometric variables R R2 P 98
34 99
Weight (kg) 0.63 0.40 <0.001
35 Height (cm) 0.56 0.32 <0.001 100
36 Age (years)
0.31 0.09 <0.001 101
37 Sex 0.52a 0.27 <0.001 102
38 Fat free mass (kg) 0.65 0.42 <0.001 103
Fat mass (kg) 0.32 0.10 <0.001
39 Waist circumference (cm) 0.48 0.23 <0.001
104
40 Hip circumference (cm) 0.29 0.08 <0.001 105
41 Wrist circumference (cm) 0.56 0.31 <0.001 106
42 Body mass index (kg/m2) 0.37 0.14 <0.001 107
43 Data were analyzed by Pearson correlation coefficient. 108
44 R2, Determination coefficient. 109
a
45 Spearman correlation coefficient. 110
46 111
47 112
Table 3
48 Resting energy expenditure prediction equation developed for Mexican adults with
Fig. 1. BlandeAltman plots displaying the agreement and difference between the 113
49 Q5 resting energy expenditure by indirect calorimetry (REE-IC) and the resting energy 114
overweight and obesity.
expenditure predicted (REE-PE) by a new equation NEQ. Dotted line represents the
50 115
Regression equation R R2 P value mean bias of the prediction equation, dashed black lines represent limits of agreement
51 (±95% CI) and dashed grey lines represent the limits of the ±10% of accuracy. 116
52 NEQ Women: 117
REE ¼ 12.114 * WT e 6.541 * A þ 835.952
53 118
0.72 0.51 <0.001
54 Men: tendency, over 30%. Separately for BMI (Overweight vs. obesity), 119
55 REE ¼ 12.114 * WT e 6.541 * A þ 1094.991 the lower percentage of accuracy remains for Bernstein and Car- 120
56 The multiple regression analysis steps to derive the new formula. Abbreviations: rasco, when REE-PE was evaluated. We observed that the NEQ 121
57 NEQ, New equation; REE, Resting energy expenditure (Kcal/day); R, Correlation equation had the highest percentage of accuracy for subjects with 122
58 coefficient; R2, Determination coefficient; WT, Weight (Kg); A, Age (Years). obesity of about 57.4% and lowest bias of
13.6 kJ/day compared 123
59 with the other equations (Supplemetary Table 3). It is important to 124
60 estimate by Bernstein, Carrasco and Huang are biased equations for point out that the Valencia and the Johnstone equations were 125
61 the subjects in our study, since they were the three equations in derived under basal metabolic conditions, whereas the rest of the 126
62 which the confidence interval excludes zero. Lowest accuracy equation corresponded to REE conditions. The BlandeAltman plots 127
63 (below 50%) and largest underestimation was provided by the evaluating the accuracy of the REE-PE over the range of REE for each 128
64 Huang Carrasco and Owen equations. In contrast, the WHO/FAO/ of the other equations are presented for overweight and obese 129
65 UNU and Valencia equations resulted in the highest overestimation subjects in Fig. 2; only overweight subjects in the Supplementary 130

Please cite this article in press as: Orozco-Ruiz X, et al., Development and validation of new predictive equation for resting energy expenditure in
adults with overweight and obesity, Clinical Nutrition (2017), https://doi.org/10.1016/j.clnu.2017.10.022
 YCLNU3294_proof ■ 16 November 2017 ■ 5/8

X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8 5

1 Table 4 66
2 Bias, precision, and percent error of REE-PE by the different equations in the validation sample. 67
3 REE predictive equation Mean REE R2 Bias ±SD CI 95% Accuracya % Overestimationb % Underestimationc % 68
4 New developed equations
69
5 Indirect calorimetry 6820 70
6 NEQ 6844 0.59 25.7 ± 950
104 to 155 60 24.8 15.2 71
7 Valencia 6983 0.55 129 ± 984
4.38 to 263.4 53.8 32.9 13.3 72
WHO/FAO/UNU 7080 0.52 270 ± 959 140 to 401 53.8 35.2 11
8 73
Mifflin St-Jeor 6409 0.54 308.5 ± 1002
444 to 172 51.9 17.6 30.5
9 Owen 6307 0.47
808 ± 1079
954 to 661 40.5 9 50.5 74
10 Carrasco 5811 0.48
1097 ± 1165
1256 to
938 29.5 6.7 63.8 75
11 Korth 6903 0.54
36.4 ± 967
167 to 96.5 57.6 22.4 20 76
12 Johnstone 6445 0.25
375 ± 1095
522 to 224 55.7 20.5 23.8 77
Livingstone 6504 0.58
315 ± 967
445 to 182 56.7 15.2 28.1
13 De Lorenzo 6792 0.59
28.3 ± 951
156 to 102 57.6 24.3 18.1
78
14 Lazzer 6696 0.55
123 ± 989
257 to 11.8 55.7 20.5 23.8 79
15 Muller 6720 0.58
99.4 ± 964
230 to 31.6 58.1 22.4 19.5 80
16 Huang 6421 0.55
399 ± 982
531 to
264 52.9 14.3 32.9 81
Bernstein 5848 0.57
1335 ± 1046
1477 to
1191 21 3.8 75.2
17 82
18 NEQ, New equation; R2, Determination coefficient; Mean REE, Mean value of REE; Bias, value of the difference between REE-IC and REE-PE expressed in kJ; kJ, KiloJoules 83
19 (1 kcal ¼ 4.186 kJ); SD, standard deviation of the bias; CI, 95% confidence interval. 84
a
Percentage of predicted values that were within ±10% of REE-IC.
20 b
Percentage of predicted values that were up of the ±10% of REE-IC.
85
21 c
Percentage of predicted values that were below ±10% of REE-IC. 86
22 87
23 88
24 Fig. 2 and subjects with obesity in the Supplementary Fig. 3. different race/ethnic groups, including Mexican Americans, have 89
25 Interestingly, the use of the HarriseBenedict equation had similar been found to differ in regional mass and body composition pro- 90
26 percentage of accuracy as well as under and overestimation in portions, which likely affects the estimates of REE based on general 91
27 overweight subjects with respect to the NEQ. However, the use of body parameters [43]. Thus, due to the effects of ethnicity- 92
28 the same equation on obese subjects had greater bias of
140 kJ/ dependent discrepancies in phenotypic characteristics on REE es- 93
29 day and slightly less accuracy than the NEQ (Supplementary timations, current equations should be adapted to account for 94
30 Table 3). ethnicity, or equations specific to ethnic groups under similar 95
31 phenotypes (normal vs. overweight/obesity subjects) should be 96
32 3.3. Equation development in subjects with normal BMI appropriately developed. In this study, the equation for overweight 97
33 and obese subjects was developed for a mestizo Mexican popula- 98
34 The correlations between all of the anthropometric variables tion including variables easy to obtain such as weight, age and sex. 99
35 and REE for normal BMI subjects were analyzed in the development In accordance with previous studies we found that for our 100
36 of the models and are shown in Supplementary Table 4. Height population with overweight and obesity the REE is highly corre- 101
37 showed a significant correlation as depicted in Supplementary lated with WT and has biological influence by sex [37] Additionally, 102
38 Fig. 4. Thus the model equation (EQNBMI) for subjects with age has been demonstrated to have an effect on REE [44] decreasing 103
39 normal BMI included HT, age and sex along with the parameters it with advancing age in relation to the decrease in muscle tissue 104
40 describing its ability to predict REE-IC (Supplementary Table 5). No associated with sarcopenic processes. Furthermore, the degree of 105
41 significant difference was observed between the predicted and body mass excess has considerable effects on age-induced de- 106
42 measured values of REE in the validation group for EQNBMI (REE- creases in REE and experience an average decline approximately 1.5 107
43 IC: 6043 kJ/day ± 1131 SD; REE-PE EQNBMI: 6135 kJ/day ± 820; times higher than that of their normal weight counterparts with 108
44 P ¼ 0.25); EQNBMI resulted in a coefficient of determination value advancing age [20]. 109
45 of R2 ¼ 0.50 (P ¼ 0.001), with a prediction mean bias of 91.7 kJ/day. As a secondary aim, EQNBMI was develop to predict REE for 110
46 subjects with normal BMI, and instead of weight included in NEQ, 111
47 4. Discussion this equation contains height, which had the greatest explanation 112
48 of the variability of the REE. It is known that subjects with over- 113
49 A correct estimation of energy requirements is essential for weight and obesity have a significantly higher REE than normal BMI 114
50 nutritional management. When this measurement is not feasible or subjects although it is still controversial if these results remain after 115
51 available, PEs became a valuable tool for estimating REE, which adjusting by body composition [45]. However, as we found in this 116
52 represents a meaningful component of daily EE. However, it is study, the anthropometric variables have a different impact on REE 117
53 known that the optimal predictive accuracy of these equations is when they are evaluated in Mexican subjects with normal BMI vs 118
54 obtained when they are employed in individuals sharing the same overweight/obese [34]. The validation of NEQ revealed that this 119
55 characteristics as those in whom the equations were developed equation was the most accurate in the selected sample of the 120
56 [14]. Mexican population with overweight or obesity and showed the 121
57 In particular, it has been reported that ethnicity can play a role in least mean bias in predicting REE compared with other available 122
58 determining an individual's energy requirement, as people equations. 123
59 belonging to a specific ethnicity may differ from others in metabolic A recent systematic reviews conducted by Madden et al. [9] as 124
60 profile or in anthropometric aspects influencing metabolic char- well as by the Expert Panel convened by the ADA [14] on the ac- 125
61 acteristics, such as body composition and energy stores [41]. In fact, curacy of several prediction equations in estimating REE in adults 126
62 Kelley et al. [42] found that race contributes considerably to the with overweight/obesity, concluded that the Mifflin/St-Jeor equa- 127
63 variability in REE, and on average, black subjects have an REE tion [26] provided the most precise prediction for BMI in the entire 128
64 approximately 565 kJ/day lower than that of white subjects, inde- range of obesity. However, our study did not completely confirm 129
65 pendent of potential confounders such as BMI or FFM. Moreover, these previous findings, as the Mifflin/St-Jeor equation (that 130

Please cite this article in press as: Orozco-Ruiz X, et al., Development and validation of new predictive equation for resting energy expenditure in
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6 X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8

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Fig. 2. BlandeAltman plots displaying the agreement and difference between the resting energy expenditure by indirect calorimetry (REE-IC) and the resting energy expenditure
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predicted (REE-PE) by the a) Valencia, b) WHO/FAO/UNU, c) Mifflin-St Jeor, d) Owen, e) Carrasco, f) Korth, g)Johnstone, h)Livingston, i) De Lorenzo, j) Lazzer, k) Muller, l) Huang and
63 m) Bernstein equations. Dotted line represents the mean bias of the prediction equation, dashed black lines represent limits of agreement (±95% CI) and dashed grey lines represent 128
64 the limits of the ±10% of accuracy. 129
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X. Orozco-Ruiz et al. / Clinical Nutrition xxx (2017) 1e8 7

1 included both healthy and obese subjects) was not the best per- developed equation account for the new trends in the habits of the 66
2 forming but did show a prevalence of underestimations. Probably, modern population. 67
3 the specific ethnic characteristics of our population may have In conclusion, this study highlights the importance of consid- 68
4 contributed to the poor predictability of this equation in the pre- ering ethnicity when predicting REE and demonstrates that NEQ 69
5 sent study. developed for this target population of Mexican adults with over- 70
6 In fact, the Mifflin/St-Jeor equation has previously been found to weight/obesity is more appropriate for predicting REE in a clinical 71
7 have a low predictive performance in the Mexican population. In a setting. However, further studies are needed to clearly establish the 72
8 study conducted in Mexico City [46] to evaluate the accuracy of variation of EE according to specific ancestry-informative markers. 73
9 several equations in predicting REE in a sample of 121 women with 74
10 obesity, the accuracy of the Mifflin/St-Jeor equation (54%) was Funding sources 75
11 comparably low to that found in our study (52%). By contrast, in that 76
12 study, the Valencia equation [24] derived from a small sample of This work was supported by CONACYT (M. G. C., grant num- 77
13 adult Mexicans yielded the most accurate prediction (69%), con- ber,181685); Medix (N. T., FNU-346BIS-12-14-1) and partial support 78
14 firming the importance of the ethnic characteristics of the sample by Danone Institute in Mexico. Q2 79
15 used to derive equations. 80
16 However, the equation obtained in the present study appeared Statement of authorship 81
17 to perform better than the Valencia equation, both in terms of mean 82
18 bias and accuracy; this finding may have been due to the small size Conception and design: MGC, XOR, ART, NT Data acquisition: 83
19 and composition of the sample, which consisted of only 32 men in a MGC, XOR, EPO, IMV, Analysis and/or interpretation: MGC, XOR, 84
20 limited age range (18e40 y) with BMIs spanning from underweight ART, FP, CLL, Writing: All authors. 85
21 to grade II obesity. Moreover, the Valencia equation is based on 86
22 different formulas for three age groups in the two sexes and in- Conflict of interest 87
23 cludes only body weight as a determinant parameter, which may 88
24 have contributed to the different predictability from those found None. 89
25 for the present equation. It is important to point out that the 90
26 Valencia equation was obtained under conditions of basal energy 91
Acknowledgements
27 expenditure instead of REE. 92
28 Huang predictive equation which was developed in an Austra- 93
We greatly appreciate Prof. Stefano Lazzer, University of Udine
29 lian population with BMI >35 Kg [35] showed the worst perfor- 94
Italy, for his invaluable critique when revising the manuscript, and
30 mance in the present study, with the highest mean bias and the 95
we extend our acknowledgements also for the chemical Guillermo
31 lowest accuracy among the tested equations. This was followed by 96
Ordaz-Nava, INCMNSZ Mexico City, for all the technical support in
32 Carrasco equation [28] that was developed in Chilean individuals 97
this study.
33 with or without obesity. 98
34 In our population with overweight and obesity, we confirmed 99
Appendix A. Supplementary data
35 the conclusions of the ADA Panel concerning the low suitability of 100
36 the Owen equation for individuals with obesity [14] as well as a 101
Supplementary data related to this article can be found at
37 suboptimal performance of the WHO/FAO/UNU equation in our 102
https://doi.org/10.1016/j.clnu.2017.10.022.
38 population, which overestimated the REE by 35.2%, with a mean 103
39 bias of 270 kJ/day. 104
40 Interestingly, when we compared the NEQ with the Har- References 105
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