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Original Communication

Journal of Parenteral and Enteral


Nutrition
Preoperative and Postoperative Resting Energy Expenditure Volume 00 Number 0
xxx 2020 1–6
of Patients Undergoing Major Abdominal Operations © 2020 American Society for
Parenteral and Enteral Nutrition
DOI: 10.1002/jpen.1825
wileyonlinelibrary.com

Thales Antônio Silva, RD, MSc1 ; Fernanda de Carvalho Pazzini Maia, RD, MSc1 ;
Maria Clara Arantes Zocrato, RD2 ; Silvia Fernandes Mauricio, RD, PhD3 ;
Maria Isabel Toulson Davisson Correia, MD, PhD4 ;
and Simone de Vasconcelos Generoso, RD, PhD5

Abstract
Background: Nutrition therapy plays a major role in the perioperative management of surgical patients. Understanding energy
metabolism and correctly establishing the adequate energy needs is a crucial step to provide optimal nutrition care. The aim
of this study was to assess the resting energy expenditure (REE) after major abdominal procedures and its associated factors.
Methods: This was a prospective observational study conducted at a single center. REEs of patients admitted for gastrointestinal
surgical procedures were measured by indirect calorimetry 24 hours prior to the procedure and reassessed at least once within the
fifth postoperative day. Substrate oxidation was calculated according to the Frayn equation. Nutrition status was evaluated using
subjective global assessment. Results: There were no significant changes in the REEs throughout the study period; however, there
was a decrease in the respiratory quotient during the postoperative period, as well as a decrease in carbohydrate oxidation and an
increase in lipid oxidation. Only 33.3% of the patients presented a postoperative increase in REE > 10%. Those patients presented
higher blood-monocyte levels. Conclusion: Postoperative REE is not increased in most of the patients. In patients who had increased
REE, associated factors included higher levels of monocytes. (JPEN J Parenter Enteral Nutr. 2020;00:1–6)

Keywords
indirect calorimetry; major abdominal surgery; nutrition status; resting energy expenditure

Clinical Relevancy Statement Introduction


Our work has shown that resting energy expenditure is Nutrition therapy plays a major role in the perioperative
not increased postoperatively in the majority of patients management of surgical patients. The high prevalence of
undergoing major abdominal surgeries. Thus, the use of malnutrition among surgical patients1,2 and its negative
stress factors added to predictive equations, as it is still clinical3-5 and economic impacts6 on postoperative out-
common in clinical practice, can lead to overfeeding and its comes have been reported in the literature for decades.
consequences and should, therefore, be avoided. Thus, nutrition therapy helps in not only minimizing the

From the 1 Pharmacy School, Food of Science Program, UFMG, Belo Horizonte, Minas Gerais, Brazil; 2 Nursing School, Department of
Nutrition, UFMG, Belo Horizonte, Minas Gerais, Brazil; 3 Faculty of Medicine, Department of Surgery, Surgery and Ophthalmology Program,
UFMG, Belo Horizonte, Minas Gerais, Brazil; 4 Faculty of Medicine, Department of Surgery, UFMG, Belo Horizonte, Minas Gerais, Brazil;
and 5 Nursing School, Department of Nutrition, Nutrition and Health Program, UFMG, Belo Horizonte, Minas Gerais, Brazil.
Financial disclosures: This work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig); Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES); and Pró Reitoria de Pesquisa da UFMG (PRPq/UFMG). M. I. T. D. Correia is a
recipient of a scientific grant by the Conselho Nacional de Pesquisa (CNPq).
Conflicts of interest: None declared.
Received for publication December 10, 2019; accepted for publication February 25, 2020.
This article originally appeared online on xxxx 0, 2020.
Corresponding Author:
Simone de Vasconcelos Generoso, RD, PhD, Nutrition Department, Federal University of Minas Gerais, Professor Alfredo Balena Avenue, 190,
3rd Floor, Room 324, Santa Efigênia, 30130-100, Belo Horizonte, MG, Brazil.
Email: simonenutufmg@gmail.com
2 Journal of Parenteral and Enteral Nutrition 00(0)

deterioration of nutrition status but also in modulating the and registered at Clinical Trials (NCT03357848) https://
immune/inflammatory response, which together can lead to clinicaltrials.gov/ct2/show/NCT03357848.
better postoperative outcomes.7 Establishing the adequate
energy needs is a crucial step in providing optimal nutrition Nutrition Status and Anthropometric and Body
care, since both underfeeding and overfeeding can have Composition Measurements
deleterious effects. Underfeeding for patients not on nutri-
tion therapy is a result of postoperative changes marked Nutrition status and anthropometric and body composition
by an inflammatory status, which leads to hyporexia.8 measurements were assessed by the same researcher 24
Conversely, overfeeding, together with insulin resistance hours before the operation. The nutrition status was as-
(which is typical of the early postoperative phase), can lead sessed via the subjective global assessment (SGA). Patients
to hyperglycemia, which is associated with increased rates of were classified as well nourished, suspected/moderately mal-
infectious complications9 that lead to longer postoperative nourished, or severely malnourished.16
hospital stay and increased morbidity and mortality, as well Body weight was measured on a Tanita digital scale with
as increased hospital costs. patients wearing light clothing and no shoes. Height was
The surgical process induces a variety of hormonal, obtained either from the patient’s medical records or from
metabolic, and inflammatory changes,10 and as a conse- self-reports by the patient. Bioimpedance was performed
quence, resting energy expenditure (REE), the major com- using the bioelectrical bioimpedance Quantum X (RJL
ponent of energy expenditure is expected to increase after Systems) with patients lying in a supine position, hands
major procedures, thereby, altering energy requirements. away from the body, and legs separated from each other at
Although, in clinical practice, it is a common belief that an angle of 30°.17 Reactance and resistance values were used
REE is increased after surgery, conflicting results have been to calculate body fat mass (FM) and fat-free mass (FFM).
reported. Long et al measured postoperative REE and FM index (FMI) and FFM index (FFMI) were generated
compared it with data derived from predictive equations.11 by dividing FM and FFM by the height squared (m2 ). These
This led to the postoperative hypermetabolism idea. How- measurements were classified as high FMI for men with an
ever, differences between measured and predicted REE do FMI ≥ 8.3 kg/m2 and for women with an FMI ≥11.8 kg/m2 .
not necessarily imply increased energy expenditure. Rather, A low FFMI was classified as an FMI ≤ 17.4 kg/m2 for men
they can represent an inherent error related to predictive and ≤ 15 kg/m2 for women.18,19
equations. Fredrix et al observed an increased REE after
abdominal operations,12 whereas other authors observed no Resting Energy Expenditure
postoperative changes in REE.13-15 Therefore, the aim of REE was measured by indirect calorimetry (IC) using the
this study was to assess the REE after major abdominal Quark RMR device (Cosmed, Rome, Italy). The test was
procedures and its associated factors. performed in a silent and temperature-controlled room for
20 minutes. All the tests were carried out with patients lying
in a supine position and breathing under a canopy and
Materials and Methods with a minimum of a 4-hour fasting state for those not
Participants on continuous enteral or parenteral feeding. Infusion rates
of patients under enteral or parenteral nutrition were kept
This is a prospective observational study conducted at a constant for at least 12 hours prior to the test. Tests were
single center (Hospital das Clínicas da Universidade Federal considered stable if they had a variation of the respiratory
de Minas Gerais). Patients aged ≥18 years and admitted quotient of ≤10%. IC was carried out again under the
at the unit for major abdominal elective operations were same conditions at 2 different times in the postoperative
eligible to participate in the study. The inclusion criteria period, that is, on the third and fifth day. Patients discharged
were as follows: (1) the preoperative REE must be measured before the fifth POD were still included if they had 1 IC
within 24 hours before the operation, and (2) at least measurement on POD 3. REE was calculated using the
1 assessment of REE should be conducted within the Weir equation.20 REE adjusted for weight was calculated
fifth postoperative day (POD). Exclusion criteria included based on the preoperative weight. Carbohydrate and lipid
patients undergoing procedures performed via laparoscopy, oxidation rates were calculated according to the Frayn
patients who underwent only exploratory laparotomies, equation21 as follows:
patients with postoperative length of stay < 3 days or those
admitted postoperatively to the intensive care unit, patients Carbohydrate oxidation (kg/min) = 4.12 × VCO2 /1000
under replacement renal therapy, and patients with previous − 2.91 × VO2 /1000
reports of hyperthyroidism or hypothyroidism. The study
was approved by the ethics committee of the Universidade Lipid oxidation(kg/min) = 1.69 × VO2 /1000
Federal de Minas Gerais (CAAE-27430714.8.0000.5149) −1.69 × VCO2 /1000
Silva et al 3

Postoperative REE measurements were compared with Table 1. General Characteristics and Nutrition Status (at
the preoperative REE values. Patients who had an increase Baseline) of Patients Undergoing Major Abdominal
of ≥10% REE during the postoperative period were con- Operations (n = 54).
sidered hypermetabolic. To analyze risk factors associated Characteristics N %
with hypermetabolism, calorimetry data collected on POD 3
alone were utilized because of the sample size requirements. Sex
Male 28 51.9
Females 26 48.1
Biochemical Parameters Age
Data for creatinine levels, C-reactive protein (CRP) levels, ≤60 y 24 44.4
and blood counts were collected from the patient’s medical ≥60 y 30 55.6
Operation
records. They had to be performed within 72 hours after the
Liver resection 8 14.8
operation. Rectosigmoidectomy 16 29.6
Gastrectomy 12 22.2
Postoperative Complications Abdominal perineal resection 5 9.3
Colectomy 5 9.3
Postoperative complications were recorded daily from medi- Pancreatoduodenectomy 4 7.4
cal records and from discussions with the surgical team from Pancreatectomy 1 1.9
the first POD until discharge. They were classified according Peritonectomy 1 1.9
to the Clavien-Dindo classification.22 Esophagectomy 2 3.7
Subjective global assessment
Nourished 15 27.8
Statistical Analysis Moderately malnourished 25 46.3
Severely malnourished 14 25.9
The sample size was calculated based on a pilot study FMI, kg/m2
involving 10 patients. The mean REE measured in the Normal FMI 38 80.9
preoperative period was 1148.9 ± 222.5 kcal, and because High FMI 9 19.1
we expected a 10% energy expenditure increase on the third FFMI, kg/m2
POD (with 80% test power and 5% significance level), a Normal FFMI 22 46.8
sample size of 48 patients was required. Low FFMI 25 53.2
Statistical analyses were performed using the Statistical
FFMI, fat-free mass index; FMI, fat mass index.
Package for Social Sciences (SPSS version 19.0, Chigaco,
IL). Descriptive data are presented as frequency for cat-
egorical variables and median and interquartile range for
continuous variables. with some degree of malnutrition, and none of the patients
The Wilcoxon test was used to compare each postoper- were receiving enteral or parenteral nutrition. The general
ative moment with the preoperative IC measurement. The characteristics of the patients included in the study are
Mann-Whitney U test was used for independent variables. shown in Table 1.
The χ 2 test was used to analyze the relationship between di- The median postoperative length of stay was 6 ± 4
chotomic variables, and for subgroups with n ≤ 5, the Fisher days, with malnourished patients staying longer than well-
exact test was performed. Binomial logistic regression was nourished patients (4 ± 1 vs 6.5 ± 5.5 days; P = .002).
utilized to test variables associated with the increased REE On the third POD, the majority of the patients were still
on POD 3. fasting. Only 6 patients were receiving nutrition therapy
(3 with parenteral nutrition [1218 ± 370 kcal/d, 50.3 ±
14.9 g of protein/d] and 3 with enteral nutrition [737.3 ±
Results 269.2 kcal/d, 29 ± 8.7 g of protein/d]). A total of 16.4% of
the patients presented postoperative complications, which
General Characteristics and Nutrition Status were also associated with the nutrition status (P = .021).
Sixty-one patients were initially assessed to participate. One Well-nourished patients presented no complications.
patient was excluded because of unstable IC measurements,
4 patients died after the operation, and 2 patients could not
be assessed before the fifth POD. Thus, 54 patients were
Preoperative and Postoperative REE
included in the analysis. The mean age of the patients was The median REE at baseline was 1224 ± 241 kcal/day
58.7 ± 14.8 years. The average operating time was 4.5 ± or 18.5 ± 5 kcal/kg. Malnourished patients presented sig-
2.2 hours. Operations are described in Table 1. At baseline, nificantly higher REE/kg than the well-nourished patients
according to the SGA, most patients (72.2%) presented (19.6 ± 4.9 vs 17.9 ± 3.7 kcal/kg; P = .036). Patients
4 Journal of Parenteral and Enteral Nutrition 00(0)

Table 2. Postoperative Evolution of REE and Substrate Table 4. Comparison of Different Variables According to
Oxidation of Patients Undergoing Major Abdominal Postoperative Changes in REE (n = 49).
Operations.
Normal Increased
Preoperative POD 3 POD 5 REE (n = 33) (n = 16) P-value
(n = 54) (n = 49) (n = 24)
Age, y 63 (22.5) 64 (17.5) .122
REE, kcal 1224 (241)a 1259 (395.5)a 1249 (156.5)a Surgery 4 (2) 4.5 (3) .917
REE, kcal/kg 18.5 (5)a 19.40 (5.5)a 20.70 (5)a duration, h
Respiratory 0.97 (0.18)a 0.88 (0.14)b 0.91 (0.14)b FMI, kg/m2 7.7 (4.4) 5.5 (4.4) .016
quotient FFMI, kg/m2 15.9 (2.6) 15.1 (3.3) .433
C-oxidation, 0.16 (0.14)a 0.13 (0.09)b 0.15 (0.07)b CRP, mg/L 150.9 (74.5) 149.8 (90.8) .908
kg/min Leukocytes, 8.4 (3.2) 11.5 (4.6) .007
L-oxidation, 0.01 (0.05)a 0.03 (0.05)b 0.03 (0.04)b cells/mm3
kg/min Neutrophils, 6.6 (2.5) 9.1 (4.9) .006
cells/mm3
C-oxidation, carbohydrate oxidation; L-oxidation, lipid oxidation; Monocytes, 0.47 (0.3) 0.61 (0.61) .005
POD, postoperative day; REE, resting energy expenditure. cells/mm3
Values expressed as median ± interquartile range. Different Lymphocytes, 1.19 (0.85) 0.96 (0.64) .504
superscript letters on the same line indicate P < .05.
cells/mm3
Postoperative 3 (0.185) 1 (0) .478
complications
having a low FFMI had a lower REE than those having a
normal FFMI (P = .005); however, when REE was adjusted CRP, C-reactive protein; FFMI, fat-free mass index; FMI, fat mass
for weight, no difference was seen (17.4 ± 5.1 vs 19.6 ± index; REE, resting energy expenditure.
3.7 kcal/kg; P = .105). Increased REE > 10% when compared with preoperative
measurements. Values expressed as median (interquartile range).
The evolution of the REE throughout the assessed Significant differences (p<0.05) are highlighted with bold numbers.
period is depicted in Table 2. There were no significant
changes in the REE at any of the assessed periods. How-
ever, we observed a shift in the type of oxidized nutrient. with normal postoperative REE. However, both groups
There was a decrease in the respiratory quotient during the had an increase in fat oxidation.
postoperative period when compared with the preoperative
assessment, accompanied by a decrease in carbohydrate Factors Associated with the Increased REE
oxidation and an increase in lipid oxidation.
After stratifying patients according to the changes Table 4 shows the differences between patients who pre-
in REE (patients who had an increase in REE > 10% sented with increased REE on the third POD compared with
vs those who did not) on the third POD, we observed those who did not. Patients with increased REE showed
that only a minority of individuals (32.7%) experienced lower FMI, as well as higher leukocytes, neutrophils, and
such changes. These patients had a median increase of monocytes. There was no significant association between
20.7% in REE, ranging from 10.2% to 34.9%. On the fifth surgical site operation and REE, as well postoperative
POD, 37.5% of the patients who had REE measured were complications (P > .05).
hypermetabolic, representing a median increase of 16.3% Binomial logistic regression was used to test for vari-
(range, 11.2%–36.9%) compared with the preoperative ables associated with the increased REE. Sex, FMI, and
assessment. Table 3 shows the difference in substrate leukocytes (monocytes and neutrophils) were significantly
utilization between the 2 groups. Patients who presented associated with REE after univariate analysis (Table 5).
with increased postoperative REE did not have a reduction However, after multivariate analysis, only monocytes re-
in carbohydrate oxidation, unlike patients who presented mained significant (P = .029).

Table 3. Preoperative and Postoperative Substrate Oxidation Stratified by REE Variation (n = 49).

REE Cho-oxid pre Cho-oxid POD 3 P-value Lip-oxid pre Lip-oxid POD 3 P-value

Normal N = 33 0.2168 0.1364 <.001 0.0017 0.0326 .001


Increased N = 16 0.1369 0.1347 .679 0.0237 0.0355 .044

Cho-oxid, carbohydrate oxidation; Lip-oxid, lipid oxidation; POD, postoperative day; Pre, preoperative; REE, resting energy expenditure.
Increased REE > 10% when compared with preoperative measurements. Significant differences are highlighted with bold numbers.
Silva et al 5

Table 5. General Characteristics, Nutrition Status, and Clinical Variables of Patients and Their Association With Postoperative
Increased Energy Expenditure.

Univariate analysis Multivariate analysis

Variables OR (95% CI) P-value OR (95% CI) P-value

Male 4.071 (1.082–15.326) .038 – –


Age, y 1.047 (0.994–1.104) .083 – –
Nutrition status 0.355 (0.084–1.493) .158 – –
FMI, kg/m2 0.732 (0.557–0.962) .025 – –
FFMI, kg/m2 0.864 (0.599–1.246) .433 – –
CRP 1.000 (0.992–1.009) .926 – –
Leukocytes, cells/mm3 1.250 (1.011–1.545) .039 – –
Neutrophils, cells/mm3 1.310 (1.028–1.670) .029 – –
Monocytes, cells/mm3 47.193 (2.111–1051) .015 34.650 (1.439–835.69) .029
Lymphocytes, cells/mm3 0.732 (0.228–2.348) .599 – –
Duration of surgery, h 1.056 (0.698–1.598) .795 – –
Postoperative complications 0.483 (0.050–4.717) .532 – –

CRP, C-reactive protein; FFMI, fat-free mass index; FMI, fat mass index; OR, odd ratio.
Significant differences are highlighted with bold numbers.

Discussion individual variability, with some patients experiencing an


increase in REE, whereas others experienced a decrease. The
In the current study, REE did not increase postoperatively authors indicate that the patients who had an increased REE
in the majority of patients. This is a controversial result were older and had longer duration of operations. In our
considering that, in theory, energy expenditure is sup- study, these variables were not associated with the increased
posed to be increased because of hormonal and metabolic REE. However, we observed that sex (males), lower FMI,
changes.10 Long et al observed a 23.9% increase in the REE and higher levels of leukocytes (especially monocytes) were
of patients undergoing elective operations.11 However, the associated with increased postoperative REE. Monocytes
authors did not perform IC in the preoperative period. The are related to the production of interleukin 6 (IL-6). IL-
REE was only measured postoperatively and subsequently 6 has been previously associated with increased energy
compared with data derived from the Harris-Benedict equa- expenditure and hormonal changes, including glucagon
tion. The authors interpreted the differences between the and norepinephrine affecting fuel utilization by increasing
predicted and measured REEs as increased postoperative fatty acids and protein utilization.24-26 To our knowledge,
energy expenditure. Fredrix et al also observed a statistically no previous study has evaluated the association between
significant increase in the REE of patients undergoing inflammatory biochemical parameters and postoperative
gastrointestinal procedures.12 However, compared with the REE. Although we combined mostly indirect markers of in-
preoperative period, the REE increased by only 3.2%, which flammation, these are postoperative routine tests that might
may have limited clinical significance. be an interesting strategy to consider when determining
More recently, Ukleja et al assessed the metabolic individual energy requirements for those using predictive
changes following partial liver resection.15 Patients’ REEs equations. Nonetheless, CRP levels were similar for the 2
were measured on the day prior to surgery and on the groups, which may be explained because this is a nonspecific
seventh day after the procedure. Similar to our data, the au- marker of the postoperative organic response to trauma that
thors did not observe any significant change in REE. Like- has its peak around the second to third POD.
wise, Chen et al also observed no changes in REE on the 5th, In the majority of our surgical patients, there was no
10th, and 15th days after liver transplantation (although, in increased REE. Thus, the use of stress factors added to the
their study, preoperative REE was not measured).14 Harris-Benedict predictive equation, which is still common
It is important to highlight that although only 33.3% of in clinical practice, might lead to overfeeding. However, we
the patients included in our study experienced an increase did observe changes in substrate oxidation, although REE
in REE after the operation, this is still a considerable was not increased. On POD 3, only 6 patients were receiv-
amount of patients. These data indicate the importance of ing nutrition therapy. We initially analyzed these patients
individually assessing REE once the postoperative response separately, regarding calorimetry, and no differences were
is individual and cannot be fully predicted. Hughes et al23 observed when comparing them to the others, potentially
measured REE on the day prior to liver resection and daily because of the minimal continuous volume of nutrition of-
until the fifth POD. Although minimal changes in REE fered throughout the 4 hours before the test (not >200 kcal).
were observed postoperatively, the authors reported a high
6 Journal of Parenteral and Enteral Nutrition 00(0)

There was an increase in lipid oxidation, which is 9. Eshuis WJ, Hermanides J, van Dalen JW, et al.. Early postoperative
expected, considering hormonal changes following the hyperglycemia is associated with postoperative complications after
pancreatoduodenectomy. Ann Surg. 2011;253(4):739-744.
surgical trauma.27,28 Carbohydrate oxidation decreased in
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patients who presented normal REE on POD 3, presenting The surgically induced stress response. J Parenter Enter Nutr.
a “compensatory” effect in energy expenditure, which might 2013;37(5_suppl):21S-29S.
explain why REE was not altered. In contrast, patients who 11. Long CL, Schaffel N, Geiger JW, Schiller WR, Blakemore WS.
presented with an increased REE on POD 3 did not Metabolic response to injury and illness: estimation of energy and
protein needs from indirect calorimetry and nitrogen balance. J
experience a decrease in carbohydrate oxidation.
Parenter Enter Nutr. 1979;3(6):452-456.
One limitation of our study is that we reached only the 12. Fredrix EWHM, Soeters PB, Von Meyenfeldt MF, Saris WHM.
calculated sample size during the first PO assessment (72 Resting energy expenditure in cancer patients before and after gastroin-
hours after the operation). However, this is the period of the testinal surgery. J Parenter Enter Nutr. 1991;15(6):604-607.
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J Pediatr Surg. 1989;24(8):825-828.
14. Chen Y, Kintner J, Rifkin SK, Keim KS, Tangney CC. Changes in
Conclusion resting energy expenditure following orthotopic liver transplantation.
J Parenter Enter Nutr. 2016;40(6):877-882.
In this study, there was no increased REE in most of the 15. Ukleja A, Andrzejewska M, Skroński MK, Ławiński M, Włodarek D,
patients. In patients who had increased REE, associated Korba M. Assessment of resting energy demand and body composi-
factors included sex (males) and higher levels of monocytes. tion in oncological patients undergoing partial resections of the liver.
Prz Gastroenterol. 2019;14(1):62-68.
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