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Published online: 2020-04-30

Nutrition Thieme

Phase Angle is Determined by Body Composition and


Cardiorespiratory Fitness in Adolescents

Authors
Raquel David Langer1 , Roseane de Fatima Guimarães2, Ezequiel Moreira Gonçalves1, Gil Guerra-Junior1,
Anderson Marques de Moraes3

Affiliations Abs trac t


1 Faculty of Medical Sciences, Growth and Development The phase angle is used to evaluate nutritional status and is an
Laboratory – Center for Investigation in Pediatrics indicator of cellular health. Cardiorespiratory fitness and body
(CIPED), State University of Campinas, Campinas, Brazil composition are strong indicators of health during adoles-
2 School of Kinesiology and Physical Activity Sciences, cence. We aimed to evaluate if body composition and cardi-
Universite de Montreal, Montreal, Canada orespiratory fitness have an association with phase angle

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3 Department of Sports Science, Pontifical Catholic among adolescents. 203 girls and 220 boys (12.8 ± 1.3 years)
University of Campinas, Campinas, Brazil were evaluated. Peak height velocity, percentage fat mass, fat-
free mass, cardiorespiratory fitness, and phase angle measure-
Key words ments were collected. Linear regression adjusted by peak
bioelectrical impedance analysis, fat mass, fat-free mass, height velocity was used to verify if predictor variables were
physical activity associated with phase angle among adolescents. Phase angle
showed correlation with fat-free mass (girls: r = 0.42 and boys:
accepted 18.03.2020 r = 0.37); with percent fat mass (girls: r = 0.23); and with cardi-
orespiratory fitness (boys: r = 0.19). Linear regression showed
Bibliography that percentage fat mass (in girls) and cardiorespiratory fitness
DOI https://doi.org/10.1055/a-1152-4865 (in boys) had an effect of 11 and 17 % in phase angle, respec-
Published online: 2020 tively, while fat-free mass had an effect of 22 and 26 % in phase
Int J Sports Med angle for girls and boys, respectively. Changes in phase angle
© Georg Thieme Verlag KG Stuttgart · New York seem to be more associated with the percentage fat mass in
ISSN 0172-4622 girls, cardiorespiratory fitness in boys, and fat-free mass in both
when controlled by peak height velocity.
Correspondence:
Raquel David Langer
Faculty of Medical Sciences, Growth and Development
Laboratory – Center for Investigation in Pediatrics (CIPED)
State University of Campinas
126 Street Tessalia Vieira de Camargo
13083-887 Campinas
Brazil
Tel.: + 551935219097, Fax : + 551935219097
raqueldlanger@gmail.com

Introduction an increase or a decrease in weight [3]. Furthermore, a higher body


Adolescence is marked by several changes in body composition, mass index (BMI) during adolescence can increase the prevalence
including the quantity and distribution of fat mass, bone mass, and of obesity and related cardiovascular disease risk factors through-
lean soft tissue [1, 2]. Early studies show that the proportion of out adult life [5].
body adiposity and fat-free mass (FFM) hydration changes over the Bioelectrical impedance analysis (BIA) is a widely used technique
process of growth, both in boys and girls [3, 4]. In boys, the percent to estimate the body composition of children, adolescents, and
of fat mass ( %FM) can increase from 13.7 % in infancy to 25.4 % at adults showing different health and disease conditions. This is due
6 months of age, and in girls increases from 14.9 % in infancy to to its usability, non-invasiveness, speed, and relative cost-effective-
26.4 % at 6 months of age. Similarly, the percentage of FFM hydra- ness [6]. BIA measures whole-body impedance using two compo-
tion also differs in boys (75.1 ± 2.5 %) and in girls (75.5 ± 1.8 %) [4]. nents: resistance (i. e., the pure opposition of a biological conduc-
Additionally, changes also occur in the total body weight, such as tor to the flow of an alternate electric current) and reactance (i. e.,

Langer RD et al. Phase Angle is Determined … Int J Sports Med


Nutrition Thieme

effect of capacitance produced by tissue interfaces and cell mem- Brazil and were conducted in accordance with the Declaration of
branes) [7]. Using these two components, it is possible to calculate Helsinki. The present study meets the ethical standards of the “In-
the phase angle (PhA) [7]. PhA is used as an indicator of cellular ternational Journal of Sports Medicine” [20].
health in relation to imbalance of cellular water and integrity of the
cell membrane [8]. However, the PhA value can be negatively in- Anthropometry
fluenced by several clinical diseases, such as malnutrition [9], dia- The total body weight (kg) was determined using a digital scale to
betes [10], human immunodeficiency virus infection (HIV infec- the nearest 0.1 kg and the total body height (cm) using a vertical
tion) [11], and some types of cancer [12, 13]. Healthy individuals stadiometer to the nearest 0.1 cm. The body mass index (BMI, kg/
show higher values of PhA (higher than 5º), indicating better cel- m2) was calculated.
lular health and cell membrane integrity compared to malnour-
ished patients [9]. In addition, improvements in the PhA value can Peak height velocity (PHV)
be seen in early studies with young adults following a period of re- The total age (years) and total body height (cm) were used to pre-
sistance training [14] and in soccer players [15]. dict the PHV (in years). Using the individual classification and ac-
It is well known that being physically active and having higher cording to sex, participants with negative predictive PHV were clas-
levels of cardiorespiratory fitness benefit health, functional ability, sified as pre-PHV, and positive predictive values of PHV were clas-
quality of life, and longevity [16, 17]. Furthermore, a recent meta- sified as post-PHV. The following published equation [21] was used:
analysis showed that children who participated in exercise inter-
PHV girls= − 7.709133 + ⎡⎣0.0042232 × ( age × height ) ⎤⎦
ventions presented significant reductions in BMI, waist circumfer-

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ence, and %FM as well as increases in cardiorespiratory fitness, low-
PHV boys= − 7.999994 + ⎡⎣0.0036124 × ( age × height ) ⎤⎦
er-body strength, and speed-agility compared to controls [18].
Additionally, adolescents who are physically active present higher
levels of cardiovascular fitness, a better blood lipid profile, and Phase angle (PhA)
lower body adiposity [16]. Overall, evidence seems to indicate that PhA was assessed using tetrapolar bioelectrical impedance analy-
being physically active during adolescence can minimize these var- sis (BIA), single frequency (50 kHz), model Quantum II (RJL Systems,
ious health risks [19]. Hence, it is necessary to evaluate body com- Detroit, MI, USA), which has been previously validated in adoles-
position with accurate methods to evaluate and follow the chang- cents [22]. Participants were instructed to remove all metallic ob-
es occurring during this stage of life. Thus, we hypothesized that jects before a BIA measurement was taken. Participants were laid
adolescents with higher values of PhA would present with lower barefoot, in a supine position, with legs abducted at a 45º angle,
levels of %FM and a high level of physical activity. Therefore, the arms far from the trunk, and hands pronated on a table isolated
aims of the current study were to: 1) evaluate the relationship be- from electrical conductors. After five minutes of rest, the adoles-
tween PhA and body composition including cardiorespiratory fit- cents’ skin was cleaned with alcohol and two electrodes were
ness, and 2) predict how PhA variability can be explained by body placed on the surface of the right hand and two on the surface of
composition and cardiorespiratory fitness among adolescents from the right foot, according to the recommended protocol [7]. The
both sexes. evaluation lasted approximately one minute. BIA provided meas-
urements with parameters of resistance (R) and reactance (Xc),
both given in Ohms (Ω). Using these variables, the PhA was calcu-
Materials and Methods lated using the following published equation [7]:

Sample ⎛ Xc ⎞ ⎛ 180 ⎞
PhA = arc-tang⎜ ⎟ × ⎜ ⎟
The sample comprised 423 adolescents aged 10–16 years from a ⎝ R ⎠ ⎝ π ⎠
local school in São Paulo, Brazil, who fulfilled the inclusion criteria
of: i) not having any cardiovascular risk and physical limitation to The reproducibility of the parameters provided by BIA was deter-
participate in the procedures, or ii) returning the Informed Consent mined by the coefficient of variation and the technical error of
Form signed. All adolescents, both boys (52 %) and girls (48 %) per- measurement, based on the test-retest method as performed in
formed the regular school routine of two days a week. Each section 23 participants of the study population of an another study [22].
lasted 45 minutes distributed by periodic sections consisting of
physical exercises (i. e., aerobic fitness, endurance, and flexibility) Fat-free mass (FFM)
and collective sports. The FFM was calculated separately for girls and boys, according to
the published equation [23] for children and adolescents aged 7–25
Ethical aspects years:
In this cross-sectional study, all adolescents and their guardians/
parents who agreed to participate in the study were adequately in- FFM = 0.438 × (H2/Z ) + ( 0.308 × Wt ) + (1.6 × Sex ) + ( 7.04 × H) × 8.50
formed about the research proposal and the procedures to which
they would be subjected. The research was approved by the Ethics where, H is height (cm), Z is impedance (Ω), Wt is weight (kg), and
Committee of the School of Medical Sciences (number 797/08), Sex is 0 (girl) or 1 (boy).
University of Campinas. All procedures followed Resolution No. 466
of 2012 of the National Health Council of the Ministry of Health of

Langer RD et al. Phase Angle is Determined … Int J Sports Med


Skinfold thickness Results
To calculate the percentage fat mass ( %FM), the measurements of More than one-half of the subjects (52 %) were boys. The mean age
the tricipital and calf skinfold in mm were evaluated using a Sanny® was 13 years (IQR: 10–16). Participants’ body composition, BIA
caliper and followed the recommendations of the ACSM [24]. Using measurements, and VO2 peak are presented in ▶Table 1. All meas-
the published equation [25] for children and adolescents aged 8–18 urements except for the weight and BMI were significantly differ-
years, the %FM was calculated as follows: ent between boys and girls (p < 0.05). Boys had larger heights
(∆ = 3.22 cm), FFM (∆ = 5.3 kg), PhA (∆ = 0.4º), and VO2 peak (∆ = 2.5
%FMGirls = 0.610 × ( TRICIPITAL + CALF ) + 5.1
ml · kg · min) compared to girls (p < 0.05). On the other hand, girls
tended to be closer to their age of PHV compared to boys and had
%FMBoys = 0.735 × ( TRICIPITAL + CALF ) + 1.0
higher %FM (∆ = 2.9 %), R (∆ = 61.2 Ω), and Xc (∆ = 2.2 Ω) values
than boys (p < 0.05).
Cardiorespiratory fitness (VO2 peak) The PHV showed a significant association with PhA (girls:
The VO2 peak was assessed using the progressive effort test proposed r = 0.22, p < 0.01, and boys: r = 0.42, p < 0.001) and with the predic-
in the literature [26]. To calculate the VO2 peak, the following pub- tor variables, such as %FM only in girls (r = 0.22, p < 0.01) and FFM
lished equation was used [26]: (girls: r = 0.60, p < 0.001, and boys: r = 0.81, p < 0.001), and an in-
verse association with VO2 peak (girls: r = –0.55, p < 0.001, and boys:
VO2 peak = 31.025 + ( 3.238 × S ) − ( 3.248 × A ) + ⎡⎣0.1536 × ( S × A ) ⎤⎦
r = –0.18, p < 0.01). For this reason, the PHV was used as a control
variable for further analysis.

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where S is the last running speed completed and A is age in years. In girls, a positive association between PhA and %FM was ob-
Due to its reliability and validity, this method has been widely used served (▶Fig. 1a), whereas in boys, PhA showed a positive associ-
as a cardiorespiratory fitness marker when an individual’s maxi- ation with VO2 peak (▶ Fig. 1b). In both girls and boys, a positive as-
mum oxygen uptake cannot be assessed in a laboratory-based test sociation between PhA and FFM was observed (▶ Fig. 1c and d, re-
[27, 28]. spectively).
Linear regression analyses were performed separately for girls
Statistical analysis and boys to verify the determinant factors for PhA, controlled by
The SPSS software version 21.0 (IBM Corp., Armonk, NY, USA) was PHV (▶Table 2). The variables that presented the best correlation
used to analyze the data. The Shapiro-Wilk test was used to verify with PhA were tested as predictors. In addition, we found no mul-
the normality of the data. All analyses were performed separately ticollinearity symptoms between predicted variables of weight
for each sex group. Descriptive analysis of data, mean, and SD val- (VIF = 1.000 in both girls and boys), BMI (VIF = 1.000 in girls and
ues were used to characterize the sample. The Student’s t-test and boys), FFM (VIF = 1.000 in girls and boys), %FM (VIF = 1.000 in girls
Mann-Whitney U test were used to test for differences between the and boys), or in VO2 peak (VIF = 1.000 in girls and boys). Among girls,
sexes, depending on the sample distribution. Bivariate (Pearson’s) BMI was the strongest predictor of variance in PhA (27 %), followed
correlation (r) was conducted to determine the relationship be- by FFM (22 %), weight (19 %), and %FM (11 %) (p < 0.05). Similarly,
tween PhA with body composition ( %FM and FFM) and VO2 peak. in boys the FFM was the strongest predictor of variance in PhA
Linear regression analysis was performed to identify the effects on (26 %), followed by BMI (23 %), weight (21 %), and VO2 peak (17 %)
PhA. The variance inflation factor (VIF) was tested to verify the mul- (p < 0.05). Interestingly, VO 2 peak was not associated with PhA
ticollinearity symptoms between the predictor’s variables. Values among girls (p = 0.814) or %FM among boys (p = 0.811).
presented are medians [interquartile range (IQR)], unless other-
wise specified. P < 0.05 was set as the level of significance.

▶Table 1 Characteristics of girls and boys who participated in the study.

Variables TOTAL (n = 423) GIRLS (n = 203) BOYS (n = 220) p-value


Median (IQR) Median (IQR) Median (IQR)
Weight (kg) 49.50 (25.70–98.80) 48.70 (25.70–85.00) 50.00 (29.40–98.80) 0.124
Height (cm) 155.38 ± 10.68 * 153.70 ± 8.84 * 156.92 ± 11.95 * 0.002
BMI (kg/m2) 19.87 (14.31–43.61) 17.74 (14.31–43.61) 20.03 (14.50–37.65) 0.759
PHV (years) −0.03 (−2.76–3.43) 0.47 (−1.89–3.43) −0.76 (−2.76–2.60) 0.000
%FM 22.14 (8.64–58.33) 23.58 (13.21–45.24) 20.11 (8.64–58.33) 0.000
FFM (kg) 34.76 (17.70–67.13) 33.41 (17.70–52.53) 36.64 (22.37–67.13) 0.000
R (Ω) 626.42 ± 80.60 * 658.16 ± 72.35 * 597.14 ± 76.78 * 0.000
Xc (Ω) 61.00 (44.00–79.00) 62.00 (46.00–79.00) 59.00 (44.00–79.00) 0.002
PhA (º) 5.53 (3.70–8.35) 5.34 (3.86–8.24) 5.66 (3.70–8.35) 0.000
VO2 peak (ml · kg · min) 41.15 (31.35–54.24) 40.32 (32.18–51.96) 42.13 (31.35–54.24) 0.000

Abbreviations: BMI, body mass index; PHV, peak of height velocity; %FM, percent of fat mass; FFM, fat-free mass; R, resistance; Xc, reactance; PhA,
phase angle. * Mean ± SD.

Langer RD et al. Phase Angle is Determined … Int J Sports Med


Nutrition Thieme

a Girls b Boys
10 10

8 8

PhA (°)
PhA (°)

6 6

4 4

r = 0.233
r = 0.189
p = 0.001
p = 0.005
2 2
10 20 30 40 50 25 30 35 40 45 50 55 60
%FM VO2 peak (ml . kg . min)

c Girls d Boys
10 10

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8 8
PhA (°)

PhA (°)

6 6

4 4

r = 0.419 r = 0.369
p = 0.000 p = 0.000
2 2
10 20 30 40 50 60 10 20 30 40 50 60 70
FFM (kg) FFM (kg)

▶Fig. 1 Pearson’s correlation between phase angle and a percent of fat mass in girls, b cardiorespiratory fitness in boys, c fat-free mass in girls, and
d fat-free mass in boys.

Discussion calculated from the R and Xc values; it expresses changes in the


The main and novel findings of this study were that PhA, when con- amount of soft tissue mass (related to the hydration) and the ca-
trolled by PHV, was directly associated with %FM only in girls, VO2 peak pacity of body cell mass (related to cell membrane permeability),
only in boys, and FFM in both sexes. respectively [29]. Additionally, the PhA value can also be affected
The study demonstrated that the mean PhA values of boys were by the total body mass; in this sample, girls had less body weight
significantly higher than that of girls. Similar results were reported compared to boys (∆ = –2.8 kg). These findings have also been de-
in other studies using a large sample of healthy or unhealthy par- scribed in other studies carried out on large samples comprising
ticipants [8, 29–31]. Higher means of PhA values were observed in children and adult subjects [29, 30]. The association between PhA
boys. This result might be explained by the higher amount of rela- and body weight can be explained by the current flow through
tive FFM present in the total body in boys. Because the PhA is cal- physiological fluids, such that the higher the body mass volume,
culated by an equation, the whole-body resistance is inversely pro- the lower the body resistance [8, 29].
portional to the PhA value, which means that the lower the value Even though the PhA is not completely understood biologically,
of resistance, the higher the PhA value [31]. it has been widely used as an important prognostic marker tool in
Despite no significant association between PhA and body height, several clinical contexts [29]. Several studies have associated lower
a positive association between PhA and BMI was found. A high cor- levels of PhA as a prognostic indicator for malnutrition, cancer, HIV-
relation between PhA and BMI has been described in several stud- infected and liver cirrhosis as well as a poor indicator of survival
ies with adults [29, 30], but it is still understudied in the adolescent time [8]. The prevalence of obesity in adolescent girls and boys has
population. In the present study, the linear regression analyses increased globally between 1975 and 2016, becoming a challenge
demonstrated that body weight and BMI are statistically significant of the 21st century [32, 33]. Previous studies carried out in obese
explanatory variables for the variation in PhA in adolescents of both women found an inverse association between PhA and biochemi-
sexes. An explanation for this association is that the PhA is directly cal parameters as well as with blood adipocytokine levels, indicat-

Langer RD et al. Phase Angle is Determined … Int J Sports Med


▶Table 2 Linear regression analyses between phase angle and determinant factors.

Variables Girls Boys


R2 β p-value R2 β p-value
Weight (kg) 0.19 0.429 0.000 0.21 0.360 0.000
BMI (kg/m2) 0.27 0.469 0.000 0.23 0.316 0.000
%FM 0.11 0.230 0.001 0.14 0.015 0.811
FFM (kg) 0.22 0.514 0.000 0.26 0.597 0.000
VO2 peak (ml · kg · min) 0.06 0.020 0.814 0.17 0.180 0.005

BMI, body mass index; %FM, percent of fat mass; FFM, fat-free mass; R2, R-square; β, standardized beta.

ing a higher cardiovascular risk in this sample [34]. However, the because they may not have correctly provided the data. The cross-
association between PhA and %FM in children has not been ex- sectional design of the present study does not provide conclusions
plored at all. In the present study, despite no association being relating to causality between PhA and the independent variables;
found between PhA and %FM in boys, the %FM predicted an 11 % however, it remains open for future research to explore this rela-
variation in the PhA value of girls. This finding is consistent with tionship in observational and experimental studies. Thus, longitu-

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previous studies that showed the effect of body fat in girls during dinal studies are necessary to verify if changes in PhA can be deter-
the pubertal phase (10–14 years old), whereas in boys this is small- mined by changes in body composition and cardiorespiratory fit-
er until late adolescence [8, 35]. In addition, cellular adipose tissue ness. Briefly, these results suggest that PhA obtained through BIA
hydration is higher compared to lean soft tissue hydration as a re- is a potential technique to evaluate the health status in children
sult of an imbalance in the amount of extra and intracellular water and adolescents in relation to physical activity levels and body com-
[36, 37]. position parameters.
Being physically active during childhood and adolescence has Therefore, we conclude that PhA can provide key information
been reported as an important factor in the improvement of meas- for the measurement and evaluation of nutritional and overall
urements related to obesity, insulin sensitivity, and metabolic syn- health status in adolescents, especially because it is a convenient,
drome [17]. In this sample, boys had higher PhA and VO2peak values easy, and non-invasive method. In this sample of adolescents, when
compared to girls (∆ = 0.32º and ∆ = 1.81 ml · kg · min, respective- controlled by somatic maturation, the changes in PhA seem to be
ly). In addition, in this sample of adolescent boys, the VO2 peak pre- explained by %FM in girls, VO2peak in boys, and FFM in both girls and
dicted a 17 % variation in the PhA value. This can be explained be- boys. These results have important implications for physical activ-
cause both PhA and VO 2peak are considered as health markers ity behavior and body composition to improve overall health in ad-
[8, 38]; their application in the clinical situation can provide impor- olescents.
tant information related to health status in adolescents and adults.
A positive correlation was observed between PhA and FFM in
both girls and boys. This result is consistent with a previous study Acknowledgement
[11], and although using a different sample, the authors observed The authors thank the Principal and students of Bradesco Founda-
a relationship between PhA and FFM in HIV-infected children and tion School of Campinas-SP for their authorization and collabora-
adolescents. The PhA is calculated using the ratio of the reactance tion in this study.
and resistance measurements provided by BIA [7]. As mentioned
above, the reactance value reflects the capacitance of cell mem-
branes and tissue interfaces – the delay in the passage of an elec- Funding
trical flow, whereas the resistance value is inversely proportional We also thank the Coordination for the Improvement of Higher Ed-
to the amount of electrolytes present in the water of tissues (i. e., ucation Personnel—CAPES [grant number: 23001.000422/98-30]
fat and muscle tissue) [6]. Therefore, the better the integrity of the for support this study.
cell membrane, the higher the reactance value will be; the higher
the amount of intracellular and extracellular water, the smaller the
resistance value of the body [6]. In other words, the association be- Conflict of Interest
tween PhA and FFM can be explained by the amount of water con-
tent in the FFM component (muscle tissue), which provides less re- The authors declare that they have no conflict of interest.
sistance against the current.
One limitation of this study is that the results cannot be extrap-
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