Body composition in sarcopenic obesity: systematic review of the literature
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Transcript of Body composition in sarcopenic obesity: systematic review of the literature
REVIEW
Body composition in sarcopenic obesity: systematic reviewof the literature
Lorenzo M. Donini • Eleonora Poggiogalle •
Silvia Migliaccio • Antonio Aversa •
Alessandro Pinto
Received: 23 August 2013 / Accepted: 27 August 2013 / Published online: 11 September 2013
� Springer-Verlag Italia 2013
Abstract Although, recently a mounting interest in the
literature has been directed to sarcopenic obesity, currently,
different definitions of sarcopenic obesity (SO) exist and
diagnostic criteria are not universally established. The aim
of the present systematic review is to summarize the state
of the art according to extant literature about this topic. A
systematic review of the literature was performed consid-
ering the revision question: ‘‘sarcopenic obesity: body
composition’’. Analysis and presentation of the outcomes
were carried out in the form of a narrative resume of the
reports. Twenty-six studies were considered eligible for the
systematic review involving globally more than 23,000
subjects. In all the studies examined, except one, the def-
inition of sarcopenic obesity was based on the co-presence
of obesity and sarcopenia. With respect to obesity, different
parameters (body mass index, fat mass and visceral fat
area) were used (as single parameters or in association to
the other adiposity measures). For sarcopenia, the appen-
dicular skeletal muscle mass standardized for height or
weight, cross-sectional area at the quadriceps level, muscle
strength and/or muscle/fat-free mass indexes were consid-
ered. Body composition analysis was performed, depend-
ing on the studies, through DXA scan, CT scan
bioimpedance analysis, dynamometer test or anthropo-
metric parameters. To date, just few papers provided clear
and shared diagnostic criteria of SO. In fact, in our review,
criteria adopted by single authors were only partially
overlapping. One of the main obstacles is represented by
the definition of SO, and especially whether it should be
based only on criteria of body composition or also func-
tional criteria should be taken into account.
Keywords Obesity � Sarcopenia �Sarcopenic obesity
Introduction
Recently, a mounting interest in the literature has been
directed to sarcopenic obesity (SO), a clinical and func-
tional condition characterized by the coexistence of excess
fat mass (FM) and reduced fat-free mass (FFM), showing
the cumulative risk derived from each of the two individual
body composition phenotypes [1–4]. Especially, sarcopenic
obesity tends to be more common in elderly subjects or in
younger obese subjects with severe disability, as well as it
may occur in obese subjects after bariatric surgery without
nutritional supervision or in response to long-lasting
incongruous dietary regimens [5–9].
Conflicting data exist about the link between sarcopenia
and functional impairment [11, 12]. However, as an asso-
ciation between obesity per se and poor physical perfor-
mance has been demonstrated, long-term consequences of
sarcopenia on physical performance are potentially more
severe in obese elder individuals [10, 13, 14]. In obese
adults, an imbalance between lean mass and excess body
fat and total body size appears earlier than the onset of old
age [5, 6]. This precocious phenomenon is due to the dis-
proportion between lean mass, even when preserved, when
compared to fat mass, exceeding the weight that lean mass
could support. The pathogenetic and functional role of
L. M. Donini (&) � E. Poggiogalle � A. Aversa � A. Pinto
Food Science and Endocrinology Section, Department of
Experimental Medicine, Medical Physiopathology, Sapienza
University of Rome, P.le Aldo Moro, 5, 00185 Rome, Italy
e-mail: [email protected]
S. Migliaccio
Unit of Endocrinology, Department of Movement, Human and
Health Sciences, University of Rome ‘‘Foro Italico’’, Rome, Italy
123
Mediterr J Nutr Metab (2013) 6:191–198
DOI 10.1007/s12349-013-0135-1
sarcopenia or ‘‘relative’’ sarcopenia in obese elderly sub-
jects as well as in younger adults remains to be better
clarified.
Currently, different definitions of sarcopenic obesity
exist and diagnostic criteria are not universally established.
Hence, prevalence of sarcopenic obesity ranges from 2.75
to over 20 %, depending on the criteria used for the diag-
nosis and methods for body composition assessment [6,
15].
As sarcopenic obese subjects require more specific
nutritional rehabilitation protocols, specific nutritional and
body composition parameters need to be better identified
and evaluated.
The aim of the present systematic review is to summa-
rize the state of the art according to extant literature about
this topic.
Materials and methods
The present systematic review was performed following
the steps by Egger et al. [16], as follows:
1. configuration of a working group at the ‘‘Sapienza’’
University of Rome: three operators skilled in clinical
nutrition in the geriatric age, of whom one acting as a
methodological operator (LMD) and two participating
as clinical operators (EP, AP);
2. formulation of the revision question on the basis of the
considerations made in the introduction: ‘‘sarcopenic
obesity: body composition’’;
3. identification of relevant studies: a research strategy
was planned, on PubMed [Public Medline run by the
National Center of Biotechnology Information (NCBI)
of the National Library of Medicine of Bethesda
(USA)], as follows:
a. definition of the key words (sarcopenic obesity,
body composition, fat-free mass, fat mass), allow-
ing the definition of the interest field of the
documents to be searched, grouped in inverted
commas (‘‘…’’) and used separately or in
combination;
b. use of: the boolean AND operator, that allows the
establishment of logical relations among concepts;
c. research modalities: advanced search;
d. limits:
i. time limits: papers published in the last
20 years;
ii. humans;
iii. languages: English, French, Italian;
e. Manual search performed by the senior researchers
(LMD and AP) experienced in clinical nutrition
through the revision of reviews and individual
articles on nutrition and body composition pub-
lished in journals qualified in the Index Medicus:
4. analysis and presentation of the outcomes: the data
extrapolated from the revised studies were collected in
tables; in particular, for each study we specified: the
author, the name of the journal where the study was
published and year of publication, study characteristics
(design, setting, selection criteria, subjects included,
duration of the study, measure of mortality, …);
5. the analysis was carried out in the form of a narrative
resume of the reports
Results
Twenty-six studies were considered eligible for the sys-
tematic review [1, 5, 10, 17–39]. Tables 1 and 2 summarize
the description of study samples, procedures used to
diagnose sarcopenic obesity and the threshold values used
for sarcopenic obesity definition.
Globally, more than 23,000 subjects were studied. In
seven papers [5, 20, 29, 32, 33, 35, 37] participants were
Caucasian; one study [21] involved also African-American
subjects whereas in eight studies Asian subjects were
included [18, 22–25, 27, 30, 34]; in two papers there were
also Hispanic participants [1, 10], and one study involved
Maori individuals and Pacific Islanders [39].
In all the studies examined, except one, the definition of
sarcopenic obesity was based on the co-presence of obesity
and sarcopenia. Only in one study another definition was
chosen [18], using the calculation of the adiposity to
muscle ratio (body adiposity bearing on a unit of muscle
mass): a value above or below 0.75 was predictive of
incident or worsening physical limitation [18].
Excluding the latter study [18] in all the papers obesity
and sarcopenia were defined separately.
With respect to obesity, the following parameters were
used (as single parameters or in association to the other
adiposity measures):
– body mass index (BMI) [30 kg/m2 in nine studies [5,
22, 28, 29, 31, 33, 35–37];
– waist circumference in four studies [5, 26, 33, 35]
[102 cm in men and 88 cm in women or values higher
than the upper sex-specific tertile or quartile;
– fat mass (FM) expressed as body weight percentage in
eleven studies (10, 18, 20–23, 34, 37, 39 e 42), with
threshold values ranging from 27 to 30 % in men and
from 35 and 40 % in women (while in two studies a
unique cut-off value was applied for both the genders).
Fat mass index (FMI) was used in two studies [35, 38]
192 Mediterr J Nutr Metab (2013) 6:191–198
123
Table 1 Methods for body composition evaluation
References Sample Sarcopenia Obesity
Aubertin-Leheudre
et al. [17]
60 postmenopausal healthy women ages 55–75 years DXA DXA
Auyeung et al. [18] 4000 community-dwelling men and women aged 65 years or over
were recruited in a project primarily examining the bone mineral
density of older Chinese adults. Only ethnical Chinese subjects
DXA DXA
Barbat-Artigas et al.
[19]
112 Postmenopausal women aged 50–77 years DXA DXA
Baumgartner [1] 831 subjects (Hispanic and nonHispanic 60 years and older) from
New Mexico Elder Health Survey and the New Mexico Aging
Process Study
DXA DXA
Baumgartner et al.
[10]
451 healthy elderly from the New Mexico Aging Process Study (with
no disability at baseline)
DXA DXA
Caucasian (90 %) and Hispanic and nonwhite (other) 60 years and
older
Bouchard et al. [20] 894 subjects from the Nutrition as a determinant of successful aging
(French-Canadians); age: 68–82 years
DXA DXA
Cesari et al. [21] 286 subjects with high cardiovascular risk profile participating to the
TRAIN study: Caucasian (75 %) African-American (23 %) and
other
DXA DXA
Chung et al. [22] 4471 subjects (1856 men, 2615 women) older than 60 years of age
from the KNHANES (cross-sectional and nationally representative
survey conducted by the Korean Ministry of Health and Welfare)
DXA Anthropometrics (BMI)
Kim et al. [23] 493 subjects (180 men and 313 women) from the Korean Sarcopenic
Obesity Study (KSOS) within three age groups; 20–39 (n = 127;
young reference group), 40–59 (n = 178), and C60 years
(n = 188).
DXA and CT DXA and CT
Kohara et al. [24] 782 independent middle-aged to elderly persons recruited from
visitors to the Anti-Aging Center at Ehime University Hospital
(Japan) from March 2006 to March 2009
CT CT
Lu et al. [25] 600 community-dwelling individuals in Northern Taiwan aged
63.6 ± 10.1 years
BIA BIA
Levine and
Crimmins [26]
Males and females aged 60 and older from the National Health and
Nutrition Examination Survey (NHANES 1999–2004)
DXA Anthropometrics (WC)
Lim et al. [27] 565 subjects from the Korean Longitudinal Study on Health and
Aging 65 and older
DXA CT
Messier et al. [28] 136 postmenopausal women participating in the Montreal Ottawa
New Emerging Team study (Canada) 46–70 years of age
DXA Anthropometrics (BMI)
Monteiro et al. [29] 239 postmenopausal healthy Caucasian women (age:
57.4 ± 6.6 years)
BIA Anthropometrics (BMI)
Ochi et al. [30] 410 Japanese middle-aged to elderly subjects CT CT
Prado et al. [31] 250 patients with cancers of the lung or gastrointestinal tracts treated
in Canada. Age range: 35–88 years
CT Anthropometrics (BMI)
Rolland et al. [32] 1308 elderly French women from EPIDemiologie de l’OSteoporose
Study [75 years
DXA DXA
Schrager et al. [33] 871 participants from the InChianti study (Tuscany, Italy) [65 years Handgrip strength Anthropometrics (BMI,
WC)
Seo et al. [34] 484 subjects from the Korean Ansan Geriatric Study aged [65 years DXA DXA and CT
Siervo et al. [35] 763 overweight and obese women; age range 18–87 years from
Naples (Italy)
BIA Anthropometrics (BMI,
WC) and BIA
Srikanthan et al.
[36]
2370 women and 2284 men participating to the National Health and
Nutrition Examination Survey
BIA Anthropometrics (BMI)
(NHANES) III [60 years
Stenholm et al. [5] 2099 subjects from Health 200 Survey Finnish population; 55 and
older
Handgrip strength Anthropometrics (BMI,
WC) and BIA
Mediterr J Nutr Metab (2013) 6:191–198 193
123
involving only female participants: threshold values
were 9.5 and 11.8 kg/m2, respectively;
– visceral fat area was measured in six studies [23–25,
27, 30, 34], all using a cut-off value of 100 cm2 in both
men and women.
For sarcopenia the following parameters were used:
– appendicular skeletal muscle mass standardized for
height (ASM/ht2) in ten studies [1, 10, 19, 20, 28, 29,
32, 34, 35, 39] or body weight (ASM/Wt) in five
studies [22, 23, 26, 27, 36]. Threshold values were
established as 1 or 2 standard deviation(SD)(s) below
values for sex-specific mean for healthy young adults;
– cross-sectional area at the quadriceps level (in relation
to body weight in three studies and to height in one
paper) [24, 25, 30, 31]. Also in this case, threshold
values were considered as 1 SD below values for sex-
specific mean for healthy young adults;
– muscle strength (handgrip strength o knee extension)
[5, 33, 37, 38] considering as cut-off value the lower
sex-specific tertile or quartile;
– muscle mass index (MMI) or fat-free mass index
(FFMI) in two studies [17, 38] compared to values in a
reference population.
Body composition analysis was performed, especially
with respect to adiposity, through: DXA scan in eleven
studies [1, 10, 17–21, 23, 32, 34, 39], CT scan in five
studies [23, 24, 27, 30, 34], bioimpedance analysis (BIA) in
four studies [5, 25, 35, 38], or anthropometric parameters
(BMI, WC) in ten studies [5, 22, 27, 29–31, 33, 35–37].
The presence of sarcopenia was assessed through DXA
scan in the majority of the studies. In the remaining studies,
CT scan [23, 24, 30, 31], BIA [25, 29, 35, 36, 38] or
dynamometer test [5, 33, 37, 38] were used.
Discussion
The number of obese elderly subjects is increasing and
aging is physiologically associated with body composition
change characterized by increased fat mass and reduced
muscle mass. In some cases these phenomena are pro-
nounced, being responsible for the occurrence of a syn-
drome, the so-called sarcopenic obesity which is associated
to the worsening of physical disability, morbidity, and
mortality. Sarcopenia and obesity might act synergistically
on metabolic and functional impairments in the elderly
[27].
To date, just few papers provided clear and shared
diagnostic criteria of SO. In fact, in our review, criteria
adopted by single authors were only partially overlapping.
This is the reason why the reported prevalence varied
significantly among the study, and, obviously, a certain part
of subjects with SO was not detected, depending on the
criteria used (with important potential consequences in
terms of clinical and functional status).
One of the main obstacles is represented by the defini-
tion of SO, and especially whether it should be based only
on criteria of body composition [reduced muscle mass
(MM) and increased fat mass (FM)] or also functional
criteria should be taken into account. On the other hand,
obesity (as one of the two components of SO) is usually
defined merely according to fat mass or BMI, whereas in
the definition of sarcopenia, to the criterion of the reduced
FFM also muscle strength and functional impairment have
been added, hence required for diagnosis.
In the consensus by Cruz-Jentoft et al., the European
Working Group on Sarcopenia in Older People (EWGSOP)
[41] recommends to consider the presence of both low
muscle mass and low muscle function (strength or perfor-
mance). By this way, the EWGSOP further classifies
conceptual stages as ‘presarcopenia’, ‘sarcopenia’ and
‘severe sarcopenia’.
In the case of SO, it is likely that the same logical
pathway should be followed, even if, at present, no study
hypothesized a diagnosis of SO besides the simple evalu-
ation of body composition.
An implementation of this definition with muscle strength
and functional parameters will probably be more useful in
clinical practice. A wide range of tests is available for
physical performance evaluation, in particular in the elderly
population, including the short physical performance battery
Table 1 continued
References Sample Sarcopenia Obesity
Stenholm et al. [39] 930 elderly subjects from in CHIANTI study (Tuscany, Italy)
[65 years
Knee extensor
strength.
Anthropometrics (BMI)
Visser et al. [38] 325 patients admitted for elective coronary artery bypass grafting and/
or heart valve surgery
Handgrip strength
and BIA
BIA
Waters et al. [39] 206 community-dwelling older adults (65 years or older; 55 ? years
for Maori and Pacific Islanders) plus having an increased risk of
falling or having had at least one fall in the past 12 months
DXA DXA
DXA dual energy X-ray absorptiometry, CT computed tomography, BMI body mass index, WC waist circumference, BIA bioimpedance analysis
194 Mediterr J Nutr Metab (2013) 6:191–198
123
Table 2 Reference values of body composition parameters for the definition of sarcopenic obesity
Reference Sarcopenia Obesity
Aubertin-Leheudreet al. [17]
MMI \14.30 kg/m2; FFMI: 1 SD lower than the MMI of a referencesample
FM [35 %
Auyeung et al. [18] Adiposity to muscle ratio (body weight or adiposity bearing on a unit of muscle mass could) equal to or greater than 0.75
Barbat-Artigaset al. [19]
Type I sarcopenia: ASM/ht2 1-2 SD below values for young adults(5.75–6.75 kg/m2)
FM [40 % obese individuals
Type II sarcopenia: ASM/ht2 \2SDs or more below 5.75 kg/m2
Baumgartner [1] ASM/ht2 \2 SD below the sex-specific mean for a young adultreference population
FM [than sex- and age specific median: 38 % forwomen and 27 % for men
Baumgartner et al.[10]
ASM/ht2 \2SD below mean of healthy young adults: \7.26 kg/m2 inmen and \5.45 kg/m2 in women
FM [40 % for women and [28 % for men
Bouchard et al. [20] ASM/ht2 \2SD below sex-specific mean for healthy young cohort:\6.29 kg/m2 in women and \8.51 kg/m2 in men
FM [35 % in women and [28 % in men
Cesari et al. [21] Lowest tertile of the residuals between ASM on FM and height(residuals of fat-adjusted ASM): 0.47 for the men and 2.79 for thewomen.
Age, gender and ethnic specific cut-offs for FMpreviously proposed by Gallagher et al. [40]
Chung et al. [22] ASM/Wt\1 SD below the mean of a reference group of healthy adultsaged 20–39 years: 32.5 % for men, 25.7 % for women
BMI [25 kg/m2
Kim et al. [23] ASM/Wt \1 SD below the sex-specific mean value for the youngreference group: 39.7 % in men and 34.1 % in women
Visceral fat area [100 cm2 in both men andwomen
Kohara et al. [24] CSA/Wt within 1SD of the distribution in reference subjects aged\50 years
Visceral fat area [100 cm2 in both men andwomen
Lu et al. [25] CSA/Wt within one standard deviation value of the CSA/BWdistribution in subjects aged, 50 years among
Visceral fat area [100 cm2 in both men andwomen
Levine andCrimmins [26]
ASM/Wt \2 SD below the mean of a young reference group: 25.72 %for males and 19.43 % for females
WC [102 cm for males and 88 cm for females
Lim et al. [27] ASM/Wt\1SD below mean reference of young cohort: 29.9 % for menand 25.1 % for women
Visceral fat area [100 cm2 in both men andwomen
Messier et al. [28] ASM/ht2 \6.44 kg/m2 and 5.05 kg/m2 respectively for class I and IIsarcopenia
BMI [27 kg/m2
Monteiro et al. [29] ASM/ht2 \1 SD of the sex-specific mean for young females BMI [25.5 kg/m2
Ochi et al. [30] Quadriceps muscle CSA/Wt \ 1SD value of the CSA distribution in ayoung reference group (independently for men and women)
Visceral fat area [100 cm2 in both men andwomen
Prado et al. [31] Sex-specific cut points for L3 muscle CSA adjusted by height definedby optimal stratification analysis cut points based on mortality:52.4 cm2/m2 for men and 38.5 cm2/m2 for women.
BMI [30 kg/m2
Rolland et al. [32] ASM/ht2 2 SD below the mean in a young female reference group:5.45 kg/m2
FM [60th percentile of study sample
Schrager et al. [33] Tertiles of muscle strength (grip strength): lowest sex-specific tertile Central obesity: waist circumference: upper sex-specific tertile
Global obesity: BMI [30 kg/m2
Seo et al. [34] ASM/ht2 1 SD below the sex-specific mean of a young reference group:6.75 kg/m2 for men and 4.96 kg/m2 for women
Visceral fat area [100 cm2 in both men andwomen
Siervo et al. [35] ASM/ht2 2SD below reference population: 6.76 kg/m2 BMI [30 kg/m2, WC [88 cm, FM [ 35 %, FMI[9.5 kg/m2
Srikanthan et al.[36]
ASM/Wt\2SD sex-specific, young adult (ages, 18–39) means: 31.0 %in men and 22.0 % in women
BMI [30 kg/m2
Stenholm et al. [5] Muscle strength: sex-specific quartiles FM and WC sex-specific quartiles; BMI: WHOcut-offs
Stenholm et al. [39] Lowest sex-specific tertile of knee extensor strength BMI [30 kg/m2
Visser et al. [38] FFM index\14.6 kgm2 for women, and 16.7 kgm2 for men; 8.3 kg/m2
for menFMI [11.8 kg/m2 for women
Handgrip strength \85 % of its age–sex standardized
Waters et al. [39] ASM/ht2 \7.2 kg/m2 in males and \5.4 kg/m2 in females FM C30 % in males and C40 % in females
ASM appendicular skeletal mass, ASM/ht2 relative skeletal muscle mass index, ASM/Wt ASM as a percentage of body weight, BMI body mass index,CSA cross-sectional area, CSA/Wt thigh muscle cross-sectional area corrected by body weight, FFMI fat-free mass index, FM fat mass, FMI fat massindex, MMI muscle mass index, SMI skeletal muscle index, WC waist circumference
Mediterr J Nutr Metab (2013) 6:191–198 195
123
(SPPB), the usual gait speed, the 6-min walk test and the stair
climb power test [42]. Encompassing functional informa-
tion, this definition will be more responsive to the patient’s
clinical status and to the severity of the disease. Moreover, it
will also make easier to imagine the course of the nutritional
and rehabilitation treatment and to identify the outcomes to
be achieved. In fact, the increase in FM together with the
deterioration of lean body mass (with possible fatty infil-
tration) may lead to a progressive worsening of functional
parameters such as aerobic capacity, muscle strength,
walking speed, and ability to maintain balance.
In addition, in our view, a definition of sarcopenia based
on the reduction of muscle mass in ‘‘absolute’’ terms is
limited in the case of obesity and does not describe thor-
oughly the picture of obese subjects in terms of body
composition. Initially, at least in younger obese subjects,
the increase of fat mass is accompanied by a physiological
increase of muscle mass [43–46] which enables to main-
tain, for a relatively long time, a good metabolic control
and a satisfactory physical efficiency. Nevertheless, signs
of sarcopenia appear at an early stage in the obese subjects;
as a matter of fact, a relative and not an absolute reduction
of muscle mass is sufficient to determine a reduced func-
tional performance. An index of sarcopenia in obese sub-
jects based on a reduction in the ratio between measured
muscle mass and ideal (estimated) muscle mass is under
validation [47].
Other indices have been used in the literature to assess
muscle mass and fat mass. One of the most commonly used
indices for the definition of sarcopenia is the total appen-
dicular skeletal muscle (ASM) index: subjects included in
the lowest quantile group or -2SD values of a gender-spe-
cific distribution of muscle mass in a reference population
of young, healthy subjects as cut-off points are identified as
sarcopenic subjects while FFM has been adjusted to height
squared to take into account the differences in body size.
The adjustment for height squared has been the preferred
method but the adjustment for body weight has also been
applied. Subjects below the 50th calculated percentile for
FFMI are considered sarcopenic [11].
Another important issue in the identification of sarco-
penic obese subjects is represented by methods and tools to
be used for the assessment of body composition as well as
the choice of functional indicators. In research settings, two
imaging techniques have been used for estimating muscle
mass or fat mass [computed tomography (CT scan) and
magnetic resonance imaging (MRI)]; these techniques, and
to a lesser extent, dual energy X-ray absorptiometry
(DXA), are considered to be very precise imaging systems,
able to separate fat from other soft tissues in the body.
However, high cost, limited access to equipment in some
facilities and concerns about radiation exposure limit the
use of these whole-body imaging methods for routine
clinical practice. BIA may represent a valid alternative to
these methods in clinical practice being inexpensive, easy
to use and readily reproducible. BIA results, obtained
under standard conditions, have been found to correlate
well with gold standard techniques [48].
In some papers, the FFM evaluation has been coupled to
or replaced by the evaluation of muscle strength, especially
of lower limb strength [37] or more frequently handgrip
strength. These measures are relevant for gait and physical
function, and have a good correlation with clinical and
functional outcomes. Low cost, availability and easiness of
use make handgrip strength a valid parameter to be
assessed in clinical practice in addition to research settings.
On the other hand, it should be underlined that these
indicators cannot replace at all neither the body composi-
tion evaluation nor functional parameters.
Finally, the choice of threshold values needs to be dis-
cussed. Cut-off points depend on the measurement tech-
nique chosen and on the availability of reference studies.
Similarly to what happens for bone mineral density, a
normative population (healthy young adults) was used,
with cut-off points at two standard deviations below the
mean reference value. In the present review, the diverse
threshold values and methods adopted by different authors
make difficult the comparison of papers. It represents a
relevant limitation, given that in the research fieldwork
different intervention procedures need to be compared as
well as in clinical practice it is important to verify the
outcomes of interventions.
In conclusion, further epidemiological data are needed
to obtain good reference values for populations in different
countries and for different ethnicities.
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