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Relationship between Physical Activity, Oxidative Stress, and Total Plasma Antioxidant Capacity in Spanish Children from the GENOBOX Study

Author: Llorente Cantarero, Francisco Jesús; Aguilar Gómez, Francisco Javier; Leis Trabazo, María Rosaura; Bueno, Gloria; Rupérez, Azahara I.; Anguita Ruiz, Augusto; Vázquez Cobela, Rocío; Mesa, María Dolores; Moreno Aznar, Luis A.; Gil, Ángel; Aguilera, María C
Publisher: MDPI
Year: 2021
DOI: 10.3390/antiox10020320
Source: https://minerva.usc.es/bitstreams/7b108152-c95a-4bcd-a2a5-7d972882638f/download
an ioxidan s
A icle
Rela ionship be ween Physical Ac i i y, Oxida i e S ess, and
To al Plasma An ioxidan Capaci y in Spanish Child en om
he GENOBOX S udy
F ancisco Jesús Llo en e-Can a e o 1,2,† , F ancisco Ja ie Aguila -Gómez 3,† , Rosau a Leis 2,4 ,
Glo ia Bueno 2,5,6, Azaha a I. Rupé ez 6, Augus o Angui a-Ruiz 2,7,8 , Rocío Vázquez-Cobela 2,4,
Ma ía Dolo es Mesa 7,8 , Luis A. Mo eno 2,6 ,Ángel Gil 2,7,8 , Concepción Ma ía Aguile a 2,7,8,*
and Me cedes Gil-Campos 2,3


Ci a ion: Llo en e-Can a e o, F.J.;
Aguila -Gómez, F.J.; Leis, R.; Bueno,
G.; Rupé ez, A.I.; Angui a-Ruiz, A.;
Vázquez-Cobela, R.; Mesa, M.D.;
Mo eno, L.A.; Gil, Á.; e al.
Rela ionship be ween Physical
Ac i i y, Oxida i e S ess, and To al
Plasma An ioxidan Capaci y in
Spanish Child en om he
GENOBOX S udy. An ioxidan s 2021,
10, 320. h ps://doi.o g/10.3390/
an iox10020320
Academic Edi o : Ba ba a Ta azz
Recei ed: 1 Feb ua y 2021
Accep ed: 18 Feb ua y 2021
Published: 20 Feb ua y 2021
Publishe ’s No e: MDPI s ays neu al
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Copy igh : © 2021 by he au ho s.
Licensee MDPI, Basel, Swi ze land.
This a icle is an open access a icle
dis ibu ed unde he e ms and
condi ions o he C ea i e Commons
A ibu ion (CC BY) license (h ps://
c ea i ecommons.o g/licenses/by/
4.0/).
1Depa men o Speci ic Didac ics, Facul y o Educa ion, Maimónides Ins i u e o Biomedicine Resea ch o
Có doba (IMIBIC), Uni e si y o Có doba, 14071 Có doba, Spain; [email p o ec ed]
2CIBEROBN, (Physiopa hology o Obesi y and Nu i ion) Ins i u e o Heal h Ca los III (ISCIII),
28029 Mad id, Spain; [email p o ec ed] (R.L.); [email p o ec ed] (G.B.);
augus oangui a@ug .es (A.A.-R.); cobela. [email p o ec ed] (R.V.-C.); lmo eno@uniza .es (L.A.M.);
agil@ug .es (Á.G.); me [email p o ec ed] (M.G.-C.)
3Me abolism and In es iga ion Uni , Reina So ía Uni e si y Hospi al, Maimónides Ins i u e o Biomedicine
Resea ch o Có doba (IMIBIC), Uni e si y o Có doba, 14004 Có doba, Spain; [email p o ec ed]
4Uni o In es iga ion in Nu i ion, G ow h and Human De elopmen o Galicia, Pedia ic Depa men ,
Uni e si y o San iago de Compos ela, Clinic Uni e si y Hospi al o San iago, Ins i u o de In es igación
Sani a ia de San iago (IDIS), 15706 San iago de Compos ela, Spain
5Pedia ic Endoc inology Uni , Clinic Uni e si y Hospi al Lozano Blesa, Facul ad de Medicina, Uni e sidad
de Za agoza, 50009 Za agoza, Spain
6
GENUD Resea ch G oup, Ins i u o Ag oalimen a io de A agón (IA2), Ins i u o de In es igación Sani a ia (IIS)
A agón, Uni e si y o Za agoza, 50009 Za agoza, Spain; ai upe ez@uniza .es
7Depa men o Biochemis y and Molecula Biology II, Ins i u e o Nu i ion and Food Technology “José
Ma aix”, Cen e o Biomedical Resea ch, Uni e si y o G anada, A milla, 18016 G anada, Spain;
mdmesa@ug .es
8Ins i u o de In es igación Biosani a ia ibs G anada, 18014 G anada, Spain
*Co espondence: caguile @ug .es; Tel.: +34-9-5824-1000 (ex . 20314)
† These au ho s con ibu ed equally o his wo k.
Abs ac :
The Wo ld Heal h O ganiza ion has ecommended pe o ming a leas 60 min a day o
mode a e- o- igo ous physical ac i i y (MVPA) and educing seden a ism in child en and adolescen s
o o e signi ican heal h bene i s and mi iga e heal h isks. Physical i ness and spo s p ac ice
seem o imp o e oxida i e s ess (OS) s a us du ing childhood. Howe e , o ou knowledge, he e
a e no da a ega ding he in luence o objec i ely-measu ed physical ac i i y (PA) and seden a ism
on OS s a us in child en and adolescen s. The p esen s udy aimed o e alua e he in luence o
mode a e and igo ous PA and seden a ism on OS and plasma o al an ioxidan capaci y (TAC) in a
selec ed Spanish popula ion o 216 child en and adolescen s om he GENOBOX s udy. PA (ligh ,
mode a e, and igo ous) and seden a ism (i.e., seden a y ime (ST)) we e measu ed by accele ome y.
A Physical Ac i i y-Seden a ism Sco e (PASS) was de eloped in eg a ing mode a e and igo ous
PA and ST le els. U ina y 8-hyd oxy-20-deoxyguanosine (8-OHdG) and isop os ane F2α(F2-IsoPs),
as ma ke s o OS, we e de e mined by ELISA; and TAC was es ima ed by colo ime y using an
an ioxidan ki . A highe PASS was associa ed wi h lowe plasma TAC and u ina y 8-OHdG and
F
2
-IsoPs, showing a be e edox p o ile. Reduced OS ma ke s (8-OHdG and F
2
-IsoPs) in child en
wi h highe PASS may diminish he need o main aining high concen a ions o an ioxidan s in
plasma du ing es o achie e edox homeos asis.
Keywo ds:
physical ac i i y; accele ome y; oxida i e s ess; plasma o al an ioxidan capaci y;
8-hyd oxy-20-deoxyguanosine; isop os ane F2α
An ioxidan s 2021,10, 320. h ps://doi.o g/10.3390/an iox10020320 h ps://www.mdpi.com/jou nal/an ioxidan s
An ioxidan s 2021,10, 320 2 o 14
1. In oduc ion
Physical ac i i y imp o es ca dio espi a o y i ness and s eng hens he musculoskele-
al sys em, helping o main ain p ope body composi ion, bo h in child en and adoles-
cen s [
1
,
2
]. Physical ac i i y p ac ice also seems o educe lipid pe oxida ion and imp o e
he an ioxidan de ense sys em, esul ing in he main enance o edox homeos asis [3].
The concep o “oxida i e s ess” has been de ined as “an imbalance be ween oxidan s
and an ioxidan s in a o o he oxidan s, leading o a dis up ion o edox signaling and
molecula damage” [
4
]. U ina y isop os anes and 8-hyd oxy-2
0
-deoxyguanosine (8-OHdG),
among o he body-oxidized compounds, a e well- ecognized bioma ke s o oxida i e
s ess, which ha e been ound o be inc eased in se e al si ua ions, including obesi y, ype
2 diabe es, and ca dio ascula diseases [
5
]. F2-8-iso-p os aglandin F2
α
, also known as
isop os ane F
2α
(F
2
-IsoPs), is gene a ed by ee adical-induced pe oxida ion o a achidonic
acid and is cu en ly ega ded as one o he mos eliable bioma ke s o
in i o
oxida i e
s ess [
6
]. In addi ion, 8-OHdG is conside ed o be a bioma ke o gene alized cellula
oxida i e s ess [
7
]; i can be easily de e mined in u ine wi h good ep oducibili y and
eco e y o un imed samples [8].
Two subsys ems in eg a e he an ioxidan de ense sys em: he i s is ela ed o he
ac i i y o se e al enzymes such as glu a hione pe oxidases, glu a hione educ ase, glu-
a hione S- ans e ase, supe oxide dismu ases, and ca alase; he second is o med by
non-enzyma ic an ioxidan s such as u ic acid, ocophe ols, asco ba e, glu a hione and
ubiquinone [
9
]. The non-enzyma ic componen can be chemically measu ed in blood
plasma by acing i o se e al oxidizing subs ances, ob aining he non-enzyma ic an ioxi-
dan capaci y (NEAC), o al an ioxidan s a us, o , hence o h, o al an ioxidan capaci y
(TAC). The use o indices o global edox s a us, such as plasma TAC, may be mo e ap-
p op ia e han he compa ison o single bioma ke s o e alua e oxida i e s ess. In his
con ex , TAC seems a use ul pa ame e o assessing he global edox s a us in child en
and adolescen s [10].
Rega dless o die a y modi ica ions, physical ac i i y in e en ions seem o imp o e
body mass index in child en and adolescen s [
11
,
12
]. Simila ly, he p ac ice o physical ac-
i i y, bo h in adul s and child en, has been associa ed wi h an inc ease in an ioxidan s and
a educ ion o p o-oxidan s [
13
]. Addi ionally, obesi y has been ela ed o an imbalanced
edox s a us [
14
]. Howe e , i is unclea whe he he e ec o exe cise on edox s a us is
media ed o no by changes in body weigh s a us.
The e ec o acu e and ch onic physical ac i i y p ac ice on oxida i e s ess esponses
in child en and adolescen s has been ecen ly e iewed [
15
]. Acu e exe cise seems o induce
a ele an , bu ansien , inc ease in ma ke s o oxida i e s ess. In con as , egula exe cise
appea s o be associa ed wi h inc eased an ioxidan s and educed sys emic oxida i e
bioma ke s, e en independen ly o body weigh s a us. Howe e , he s udies included
in ha e iew a e he e ogeneous in e ms o he ype o exe cise, in ensi y, and ime o
physical ac i i y p ac iced [15].
The Wo ld Heal h O ganiza ion (WHO) and o he in e na ional ins i u ions ha e
ecommended ha child en and adolescen s should pe o m a leas an a e age o 60 min
pe day o mode a e o igo ous-in ensi y, mos ly ae obic ac i i ies ac oss he week, in
o de o achie e se e al posi i e ou comes ega ding ca dio ascula , me abolic, and mus-
culoskele al heal h [
16
]. Howe e , he impac o physical ac i i y, especially in e ms o
ime and in ensi y, on edox s a us, has no been accu a ely desc ibed o child en and
adolescen s. In ac , o ou knowledge, e alua ion o he edox s a us o child en acco ding
o objec i ely-measu ed physical ac i i y by accele ome y has no been in es iga ed.
We hypo hesized ha physical ac i i y p ac ice, especially mode a e- o- igo ous
physical ac i i y (MVPA), and seden a y ime could be ela ed o highe plasma le els o
TAC in child en and adolescen s, showing a be e global edox s a us. Fo his pu pose, we
aimed o compa e plasma le els o TAC and bioma ke s o oxida i e s ess (u ina y F
2
-IsoPs
and 8-OHdG) acco ding o a Physical Ac i i y-Seden a ism Sco e (PASS), cha ac e ized by
An ioxidan s 2021,10, 320 3 o 14
mode a e and igo ous physical ac i i y and seden a y ime measu ed by accele ome y,
in a c oss-sec ional sample o Spanish child en om he GENOBOX s udy.
2. Ma e ials and Me hods
2.1. Popula ion
The p esen wo k was pa o he GENOBOX s udy. GENOBOX is a case-con ol,
mul icen e s udy ca ied ou in a o al o 1444 child en (706 males and 738 emales), aged 3
o 17 yea s Spanish child en du ing 2012–2015. De ailed inclusion and exclusion c i e ia as
well as in o med consen and app o al by he local E hics Commi ees o he h ee Spanish
Hospi als (Hospi al Uni e si a io Reina So ía, Có doba; Hospi al Clínico Uni e si a io,
San iago de Compos ela; and Hospi al Clínico Uni e si a io Lozano Blesa, Za agoza, Spain;
Code IDs: Có doba 01/2017, San iago 2011/198, Za agoza 12/2010) whe e child en we e
ec ui ed ha e been epo ed elsewhe e [
14
]. A subsample o 216 child en (111 boys) was
selec ed based on he ollowing inclusion c i e ia o he p esen s udy: Caucasian child en
and adolescen s aged 6 o 14 wi h body composi ion measu ed by bioelec ical impedance
analysis, alid blood measu emen s including sex ho mones ( ollicle-s imula ing ho mone,
lu einizing ho mone, es os e one in boys, and es adiol in gi ls), and accu a e da a om an
accele ome y s anda dized p o ocol, as well as measu ed plasma le els o TAC and u ina y
F
2
-IsoPs and 8-OHdG. Wi hin he subsample o 216 subjec s, a subg oup o 74 child en
(33 boys) also had measu es o plasma ca o enes, e inol, and ocophe ols.
2.2. Clinical and An h opome ic Examina ion
Medical his o y and a physical exam including he e alua ion o sexual ma u i y
acco ding o Tanne ’s i e-s ages we e assessed and con i med wi h sexual ho mone
measu emen s. An h opome ic measu emen s we e aken by a single examine , and
de ails ha e been p e iously epo ed [17].
2.3. Blood Sampling
Blood samples we e d awn om he an ecubi al ein be ween 08:00 and 09:30 h a e
an o e nigh as . Rou ine blood es s (Glucose (CV = 3.0%), plasma insulin (CV = 2.6%),
ollicle-s imulan ho mone (CV = 3.6%); lu einizing ho mone (CV = 3.1%), es os e one
(CV = 2%), and es adiol (CV = 1.8%) we e measu ed as p e iously epo ed using au o-
ma ed analyze s [
17
] The homeos asis model assessmen o insulin esis ance (HOMA-IR)
was calcula ed based on he published equa ion: HOMA-IR = as ing glucose (mmol)
×
as ing insulin (mU/mL)/22.5 [18].
Plasma TAC was de e mined by colo ime y using a comme cial an ioxidan assay
ki (Ca no. 709001, Cayman Chemical, Ann A bo , MI, USA). U ina y F
2
-IsoPs was de e -
mined by using a comme cial compe i i e ELISA ki (EA85 Ox o d Biomedical Resea ch,
Ox o d, MI, USA) (CV): 14.13%). U ina y 8-OHdG was also de e mined by using a com-
me cial compe i i e ELISA ki (KOG-200S/E JaICA, Fuku oi, Japan) (CV: 5.73%). The
concen a ions we e no malized by u ina y c ea inine and exp essed in ng/mg o c ea i-
nine. C ea inine concen a ion in u ine samples was de e mined wi h a colo ime ic ki (Re .
1001115, Spin eac , Ba celona, Spain) (CV: 2.89%). Measu emen o plasma concen a ions
o e inol, ca o enes, and ocophe ols we e de e mined a e ex ac ion wi h 1-p opanol by
ul a-high-p essu e liquid ch oma og aphy coupled o mass spec ome y UHPLC-MS as
epo ed elsewhe e [14].
2.4. Accele ome y
Ac iG aph GT3X and GT3X+ accele ome e s (Ac iG aph; Pensacola, FL, USA) we e
used o assess physical ac i i y le els in his s udy. Accele ome e s we e placed o e he
igh iliac c es and held in place using an adjus able elas ic bel o 24 h a day wi h a
minimum o 8 h o moni o ing pe day o a leas 3 days (a leas one weekend day). I was
p og ammed o 15 epochs (pe iod o 15 s), as p e iously ecommended [
19
]. Accele ome y
da a we e p ocessed using he Ac ili e 6.13.3 p og am (Ac iG aph; Pensacola, FL, USA)
An ioxidan s 2021,10, 320 4 o 14
eplacing, as a missing da a code be o e u he analysis, all nega i e coun s and pe iods
o 20 min o mo e o consecu i e ze o coun s we e eplaced [
20
]. The ou pu gene a ed
by he Ac iG aph GT3X+ included he o al olume o physical ac i i y and each physical
ac i i y in ensi y as de ined by he cu -poin s o coun s pe minu e (CPMs) based in he
classi ica ion by E enson e al. [21].
2.5. S a is ical Analysis
All con inuous a iables we e es ed o no mali y using he Shapi o–Wilk and Kol-
mogo o es s; he a iables ollowing a non-no mal dis ibu ion we e squa e- oo (TAC,
8-OHdG, F
2
-IsoPs, a body mass (FM), mode a e and igo ous physical ac i i y) o loga-
i hm ans o med (seden a y ime). The homogenei y o a iances was es ima ed using
Le ene’s es . Di e ences be ween p e-pube al and pube al child en we e analyzed
by wo-independen -sample - es s o Mann–Whi ney U es s.
χ2
es s we e applied o
ca ego ical a iables exp essed in pe cen age.
P incipal componen analysis (PCA) was pe o med o in es iga e he ela ionships
among body mass index, body composi ion, pe iphe al issue insulin esis ance—as a isk
ea u e o me abolic synd ome—physical ac i i y le els, and oxida i e s ess and TAC in
he 210 child en. Ex ac ion o he ini ial se o unco ela ed componen s was accomplished
wi h he p incipal ac o me hod, and hen Va imax o hogonal o a ion o componen s
was used o acili a e in e p e a ion. High loading alues indica e a s onge ela ionship
be ween a ac o and an obse ed a iable. Fac o loadings lowe han 0.359 (c i ical ac o ,
p< 0.001) e ealed ma ginal co ela ions.
To es ima e he o e all physical ac i i y and seden a ism le els, a composi e ac i i y
sco e o seden a y ime, mode a e and igo ous in ensi ies was calcula ed (i.e., PASS). Fo
his pu pose, qua iles o each a iable we e designed, being he minu es o mode a e and
igo ous physical ac i i y highe o he ou h qua ile compa ed o he i s one, and he
opposi e o seden a y ime. Each subjec ob ained 1 o 4 poin s acco ding o he qua ile o
each a iable (e.g., 1 poin o being in Q1 o mode a e physical ac i i y o 4 poin s o
being in Q4 o seden a y ime). By summing he poin s o he h ee a iables, he PASS
was ob ained o each subjec . The PASS anged om 3 (all a iables in he i s qua ile) o
12 (all a iables in he ou h qua ile); a highe sco e indica ed a highe ac i e habi . Based
on his sco e, ou g oups o PASS we e es ablished: e y low ac i e (VLA; a sco e o 3), low
ac i e (LA; sco e om 4 o 6), mode a ely ac i e (MA; sco e om 7 o 9), and high ac i e
(HA; sco e om 10–12). MANOVA was used o es he di e ence be ween he ou g oups
ac oss se e al ou come a iables/ou comes simul aneously and Box’s es looks a he
assump ion o equal co a iance ma ices. Pillai’s ace alue lowe han 0.05 was conside ed
s a is ically signi ican o he MANOVA es . Di e ences be ween he ou g oups based
on he PASS we e la e analyzed using uni a ian ANCOVA (UNIANCOVA), adjus ing
o age and/o body mass index (BMI) z-sco e; pai wise di e ences we e assessed by pos
hoc analyses o de e mine di e ences be ween expe imen al g oups. Fo hose a iables
no ollowing no mali y, a K uskal–Wallis es was used o e alua e di e ences be ween
g oups. Values in he desc ip i e ables and esul s a e exp essed as means and s anda d
de ia ions. Di e ences we e conside ed signi ican when p< 0.05. All s a is ical p ocedu es
we e conduc ed using SPSS (IBM SPSS S a is ics, Ve sion 25.0. A monk, NY, USA).
3. Resul s
Gene al demog aphic, an h opome ic, physical ac i i y, and pe iphe al insulin e-
sis ance a iables in p epube al and pube al selec ed child en wi hin he GENOBOX
s udy a e shown in Table 1. Wi hin he 216 subjec s, 105 we e a p epube al and 111 a
he pube al s age. The e we e no di e ences be ween p epube al and pube al g oups
ega ding BMI z-sco e and pe cen ages o FM and a ee mass (FFM). No di e ences
we e also ound o mode a e physical ac i i y, bu i was closed o s a is ical signi icance.
A he same ime, HOMA-IR and seden a y ime we e signi ican ly highe o hose a
pube al s a us.
An ioxidan s 2021,10, 320 5 o 14
Table 1.
Gene al demog aphic, an h opome ic, physical ac i i y, and pe iphe al insulin esis ance
a iables in p epube al and pube al Spanish child en om he GENOBOX s udy.
Va iables All Pa icipan s
(216)
P epube al
(105)
Pube al
(111) p-Value
Age (yea s) 10.8 ±2.2 9.4 ±1.7 12.1 ±1.7 <0.001
Weigh (kg) 50.3 ±17.3 41.8 ±12 58.2 ±17.9 <0.001
Heigh (m) 1.47 ±0.13 1.38 ±0.10 1.55 ±0.10 <0.001
BMI (kg/m2)22.9 ±5.2 21.7 ±4.5 23.9 ±5.6 0.003
BMI z-sco e 1.15 ±2.14 1.11 ±2.38 1.15 ±2.18 0.886
FM (kg) 15.2 ±9.3 12.8 ±7 17.3 ±10.6 0.001
FM (%) 27.8 ±9.9 27.9 ±9.3 27.6 ±10.4 0.836
FFM (kg) 35.1 ±10.2 29.4 ±6.4 40.4 ±10.3 <0.001
FFM (%) 71.6 ±11.1 71.5 ±10.4 71.7 ±11.8 0.887
No mal weigh (%) 34.9 14.9 20.2 0.342 *
O e weigh (%) 23 11.5 11.5 0.342 *
Obesi y (%) 42.1 22.6 19.2 0.342 *
HOMA-IR 2.91 ±1.81 2.32 ±1.54 3.40 ±1.83 <0.001
ST (min/d) 482 ±97 467 ±103 495 ±89 0.018
PA Mode a e (min/d) 38 ±14 40 ±13 36 ±15 0.050
PA Vigo ous (min/d) 15 ±10 14 ±8 16 ±11 0.251
MVPA (min/d) 53 ±21 54 ±20 52 ±23 0.494
BMI: body mass index; FM: a mass; FFM: a - ee mass; HOMA-IR: homeos asis model assessmen -insulin
esis ance; ST: seden a y ime; PA: physical ac i i y; MVPA: mean mode a e- igo ous physical ac i i y. Da a
a e shown as mean
±
SD. S uden ’s - es o pa ame ic analysis and U de Mann–Whi ney o non-pa ame ic
analysis was used o compa e a iables be ween p epube al and pube al s ages. * ep esen s p alue o
Chi-squa e es .
F om he eigh i ems included in he PCA (physical ac i i y, body composi ion, in-
sulin esis ance, oxida i e s ess, and o al plasma an ioxidan capaci y), h ee p incipal
componen s we e ex ac ed (Table 2), which explained 64.4% o he o al a iance (30%
o he a iance was explained by he i s ac o , an addi ional 21% by he second ac o ,
and ano he 13% by he hi d ac o ) (Table 3). The i s p incipal componen , e med
“me abolic isk” showed a posi i e co ela ion be ween HOMA-IR, FM, and FFM, and
humble co ela ions o seden a y ime (nega i e) and MVPA (posi i e). The second com-
ponen , e med “oxida i e s ess”, included co ela ions among u ina y F
2
-IsoPs, 8-OHdG,
and seden a y ime. The hi d componen named “physical ac i i y” included a posi i e
co ela ion be ween FFM and MVPA, and nega i e wi h seden a y ime. TAC did no each
he c i ical alue o be included in any o he componen s.
The di e ences be ween PASS le els o he a iables included in he PCA a e p e-
sen ed in Table 4and Figu es 1–3. Child en wi h a highe PASS alloca ed in he high ac i e
g oup had a lowe BMI z-sco e han hose in he mode a ely ac i e and low ac i e g oups.
Figu e 1depic s he di e ences be ween he PASS le els o he a iables wi h a highe
ac o loading o he “me abolic isk” componen (FM, FFM, and HOMA-IR). Child en in
he high ac i e g oup showed he lowes le els o FM and HOMA-IR. No di e ences we e
ound be ween g oups o FFM.
The in luence o PASS on edox s a us, assessed by plasma TAC, and u ina y F
2
-IsoPs
and 8-OHdG, is ep esen ed in Figu e 2. TAC’s plasma le el was lowe o hose child en
in he high ac i e g oup compa ed o hose in he mode a ely ac i e and low ac i e g oups
(UNIANCOVA p= 0.035, Figu e 2a). Rega ding he e alua ion o he oxida i e s ess s a us,
child en in he high ac i e g oup showed lowe u ine le els o 8-OHdG (Figu e 2b) and
F
2
-IsoPs (Figu e 2c) han he es o he g oups (UNIANCOVA p= 0.005 and p= 0.036,
espec i ely).

An ioxidan s 2021,10, 320 6 o 14
Table 2.
P incipal componen analysis o he GENOBOX s udy ex ac ed om physical ac i i y,
body composi ion, pe iphe al issue insulin esis ance, oxida i e s ess, and o al plasma an ioxidan
capaci y a iables.
Va iables
Componen ma ix a
Fac o *
Me abolic Risk Oxida i e S ess Physical Ac i i y
HOMA-IR 0.831
FM (kg) 0.804
FFM (kg) 0.798 0.388
TAC (mM) 0.356
8-OHdG (ng/mL) 0.859
F2-IsoPs (ng/mL) 0.831
MVPA (min/d) −0.377 0.771
ST (min/d) 0.366 0.387 −0.422
HOMA-IR: homeos asis model assessmen -insulin esis ance; FM: a mass; FFM: a - ee mass; TAC: plasma o al
an ioxidan capaci y; 8-OHdG: u ina y 8-hyd oxy-2
0
-deoxyguanosine; F
2
-IsoPs: u ina y F2
α
-isop os anes; MVPA:
mean mode a e- igo ous physical ac i i y; ST: seden a y ime.
a
Ex ac ion o he ini ial se o unco ela ed
componen s was accomplished wi h he p incipal ac o me hod, and hen he Va imax o hogonal o a ion o
componen s was used o acili a e in e p e a ion. The numbe o componen s e ained was based on Sc ee plo
analysis and eigen alues g ea e han 1 (wi h he componen s accoun ing o mo e o he o al a iance han any
single a iable).
*
Fac o loading is he p oduc -momen co ela ion (a measu e o linea associa ion) be ween
an obse ed a iable and an unde lying ac o . A signi ican loading ac o was de ined as a alue g ea e han
0.359 (p< 0.01).
Table 3.
Eigen alues and pe cen ages o a iance associa ed wi h each linea componen ( ac o ) be o e ex ac ion, a e
ex ac ion, and a e o a ion, in he p incipal componen analysis o he GENOBOX s udy o child en ela ing physical
ac i i y, body composi ion, and pe iphe al issue insulin esis ance o isk ac o s o oxida i e s ess and o al plasma
an ioxidan capaci y.
Componen
To al Va iance Explained
Ini ial Eigen alues Sums o Loads Squa ed om
Ex ac ion
Sums o Loads Squa ed o
Ro a ion
To al % o
a iance
%
Accumula ed To al % o
Va iance
%
Accumula ed To al % o
Va iance
%
Accumula ed
1
2.402
30.029 30.029 2.402 30.029 30.029
2.232
27.901 27.901
2
1.694
21.175 51.204 1.694 21.175 51.204
1.634
20.424 48.325
3
1.063
13.293 64.496 1.063 13.293 64.496
1.294
16.171 64.496
The i s alue in he ow gi es he p opo ion o a iance ( he deg ee o sp ead in he da a se ) explained by body composi ion and issue
pe iphe al esis ance; he second alue, he p opo ion explained by oxida i e s ess; and he hi d alue, he p opo ion explained by he
le el o MVPA and seden a ism.
Table 4.
Di e ences in body mass index (BMI) z-sco e, mode a e- igo ous physical ac i i y and seden a y ime be ween
g oups o Physical Ac i i y-Seden a ism Sco e (PASS) o he Spanish child en om he GENOBOX s udy.
Va iables Physical Ac i i y-Seden a ism Sco e Le els p-Value p-Value o
T end
Ve y Low
Ac i e
(12)
Low Ac i e
(65)
Mode a e
Ac i e
(82)
High Ac i e
(57)
BMI z-sco e 1.25 ±1.4 a,b 1.57 ±2.1 a,b 1.41 ±1.9 a,b 0.51 ±2.9 a,c 0.046 0.029
PASS 3 a5.27 ±0.78 b8±0.84 c10.88 ±0.81 d<0.001 <0.001
MVPA (min/d) 22 ±5a34 ±11 b55 ±12 c76 ±17 d<0.001 <0.001
ST (min/d) 601 ±70 a517 ±92 b471 ±95 c397 ±54 d<0.001 <0.001
BMI: body mass index; PASS: Physical Ac i i y-Seden a ism Sco e; PA: physical ac i i y; MVPA: mode a e- igo ous physical ac i i y; ST:
Seden a y ime. Da a a e shown as mean
±
SD. One-way ANOVA es was used o compa e a iables among he di e en PASS le els. No
ma ching supe sc ip le e s (a, b, c, d) indica e signi ican di e ences (p< 0.05) by pai wise pos hoc es adjus ed o age and/o BMI
z-sco e o de e mine which expe imen al g oups di e ed om each o he .
An ioxidan s 2021,10, 320 7 o 14
Figu e 1.
Fa mass, a - ee mass and HOMA-IR acco ding o Physical Ac i i y-Seden a ism Sco e (PASS) g oups in Spanish
child en om he GENOBOX s udy. FM: a mass; FFM: a - ee mass; HOMA-IR: homeos asis model assessmen -insulin
esis ance; VLA: e y low ac i e; LA: low ac i e; MA: mode a ely ac i e; HA: high ac i e. Di e ences be ween PASS le els
we e analyzed using one-way ANCOVA, adjus ing o age and/o BMI z-sco e; pai wise di e ences we e assessed by
pos hoc analyses o de e mine di e ences be ween expe imen al g oups. Fo hose a iables no ollowing no mali y,
a K uskal–Wallis es was used o e alua e di e ences be ween g oups. FM: # Di e ences be ween he HA and VLA o
(p= 0.003). HOMA-IR (UNIANCOVA, p=0.005):
†
Di e ences be ween HA s. LA and VLA (p= 0.018 and p= 0.010,
espec i ely); * Di e ences be ween A s. LA and VLA (p= 0.014 and p= 0.010, espec i ely). p o end o HOMA-IR
(p= 0.001) and FM (p= 0.044).
Finally, he plasma concen a ion o some componen s o he non-enzyma ic an ioxi-
dan de ense sys em, e inol, be a-ca o ene, and ocophe ols we e measu ed in a subg oup
o ou s udy. Di e ences in he plasma le els o hese bioma ke s, acco ding o he PASS
g oups, a e p esen ed in Figu e 3. Child en in he low ac i e g oup showed he highes
alues o e inol (UNIANCOVA, p= 0.002) compa ed o hose in o he g oups. Rega ding
ocophe ols (UNIANCOVA, p= 0.022), child en in he high ac i e g oup showed lowe
le els compa ed wi h child en wi h e y low ac i e and mode a ely ac i e g oups.
An ioxidan s 2021,10, 320 8 o 14
An ioxidan s 2021, 10, 320 8 o 14
Figu e 2. (a)To al plasma an ioxidan capaci y, (b) u ina y 8-hyd oxy-2’-deoxyguanosine and (c)
F
2α
-Isop os anes by Physical Ac i i y-Seden a ism Sco e (PASS) g oups in Spanish child en om
he GENOBOX s udy. TAC: o al plasma an ioxidan capaci y; 8-OHdG: 8-hyd oxy-2’-
deoxyguanosine; F
2
-IsoPs: F
2α
-isop os anes; PA: physical ac i i y; VLA: e y low ac i e; LA: low
ac i e; MA: mode a ely ac i e; HA: high ac i e. Di e ences be ween PASS le els we e analyzed
using one-way ANCOVA, adjus ing o age and/o BMI z-sco e; pai wise di e ences we e
assessed by pos hoc analyses o de e mine di e ences be ween expe imen al g oups. Fo hose
a iables no ollowing no mali y, a K uskal–Wallis es was used o e alua e di e ences be ween
g oups. * Di e ences wi h HA sco e. p o end o TAC (p = 0.020).
Finally, he plasma concen a ion o some componen s o he non-enzyma ic
an ioxidan de ense sys em, e inol, be a-ca o ene, and ocophe ols we e measu ed in a
subg oup o ou s udy. Di e ences in he plasma le els o hese bioma ke s, acco ding o
he PASS g oups, a e p esen ed in Figu e 3. Child en in he low ac i e g oup showed he
Figu e 2.
(
a
)To al plasma an ioxidan capaci y, (
b
) u ina y 8-hyd oxy-2’-deoxyguanosine and (
c
)
F
2α
-Isop os anes by Physical Ac i i y-Seden a ism Sco e (PASS) g oups in Spanish child en om he
GENOBOX s udy. TAC: o al plasma an ioxidan capaci y; 8-OHdG: 8-hyd oxy-2’-deoxyguanosine;
F
2
-IsoPs: F
2α
-isop os anes; PA: physical ac i i y; VLA: e y low ac i e; LA: low ac i e; MA: mod-
e a ely ac i e; HA: high ac i e. Di e ences be ween PASS le els we e analyzed using one-way
ANCOVA, adjus ing o age and/o BMI z-sco e; pai wise di e ences we e assessed by pos hoc
analyses o de e mine di e ences be ween expe imen al g oups. Fo hose a iables no ollowing
no mali y, a K uskal–Wallis es was used o e alua e di e ences be ween g oups. * Di e ences wi h
HA sco e. p o end o TAC (p= 0.020).
An ioxidan s 2021,10, 320 9 o 14
An ioxidan s 2021, 10, 320 9 o 14
highes alues o e inol (UNIANCOVA, p = 0.002) compa ed o hose in o he g oups.
Rega ding ocophe ols (UNIANCOVA, p = 0.022), child en in he high ac i e g oup
showed lowe le els compa ed wi h child en wi h e y low ac i e and mode a ely ac i e
g oups.
Figu e 3. (a) Plasma e inol, (b) be a-ca o ene, and (c) ocophe ols le els acco ding o he Physical-
Ac i i y-Seden a ism Sco e (PASS) le els in Spanish child en om he GENOBOX s udy. PA:
physical ac i i y; VLA: e y low ac i e; LA: low ac i e; MA: mode a ely ac i e; HA: high ac i e.
Di e ences be ween PASS le els we e analyzed using one-way ANCOVA, adjus ing o age
and/o BMI z-sco e; pai wise di e ences we e assessed by pos hoc analyses o de e mine
di e ences be ween expe imen al g oups. Fo hose a iables no ollowing no mali y, a K uskal–
Wallis es was used o e alua e di e ences be ween g oups. * Di e ences wi h HA; # Di e ences
wi h VLA; † Diffe ences MA. p o end o e inol (p = 0.043) and ocophe ols (p = 0.040).
Figu e 3.
(
a
) Plasma e inol, (
b
) be a-ca o ene, and (
c
) ocophe ols le els acco ding o he Physical-
Ac i i y-Seden a ism Sco e (PASS) le els in Spanish child en om he GENOBOX s udy. PA: physical
ac i i y; VLA: e y low ac i e; LA: low ac i e; MA: mode a ely ac i e; HA: high ac i e. Di e ences
be ween PASS le els we e analyzed using one-way ANCOVA, adjus ing o age and/o BMI z-
sco e; pai wise di e ences we e assessed by pos hoc analyses o de e mine di e ences be ween
expe imen al g oups. Fo hose a iables no ollowing no mali y, a K uskal–Wallis es was used o
e alua e di e ences be ween g oups. * Di e ences wi h HA; # Di e ences wi h VLA;
†
Di e ences
MA. p o end o e inol (p= 0.043) and ocophe ols (p= 0.040).
4. Discussion
The in luence o objec i ely measu ed physical ac i i y and seden a y ime on edox
s a us o child en and adolescen s has been sca cely desc ibed so a . In he p esen analysis,
a high PASS, cha ac e ized by a high ime spen on mode a e and igo ous physical ac i i y,