-
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ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 6Digestive and
Liver Disease xxx (2015) xxxxxx
Contents lists available at ScienceDirect
Digestive and Liver Disease
jou rna l h om epage: www.elsev ier .com/ locate /d ld
Liver, Pancreas and Biliary Tract
Sarcopenia is a risk factor for elevated aminotranindepe
itsactivity
Ki Deok Y e, OByung ChDepartment of
a r t i c l
Article history:Received 19 August 2014Accepted 24 December
2014Available online xxx
Keywords:Alanine aminotransferaseAspartate amiMuscle
massSarcopeniaSkeletal muscl
y is awith obesity and metabolic syndrome. However, elevated
aminotransferase activity is not uncommon innon-obese and
non-alcoholic patients in clinical practice.Aim: To examine the
relationship between sarcopenia and aminotransferase activity in a
large population-based cohort.Methods: Data from the Korean
National Health and Nutrition Examinations were used. A total of
13,431subjects were included. A whole-body dual X-ray
absorptiometry scan was performed on each patient to
1. Introdu
Alanine (AST) are twhepatitis, hare commoels [1]. Hoelevated
livmetabolic dhepatitis, owho presenand metabo
CorresponCollege of MedKorea. Tel.: +8
E-mail add
http://dx.doi.o1590-8658/ this article in press as: Yoo KD, et
al. Sarcopenia is a risk factor for elevated aminotransferase in
men independently of bodyx, dietary habits, and physical activity.
Dig Liver Dis (2015),
http://dx.doi.org/10.1016/j.dld.2014.12.014
notransferase
e index
measure total and regional muscle mass. Appendicular skeletal
muscle mass indices were also obtained.Results: The prevalence of
sarcopenia was signicantly higher in the group with elevated
aminotrans-ferase levels than in the normal liver enzyme group
(males: 26.5% vs. 16.9%; females: 38.3% vs. 22.1%,p < 0.05). The
skeletal muscle index was negatively correlated with most
cardiometabolic risk factors,including fasting glucose and
cholesterol levels. The frequency of elevated aminotransferase
increasedin male patients with sarcopenia after adjusting for
potential confounding factors including age, bodymass index,
fasting glucose level, dietary, and exercise habits. However, the
correlation was no longerobserved in women after adjusting for body
mass index.Conclusion: Sarcopenia is a risk factor for elevated
aminotransferase in men, independently of body massindex, dietary
habits, and physical activity.
2015 Editrice Gastroenterologica Italiana S.r.l. Published by
Elsevier Ltd. All rights reserved.
ction
aminotransferase (ALT) and aspartate aminotransferaseo
well-known serologic markers of liver injury. Viral
eavy alcohol use, hepatotoxic drug use, and obesityn risk
factors for abnormal aminotransferase lev-wever, it is not uncommon
for patients who shower enzymes to lack the traditional risk
factors forisease, including obesity, herbal medication use, viralr
signicant alcohol consumption. Non-obese patientst metabolic
diseases, including diabetes, hypertension,lic syndrome, are also
common. Despite using strict,
ding author at: Department of Internal Medicine, Hanyang
University,icine, 17 Haengdang-dong, Sungdong-gu, Seoul 133-792,
Republic of2 2 2290 8338; fax: +82 2 972 0068.ress:
[email protected] (D.W. Jun).
ethnicity-specic criteria, many Asian-Pacic subjects
havingdiabetes or hypertension are also non-obese [1,2]. Genetic
back-ground, fat distribution, unhealthy dietary habits, and
lifestyleshave all been suggested as risk factors for the
development ofmetabolic disease in non-obese subjects [35].
Recently, several studies have addressed metabolic diseasesin
non-obese patients [2,3,6]. Some researchers have reportedthe
impact of muscle mass on metabolic disease incidence
[69].Sarcopenia is a syndrome characterized by progressive and
gen-eralized loss of skeletal muscle mass and strength [10].
Severalresearch groups have found that sarcopenia is associated
withinsulin resistance, type 2 diabetes, dyslipidemia, and
hypertension[8,9,11]. Sarcopenia often occurs in elderly people
with normalbody mass index (BMI) [12]. However, the relationship
betweensarcopenia and liver enzymes or fatty liver disease has been
rarelystudied. Hong et al. showed that the skeletal muscle index
(SMI) isnegatively associated with intrahepatic fat accumulation
[13]. Thisprovided a novel insight into the mechanism linking
sarcopenia
rg/10.1016/j.dld.2014.12.0142015 Editrice Gastroenterologica
Italiana S.r.l. Published by Elsevier Ltd. All rights
reserved.ndently of body mass index, dietary hab
oo, Dae Won Jun , Kang Nyeong Lee, Hang Lak Leul Yoon, Ho Soon
Choi
Internal Medicine, Hanyang University, College of Medicine,
Seoul, Republic of Korea
e i n f o a b s t r a c t
Background: Aminotransferase activitsferase in men, and
physical
h Young Lee,
surrogate marker of liver injury showing strong correlations
-
Please cit r elevmass inde /dx.d
ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 62 K.D. Yoo et
al. / Digestive and Liver Disease xxx (2015) xxxxxx
and non-alcoholic fatty liver disease (NAFLD) [13]. However,
itis still unclear whether an elevated aminotransferase activity
isassociated with sarcopenia in non-obese subjects or in the
generalpopulation with few or no risk factors for liver
disease.
The effeprovide clienzymes inevaluation iapproachesto identify
aactivity, indand amoun
2. Method
2.1. Subject
This stuNational He1) (200920the KNHANPopulation type, the ntive
districtmethod to with the powere extracregion. Gropling unit, was
samples
The KNHsurvey, a ninterview sviewer in ohypertensioother
diseaand, in thishol intake wuse by the measured nmethod, astrained
inte
2.2. Selectio
A total underwentabsorptiom472 individmales and fa week,
resliver cirrhotest or for were also ethe study (S
2.3. Termin
Appendiwhole-bodyUSA) to meeral contenbody fat petargeted
thsubtractingfollows: sta
and bone mineral contents were subtracted, supposing that the
tis-sue without bone and fat is skeletal muscle. The SMI was
calculatedby dividing the ASM by weight according to the method
used inprevious studies [SMI (%) = total skeletal muscle mass
(kg)/weight
100] ne stts (19
than
ood c
od teast, wterolDL), iatelthe sal chteroler (Sichemated
atisti
Stuaractmineactorwas f sar
and.05 wicag
ults
ver es
freqn ma(mal1). d lowglucoactivl dels. In
oldeto then snciesevels
amo abnoed (
rrelan bot
en wiver en coLT lee this article in press as: Yoo KD, et al.
Sarcopenia is a risk factor fox, dietary habits, and physical
activity. Dig Liver Dis (2015), http:/
cts of muscle mass on aminotransferase activity maynicians a
better understanding of the elevated liver
non-obese patients who show no risk factors uponn outpatient
clinics, and could also suggest therapeutic
for lean NAFLD patients. The purpose of this study was
correlation between sarcopenia and aminotransferaseependently of
BMI, body fat percentage, dietary habits,t of exercise.
s
s
dy used source data from the Fourth and Fifth Koreaalth and
Nutrition Examination Surveys (KNHANES V-10, Korea Centers for
Disease Control and Prevention);ES includes every household and
individual in its latestand Housing Census. With regard to region
and housingation was divided into 29 strata, and 200 administra-s
were extracted by applying a proportional allocationmatch the
sample component ratios for each stratumpulation stratication
variable. Enumeration districtsted to reect the house
characteristics in the selectedups of 2030 houses, which made up
the third sam-ere extracted from the enumeration districts
selected
in systematic sampling.ANES survey was subdivided into a health
interview
utrition survey, and a health examination. The healthurvey was
carried out face-to-face by a trained inter-rder to identify
individuals diagnosed with diabetes,n, hepatitis C, liver
cirrhosis, liver cancer, or variousses, as well as to identify the
subjects taking medicines
latter case, the type of medicines being taken. Alco-as
calculated by multiplying the frequency of alcohol
amount of alcohol consumption. The nutrition surveyutrient
intake levels using the one-day 24-hour recall
determined in the one-on-one conversations with arviewer.
n of the subject group
of 15,119 subjects older than 19 years of age who a blood test,
dietary survey, and dual-energy X-rayetry (DXA) were initially
selected. Of these, we excludeduals who tested positive for
hepatitis B antigen, 1197emales who drank more than 210 and 140 g
of alcoholpectively, and 19 subjects with a history of hepatitis
C,sis, or liver cancer. Patients who did not receive a bloodwhom
there was insufcient data on nutrient intakexcluded. Finally,
14,628 individuals were included inupplementary Figure S1).
ology
cular skeletal muscle mass (ASM) was measured by DXA using a fan
beam densitometer (Hologic Inc., MA,asure total and regional lean
mass (kg), total bone min-ts (kg), BMD (kg/m2), total body fat mass
(kg), and totalrcentage. Two X-ray beams with different energy
levelse subjects bones. The BMD could then be calculated by
the soft tissue absorption. The ASM was calculated asrting from
the total lean mass, the total body fat mass
(kg) least osubjechigher[14].
2.4. Bl
Blohour fcholestein (Himmedlab on for
totcholesanalyselectroautom
2.5. St
Theical chto exaother fmass mine ihabits,A p < 0Inc., Ch
3. Res
3.1. Lisubject
Theboth igroup p < 0.00showeblood ferase
mineracontroobese,pared
Whfrequeeride las thecies ofincreas
3.2. Colevels i
Whmass, lrelatiowith Aated aminotransferase in men independently
of bodyoi.org/10.1016/j.dld.2014.12.014
[9,10,13]. Sarcopenia was dened if the result was as atandard
deviation (SD) below the muscle mass of young39 years) [9,10,13].
Abnormal ALT was dened as ALT
30 U/L for males, and higher than 19 U/L for females
hemistry
sts, which were performed on all subjects after a 12-ere
conducted for hepatitis B antigen, AST, ALT, total
, low density lipoprotein (LDL), high density lipopro-and
triglycerides. Blood samples were centrifuged, theny refrigerated
and sent in iceboxes to a single centralame day of blood
collection. Routine biochemical testsolesterol, triglycerides,
glucose, HDL cholesterol, LDL, ALT, and AST were performed with an
ADIVIA 1650emens, Deereld, IL, USA). HBsAg was measured with
aniluminescence immunoassay method using an E-170
analyser (Roche, Penzberg, Germany).
cal analysis
dents t-test was used to compare the patients clin-eristics, and
partial Pearsons correlations were used
the relationships between skeletal muscle mass ands associated
with metabolic syndrome. Skeletal muscledivided into four levels
for the analysis. To deter-copenia was a risk factor independent of
BMI, dietary
exercise, a logistic regression analysis was performed.as
considered statistically signicant. SPSS 17.0 (SPSSo, IL) for
Windows was used for all statistical analyses.
nzymes and metabolic parameters in sarcopenic
uency of elevated aminotransferase activity was higherles and
females with sarcopenia than in the controles: 26.5% vs. 16.3%, p
< 0.001; females: 38.3% vs. 16.3%,Although male and female
subjects with sarcopeniaer total calorie intake, they showed higher
fastingse, insulin, triglyceride, cholesterol, and aminotrans-ity
levels (Table 1). Weekly exercise hours and bonensity were lower in
the sarcopenic group than normal
the sarcopenic group we found more subjects that werer, more
sedentary, and had lower calorie intake com-e control group, and
this was true for both genders.keletal muscle mass was classied
into quartiles, the
of abnormal ALT, fasting blood glucose, and triglyc- were
negatively correlated with muscle mass. Namely,unt of skeletal
muscle mass decreased, the frequen-rmal LFT, fasting blood glucose,
and triglyceride levelsFig. 1).
tions between skeletal muscle mass and liver enzymeh genders
after adjusting for body mass index and age
e examined the correlations between skeletal musclenzymes, and
metabolic parameters using Pearsons cor-efcients, ASM was found to
be negatively correlatedvels for both genders (r = 0.222 for males
and r = 3.17
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ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 6K.D. Yoo et al.
/ Digestive and Liver Disease xxx (2015) xxxxxx 3
Table 1Comparison of clinical and metabolic parameters according
to skeletal muscle index.
Males Females
Normal SMI Sarcopenia *p Normal SMI Sarcopenia *pN = 4064 N =
960 N = 5315 N = 1901
Age (years) 43.3 19.0 48.1 22.4
-
Please cite this article in press as: Yoo KD, et al. Sarcopenia
is a risk factor for elevated aminotransferase in men independently
of bodymass index, dietary habits, and physical activity. Dig Liver
Dis (2015), http://dx.doi.org/10.1016/j.dld.2014.12.014
ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 64 K.D. Yoo et
al. / Digestive and Liver Disease xxx (2015) xxxxxx
Table 2Partial correlations of skeletal muscle index and
clinical parameters.
Partial correlation (I) Age Partial correlation (II) Age,
BMI
Male Female Male Female
r *p r *p r *p r *p
ALT (U/L) 0.284
-
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ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 6K.D. Yoo et al.
/ Digestive and Liver Disease xxx (2015) xxxxxx 5
3.3. Multivariate analysis of the effect of skeletal muscle mass
onthe frequencies of elevated liver enzymes and fatty liver
disease
Multiple logistic regression analysis with abnormal liverenzyme
as an increasecopenic maglucose lev(Supplemenobserved in
4. Discussi
BMI, diewith aminomuscle mascontrolling in males. Sshowed
grepresenting
Several metabolic ssimilar to thgated the efHong and MDXA, and
bcle mass waet al. showfat accumulanism linkisubjects
wegeneralizatwhich inclu
An emeris a risk facbody shapecopenia onadjust for fsarcopenia
ple ratio beaffected byadjust for Bmass, as wecle mass onimpact of
saeffects of mfor women tal muscle dto play an e
To bettemen and wand 2893 psis showed disease
did(Supplemendependent liver is not dfact that woimpact of b
Other mdietary haba relationshpendently omuch lowewith the
co
subjects were higher than those of the controls (Table 1).
Anotherinteresting nding is that low protein intake, and not high
fatintake, was correlated with sarcopenia and elevated liver
enzymes.Sarcopenic subjects were also characterised by lower serum
vita-
levelenic thaned pd as tion.
cohtion te thcidecise.ur st
masndic
squaf sathe easeht; height0% inropris wa
c lowhis stscleopen
for senia,
prelow tlinicaal L
histdiolo
somgic eplaina coulaineare is stu
habethoietarere gatoucat
to pts (0ce atwees are, althl userformc livee theNHA, and.
Thi
hav this article in press as: Yoo KD, et al. Sarcopenia is a
risk factor forx, dietary habits, and physical activity. Dig Liver
Dis (2015), http:/
the dependent variable was performed and showedd frequency of
elevated aminotransferase levels in sar-le patients after
controlling for age, BMI, smoking status,el, insulin level, as well
as dietary and exercise habitstary Table S1). However, this
correlation was no longer
women after controlling for BMI.
on
tary habits, and physical exercise have been
correlatedtransferase activity. Our results show that the skeletals
was correlated with aminotransferase activity afterfor BMI, dietary
habits, and amount of exercise onlyarcopenic subjects were older,
more sedentary, andater central obesity compared with controls,
despitea lower total calorie intake.studies have investigated the
impact of sarcopenia onyndrome [9,11,15]. The pathophysiology of
NAFLD isat of metabolic syndrome, but few studies have investi-fect
of muscle mass on the incidence of NAFLD. Recently,oon used
abdominal computed tomography (CT) scan,ody impedance assay (BIA)
to show that skeletal mus-s associated with the incidence of NAFLD
[13,16]. Honged that SMI is negatively associated with
intrahepatication [13]. This provided a novel insight into the
mech-ng sarcopenia and NAFLD. Although more than 450re enrolled in
their study, a selection bias may limit theion of their results. We
used data from the KNHANES,des the most relevant and representative
data.ging issue regarding sarcopenia is whether muscle masstor for
NAFLD and metabolic disease independently of
or BMI. Therefore, when analysing the impact of sar- fatty liver
and metabolic diseases, it is important toat mass and BMI. In Moons
study, the denition offollowed the Janssens method [17]. However,
the sim-tween body weight and muscle mass may be greatly
the amount of total fat. Likewise, Hong et al did notMI [13]. In
the present study, we adjusted for body fatll as total body fat,
when analysing the effects of mus-
metabolic disease and fatty liver. We found that thercopenia on
liver enzymes was gender-dependent: theuscle mass on liver enzymes
were no longer signicantafter controlling for BMI. The absolute
volume of skele-iffers between genders, and sex hormones are
knownssential role in muscle growth and development [18].r
understand the reasons for these differences betweenomen, we
compared 4020 premenopausal women
ostmenopausal women. However, multivariate analy-that the
effects of ASM on liver enzymes and fatty liver
not differ between pre- or post-menopausal womentary Table S2).
Thus, it seems likely that the gender-effect of sarcopenia on both
ALT and incidence of fattyue to female sex hormones, but rather
results from themen have less muscles than men, resulting in a
greaterody fat mass rather than muscle mass.ajor risk factors of
abnormal liver enzyme levels areits, physical activity, and age.
This study clearly showedip between liver enzymes and peripheral
ASM, inde-f BMI, dietary habits, and physical activity. Despite
ther total calorie intake of the sarcopenic group comparedntrol
group, BMI and body weight of the sarcopenic
min D sarcoprather increasmenderestrica largepopulaevalualevel
inof exer
In omuscleOther iby thecator obelow be incrof heigoverwbeing be
appand thuspeci
In tthe muon SarcinitionsarcopsideredSDs be
In cabnormcarefuland raever, inradiolocan excopeniunexpis not
r
Thidietarythis mterm ddata winvesticic edabilitypatienin Franing
bereportSecondalcohonot pechroniDespitfrom Kbiopsysurveytend toated
aminotransferase in men independently of
bodyoi.org/10.1016/j.dld.2014.12.014
s and less physical activity. The clinical characteristics
ofobesity were sedentary lifestyle and low protein intake
high calorie intake or high fat diet. This suggests thathysical
activity and protein intake should be recom-lifestyle modications
rather than calorie or fat intakeAnother strong point of this study
is that it includedort of 14,628 subjects representative of the
Koreanand based on the KNHANES data. This allowed us toe impact of
sarcopenia on abnormal aminotransferasence after correcting for
BMI, dietary habits, and amount
udy, we used the SMI, which is dened as total skeletals
(kg)/weight (kg) 100, as an indicator of sarcopenia.ators of
sarcopenia were also present. The ASM dividedred height
(ASM/height2) is also often used as an indi-rcopenia. Sarcopenia
can also be dened as two SDsmean ASM/height2. As the height
increases, ASM cand. The indicator ASM/height2 could adjust the
inuenceowever, this indicator could be inuenced by obesity. In
subjects the prevalence of sarcopenia was 8.9%, while obese
people. Therefore, this indicator seems not toate for obese people
in the diagnosis of sarcopenia [19],s not used in our study.
Another indicator is the gender-est 20th percentile of ASM.udy, we
dened sarcopenia as a value at least 1 SD below
mass of young subjects. The European Working Groupia in Older
People (EWGSOP) developed a practical def-arcopenia [10]: in their
report, they used SDs to dene
measured in terms of SMI. Class-I sarcopenia was con-sent in
subjects whose SMI was between one and twohe mean values for young
adults [9,10,13,17,20].l practice, there are several aetiologies
that could causeFT. In almost all cases of patients with abnormal
LFT, aory and physical examination with a simple blood testgic test
can reveal the aetiology of abnormal LFT. How-e cases, the
aetiology is unclear after both serologic andvaluation. Our current
study suggests that sarcopenia
several abnormal LFT of unclear aetiology. Also, sar-ld be an
aetiologic clue for non-obese patients with
d elevation of serum aminotransferase, a condition thatn the
Asian population.dy had some limitations. First, the KNHANES
surveyedits using the one-day 24-hour recall method. Thus,d does
not allow an easy quantication of the long-y habits, since it
relies on the subjects memory. Allcollected by well-trained
investigators; despite thers were not physicians, they received
regular and spe-ion for this large-scale survey providing them a
gooderform a survey. In our study, 19 among the 15,000.13%) had
liver cirrhosis. Previous studies conductednd UK reported a
prevalence of liver cirrhosis rang-n 0.076% and 0.3% [21,22]. Thus,
we believe that our
comparable with the results of the previous studies.ough we
excluded HBsAg-positive subjects, signicantrs, and subjects with a
history of liver disease, we did
further analysis to help revealing the aetiology of ther disease
(e.g. HCV-RNA, PCR test, and autoantibodies).
large part of the data used in our study was obtainedNES,
platelet counts, abdominal ultrasonography, liver
liver stiffness test were not performed within this samerd,
studies analysing large amounts of data generallye low p-values.
Although several metabolic parameters
-
Please cit r elevmass inde /dx.d
ARTICLE IN PRESSG ModelYDLD-2798; No. of Pages 66 K.D. Yoo et
al. / Digestive and Liver Disease xxx (2015) xxxxxx
showed correlations with sarcopenia in our study, the presence
ofa statistical signicance is not always indicative of clinical
signi-cance.
In conclusion, sarcopenia is a risk factor for elevated
amino-transferase levels in men, independently of BMI, dietary
habits, andphysical activity. Sarcopenic subjects with abnormal
aminotrans-ferase levels showed different clinical characteristics
comparedwith non-sarcopenic subjects. We believe that not all
patients withabnormal liver function test require further
examination of mus-cle mass. However, subjects who have abnormal
aminotransferaseactivity with uncertain aetiology, and especially
those with a nor-mal BMI, need to undergo an estimation of muscle
mass.
Conict of interestNone declared.
Funding
This study was supported by a grant from the Korea
HealthcareTechnology R&D Project, Ministry of Health &
Welfare, Republicof Korea (A121185). The funding source had no role
in the studydesign or conduct; in data collection, analysis, or
interpretation; orin manuscript preparation, review, or
approval.
Appendix A. Supplementary data
Supplementary data associated with this article can be found,
inthe online version, at
http://dx.doi.org/10.1016/j.dld.2014.12.014.
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Sarcopenia is a risk factor for elevated aminotransferase in men
independently of body mass index, dietary habits, and phy...1
Introduction2 Methods2.1 Subjects2.2 Selection of the subject
group2.3 Terminology2.4 Blood chemistry2.5 Statistical analysis
3 Results3.1 Liver enzymes and metabolic parameters in
sarcopenic subjects3.2 Correlations between skeletal muscle mass
and liver enzyme levels in both genders after adjusting for body
mass index ...3.3 Multivariate analysis of the effect of skeletal
muscle mass on the frequencies of elevated liver enzymes and fatty
liv...
4 DiscussionConflict of interestFundingAppendix A Supplementary
dataReferences