- Email: [email protected]
Current technologies in body composition assessment: advantages and disadvantages
Accepted Manuscript
Current technologies in body composition assessment: advantages and disadvantages Guilherme Duprat Ceniccola RD, PhD. , Melina Gouveia Castro MD, PhD. , Silvia Maria Fraga Piovacari RD. , Lilian Mika Horie RD, Msc. , Fabiano Girade Correa ˆ MD. , Ana Paula Noronha Barrere RD. Msc. , Diogo Oliveira Toledo MD. Msc. PII: DOI: Reference:
S0899-9007(18)31318-2 https://doi.org/10.1016/j.nut.2018.11.028 NUT 10409
To appear in:
Nutrition
Received date: Revised date: Accepted date:
3 March 2018 14 September 2018 14 November 2018
Please cite this article as: Guilherme Duprat Ceniccola RD, PhD. , Melina Gouveia Castro MD, PhD. , Silvia Maria Fraga Piovacari RD. , Lilian Mika Horie RD, Msc. , Fabiano Girade Correa ˆ MD. , Ana Paula Noronha Barrere RD. Msc. , Diogo Oliveira Toledo MD. Msc. , Current technologies in body composition assessment: advantages and disadvantages, Nutrition (2018), doi: https://doi.org/10.1016/j.nut.2018.11.028
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ACCEPTED MANUSCRIPT Highlights: Bedside ultrasonography has emerged as a common method to quantify muscle mass. Main limitations of the method are lack of cut-off points to do diagnoses, paucity of clinical protocols and agreement on its use and imprecision under excessive edema situations.
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Bioelectrical impedance analysis is a widely used method to estimate body composition in different clinical conditions, such as cancer, obesity, sarcopenia and elderly it main limitations are because it is an Indirect method, is limited by
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hydration status and demands Specific equation for each population.
The assessment of body composition through Computed tomography is considered a method of great accuracy to analyze body compartments. It is limited by non-portability, high cost, radiation exposure and trained personnel
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requirements.
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Originally developed for measuring bone mineral density, Dual X-ray absorptiometry has become recognized for its ability to accurately and
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precisely measure total body composition. It main limitation is due to non-
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portability, high cost, trained personnel requirements and inability to discriminate
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the different types of fat.
ACCEPTED MANUSCRIPT Current technologies in body composition assessment: advantages and disadvantages
Guilherme Duprat Ceniccola, RD, PhD. E-mail: [email protected]
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Departmental contact: Instituto Hospital de Base. Address: MHS Q 101, Brasília-DF, Brazil, Zip code 7033000. Phone 55 61 32455302, 55 61 992340657. Permanent Address: SQS 314 Bl I apt 605, Brasília - DF, Brazil. Zip code: 70383-090
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Melina Gouveia Castro, MD, PhD. Email: [email protected]
Departamental contact: Faculdade de Medicina da Universidade de São Paulo. Av. Dr. Arnaldo, 455 - Cerqueira César, São Paulo - SP,
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Zip code: 01246-903
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Silvia Maria Fraga Piovacari, RD. Email: [email protected]
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Departmental contact: Department of Clinical Nutrition, Hospital Israelita Albert Einstein. Address: Av. Albert Einstein, 627/701 – Morumbi - São Paulo - SP, Brazil.
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Zip code: 05652-900.
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Lilian Mika Horie, RD, Msc. Email: [email protected] Departamental contact: Faculdade de Medicina da Universidade de São Paulo. Av. Dr. Arnaldo, 455 - Cerqueira César, São Paulo - SP, Zip code: 01246-903 Fabiano Girade Corrêa, MD. Email: [email protected]
ACCEPTED MANUSCRIPT Departmental contact: Hospital Santa Lúcia. Address: SHLS Condomínio do Centro Medico de Brasília - Brasília, DF, Brazil. zip code: 70297-400 Ana Paula Noronha Barrere, RD. Msc. Email: [email protected] Departmental contact: Department of Clinical Nutrition, Hospital Israelita Albert Einstein Address: Av. Albert Einstein, 627/701 - Morumbi, São Paulo - SP, Brazil. Zip
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code: 05652-900
Diogo Oliveira Toledo, MD. Msc. Email: [email protected]
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Departmental contact: Department of Critical Care, Hospital Israelita Albert Einstein Address: Av. Albert Einstein, 627/701, Morumbi - São Paulo - SP, Brazil. Zip code 05652-900.
Abstract
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The interest in non-invasive methods of body composition assessment is at rise in the health care scenario, especially due to its association to clinical outcomes. Technology has revolutionized our understanding of body composition abnormalities, clinical prognostication and disease follow-up, but translation to bedside is limited, especially in the costeffectiveness view point. Computed tomography gained increased attention in cancer and sarcopenia studies for instance. Other methods have also interesting features and applications, which includes Bedside ultrasonography, Bioelectrical impedance analysis and Dual X-ray absorptiometry. Compelling evidence is highlights these methods to accurately and precisely measure skeletal muscle mass, adipose tissue, edema, diagnose malnutrition related diseases and prognostic tool measuring. To apply this technology properly, it is demanding the understanding about the advantages and disadvantages that pertain each technique in specific situations of interest. This way, this review introduces concepts and reference studies published in the scientific literature about Bedside ultrasonography, Bioelectrical impedance analysis, Computed Tomography and Dual X-ray absorptiometry, mentions important limitations and considerations to be done in order to bring those methods to the practical field. Keywords Body composition, Bedside ultrasonography, Bioelectrical impedance analysis, Computed Tomography and Dual X-ray absorptiometry
ACCEPTED MANUSCRIPT Introduction The need for accurate methods to assess body composition as a diagnostic and prognostic tool is coupled with the introduction of quality concepts and the improvements in hospital routines, which involves the translation of new technologies and procedures to practice field. Regarding to health care, in the recent past, more
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invasive interventions were prioritized, such as mechanical ventilation, catheter monitoring and heavy sedation. Nowadays, interventions are based on less invasive and safer techniques, replicable diagnostic methods, pros and cons related to the target population and situation of concern. It is this cost-effective, less invasive and
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replicable context that fits body composition assessment into the current clinical scenario.1
Additionally, the conventional methods used for nutritional diagnosis (anthropometry,
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biochemical tests, physical examination and dietary parameters) are weakly associated to body components estimations such as skeletal muscle, adipose tissue
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and body water. For instance, the sarcopenia’s definition is one of the most debated
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topics considering body composition and several cut points using different methodologies have been proposed. Body mass index (BMI), one of the most
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widespread measures, falls short regarding to association with these body components and sarcopenia.2
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To fulfill this gap, accurate and noninvasive techniques are important to assess body composition and to diagnose diseases related to malnutrition, sarcopenia and frailty, and also to guide rehabilitation of hospitalized patients, which may save resources and promote better clinical outcomes.3 As examples of these techniques, ultrasonography
(US),
Bioelectrical
impedance
analysis
(BIA),
Computed
Tomography (CT) and dual X-ray absorptiometry (DXA) will be addressed and
ACCEPTED MANUSCRIPT compared on a body composition assessment bases. This review aims to present the current techniques used in the evaluation of body composition concerning to its advantages and disadvantages to the hospitalized patient.
Bedside ultrasonography (US)
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The use of ultrasound to assess body composition has increased in daily practices, motivated by validation studies.4 Ultrasound has emerged as a common method to quantify muscle mass and it has recently caught a lot of attention with the growing importance of the skeletal muscle role in the recovery process.5 In 2014,
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Tillquist et al, showed that the technique had an excellent reliability between trainer and trainee when applied to healthy volunteers.6 Paris et al, demonstrated in a multicenter study that this technique is also applicable to critically ill patients with
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satisfactory intra and inter-rater reliability, and even more, to assess longitudinal changes in muscles.7
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In addition, muscle mass measurement by US has shown to be a reliable
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technique in most patients, even when fluid retention is present. 8,9 In chronic obstructive pulmonary disease, the US quadriceps musculature measurement
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proved to be effective in identifying patients with greater muscle loss during hospitalization.10
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Currently, the US technique has not been capable of diagnosing sarcopenia yet, for the lack of recent studies identifying a cutoff value or a theoretical protocol. However, some studies were able to show different baseline values of skeletal muscles between men and women of different age groups.11,12 Puthucheary et al by compared three methods: US, muscle biopsy and molecular biology. This study revealed a significant 10% reduction of rectus femoris muscle, measured by the US,
ACCEPTED MANUSCRIPT during the first 7 days in intensive care units (ICU).13 A similar result was also found in a Brazilian study with critically ill patients, which presented approximately 1.5% loss of quadriceps thickness per day, assessed by the US. 14 Table 1 describes the advantages and disadvantages of US for muscle mass assessment.
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Table 1. Advantages and disadvantages of US method Advantages (Pros)
Disadvantages (Cons)
Portable
Lack of cut-off points to do diagnoses
Low cost
Paucity of clinical protocols and agreement on its use
Satisfactory reliability intra and inter rater
Safe for repeated measures
Limited by excessive edema situations
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Noninvasive
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Description of the Technique
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Assess longitudinal changes in muscles
Body skeletal muscle can be estimated using ultrasound imaging with
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different protocols, what comprises the use of one or more anatomical sites. 15 Two
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main reference methods of measuring have been reported to quantify wasting: (a) measuring quadriceps muscle layer thickness (QMLT), combined thickness of the
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rectus femoris (RF) and vastus intermedius muscles. The QMLT was quantified using onscreen calipers and taken as the distance between the upper margin of the femoral bone and the lower boundary of the deep fascia of the rectus femoris (Figure 1)6,8,14,16 and (b) rectus femoris cross-sectional area, where scanning depth was quantified and set to where the femur could be distinguished for orientation. RF CSA was calculated by a planimetric technique (by US) after the inner echogenic line of the rectus femoris was outlined by a movable cursor on a frozen image (figure 2).10
ACCEPTED MANUSCRIPT Both techniques were effective in demonstrating muscle loss in hospitalized patients, but CSA was better at demonstrating muscle strength measurements. 17 Although the ultrasound measurements providers will be able to assess muscle wasting longitudinally, it does not provide a whole-body composition
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assessment and may be useless in a single assessment.15
Figure 1. Quadriceps muscle layer thickness
Figure 2. Rectus femoris CSA
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Results of Studies
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RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; VI: vastus intermedius.
US studies applied in hospitalized patients reveal that those who lose more muscle
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mass may present worse outcomes during hospitalization.10,13 In a longitudinal study
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comprising 1-year follow-up after hospital discharge, patients with chronic respiratory disease classified in the lower quartile of the quadriceps muscle size, had a higher mortality rate compared with patients classified in the upper quartile. In addition, a smaller quadriceps muscle size measured by US is an independent risk factor for readmission.10 In a population of critically ill patients, muscle loss assessed by crosssectional area technique was associated with increased organic dysfunction and inflammation 7 days after ICU admission.13 Parry et al, demonstrated a strong
ACCEPTED MANUSCRIPT association between quadriceps muscle architecture and strength, and function measurements at ICU discharge. 16 This tool can also be used to track muscle atrophy allowing nutrient delivery calculation and rehabilitative interventions. This way, US assessment could guide not only nutritional diagnosis but its consequent intervention. 15 A case study which
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used the US as a guide to optimize protein supply, showed good correlation between increased protein intake, muscle thickness gain and consequent nitrogen balance improvement.18 Other studies which applied that technique revealed an association between muscle mass loss and worse outcomes during hospitalization. 10,13
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Broad validation protocols comparing ultrasound to reference techniques still need to be undertaken, special in the critically ill patient with edematous areas that the muscle wasting may occur without changes in QMLT, were water content could
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affect measurements. Future research will aim to address these questions, for example, measuring severe edematous patients with maximum ultrasound
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compression protocols could be an alternative to explore.
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Overall, the US provides precise and reliable measures of muscle stores and potential changes in muscle mass and adipose tissue. In order to optimize its
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capabilities, further work is needed to comprehensively understand its limitations
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related to excessive edema situations and disease diagnosis, and also to unify clinical usage protocols.
Bioelectrical impedance analysis (BIA) The BIA is a widely used method to estimate body composition in different clinical conditions, such as cancer, obesity, sarcopenia and elderly.19,20 Several BIA devices are available in the market and can be classified based on the
ACCEPTED MANUSCRIPT number of electrical frequencies: single-frequency (SF-BIA) and multifrequential (MF-BIA).21 In general, the precision level produced by SF-BIA and MF-BIA devices is usually very good, 1-2% of variability between repeated measures.21 Precision and accuracy of BIA devices are influenced by a several factors, including: patient ( adiposity degree, fluid and electrolyte status, skin temperature) and environmental
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factors (ambient temperature, proximity to metal surfaces and electronic devices), assumptions underlying prediction (SF-BIA or MF-BIA), instrumentation factors, and variations in measurement protocols.22 Table 2 shows BIA's advantages and
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disadvantages.
Table 2. Advantage and disadvantage of BIA method Advantages (Pros)
Disadvantages (Cons)
Portable
Indirect method Limited by hydration status - Fat free
Quick and noninvasive Very simple and reproducible
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Low cost
mass hydration fixed in 73%
Specific equation needed for each population
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Safe for repeated measures
Description of the Technique
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The simplest way to estimate body composition through BIA is by using the bicompartmental model, which analyzes the body's lean mass and fat mass content.
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More accurate results are obtained when each specific population is assessed by its own equation.23 BIA devices do not directly measure body composition; they provide indirect estimates from resistance measurement of body tissues to an electric current. Besides, some assumptions have to be considered to use BIA for body composition:
ACCEPTED MANUSCRIPT 1. The human body is divides into five cylinders; trunk, upper and lower extremities, with a uniform electric conductivity; 2. FFM contains virtually all the water and conducting electrolytes in the body; 3. FFM hydration is constant; 4. Conductive length is conventionally considered stature.
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The BIA use for body composition assessment is carried out through the electric current passage in low intensity (500-800 mA) and high frequency (50 kHz), measuring the primary components: Resistance (R), Reactance (Xc), Impedance (Z) and Phase Angle (PhA).
22,23
This technique assesses total body water and, by
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assuming a constant hydration, can predict the amount of the fat free mass (FFM). The FFM is calculated from the TBW, using the assumption that 73% of the FFM is water in adults. However, the 73.2% reference factor for the water content of FFM
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results in an overestimation of FFM and underestimation of FM in children who have 75–76% water for the FFM. Therefore, changes in the hydration state are the main
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Results of Studies
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limitation of this method.21
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A recent study comparing the use of BIA, CT and DXA in surgical patients recognized the importance of BIA, especially because of its cost-effectiveness. The
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advantages of BIA compared to those two gold standard methods are the portability of the device, ease of use, affordability and non-invasiveness technique. When comparing accuracy, the fat free mass results between BIA and DXA reached r2=0.6275 (p<0.0001) and between BIA and CT it reached r2=0.274 (p-0,0001), which is a satisfactory result considering clinical and research settings. 23,24 Deurenberg evaluated the body composition of 661 people of different weights and BMI. The differences observed in body cell mass (BCM) and body fat mass (FM)
ACCEPTED MANUSCRIPT estimated by DXA and BIA, respectively, were higher in people with BMI <18 kg/m 2 and >34 kg/m2. In these cases, BIA overestimated lean cell mass amount in both super-obese and low-weight individuals, and underestimated body fat in extremely obese individuals.25 In studies with healthy individuals, BIA assessment achieved 3-5% accuracy
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compared to different gold standard methods (air-displacement plethysmography, DXA, MRI - Magnetic Resonance Imaging and CT). On the other hand, a recent systematic review published by Haverkort et al concluded that the BIA use in surgical and oncological patients reached low precision (underestimated total body water,
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which ranged between −18.8% to +7.2% and fat free mass, which ranged between −15.2% to +3.8%), suggesting that BIA estimations should be performed and interpreted longitudinally.26
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The use of BIA to monitor longitudinal changes in body composition below 5 kg should be interpreted with caution.27 Moreover, BIA acquires special value when
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estimating body fat, both in isolated individuals and in epidemiological groups, since
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it appears to be more sensitive than body weight, height or BMI to assess nutritional status. This way, because of its ability to assess lean and adipose tissues, BIA is
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considered a valid tool to longitudinal follow-ups. Recent researches in this area have focused on segmental bioimpedance, which
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evaluates each body limb, aiming at greater measurement precision and skeletal muscle mass assessment and working as a prognostic marker through the phase angle (PhA) and Bioelectrical impedance vector analysis (BIVA).28 When comparing patients at hospital admission to healthy control group, Kyle et al found that PhA was significantly lower in hospitalized patients than in the control
ACCEPTED MANUSCRIPT group. In this context, patients who presented lower values of PhA had longer hospital stay than 20 days.29 When investigating determinants of PhA in 770 hospitalized patients by 50KHz BIA analysis, in association with parameters of age, sex, BMI, C-reactive protein and Subjective Global Assessment (SGA), Stobäus et al observed that PhA ranged from
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1.6° to 8.4°. They concluded that PhA could be used as a prognostic parameter.30 When conducting a prospective study with 399 cancer patients, Norman et al suggested that standardized PhA is an independent predictor of nutritional imbalance, functional status and survival. The use of PhA in the 50th percentile as a
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reference, has a relevant prognostic value for cachexia risk detection in cancer. The authors found that patients with PhA below the median value had more comorbidities, significantly increased mortality risk after 6 months, and consumed
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more drugs per day, that is, they had worse nutritional and functional status, decreased quality of life, increased morbidity and shorter survival time. The PhA
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standardization according to sex, age and stratified BMI values would increase the PhA prognostic relevance, allowing the 50th percentile reference to identify patients
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who need enhanced nutritional and medical attention.31 However, PhA should be
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interpreted together with other biological parameters and the population reference values should be taken into account to identify risk groups.
32
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The use of BIVA has a potential interest in determining fluid variations in renal and ICU patients, as well as in obese individuals. Nonetheless, this emerging methodology has some limitations that deserve to be mention, such as high intervariability, no distinction between BCM and FM, nor fluid volumes quantification, thus providing only a qualitative indication of nutritional status and fluid variations.20,33,34
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Computed tomography (CT) The assessment of body composition through CT is considered a method of great accuracy to analyze body compartments. CT is an important tool to assess overall body compartments and to recognize sarcopenia patients in hospital settings since it
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allows the assessment of visceral, intramuscular, subcutaneous and skeletal muscle tissue as well as the fat infiltration into lean tissues. 35-37 Body composition assessment through CT has become a choice method in oncology, since many patients have diagnosis or staging disease follow-up images. Asking for a CT exam
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only to assess body composition is still a concern due to the radiation involved, and because of that, it is considered a convenience method. 38 However, it may be used in other clinical conditions where CT images are available, such as on patients with
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respiratory failure or trauma.38
The evaluation of a single cross-sectional image may be used to determine total
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body composition. The anatomical area commonly used as a reference is located 5 cm above the transition of the fourth and fifth lumbar vertebra (L4/L5), approximately
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at the third lumbar vertebra (L3) area.35,36
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This measure was identified to have the greatest association with muscle mass and total adipose tissue, according to Shen et al. The predictive equation available is
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useful to estimate the whole body muscle mass and total adipose tissue.6 CT also allows radiological quality assessment of the skeletal muscle area, muscle attenuation, as well as skeletal muscle index (SMI). The SMI is a representation of the L3 muscular area with the individual squared height. A study by Prado et al. identified cut-off points for L3 SMI: ♂ <52.4 cm2/m2, ♀ <38.5 cm2/m2. This cut-off point was associated with higher mortality in patients with solid tumors. 39 Another
ACCEPTED MANUSCRIPT study, Toledo et al involved 99 Brazilian critical patients and the cutoff was 41, 2 cm2/m2 for both sex.40 Despite technique advantages, it presents limitations such as radiation exposure, high cost and possible biases in the evaluation related to inadequate selection and interpretation of the patient's positioning image.37 Moreover, the need for specific
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skills regarding the technique to perform the analysis and tissue recognition must be considered. Another limitation includes images availability at the L3 and T4 (fourth thoracic vertebra) levels. The T4 images have not been validated yet.37,41 Table 3
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presents the most relevant pros and cons of this technique.
Table 3. Advantages and disadvantages of CT method Advantages (Pros) Validated cut-off values
Disadvantages (Cons) Not portable
High quantitative and qualitative accuracy
High image resolution
Able to determine tissue quality
High Precision
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High cost
Large radiation exposure
Requires technical skill for image analysis
Convenience examination
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Adapted from: Heymsfield, S.B.42
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Description of the Technique It is based on the emission and capture of x-ray bundles of internal areas of
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the body, attenuated as they pass through the tissues. From the images, which are constituted by pixels, it is possible to identify different compartments according to density, which corresponds to the mean absorption in the evaluated areas expressed in Hounsfield units (HU).35,36 Each CT image pixel presents HU as a measure of body tissue attenuation compared to water (HU water = 0; HU air = -1000). From there, it generates two-
ACCEPTED MANUSCRIPT dimensional images of the human body in cross sections, that allows the analysis of different body tissues.3,35,36 Predetermined HU scales can be used to identify body tissues and organs by quantifying muscle mass (HU = -29 to +150), subcutaneous and intramuscular
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adipose tissue (HU = -190 to -30) and visceral adipose tissue (HU = -150 to -50).35,36 The cross-sectional area (cm2) for the different tissues in each image can be determined manually or through software.35 Figure 3 shows a transversal cross-
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section of the 3rd Lumbar Vertebra with colored tissues.
Skeletal muscle
Subcutaneous adipose tissue Intramuscular adipose tissue
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Visceral adipose tissue
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Figure 3. Transverse image of abdominal segment (approximately at the time
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of L3) by computed tomography (CT)
Results of Studies Resent researches are showing that muscle mass plays an important role in clinical outcomes, and the diagnosis of sarcopenia adds a worse prognosis and shorter survival.41,43,44 A study by Tan et al found that 56% of patients with pancreatic cancer had sarcopenia.45 Other studies which used the same method applied to
ACCEPTED MANUSCRIPT gastrointestinal, pancreatic and pulmonary tumors found sarcopenia rates ranging from 15 to 56%.39,46,47 A study including 190 patients with head and neck cancer and radiotherapy observed that individuals who presented weight loss but maintained muscle mass (through CT scan) obtained better clinical outcomes.48 CT studies have also
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revealed that the presence of visceral adipose tissue is associated with unfavorable prognosis in patients with colorectal cancer, and that sarcopenic obesity condition is related with worse clinical outcomes. 35,39,46
This technique applied to investigate body composition and its alterations is an
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excellent option due to its ability to discriminate different tissues and for its use in the investigation of many diseases.43 This is relevant since early identification of risk factors, such as obesity, sarcopenia and sarcopenic obesity, will allow the detection
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of individuals with a higher nutritional risk and enable early dietary interventions.
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Dual X-ray absorptiometry (DXA)
Originally developed for measuring bone mineral density, DXA has become
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recognized for its ability to accurately and precisely measure total body composition.49 DXA is the gold standard technique in body composition analysis at
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molecular level, providing fat quantification, lean mass and bone mineral content, both in a single body region and at whole-body level.50 The latest generation densitometers allow body composition assessment with a single whole-body scanning (which means low radiation exposure and fast acquisition time).51 Due to DXA favorability in terms of accuracy, simplicity, availability and low radiation exposure, its role in sarcopenia diagnosis is becoming increasingly important,
ACCEPTED MANUSCRIPT emerging as a reference technique in muscle mass evaluation. 50 Table 4 describes advantages and disadvantages of DXA to assess body composition. Table 4. Advantages and disadvantages of DXA method Advantages (Pros)
Able to differentiate fat, lean and bone tissue
Disadvantages (Cons) Not portable
High cost
Variability of instrument calibration procedures, hardware and software version between manufacturers
Quick and noninvasive
Low radiation exposure
Possibility of obtaining regional measures
Body thickness and hydration status may influence the measurements
Safe for repeated measures
Contraindicated in pregnancy
High precision and accuracy
Inability to discriminate the different types of fat (visceral, subcutaneous and intramuscular)
Requires specific technical skills and operator experience
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Description of the Technique
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DXA is based on the physical principle of measurement of the X-ray transmission in
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human body crossing tissues at two different energy levels. The energy radiation is
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variably attenuated (absorbed or scattered) by anatomical structures, depending on energy intensity and on the human tissues density and thickness.
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Attenuation of X-ray beam decreases with increasing photon energy. Low-density materials (e.g. soft tissue) allows more photons to pass through; hence, they attenuate the X-ray beam less than materials with higher density, such as bone tissue.50 DXA estimates the R-value, which is the coefficient of ratio attenuation at two different energy levels. R-value of soft tissue varies depending on subject’s soft tissue composition (the lower are R-values, the higher is fat percentage), while it is
ACCEPTED MANUSCRIPT constant for bone and fat in all patients. Although DXA provides three body composition measurements (fat mass, lean mass and body mineral content — regionally and whole body), it does not measure directly the three components. 52-54 The quantity of fat mass (FM) and lean mass (LM) is deducted on the basis of the FM/LM calculated in neighboring bone-free pixels, assuming therefore that the fatty
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amount over bone is similar as that over the adjacent bone-free tissues.51
The latest generation densitometers allow the evaluation of body composition with a single whole-body scan (that means low radiation exposure and fast acquisition
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and very accurate and precise data.51
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time), providing high-resolution images (almost comparable to a radiological image)
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Figure 4. Image of DXA exam
Results of Studies
Some studies have demonstrated an association of a low lean mass index (LMI) with certain pathological conditions, like osteoporosis55,56 polycystic ovarian syndrome57
ACCEPTED MANUSCRIPT and chronic kidney disease.58 Body fat excess may be associated with a reduced muscle mass and/or strength (sarcopenic obesity), SMI can be useful to identify subjects with an increased risk of sarcopenic obesity or metabolic syndrome.59 DXA is well correlated with CT, MRI, and BIA
24,60
and should be considered when
quantitative body composition measurement is desired. In some circumstances,
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other body composition technologies may be superior to DXA. For example, CT and MRI offer more detailed measurements of specific regions or tissues, such as visceral adipose fat or fat infiltration among tissues.61 Although most DXA software allows a visceral adipose tissue estimation, the detail level is inferior compared to CT
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or MRI.62 Nevertheless, DXA may be preferred as the whole body is easily quantified and the radiation exposure is lower than CT.52
DXA allows appendicular skeletal muscle (ASM) mass estimation by measuring lean
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soft tissue amount in the upper and lower extremities, which is mainly composed by muscles. The ASM mass has been widely used in sarcopenia studies; indeed, low
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ASM is one of the parameters on which all the available definitions of sarcopenia
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rely.42
In most recently published sarcopenia definitions, DXA is the suggested technique
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for muscle mass assessment.56 It is emerging as a gold standard method in the sarcopenia diagnosis and characterization, since it provides an accurate and precise
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evaluation of non-bone lean mass parameters.56 Therefore, DXA can be useful in treatment planning and its follow-up by measuring muscle mass loss. The main DXA disadvantage is that the equipment is not portable, which may preclude its use in large-scale epidemiological studies or some clinical scenarios. In addition, body thickness, hydration status and diseases with water retention (e.g., heart, kidney or liver failure) can affect DXA results. 3 DXA underestimates trunk and
ACCEPTED MANUSCRIPT thigh fat mass, overestimates thigh muscle mass in obese persons, which is increased in heavier individuals.63 In contrast, DXA may overestimate muscle mass in individuals with extracellular fluid accumulation, due to its inability to distinguish water from bone-free lean tissue. Furthermore, DXA is unable to measure intramuscular adipose tissue, which interferes with muscle quality estimation. 64
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By taking all strengths and weaknesses into consideration, DXA may be considered the current reference technique for assessing muscle mass and body composition in research and clinical practices.65
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Conclusions
All the methods shown are cutting-edge technology in terms of body composition
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assessment and can be very useful considering the exposed pros and cons and hence, contribute to increasing knowledge and for monitoring nutritional interventions
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introduced during the treatments, information summarized in the table 5. The use of
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US to assess body composition is featured by the ease and cost of the examination. The CT is adding knowledge to the oncological patient and sarcopenia fields. BIA
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can be used as a prognostic and assessment body composition tool. The DXA method is of great value to the study of sarcopenia. However, further studies are
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needed to fill the limitations imposed by each method.
Table 5. Comparative evaluation of the methods exposed.
Characteristic
US
BIA
CT
DXA
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Broad Spectrum
Notintubated
Not utilized exclusively to body composition assessment due to radiation exposition
Intubated
+
+
++
++
+++ +++
++ +++
No
Pregnant
Low-Cost
+++
+++
Safeness
+++
+++
Replicability Accuracy
++ ++
++ ++
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Contraindication
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Broad Spectrum
Population
Cancer; abdominal surgery. Patients that already possess the exam.
BIA, Bioelectrical impedance analysis; CT, Computed tomography; DXA, Dual X-ray absorptiometry; US, Bedside ultrasonography. Redrawn from: Guglielmi, G, 2016 50
Vincent JL. Critical care--where have we been and where are we going? Crit Care. 2013;17 Suppl 1:S2.
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References
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2. Sheean PM, Peterson SJ, Gurka DP, Braunschweig CA. Nutrition assessment: the reproducibility of subjective global assessment in patients requiring mechanical ventilation. European journal of clinical nutrition. 2010;64(11):1358-1364.
Utter AC, Hager ME. Evaluation of ultrasound in assessing body composition of high school wrestlers. Med Sci Sports Exerc. 2008;40(5):943-949.
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4.
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3. Prado CM, Heymsfield SB. Lean tissue imaging: a new era for nutritional assessment and intervention. JPEN Journal of parenteral and enteral nutrition. 2014;38(8):940-953.
5. Ferrie S, Allman-Farinelli M, Daley M, Smith K. Protein Requirements in the Critically Ill: A Randomized Controlled Trial Using Parenteral Nutrition. JPEN Journal of parenteral and enteral nutrition. 2016;40(6):795-805. 6. Tillquist M, Kutsogiannis DJ, Wischmeyer PE, et al. Bedside ultrasound is a practical and reliable measurement tool for assessing quadriceps muscle layer thickness. JPEN Journal of parenteral and enteral nutrition. 2014;38(7):886-890. 7. Paris MT, Mourtzakis M, Day A, et al. Validation of Bedside Ultrasound of Muscle Layer Thickness of the Quadriceps in the Critically Ill Patient (VALIDUM Study). JPEN Journal of parenteral and enteral nutrition. 2017;41(2):171-180.
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Reid CL, Campbell IT, Little RA. Muscle wasting and energy balance in critical illness. Clin Nutr. 2004;23(2):273-280.
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16. Parry SM, El-Ansary D, Cartwright MS, et al. Ultrasonography in the intensive care setting can be used to detect changes in the quality and quantity of muscle and is related to muscle strength and function. Journal of critical care. 2015;30(5):1151 e1159-1114.
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18. Santos D, Freitas B, Carneiro D, Piovacari S, Figueiredo E, Toledo D. Protein intake guided by the quadriceps muscle ultrasound in a patient with GBS: case report. Crit Care. 2017;21(Suppl 2).
19. Bohm A, Heitmann BL. The use of bioelectrical impedance analysis for body composition in epidemiological studies. European journal of clinical nutrition. 2013;67 Suppl 1:S79-85. 20. Buffa R, Mereu E, Succa V, Latini V, Marini E. Specific BIVA recognizes variation of body mass and body composition: Two related but different facets of nutritional status. Nutrition. 2017;35:1-5. 21.
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ACCEPTED MANUSCRIPT 22. Earthman CP. Body Composition Tools for Assessment of Adult Malnutrition at the Bedside: A Tutorial on Research Considerations and Clinical Applications. JPEN Journal of parenteral and enteral nutrition. 2015;39(7):787-822. 23. Bosaeus I, Wilcox G, Rothenberg E, Strauss BJ. Skeletal muscle mass in hospitalized elderly patients: comparison of measurements by single-frequency BIA and DXA. Clin Nutr. 2014;33(3):426-431. 24.
Tewari N, Awad S, Macdonald IA, Lobo DN. A comparison of three methods to assess body composition. Nutrition. 2018;47:1-5.
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25. Deurenberg P. Limitations of the bioelectrical impedance method for the assessment of body fat in severe obesity. The American journal of clinical nutrition. 1996;64(Suppl 3 ):449S-452S. 26. Haverkort EB, Reijven PL, Binnekade JM, et al. Bioelectrical impedance analysis to estimate body composition in surgical and oncological patients: a systematic review. European journal of clinical nutrition. 2015;69(1):3-13.
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27. Moon JR, Stout JR, Smith-Ryan AE, et al. Tracking fat-free mass changes in elderly men and women using single-frequency bioimpedance and dual-energy X-ray absorptiometry: a four-compartment model comparison. European journal of clinical nutrition. 2013;67 Suppl 1:S40-46.
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28. Buffa R, Mereu E, Comandini O, Ibanez ME, Marini E. Bioelectrical impedance vector analysis (BIVA) for the assessment of two-compartment body composition. European journal of clinical nutrition. 2014;68(11):1234-1240.
Stobaus N, Pirlich M, Valentini L, Schulzke JD, Norman K. Determinants of bioelectrical phase angle in disease. The British journal of nutrition. 2012;107(8):1217-1220.
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29. Kyle UG, Soundar EP, Genton L, Pichard C. Can phase angle determined by bioelectrical impedance analysis assess nutritional risk? A comparison between healthy and hospitalized subjects. Clin Nutr. 2012;31(6):875-881.
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31. Norman K, Stobaus N, Zocher D, et al. Cutoff percentiles of bioelectrical phase angle predict functionality, quality of life, and mortality in patients with cancer. The American journal of clinical nutrition. 2010;92(3):612-619.
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32. Paiva SI, Borges LR, Halpern-Silveira D, Assuncao MC, Barros AJ, Gonzalez MC. Standardized phase angle from bioelectrical impedance analysis as prognostic factor for survival in patients with cancer. Supportive care in cancer : official journal of the Multinational Association of Supportive Care in Cancer. 2010;19(2):187-192. 33.
Kyle UG, Bosaeus I, De Lorenzo AD, et al. Bioelectrical impedance analysispart II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430-1453.
34. Pineda-Juárez JA, Lozada-Mellado M, Ogata-Medel M, et al. Body composition evaluated by body mass index and bioelectrical impedance vectorial analysis in women with rheumatoid arthritis. Nutrition. 2018;Article in press.
ACCEPTED MANUSCRIPT 35. Yip C, Dinkel C, Mahajan A, Siddique M, Cook GJ, Goh V. Imaging body composition in cancer patients: visceral obesity, sarcopenia and sarcopenic obesity may impact on clinical outcome. Insights Imaging. 2015;6(4):489-497. 36. Fosbol MO, Zerahn B. Contemporary methods of body composition measurement. Clinical physiology and functional imaging. 2015;35(2):81-97. 37. Prado CM, Birdsell LA, Baracos VE. The emerging role of computerized tomography in assessing cancer cachexia. Curr Opin Support Palliat Care. 2009;3(4):269-275.
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38. Aubrey J, Esfandiari N, Baracos VE, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol (Oxf). 2014;210(3):489-497.
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39. Prado CM, Lieffers JR, McCargar LJ, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9(7):629635. 40. Toledo DO, Carvalho AM, Oliveira A, et al. The use of computed tomography images as a prognostic marker in critically ill cancer patients. Clin Nutr ESPEN. 2018;25:114-120.
Heymsfield SB, Adamek M, Gonzalez MC, Jia G, Thomas DM. Assessing skeletal muscle mass: historical overview and state of the art. J Cachexia Sarcopenia Muscle. 2014;5(1):9-18.
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41. Wysham NG, Nipp RD, LeBlanc TW, Wolf SP, Ekstrom MP, Currow DC. A practical measurement of thoracic sarcopenia: correlation with clinical parameters and outcomes in advanced lung cancer. ERJ Open Res. 2016;2(2).
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43. Baracos V, Caserotti P, Earthman CP, et al. Advances in the science and application of body composition measurement. JPEN Journal of parenteral and enteral nutrition. 2012;36(1):96-107.
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44. Martin L, Birdsell L, Macdonald N, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31(12):1539-1547.
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45. Tan BH, Birdsell LA, Martin L, Baracos VE, Fearon KC. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clinical cancer research : an official journal of the American Association for Cancer Research. 2009;15(22):6973-6979. 46. Cooper AB, Slack R, Fogelman D, et al. Characterization of Anthropometric Changes that Occur During Neoadjuvant Therapy for Potentially Resectable Pancreatic Cancer. Ann Surg Oncol. 2015;22(7):2416-2423. 47. Moryoussef F, Dhooge M, Volet J, et al. Reversible sarcopenia in patients with gastrointestinal stromal tumor treated with imatinib. J Cachexia Sarcopenia Muscle. 2015;6(4):343-350.
ACCEPTED MANUSCRIPT 48. Grossberg AJ, Chamchod S, Fuller CD, et al. Association of Body Composition With Survival and Locoregional Control of Radiotherapy-Treated Head and Neck Squamous Cell Carcinoma. JAMA Oncol. 2016;2(6):782-789. 49. Marinangeli CP, Kassis AN. Use of dual X-ray absorptiometry to measure body mass during short- to medium-term trials of nutrition and exercise interventions. Nutrition reviews. 2013;71(6):332-342. 50.
Guglielmi G, Ponti F, Agostini M, Amadori M, Battista G, Bazzocchi A. The role of DXA in sarcopenia. Aging Clin Exp Res. 2016;28(6):1047-1060.
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51. Bazzocchi A, Diano D, Ponti F, et al. A 360-degree overview of body composition in healthy people: relationships among anthropometry, ultrasonography, and dual-energy x-ray absorptiometry. Nutrition. 2014;30(6):696-701. 52. Kendler DL, Borges JL, Fielding RA, et al. The Official Positions of the International Society for Clinical Densitometry: Indications of Use and Reporting of DXA for Body Composition. J Clin Densitom. 2013;16(4):496-507.
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53. Bazzocchi A, Ponti F, Cariani S, et al. Visceral fat and body composition changes in a female population after RYGBP: a two-year follow-up by DXA. Obes Surg. 2015;25(3):443-451. Bazzocchi A, Diano D. Dual-energy x-ray absorptiometry in obesity. CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne. 2014;186(1):48.
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55. Rikkonen T, Sirola J, Salovaara K, et al. Muscle strength and body composition are clinical indicators of osteoporosis. Calcif Tissue Int. 2012;91(2):131138.
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56. Goulding A, Taylor RW, Grant AM, Jones S, Taylor BJ, Williams SM. Relationships of appendicular LMI and total body LMI to bone mass and physical activity levels in a birth cohort of New Zealand five-year olds. Bone. 2009;45(3):455459.
Han SS, Heo NJ, Na KY, et al. Age- and gender-dependent correlations between body composition and chronic kidney disease. Am J Nephrol. 2010;31(1):83-89.
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57. Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Nagata Y. Serum androgen levels and muscle mass in women with polycystic ovary syndrome. Obstet Gynecol. 1999;94(3):337-340.
59. Kim TN, Yang SJ, Yoo HJ, et al. Prevalence of sarcopenia and sarcopenic obesity in Korean adults: the Korean sarcopenic obesity study. Int J Obes (Lond). 2009;33(8):885-892.
60. Xu L, Cheng X, Wang J, et al. Comparisons of body-composition prediction accuracy: a study of 2 bioelectric impedance consumer devices in healthy Chinese persons using DXA and MRI as criteria methods. J Clin Densitom. 2011;14(4):458464.
ACCEPTED MANUSCRIPT 61. Woodrow G. Body composition analysis techniques in the aged adult: indications and limitations. Current opinion in clinical nutrition and metabolic care. 2009;12(1):8-14. 62.
Micklesfield LK, Goedecke JH, Punyanitya M, Wilson KE, Kelly TL. Dualenergy X-ray performs as well as clinical computed tomography for the measurement of visceral fat. Obesity (Silver Spring). 2012;20(5):1109-1114.
Bredella MA, Ghomi RH, Thomas BJ, et al. Comparison of DXA and CT in the assessment of body composition in premenopausal women with obesity and anorexia nervosa. Obesity (Silver Spring). 2010;18(11):2227-2233.
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64. Proctor DN, O'Brien PC, Atkinson EJ, Nair KS. Comparison of techniques to estimate total body skeletal muscle mass in people of different age groups. The American journal of physiology. 1999;277(3 Pt 1):E489-495. Tosato M, Marzetti E, Cesari M, et al. Measurement of muscle mass in sarcopenia: from imaging to biochemical markers. Aging Clin Exp Res. 2017;29(1):19-27.
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Current technologies in body composition assessment: advantages and disadvantages Guilherme Duprat Ceniccola RD, PhD. , Melina Gouveia Castro MD, PhD. , Silvia Maria Fraga Piovacari RD. , Lilian Mika Horie RD, Msc. , Fabiano Girade Correa ˆ MD. , Ana Paula Noronha Barrere RD. Msc. , Diogo Oliveira Toledo MD. Msc. PII: DOI: Reference:
S0899-9007(18)31318-2 https://doi.org/10.1016/j.nut.2018.11.028 NUT 10409
To appear in:
Nutrition
Received date: Revised date: Accepted date:
3 March 2018 14 September 2018 14 November 2018
Please cite this article as: Guilherme Duprat Ceniccola RD, PhD. , Melina Gouveia Castro MD, PhD. , Silvia Maria Fraga Piovacari RD. , Lilian Mika Horie RD, Msc. , Fabiano Girade Correa ˆ MD. , Ana Paula Noronha Barrere RD. Msc. , Diogo Oliveira Toledo MD. Msc. , Current technologies in body composition assessment: advantages and disadvantages, Nutrition (2018), doi: https://doi.org/10.1016/j.nut.2018.11.028
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Highlights: Bedside ultrasonography has emerged as a common method to quantify muscle mass. Main limitations of the method are lack of cut-off points to do diagnoses, paucity of clinical protocols and agreement on its use and imprecision under excessive edema situations.
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Bioelectrical impedance analysis is a widely used method to estimate body composition in different clinical conditions, such as cancer, obesity, sarcopenia and elderly it main limitations are because it is an Indirect method, is limited by
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hydration status and demands Specific equation for each population.
The assessment of body composition through Computed tomography is considered a method of great accuracy to analyze body compartments. It is limited by non-portability, high cost, radiation exposure and trained personnel
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requirements.
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Originally developed for measuring bone mineral density, Dual X-ray absorptiometry has become recognized for its ability to accurately and
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precisely measure total body composition. It main limitation is due to non-
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portability, high cost, trained personnel requirements and inability to discriminate
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the different types of fat.
ACCEPTED MANUSCRIPT Current technologies in body composition assessment: advantages and disadvantages
Guilherme Duprat Ceniccola, RD, PhD. E-mail: [email protected]
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Departmental contact: Instituto Hospital de Base. Address: MHS Q 101, Brasília-DF, Brazil, Zip code 7033000. Phone 55 61 32455302, 55 61 992340657. Permanent Address: SQS 314 Bl I apt 605, Brasília - DF, Brazil. Zip code: 70383-090
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Melina Gouveia Castro, MD, PhD. Email: [email protected]
Departamental contact: Faculdade de Medicina da Universidade de São Paulo. Av. Dr. Arnaldo, 455 - Cerqueira César, São Paulo - SP,
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Zip code: 01246-903
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Silvia Maria Fraga Piovacari, RD. Email: [email protected]
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Departmental contact: Department of Clinical Nutrition, Hospital Israelita Albert Einstein. Address: Av. Albert Einstein, 627/701 – Morumbi - São Paulo - SP, Brazil.
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Zip code: 05652-900.
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Lilian Mika Horie, RD, Msc. Email: [email protected] Departamental contact: Faculdade de Medicina da Universidade de São Paulo. Av. Dr. Arnaldo, 455 - Cerqueira César, São Paulo - SP, Zip code: 01246-903 Fabiano Girade Corrêa, MD. Email: [email protected]
ACCEPTED MANUSCRIPT Departmental contact: Hospital Santa Lúcia. Address: SHLS Condomínio do Centro Medico de Brasília - Brasília, DF, Brazil. zip code: 70297-400 Ana Paula Noronha Barrere, RD. Msc. Email: [email protected] Departmental contact: Department of Clinical Nutrition, Hospital Israelita Albert Einstein Address: Av. Albert Einstein, 627/701 - Morumbi, São Paulo - SP, Brazil. Zip
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code: 05652-900
Diogo Oliveira Toledo, MD. Msc. Email: [email protected]
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Departmental contact: Department of Critical Care, Hospital Israelita Albert Einstein Address: Av. Albert Einstein, 627/701, Morumbi - São Paulo - SP, Brazil. Zip code 05652-900.
Abstract
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The interest in non-invasive methods of body composition assessment is at rise in the health care scenario, especially due to its association to clinical outcomes. Technology has revolutionized our understanding of body composition abnormalities, clinical prognostication and disease follow-up, but translation to bedside is limited, especially in the costeffectiveness view point. Computed tomography gained increased attention in cancer and sarcopenia studies for instance. Other methods have also interesting features and applications, which includes Bedside ultrasonography, Bioelectrical impedance analysis and Dual X-ray absorptiometry. Compelling evidence is highlights these methods to accurately and precisely measure skeletal muscle mass, adipose tissue, edema, diagnose malnutrition related diseases and prognostic tool measuring. To apply this technology properly, it is demanding the understanding about the advantages and disadvantages that pertain each technique in specific situations of interest. This way, this review introduces concepts and reference studies published in the scientific literature about Bedside ultrasonography, Bioelectrical impedance analysis, Computed Tomography and Dual X-ray absorptiometry, mentions important limitations and considerations to be done in order to bring those methods to the practical field. Keywords Body composition, Bedside ultrasonography, Bioelectrical impedance analysis, Computed Tomography and Dual X-ray absorptiometry
ACCEPTED MANUSCRIPT Introduction The need for accurate methods to assess body composition as a diagnostic and prognostic tool is coupled with the introduction of quality concepts and the improvements in hospital routines, which involves the translation of new technologies and procedures to practice field. Regarding to health care, in the recent past, more
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invasive interventions were prioritized, such as mechanical ventilation, catheter monitoring and heavy sedation. Nowadays, interventions are based on less invasive and safer techniques, replicable diagnostic methods, pros and cons related to the target population and situation of concern. It is this cost-effective, less invasive and
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replicable context that fits body composition assessment into the current clinical scenario.1
Additionally, the conventional methods used for nutritional diagnosis (anthropometry,
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biochemical tests, physical examination and dietary parameters) are weakly associated to body components estimations such as skeletal muscle, adipose tissue
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and body water. For instance, the sarcopenia’s definition is one of the most debated
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topics considering body composition and several cut points using different methodologies have been proposed. Body mass index (BMI), one of the most
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widespread measures, falls short regarding to association with these body components and sarcopenia.2
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To fulfill this gap, accurate and noninvasive techniques are important to assess body composition and to diagnose diseases related to malnutrition, sarcopenia and frailty, and also to guide rehabilitation of hospitalized patients, which may save resources and promote better clinical outcomes.3 As examples of these techniques, ultrasonography
(US),
Bioelectrical
impedance
analysis
(BIA),
Computed
Tomography (CT) and dual X-ray absorptiometry (DXA) will be addressed and
ACCEPTED MANUSCRIPT compared on a body composition assessment bases. This review aims to present the current techniques used in the evaluation of body composition concerning to its advantages and disadvantages to the hospitalized patient.
Bedside ultrasonography (US)
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The use of ultrasound to assess body composition has increased in daily practices, motivated by validation studies.4 Ultrasound has emerged as a common method to quantify muscle mass and it has recently caught a lot of attention with the growing importance of the skeletal muscle role in the recovery process.5 In 2014,
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Tillquist et al, showed that the technique had an excellent reliability between trainer and trainee when applied to healthy volunteers.6 Paris et al, demonstrated in a multicenter study that this technique is also applicable to critically ill patients with
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satisfactory intra and inter-rater reliability, and even more, to assess longitudinal changes in muscles.7
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In addition, muscle mass measurement by US has shown to be a reliable
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technique in most patients, even when fluid retention is present. 8,9 In chronic obstructive pulmonary disease, the US quadriceps musculature measurement
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proved to be effective in identifying patients with greater muscle loss during hospitalization.10
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Currently, the US technique has not been capable of diagnosing sarcopenia yet, for the lack of recent studies identifying a cutoff value or a theoretical protocol. However, some studies were able to show different baseline values of skeletal muscles between men and women of different age groups.11,12 Puthucheary et al by compared three methods: US, muscle biopsy and molecular biology. This study revealed a significant 10% reduction of rectus femoris muscle, measured by the US,
ACCEPTED MANUSCRIPT during the first 7 days in intensive care units (ICU).13 A similar result was also found in a Brazilian study with critically ill patients, which presented approximately 1.5% loss of quadriceps thickness per day, assessed by the US. 14 Table 1 describes the advantages and disadvantages of US for muscle mass assessment.
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Table 1. Advantages and disadvantages of US method Advantages (Pros)
Disadvantages (Cons)
Portable
Lack of cut-off points to do diagnoses
Low cost
Paucity of clinical protocols and agreement on its use
Satisfactory reliability intra and inter rater
Safe for repeated measures
Limited by excessive edema situations
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Noninvasive
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Description of the Technique
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Assess longitudinal changes in muscles
Body skeletal muscle can be estimated using ultrasound imaging with
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different protocols, what comprises the use of one or more anatomical sites. 15 Two
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main reference methods of measuring have been reported to quantify wasting: (a) measuring quadriceps muscle layer thickness (QMLT), combined thickness of the
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rectus femoris (RF) and vastus intermedius muscles. The QMLT was quantified using onscreen calipers and taken as the distance between the upper margin of the femoral bone and the lower boundary of the deep fascia of the rectus femoris (Figure 1)6,8,14,16 and (b) rectus femoris cross-sectional area, where scanning depth was quantified and set to where the femur could be distinguished for orientation. RF CSA was calculated by a planimetric technique (by US) after the inner echogenic line of the rectus femoris was outlined by a movable cursor on a frozen image (figure 2).10
ACCEPTED MANUSCRIPT Both techniques were effective in demonstrating muscle loss in hospitalized patients, but CSA was better at demonstrating muscle strength measurements. 17 Although the ultrasound measurements providers will be able to assess muscle wasting longitudinally, it does not provide a whole-body composition
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assessment and may be useless in a single assessment.15
Figure 1. Quadriceps muscle layer thickness
Figure 2. Rectus femoris CSA
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Results of Studies
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RF: rectus femoris; VL: vastus lateralis; VM: vastus medialis; VI: vastus intermedius.
US studies applied in hospitalized patients reveal that those who lose more muscle
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mass may present worse outcomes during hospitalization.10,13 In a longitudinal study
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comprising 1-year follow-up after hospital discharge, patients with chronic respiratory disease classified in the lower quartile of the quadriceps muscle size, had a higher mortality rate compared with patients classified in the upper quartile. In addition, a smaller quadriceps muscle size measured by US is an independent risk factor for readmission.10 In a population of critically ill patients, muscle loss assessed by crosssectional area technique was associated with increased organic dysfunction and inflammation 7 days after ICU admission.13 Parry et al, demonstrated a strong
ACCEPTED MANUSCRIPT association between quadriceps muscle architecture and strength, and function measurements at ICU discharge. 16 This tool can also be used to track muscle atrophy allowing nutrient delivery calculation and rehabilitative interventions. This way, US assessment could guide not only nutritional diagnosis but its consequent intervention. 15 A case study which
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used the US as a guide to optimize protein supply, showed good correlation between increased protein intake, muscle thickness gain and consequent nitrogen balance improvement.18 Other studies which applied that technique revealed an association between muscle mass loss and worse outcomes during hospitalization. 10,13
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Broad validation protocols comparing ultrasound to reference techniques still need to be undertaken, special in the critically ill patient with edematous areas that the muscle wasting may occur without changes in QMLT, were water content could
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affect measurements. Future research will aim to address these questions, for example, measuring severe edematous patients with maximum ultrasound
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compression protocols could be an alternative to explore.
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Overall, the US provides precise and reliable measures of muscle stores and potential changes in muscle mass and adipose tissue. In order to optimize its
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capabilities, further work is needed to comprehensively understand its limitations
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related to excessive edema situations and disease diagnosis, and also to unify clinical usage protocols.
Bioelectrical impedance analysis (BIA) The BIA is a widely used method to estimate body composition in different clinical conditions, such as cancer, obesity, sarcopenia and elderly.19,20 Several BIA devices are available in the market and can be classified based on the
ACCEPTED MANUSCRIPT number of electrical frequencies: single-frequency (SF-BIA) and multifrequential (MF-BIA).21 In general, the precision level produced by SF-BIA and MF-BIA devices is usually very good, 1-2% of variability between repeated measures.21 Precision and accuracy of BIA devices are influenced by a several factors, including: patient ( adiposity degree, fluid and electrolyte status, skin temperature) and environmental
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factors (ambient temperature, proximity to metal surfaces and electronic devices), assumptions underlying prediction (SF-BIA or MF-BIA), instrumentation factors, and variations in measurement protocols.22 Table 2 shows BIA's advantages and
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disadvantages.
Table 2. Advantage and disadvantage of BIA method Advantages (Pros)
Disadvantages (Cons)
Portable
Indirect method Limited by hydration status - Fat free
Quick and noninvasive Very simple and reproducible
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Low cost
mass hydration fixed in 73%
Specific equation needed for each population
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Safe for repeated measures
Description of the Technique
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The simplest way to estimate body composition through BIA is by using the bicompartmental model, which analyzes the body's lean mass and fat mass content.
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More accurate results are obtained when each specific population is assessed by its own equation.23 BIA devices do not directly measure body composition; they provide indirect estimates from resistance measurement of body tissues to an electric current. Besides, some assumptions have to be considered to use BIA for body composition:
ACCEPTED MANUSCRIPT 1. The human body is divides into five cylinders; trunk, upper and lower extremities, with a uniform electric conductivity; 2. FFM contains virtually all the water and conducting electrolytes in the body; 3. FFM hydration is constant; 4. Conductive length is conventionally considered stature.
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The BIA use for body composition assessment is carried out through the electric current passage in low intensity (500-800 mA) and high frequency (50 kHz), measuring the primary components: Resistance (R), Reactance (Xc), Impedance (Z) and Phase Angle (PhA).
22,23
This technique assesses total body water and, by
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assuming a constant hydration, can predict the amount of the fat free mass (FFM). The FFM is calculated from the TBW, using the assumption that 73% of the FFM is water in adults. However, the 73.2% reference factor for the water content of FFM
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results in an overestimation of FFM and underestimation of FM in children who have 75–76% water for the FFM. Therefore, changes in the hydration state are the main
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Results of Studies
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limitation of this method.21
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A recent study comparing the use of BIA, CT and DXA in surgical patients recognized the importance of BIA, especially because of its cost-effectiveness. The
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advantages of BIA compared to those two gold standard methods are the portability of the device, ease of use, affordability and non-invasiveness technique. When comparing accuracy, the fat free mass results between BIA and DXA reached r2=0.6275 (p<0.0001) and between BIA and CT it reached r2=0.274 (p-0,0001), which is a satisfactory result considering clinical and research settings. 23,24 Deurenberg evaluated the body composition of 661 people of different weights and BMI. The differences observed in body cell mass (BCM) and body fat mass (FM)
ACCEPTED MANUSCRIPT estimated by DXA and BIA, respectively, were higher in people with BMI <18 kg/m 2 and >34 kg/m2. In these cases, BIA overestimated lean cell mass amount in both super-obese and low-weight individuals, and underestimated body fat in extremely obese individuals.25 In studies with healthy individuals, BIA assessment achieved 3-5% accuracy
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compared to different gold standard methods (air-displacement plethysmography, DXA, MRI - Magnetic Resonance Imaging and CT). On the other hand, a recent systematic review published by Haverkort et al concluded that the BIA use in surgical and oncological patients reached low precision (underestimated total body water,
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which ranged between −18.8% to +7.2% and fat free mass, which ranged between −15.2% to +3.8%), suggesting that BIA estimations should be performed and interpreted longitudinally.26
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The use of BIA to monitor longitudinal changes in body composition below 5 kg should be interpreted with caution.27 Moreover, BIA acquires special value when
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estimating body fat, both in isolated individuals and in epidemiological groups, since
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it appears to be more sensitive than body weight, height or BMI to assess nutritional status. This way, because of its ability to assess lean and adipose tissues, BIA is
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considered a valid tool to longitudinal follow-ups. Recent researches in this area have focused on segmental bioimpedance, which
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evaluates each body limb, aiming at greater measurement precision and skeletal muscle mass assessment and working as a prognostic marker through the phase angle (PhA) and Bioelectrical impedance vector analysis (BIVA).28 When comparing patients at hospital admission to healthy control group, Kyle et al found that PhA was significantly lower in hospitalized patients than in the control
ACCEPTED MANUSCRIPT group. In this context, patients who presented lower values of PhA had longer hospital stay than 20 days.29 When investigating determinants of PhA in 770 hospitalized patients by 50KHz BIA analysis, in association with parameters of age, sex, BMI, C-reactive protein and Subjective Global Assessment (SGA), Stobäus et al observed that PhA ranged from
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1.6° to 8.4°. They concluded that PhA could be used as a prognostic parameter.30 When conducting a prospective study with 399 cancer patients, Norman et al suggested that standardized PhA is an independent predictor of nutritional imbalance, functional status and survival. The use of PhA in the 50th percentile as a
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reference, has a relevant prognostic value for cachexia risk detection in cancer. The authors found that patients with PhA below the median value had more comorbidities, significantly increased mortality risk after 6 months, and consumed
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more drugs per day, that is, they had worse nutritional and functional status, decreased quality of life, increased morbidity and shorter survival time. The PhA
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standardization according to sex, age and stratified BMI values would increase the PhA prognostic relevance, allowing the 50th percentile reference to identify patients
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who need enhanced nutritional and medical attention.31 However, PhA should be
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interpreted together with other biological parameters and the population reference values should be taken into account to identify risk groups.
32
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The use of BIVA has a potential interest in determining fluid variations in renal and ICU patients, as well as in obese individuals. Nonetheless, this emerging methodology has some limitations that deserve to be mention, such as high intervariability, no distinction between BCM and FM, nor fluid volumes quantification, thus providing only a qualitative indication of nutritional status and fluid variations.20,33,34
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Computed tomography (CT) The assessment of body composition through CT is considered a method of great accuracy to analyze body compartments. CT is an important tool to assess overall body compartments and to recognize sarcopenia patients in hospital settings since it
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allows the assessment of visceral, intramuscular, subcutaneous and skeletal muscle tissue as well as the fat infiltration into lean tissues. 35-37 Body composition assessment through CT has become a choice method in oncology, since many patients have diagnosis or staging disease follow-up images. Asking for a CT exam
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only to assess body composition is still a concern due to the radiation involved, and because of that, it is considered a convenience method. 38 However, it may be used in other clinical conditions where CT images are available, such as on patients with
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respiratory failure or trauma.38
The evaluation of a single cross-sectional image may be used to determine total
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body composition. The anatomical area commonly used as a reference is located 5 cm above the transition of the fourth and fifth lumbar vertebra (L4/L5), approximately
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at the third lumbar vertebra (L3) area.35,36
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This measure was identified to have the greatest association with muscle mass and total adipose tissue, according to Shen et al. The predictive equation available is
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useful to estimate the whole body muscle mass and total adipose tissue.6 CT also allows radiological quality assessment of the skeletal muscle area, muscle attenuation, as well as skeletal muscle index (SMI). The SMI is a representation of the L3 muscular area with the individual squared height. A study by Prado et al. identified cut-off points for L3 SMI: ♂ <52.4 cm2/m2, ♀ <38.5 cm2/m2. This cut-off point was associated with higher mortality in patients with solid tumors. 39 Another
ACCEPTED MANUSCRIPT study, Toledo et al involved 99 Brazilian critical patients and the cutoff was 41, 2 cm2/m2 for both sex.40 Despite technique advantages, it presents limitations such as radiation exposure, high cost and possible biases in the evaluation related to inadequate selection and interpretation of the patient's positioning image.37 Moreover, the need for specific
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skills regarding the technique to perform the analysis and tissue recognition must be considered. Another limitation includes images availability at the L3 and T4 (fourth thoracic vertebra) levels. The T4 images have not been validated yet.37,41 Table 3
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presents the most relevant pros and cons of this technique.
Table 3. Advantages and disadvantages of CT method Advantages (Pros) Validated cut-off values
Disadvantages (Cons) Not portable
High quantitative and qualitative accuracy
High image resolution
Able to determine tissue quality
High Precision
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High cost
Large radiation exposure
Requires technical skill for image analysis
Convenience examination
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Adapted from: Heymsfield, S.B.42
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Description of the Technique It is based on the emission and capture of x-ray bundles of internal areas of
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the body, attenuated as they pass through the tissues. From the images, which are constituted by pixels, it is possible to identify different compartments according to density, which corresponds to the mean absorption in the evaluated areas expressed in Hounsfield units (HU).35,36 Each CT image pixel presents HU as a measure of body tissue attenuation compared to water (HU water = 0; HU air = -1000). From there, it generates two-
ACCEPTED MANUSCRIPT dimensional images of the human body in cross sections, that allows the analysis of different body tissues.3,35,36 Predetermined HU scales can be used to identify body tissues and organs by quantifying muscle mass (HU = -29 to +150), subcutaneous and intramuscular
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adipose tissue (HU = -190 to -30) and visceral adipose tissue (HU = -150 to -50).35,36 The cross-sectional area (cm2) for the different tissues in each image can be determined manually or through software.35 Figure 3 shows a transversal cross-
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section of the 3rd Lumbar Vertebra with colored tissues.
Skeletal muscle
Subcutaneous adipose tissue Intramuscular adipose tissue
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Visceral adipose tissue
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Figure 3. Transverse image of abdominal segment (approximately at the time
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of L3) by computed tomography (CT)
Results of Studies Resent researches are showing that muscle mass plays an important role in clinical outcomes, and the diagnosis of sarcopenia adds a worse prognosis and shorter survival.41,43,44 A study by Tan et al found that 56% of patients with pancreatic cancer had sarcopenia.45 Other studies which used the same method applied to
ACCEPTED MANUSCRIPT gastrointestinal, pancreatic and pulmonary tumors found sarcopenia rates ranging from 15 to 56%.39,46,47 A study including 190 patients with head and neck cancer and radiotherapy observed that individuals who presented weight loss but maintained muscle mass (through CT scan) obtained better clinical outcomes.48 CT studies have also
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revealed that the presence of visceral adipose tissue is associated with unfavorable prognosis in patients with colorectal cancer, and that sarcopenic obesity condition is related with worse clinical outcomes. 35,39,46
This technique applied to investigate body composition and its alterations is an
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excellent option due to its ability to discriminate different tissues and for its use in the investigation of many diseases.43 This is relevant since early identification of risk factors, such as obesity, sarcopenia and sarcopenic obesity, will allow the detection
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of individuals with a higher nutritional risk and enable early dietary interventions.
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Dual X-ray absorptiometry (DXA)
Originally developed for measuring bone mineral density, DXA has become
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recognized for its ability to accurately and precisely measure total body composition.49 DXA is the gold standard technique in body composition analysis at
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molecular level, providing fat quantification, lean mass and bone mineral content, both in a single body region and at whole-body level.50 The latest generation densitometers allow body composition assessment with a single whole-body scanning (which means low radiation exposure and fast acquisition time).51 Due to DXA favorability in terms of accuracy, simplicity, availability and low radiation exposure, its role in sarcopenia diagnosis is becoming increasingly important,
ACCEPTED MANUSCRIPT emerging as a reference technique in muscle mass evaluation. 50 Table 4 describes advantages and disadvantages of DXA to assess body composition. Table 4. Advantages and disadvantages of DXA method Advantages (Pros)
Able to differentiate fat, lean and bone tissue
Disadvantages (Cons) Not portable
High cost
Variability of instrument calibration procedures, hardware and software version between manufacturers
Quick and noninvasive
Low radiation exposure
Possibility of obtaining regional measures
Body thickness and hydration status may influence the measurements
Safe for repeated measures
Contraindicated in pregnancy
High precision and accuracy
Inability to discriminate the different types of fat (visceral, subcutaneous and intramuscular)
Requires specific technical skills and operator experience
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Description of the Technique
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DXA is based on the physical principle of measurement of the X-ray transmission in
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human body crossing tissues at two different energy levels. The energy radiation is
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variably attenuated (absorbed or scattered) by anatomical structures, depending on energy intensity and on the human tissues density and thickness.
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Attenuation of X-ray beam decreases with increasing photon energy. Low-density materials (e.g. soft tissue) allows more photons to pass through; hence, they attenuate the X-ray beam less than materials with higher density, such as bone tissue.50 DXA estimates the R-value, which is the coefficient of ratio attenuation at two different energy levels. R-value of soft tissue varies depending on subject’s soft tissue composition (the lower are R-values, the higher is fat percentage), while it is
ACCEPTED MANUSCRIPT constant for bone and fat in all patients. Although DXA provides three body composition measurements (fat mass, lean mass and body mineral content — regionally and whole body), it does not measure directly the three components. 52-54 The quantity of fat mass (FM) and lean mass (LM) is deducted on the basis of the FM/LM calculated in neighboring bone-free pixels, assuming therefore that the fatty
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amount over bone is similar as that over the adjacent bone-free tissues.51
The latest generation densitometers allow the evaluation of body composition with a single whole-body scan (that means low radiation exposure and fast acquisition
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and very accurate and precise data.51
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time), providing high-resolution images (almost comparable to a radiological image)
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Figure 4. Image of DXA exam
Results of Studies
Some studies have demonstrated an association of a low lean mass index (LMI) with certain pathological conditions, like osteoporosis55,56 polycystic ovarian syndrome57
ACCEPTED MANUSCRIPT and chronic kidney disease.58 Body fat excess may be associated with a reduced muscle mass and/or strength (sarcopenic obesity), SMI can be useful to identify subjects with an increased risk of sarcopenic obesity or metabolic syndrome.59 DXA is well correlated with CT, MRI, and BIA
24,60
and should be considered when
quantitative body composition measurement is desired. In some circumstances,
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other body composition technologies may be superior to DXA. For example, CT and MRI offer more detailed measurements of specific regions or tissues, such as visceral adipose fat or fat infiltration among tissues.61 Although most DXA software allows a visceral adipose tissue estimation, the detail level is inferior compared to CT
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or MRI.62 Nevertheless, DXA may be preferred as the whole body is easily quantified and the radiation exposure is lower than CT.52
DXA allows appendicular skeletal muscle (ASM) mass estimation by measuring lean
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soft tissue amount in the upper and lower extremities, which is mainly composed by muscles. The ASM mass has been widely used in sarcopenia studies; indeed, low
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ASM is one of the parameters on which all the available definitions of sarcopenia
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rely.42
In most recently published sarcopenia definitions, DXA is the suggested technique
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for muscle mass assessment.56 It is emerging as a gold standard method in the sarcopenia diagnosis and characterization, since it provides an accurate and precise
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evaluation of non-bone lean mass parameters.56 Therefore, DXA can be useful in treatment planning and its follow-up by measuring muscle mass loss. The main DXA disadvantage is that the equipment is not portable, which may preclude its use in large-scale epidemiological studies or some clinical scenarios. In addition, body thickness, hydration status and diseases with water retention (e.g., heart, kidney or liver failure) can affect DXA results. 3 DXA underestimates trunk and
ACCEPTED MANUSCRIPT thigh fat mass, overestimates thigh muscle mass in obese persons, which is increased in heavier individuals.63 In contrast, DXA may overestimate muscle mass in individuals with extracellular fluid accumulation, due to its inability to distinguish water from bone-free lean tissue. Furthermore, DXA is unable to measure intramuscular adipose tissue, which interferes with muscle quality estimation. 64
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By taking all strengths and weaknesses into consideration, DXA may be considered the current reference technique for assessing muscle mass and body composition in research and clinical practices.65
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Conclusions
All the methods shown are cutting-edge technology in terms of body composition
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assessment and can be very useful considering the exposed pros and cons and hence, contribute to increasing knowledge and for monitoring nutritional interventions
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introduced during the treatments, information summarized in the table 5. The use of
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US to assess body composition is featured by the ease and cost of the examination. The CT is adding knowledge to the oncological patient and sarcopenia fields. BIA
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can be used as a prognostic and assessment body composition tool. The DXA method is of great value to the study of sarcopenia. However, further studies are
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needed to fill the limitations imposed by each method.
Table 5. Comparative evaluation of the methods exposed.
Characteristic
US
BIA
CT
DXA
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Broad Spectrum
Notintubated
Not utilized exclusively to body composition assessment due to radiation exposition
Intubated
+
+
++
++
+++ +++
++ +++
No
Pregnant
Low-Cost
+++
+++
Safeness
+++
+++
Replicability Accuracy
++ ++
++ ++
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Contraindication
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Broad Spectrum
Population
Cancer; abdominal surgery. Patients that already possess the exam.
BIA, Bioelectrical impedance analysis; CT, Computed tomography; DXA, Dual X-ray absorptiometry; US, Bedside ultrasonography. Redrawn from: Guglielmi, G, 2016 50
Vincent JL. Critical care--where have we been and where are we going? Crit Care. 2013;17 Suppl 1:S2.
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