IMiD, Wydawnictwo Aluna Developmental Period Medicine, 2015;XIX,3(I) 297 Nina Mól 1, Przemko Kwinta 1,2 ASSESSMENT OF BODY COMPOSITION USING BIOELECTRICAL IMPEDANCE ANALYSIS IN PRETERM NEONATES RECEIVING INTENSIVE CARE* OCENA SKŁADU CIAŁA PRZY UŻYCIU BIOIMPEDANCJI ELEKTRYCZNEJ U NOWORODKÓW URODZONYCH PRZEDWCZEŚNIE WYMAGAJĄCYCH INTENSYWNEJ TERAPII 1 University Children s Hospital of Krakow, Department of Pediatrics, Poland 2 Department of Pediatrics, Chair of Pediatrics, Polish-American Institute of Pediatrics, Jagiellonian University, Medical College, Krakow, Poland Abstract Aim: Evaluation of bioelectrical impedance values and body composition during early infancy in groups of preterm newborns and full term newborns. Material and methods: A total of 38 newborns was enrolled in the study: 26 very low birth weight preterm newborns with the mean birth weight of 1236 g (SD: 161) as the study group and 12 term newborns with birth weight of 2500-4000 g as the control group. Anthropometric measurements and body composition using bioimpedance analysis at the age of 1 week and at the age of 3 months were assessed. Results: At the age of 1 week we noted higher resistance with the impedance variables R 5, R 50, R 100 in the group of preterm newborns compared to the full term newborns group (923 (144) vs. 647 (78) p<0.01; 870 (140) vs. 615 (73) p<0.01; 844 (141) vs. 599 (72) p<0.01). Moreover, the bioimpedance index and fat mass (%) were significantly lower in the group of preterm infants at the age of 3 months (3.81 (0.9) vs. 5.72 (1.1) p<0.01; 16.1% (1.7) vs. 18.9% (2.7) p=0.006). We observed a decreased amount of the percentage of total body water (TBW%) in both of the analyzed infant groups throughout the observational period. At the age of 3 months the amount of TBW % was similar in both groups (71.5% (7.03) vs. 70.8% (8.8) p=0.8). Conclusions: Bioimpedance analysis is a simple, non-invasive, repeatable method to estimate total body water, fat-free mass, and fat mass, both in term and preterm newborns. The study confirms differences in body composition between preterm newborns and full term newborns. Moreover, we have shown that the differences are present until the end of the 3 rd month of life, with the exception of the amount of water percentage (TBW%), which are similar in both groups. Key words: preterm infants, body composition Streszczenie Cel pracy: Porównanie wartości impedancji bioelektrycznej oraz składu ciała w ciągu pierwszych 3 miesięcy życia w grupie noworodków urodzonych przedwcześnie oraz w grupie noworodków urodzonych w fizjologicznym terminie porodu Materiał i metody: Badaniem objęto łącznie grupę 38 pacjentów, w tym 28 noworodków urodzonych z bardzo małą urodzeniową masą ciała (średnia 1236 g (SD: 161 g)) oraz 12 noworodków urodzonych w fizjologicznym terminie porodu, z masą ciała 2500g-4000g. W pierwszym tygodniu życia oraz w wieku 3 miesięcy wykonano pomiary antropometryczne oraz oceniono skład ciała przy użyciu metody bioimpedancji elektrycznej *Study sponsored by Grant number RG1/2013 obtained from NUTRICIA Foundation.
298 Nina Mól, Przemko Kwinta Wyniki: W pierwszym tygodniu życia wartości oporu mierzone przy częstotliwościach 5, 50 i 100 Hz były istotnie większe w grupie noworodków urodzonych przedwcześnie (923 (144) vs. 647 (78) p<0,01; 870 (140) vs. 615 (73) p<0,01; 844 (141) vs. 599 (72) p<0,01). Dodatkowo, noworodki urodzone przedwcześnie w wieku 3 miesięcy charakteryzowały się: niższym indeksem impedancji bioelektrycznej oraz niższą procentową zawartością tkanki tłuszczowej (3,81 (0,9) vs. 5,72 (1,1) p<0,01; 16,1% (1,7) vs. 18,9% (2,7) p=0,006). Zarówno w grupie noworodków urodzonych przedwcześnie, jak i fizjologicznym terminie porodu stwierdzono zmniejszanie się procentowej ilości całkowitej zawartości wody w organizmie (TBW%) wraz z wiekiem dziecka. W 3. miesiącu życia w obu grupach ilość wody w organizmie była porównywalna (71,5% (7,03) vs. 70,8% (8,8) p=0,8). Wnioski: Metoda impedancji bioelektrycznej jest prostą, nieinwazyjną metodą oceny ilości całkowitej wody ciała, beztłuszczowej masy ciała oraz tkanki tłuszczowej u noworodków urodzonych przedwcześnie oraz w fizjologicznym terminie porodu. Prezentowane badanie wskazuje na istotne różnice składu ciała między grupą noworodków urodzonych przedwcześnie w stosunku do noworodków urodzonych w fizjologicznym terminie porodu. Różnice te utrzymują się przez 3 pierwsze miesiące życia dzieci z wyjątkiem zawartości wody w organizmie (TBW%), która w 3 miesiącu życia jest podobna w obu grupach. Słowa kluczowe: noworodki urodzone przedwcześnie, skład ciała DEV PERIOD MED. 2015;XIX,3,I:297 304 INTRODUCTION Extreme prematurity is a crucial problem in neonatology. Compared to full term infants, preterm newborns are more susceptible to malnutrition and extrauterine growth retardation early in life, while in later life they are more likely to experience growth failure, skeletal mineral deficiencies, and neuropsychological development restrictions [1]. On top of that, there is an increasing prevalence of obesity in that group, which becomes an important public health problem in childhood and leads to numerous complications. Body composition disorders in early life may play a key role in the programming of a variety of health disorders in the future, including hypertension, stroke, type 2 diabetes, and obesity [2, 3]. Thus, the energy balance and nutritional status are of vital importance in the early stages of infancy, in particular in preterm babies. An accurate assessment of neonatal body composition is essential to determine the energy status of preterm newborns, project their development and to monitor their feeding interventions. Routine methods used in clinical settings to assess body composition in infants and children are largely based on anthropometric measurements (such as length, weight, skinfold thickness) and recently introduced bioelectrical impedance analysis (BIA) techniques. The theory behind BIA provides good grounds for the assessment of total body water (TBW). The method implements a phenomenon that only water (containing electrolytes) can conduct electricity in the human body. The examination is quick, relatively low-cost, and BIA equipment is inexpensive and portable. The aim of the present study is to evaluate whether there is a difference in bioelectrical impedance values and body composition between preterm newborns and newborns born at term over the first 3 months of their lives. MATERIALS AND METHODS The research project included preterm newborns with birth weight between 1000-1500 g, and term newborns with birth weight between 2500-4000 g, hospitalized due to frequent, moderate complications in the neonatal period (e.g. severe hiperbilirubinaemia, adaptation disorders), admitted to the Neonatal Intensive Care Unit (Chair and Department of Pediatrics, Jagiellonian University, Krakow) between February 2014 and January 2015. A total of 38 newborns were enrolled in the study: 26 preterm infants as the study group and 12 term infants as the control group. Exclusion criteria for both groups were severe congenital malformations, chromosomal aberrations, asphyxia with Apgar Score in the 5th min. below 3 points, intraventricular hemorrhage grade IV, and severe infections. The study protocol was approved by the Jagiellonian University Medical College Ethical Committee (issue No KBET/58/B/2013 from 4.04.2013). Written and informed consent was obtained from the parents. Anthropometric measurements such as: birth weight, birth length, and head circumference were collected. All the infants were weighed naked on an electronic baby scale to the nearest 10 g. Crown-heel length was measured to the nearest 0.5 cm. The occipitofrontal circumference was measured by using a measuring tape. A single investigator made all the measurements. Body composition was measured with the multi-frequency impedance body composition monitor (BCM; Fresenius Medical Care, Bad Homburg, Germany), and special disposable electrodes BCM-FMC (<25 kg). The BCM measured resistance and reactance at 50 frequencies between 5 and 1000 khz. The amplitude of the electric current was 0.8mA. The newborns examined were placed in the supine position with arms and legs extended. Two electrodes were attached to each dorsal surface of hand and foot. Measurements were made
Assessment of body composition using bioelectrical impedance analysis in preterm neonates receiving intensive care 299 Placing of electrodes/umieszczenie elektrod Distal electrode Red clip Elektroda dystalna Zacisk czerwony Proximal electrode Black clip Elektroda proksymalna Zacisk czarny Distal electrode Red clip Elektroda dystalna Zacisk czerwony Proximal electrode Black clip Elektroda proksymalna Zacisk czarny Fig. 1. Electrodes posi on. Ryc. 1. Umieszczenie elektrod. after 2 minutes following attachment of the electrodes at their respective sites (appropriate electrode positions are presented in figure 1). STATISTICAL ANALYSES Our null hypothesis stated that there was no difference in bioelectrical impedance values and body composition between preterm infants and full term infants. Demographic and clinical data comparisons between the study and control groups were performed using Student s t-test, Mann-Whitney U-test, and chi-square test. The comparison between the measurements acquired in the 1 st week of life and in the 3 rd month of life were performed using the paired t-test. The detected differences were considered to be statistically significant in case of p<0.05. RESULTS Thirty-eight newborns (26 preterm infants and 12 full-term infants) were included in the study. Their anthropometric characteristics at birth and during the second BIA examination are shown in table I. We noted higher resistance with the impedance variables R 5, R 50, R 100 in the group of preterm infants in comparison with the full term infants group; however only at the 1 st examination was the difference statistically significant (923 (144) vs. 647 (78) p<0.01; 870 (140) vs. 615 (73) p<0.01; 844 (141) vs. 599 (72) p<0.01). A similar correlation was observed with reactance using 50 Hz frequency. Measurements in the 1 st week of life were statistically higher in the group of preterm infants (tab. II, III, IV). The bioimpedance index was positively correlated with total body water (TBW) in both groups. Both the bioimpedance index (3.81 (0.9) vs. 5.72 (1.1) p<0.01) and total body water (2.52 l (0.6) vs. 3.77 l (0.72); p<0.010) were significantly lower in the group of preterm infants at the age of 3 months. Moreover, the amount of adipose tissue was also significantly lower in that group (16.1% vs 18.9%; p=0.006) tab. V. We observed a decreased amount of the percentage of total body water (TBW%) in both of the infant groups analyzed throughout the observational period (tab. VI and VII) At the age of 3 months the amount of TBW% was similar in both groups (71.5% (7.03) vs. 70.8% (8.8) p=0.8 tab. V). DISCUSSION Bioimpedance analysis is a noninvasive, low cost and commonly used approach for body composition measurements and the assessment of the patient s clinical condition. Bioimpedance or biological impedance is defined as the ability of biological tissue to impede electric current [4]. The measurement of bioimpedance is obtained from the whole body and body segments separately, using single frequency, multiple frequencies and bioimpedance spectroscopy analysis. BIA is a method consisting in the passage of a painless electric current of low amplitude ( 1 ma), and low and high frequencies through the organism. The analysis of bioimpedance information obtained at 50 KHz electric current is known as single-frequency bioimpedance analysis (SF-BIA). SF-BIA is the most common, and one of the earliest methods for the estimation of body compartments. The analysis of bioimpedance that is obtained at more than two frequencies (frequency range between 5-1000 khz) is known as multiple-frequency bioimpedance analysis (MF-BIA). MF-BIA is based on the finding that exposing it to low and high frequency electric currents can assess the ECF and TBW, respectively [5]. Bioelectrical impedance analysis (BIA) is possible, because impedance is a function of resistance (R) and reactance (Xc) [6]. Due to its reduced water and electrolyte content adipose tissue is non-conductive and shows high electrical resistance. In contrast, lean tissue mass, due to the high amount of intra- and extracellular water is a good conductor, and shows low resistance to the passage of an electric current. Low frequency electric current passes through the extracellular compartment. Depending on the frequency used, cell membranes act as small capacitors or resistors. Having identified the levels of resistance and reactance of the organism to electrical current, it is possible to evaluate intra- (ICW) and extracellular water (ECW) [7]. The introduction of different frequencies,
300 Nina Mól, Przemko Kwinta Table I. Baseline characteris cs of the study popula on (mean values and standard devia on). Tabela I. Charakterystyka badanych grup (dane przedstawiono jako średnią i odchylenie standardowe). n= 26 p value Gesta onal age (wk.) Wiek ciążowy (tyg.) 30.5 (26-33) 39 (37-41) <0.01 a Birth weight (g) Urodzeniowa masa ciała (g) 1236 (165) 3262 (385) <0.01 a Birth length (cm) Urodzeniowa długość ciała (cm) 39.1 (2.12) 51.4 (3.15) <0.01 a Sex (boys/girls) Płeć (męska/żeńska) 11/15 9/3 n.s. b Age at 1 st BIA study (days) Wiek w czasie 1-szego badania (dni) 4.7 (2.8) 4.6 (1.6) n.s. c Age at 2 nd BIA study (days) Wiek w czasie 2-go badania (dni) 84 (22) 87 (8) n.s. c Weight at 2 nd BIA study (kg) Masa ciała w czasie 2-go badania (kg) 3.52 (0.69) 5.44 (1.36) <0.01 a Length at 2 nd BIA study (cm) Długość ciała w czasie 2-go badania (cm) 50.8 (3.7) 60.7 (5.1) <0.01 a P value for: astudent s t test, bfisher s exact test, cmann-whitney U test; BIA bioimpedance analysis/bioimpedancja elektryczna; n.s. non significant/nie istotne statystycznie. Table II. Comparison of BIA values at the age of 1 week (1 st examina on). Tabela II. Porównanie zmierzonych w 1. tygodniu życia (1. badanie) wartości impedancji w badanych grupach. n=26 p value for Student s t test R if f=5 Hz 923 (144) 647 (78) <0.01 R if f=50 Hz 870 (140) 615 (73) <0.01 Xc if f=50 Hz 52.7 (19) 34.2 (8.4) <0.01 Phase angle if f=50 Hz Kąt fazowy przy f=50 Hz 3.56 (1.53) 3.19 (0.67) 0.4 R if f=100hz 844 (141) 599 (72) <0.01 R resistance/r rezystancja Xc reactance/xc reaktancja BIA bioimpedance analysis/bioimpedancja elektryczna
Assessment of body composition using bioelectrical impedance analysis in preterm neonates receiving intensive care 301 Table III. Comparison of BIA values at the age of 3 months (2 nd examina on). Tabela III. Porównanie zmierzonych w 3. miesiącu życia (2. badanie) wartości impedancji w badanych grupach. n=26 p value for Student s t test R if f=5 Hz 730 (87) 697 (48) 0.4 R if f=50 Hz 692 (81) 653 (53) 0.25 Xc if f=50 Hz 39.4 (10) 40.7 (6.2) 0.8 Phase angle if f=50 Hz Kąt fazowy przy f=50 Hz 3.25 (0.7) 3.59 (0.7) 0.3 R if f=100hz 673 (79) 633 (53) 0.24 R resistance/r rezystancja Xc reactance/xc reaktancja BIA bioimpedance analysis/bioimpedancja elektryczna Table IV. Comparison of body composi on assessed using BIA values at the age of 1 week (1 st examina on). Tabela IV. Porównanie oszacowanego na podstawie pomiaru BIA składu ciała wartości dla 1. tygodnia życia. (pierwsze badanie). Impedance index (ht 2 /R if f=50 Hz) Index impedancji n=26 p value for Student s t test 1.81 (0.35) 4.35 (0.64) <0.01 TBW (l) 1.1 (0.15) 2.82 (0.39) <0.01 TBW (%) 89.4 (6) 86.7 (9.9) 0.3 FFM (kg) 2.77 (0.29) FFM (%) 85.3 (1.4) FM (kg) 0.48 (0.1) FM (%) 14.6 (1.4) ht height; R resistance; TBW total body water; FFM fat-free mass; FM fat mass ht długość ciała; TBW całkowita zawartość wody w organizmie; FFM beztłuszczowa masa ciała; FM masa tkanki tłuszczowej Table V. Comparison of body composi on assessed using BIA values at the age of 3 months (2 nd examina on). Tabela V. Porównanie oszacowanego na podstawie pomiaru BIA składu ciała wartości dla 3. miesiąca życia (drugie badanie). n=26 p value for Student s t test Impedance index (ht2/r if f=50 Hz) 3.81 (0.9) 5.72 (1.1) <0.01 Index impedancji TBW (l) 2.52 (0.6) 3.77 (0.72) <0.01 TBW (%) 71.5 (7.03) 70.8 (8.8) 0.8 FFM (kg) 2.94 (0.5) 4.38 (1.0) <0.01 FFM (%) 83.9 (1.7) 81 (2.7) 0.01 FM (kg) 0.58 (0.17) 1.06 (0.35) <0.001 FM (%) 16.1 (1.7) 18.9 (2.7) 0.006 ht height; R resistance; TBW total body water; FFM fat-free mass; FM fat mass ht długość ciała; TBW całkowita zawartość wody w organizmie; FFM beztłuszczowa masa ciała; FM masa tkanki tłuszczowej
302 Nina Mól, Przemko Kwinta Table VI. Comparison of BIA values and assessed body composi on in full- term neonates () at the age of 1 week and 3 months (1st and 2nd examina on). Tabela VI. Porównanie wartości impedancji oraz oszacowanego składu ciała w pomiarach w 1. tż. oraz 3. mż. (1. i 2. badanie) w grupie noworodków urodzonych w fizjologicznym terminie porodu. Weight at me of study (g) Masa ciała w trakcie badania (g) 1 st examina on pierwsze badanie 2 nd examina on drugie badanie p value for paired t-test 3.3 (0.42) 5.44 (1.4) <0.01 R if f=5 Hz 628 (54) 697 (48) 0.05 R if f=50 Hz 600 (52) 653 (53) 0.1 Xc if f=50 Hz 30 (5.3) 40.7 (6.2) 0.01 Phase angle if f=50 Hz Kąt fazowy przy f=50 Hz 2.83 (0.6) 3.6 (0.7) 0.044 R if f=100 Hz 586 (53) 633 (53) 0.1 Impedance index (ht2/r if f=50 Hz) 4.55 (0.4) 5.7 (1.1) 0.014 Index impedancji TBW (l) 2.94 (0.3) 3.76 (0.72) 0.1 TBW (%) 89 (6.5) 71 (8.8) <0.01 FFM (kg) 2.81 (0.3) 4.38 (1.0) 0.003 FFM (%) 85.5 (1.4) 81 (2.7) 0.001 FM (kg) 0.48 (0.1) 1.05 (0.35) 0.002 FM (%) 14.5 (1.4) 18.9 (2.7) 0.001 ht height; R resistance; Xc reactance; TBW total body water; FFM fat-free mass; FM fat mass; BIA bioimpedance analysis ht długość ciała; R rezystancja; Xc reaktancja; TBW całkowita zawartość wody w organiźmie; FFM beztłuszczowa masa ciała; FM masa tkanki tłuszczowej; BIA bioimpedancja elektryczna total body water (TBW), fat-free mass (FFM) and fat mass (FM) can be estimated [8. 9]. Reactance causes the electric current to lag behind the voltage creating a phase shift. This shift is quantified geometrically as the angular transformation of the ratio of reactance to resistance or the phase angle φ [10]. The phase angle has proved to be a good predictor of prognosis and mortality in patients that undergo hemodialysis [11] or are diagnosed with cancer [12], human immunodeficiency syndrome (HIV) [13], and liver [14] and geriatric [15] diseases. The phase angle depends on cell membrane integrity and body cell mass. There is a correlation between phase angle values and body cell mass. The phase angle gives indirect information about nutritional status [6]. The use of bioimpedance to estimate fat-free mass (FFM) is based on the assumption that adipose tissue, due to reduced water and electrolyte content is non-conductive. However, it has been observed that in fact adipose tissue has a wide range of conductivity depending on the degree of its perfusion. Moreover, the composition of fat in a newborn is different from that in an adult. The water content is highest at birth (45-48%), decreasing to 27-38% at the age of 6-10 months and further down to 20-26% in adulthood [16]. The increased vascularization and high water content in adipose tissue in the first months of life may be the reason for the increased conductivity of the fat. Such changes in fat composition might account for our inability to determine fat mass and fat-free mass during the 1 st week of life in the preterm infant group in our study. Kushner et al. [17] concluded that the impedance index (ht2/r) is a significant predictor of total body water at various ages from infancy to adulthood. Our study confirms the correlation between the impedance index and total body water in both the groups examined. Uthaya et al. assessed the quantity and distribution of adipose tissue in term infants of equivalent age using magnetic resonance imaging. The authors reported that their preterm infants had a highly significant decrease in their subcutaneous adipose tissue and significantly increased intra-abdominal adipose tissue compared withthe control group of neonates born at term. Accelerated postnatal weight gain was accompanied by increased total and subcutaneous adiposity. Increased and aberrant adiposity are risk factors of cardio-vascular diseases in later life [18]. Gianni et al. [19] examined children with birth weight <1800 g and gestational age <34 weeks at the age of 4.8-6.6 years using dual energy X-ray absorptiometry (DXA). They found a significantly lower amount of adipose tissue in the group of preterm infants in comparison with the full term infants group. Moreover, aberrant fat distribution with reduced subcutaneous and increased intra-abdominal amount of adipose tissue was noted.
Assessment of body composition using bioelectrical impedance analysis in preterm neonates receiving intensive care 303 Table VII. Comparison of BIA values and assessed body composi on in preterm neonates (n=26) at the age of 1 week and 3 months (1st and 2nd examina on). Tabela VII. Porównanie wartości impedancji oraz oszacowanego składu ciała w pomiarach w 1. tż. oraz 3. mż. (1. i 2. badanie) w grupie noworodków urodzonych przedwcześnie. 1 st examina on pierwsze badanie 2 nd examina on drugie badanie p value for paired t-test Weight at me of study (g) Masa ciała 1.24 (0.19) 3.52 (0.7) <0.01 w trakcie badania (g) R if f=5 Hz 911 (150) 730 (87) 0.012 R if f=50 Hz 868 (148) 692 (81) 0.001 Xc if f=50 Hz 47 (13) 39 (10) 0.09 Phase angle if f=50 Hz Kąt fazowy przy f=50 Hz 3.21 (1.2) 3.25 (0.7) 0.9 R if f=100 Hz 844 (149) 673 (79) 0.001 Impedance index (ht2/r if f=50 Hz) 1.85 (0.4) 3.82 (0.91) <0.001 Index impedancji TBW (l) 1.12 (0.2) 2.52 (0.6) <0.001 TBW (%) 90 (6.4) 71.6 (7) <0.001 FFM (kg) 2.94 (0.5) FFM (%) 84 (1.7) FM (kg) 0.58 (0.17) FM (%) 16.1 (1.7) ht height; R resistance; Xc reactance; TBW total body water; FFM fat-free mass; FM fat mass; BIA bioimpedance analysis ht długość ciała; R rezystancja; Xc reaktancja; TBW całkowita zawartość wody w organiźmie; FFM beztłuszczowa masa ciała; FM masa tkanki tłuszczowej; BIA bioimpedancja elektryczna Our observations in children examined at the age of 3 months were in agreement with data reported from other groups showing lower body fat percentage in the infants born preterm compared with those born at term. Kwinta et al. [20] examined children with extremely low birth weight (<1000 g) at the age of 7 years using the BIA method. They reported a significantly lower amount of adipose tissue in the group of preterm infants in comparison with the full term infants group (11% vs. 16%). In this study at the age of 3 months we noticed a lower amount of fat tissue (16.1% vs 18.9%), a greater amount of fat-free mass and increased total body water in the group of preterm infants compared with the group of neonates born at term. CONCLUSIONS Bioimpedance analysis is a simple, non-invasive, repeatable method to estimate total body water, fat-free mass, and fat mass both in term and preterm infants. This study should prove to be a useful tool for the assessment of the changes in total body water and body composition in the neonatal care department. REFERENCES 1. Hovi P, Andersson S, Jarvenpaa AL, Eriksson JG, Strang- Karlsson S, Kajantie E, et al. Decreased bone mineral density in adults born with very low birth weight: a cohort study. PLoS Med. 2009;6:e1000135. 2. Ram Weiss MD, James Dziura PhD, Tania S Burgert MD, William V Tamborlane MD, Sara E Taksali MPH, Catherine W Yeckel PhD, Karin Allen RN, Melinda Lopes RN, Mary Savoye RD, John Morrison MD, Robert S Sherwin MD and Sonia Caprio MD Obesity and the Metabolic Syndrome in Children and Adolescents N Engl J Med. 2004;350:2362-2374. 3. Chen F, Wang Y, Shan X, Cheng H, Hou D, Zhao X, Wang T, Zhao D, Mi J. Association between childhood obesity and metabolic syndrome: evidence from a large sample of Chinese children and adolescents. PLoS One. 2012;7(10):e47380. 4. Martinsen OG, Grimnes S. Bioimpedance and Bioelectricity Basics. Academic Press; Waltham. MA. USA: 2011. 5. Scheltinga MR, Jacobs DO. Kimbrough TD. Wilmore DW. Identifying body fluid distribution by measuring electrical impedance. J Trauma. 1992 Nov;33(5):665-670.
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