1
The impac o physical exe cise on cogni i e and a ec i e unc ions and b ain-de i ed
neu o ophic ac o le els in nu sing home esiden s: a andomized con olled ial
Ha i z A ie aa, Chloe Rezola-Pa doa, Maide Ko aja enab, Go zone He ása, Ja ie Gila, José
J. Yanguasc, Mi en I u bu uc, Susana M. Gila, Jon I azus aa, Ana Rod iguez-La ada
aDepa men o Physiology, Facul y o Medicine and Nu sing, Uni e si y o he Basque Coun y
(UPV/EHU), Spain.
bDepa men o Nu sing II, Facul y o Medicine and Nu sing, Uni e si y o he Basque Coun y
(UPV/EHU), Spain.
cMa ia Ins i u o, Spain.
Co esponding au ho : Ha i z A ie a
Depa men o Physiology, Facul y o Medicine and Nu sing, Uni e si y o he Basque Coun y
(UPV/EHU). Ba io Sa iena s/n, E-48940 Leioa (Bizkaia) – Spain
+34 610970906
ha i z.a ie [email protected]
This is he accep ed manusc ip o he a icle ha appea ed in inal o m in Ma u i as 131 : 72-77 (2020), which has
been published in inal o m a h ps://doi.o g/10.1016/j.ma u i as.2019.10.014. © 2019 Else ie unde CC BY-NC-ND
license (h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/)
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Abs ac
Objec i es: To de e mine he e ec s o a mul icomponen physical exe cise p og am on
cogni i e and a ec i e unc ioning among nu sing home esiden s and o cla i y whe he he e
a e any changes in se um b ain-de i ed neu o ophic ac o (BDNF) le els among pa icipan s.
S udy design: This was a single-blind andomized con olled ial among en nu sing homes in
Gipuzkoa, Spain. The s udy included 112 men and women (ACTRN12616001044415).
Pa icipan s in he con ol g oup pa icipa ed in ou ine ac i i ies while he in e en ion g oup
pa icipa ed in a six-mon h indi idualized, p og essi e, mul icomponen physical exe cise
p og am ocused on s eng h, balance, and walking.
Main ou come measu es: Cogni i e and a ec i e unc ions we e assessed a baseline and a
six mon hs. Se um BDNF le els we e assessed ia ELISA.
Resul s: A e six mon hs, a g oup by ime in e ac ion in a o o he in e en ion g oup was
obse ed on he Mon eal Cogni i e Assessmen (MOCA), symbol sea ch and De Jong-
Gie eld Loneliness Scale (P < 0.05). Meanwhile, he con ol g oup sco ed mo e poo ly on he
MOCA, WAIS-IV (coding and symbol sea ch), e bal luency, and seman ic luency es s a e
six mon hs (P < 0.05) han hey did a baseline. The in e en ion g oup showed poo e esul s
on he coding es (P < 0.05). Loneliness pe cep ion was educed in he in e en ion g oup (P <
0.05). No changes in se um BDNF we e obse ed (g oup x ime and wi hin g oups, P > 0.05).
Conclusion: A six-mon h indi idualized, p og essi e, mul icomponen physical exe cise
in e en ion is e ec i e a main aining cogni i e unc ion and dec easing loneliness pe cep ion
among nu sing home esiden s. Blood le els o BDNF we e no a ec ed by he in e en ion.
Keywo ds: exe cise aining, cogni ion, loneliness, neu o ophin, nu sing home, quali y o li e.
Abb e ia ions: ANCOVA, Analysis o Co a iance; BDNF, b ain-de i ed neu o ophic ac o ;
CG, con ol g oup; CV, co-e icien o a iabili y; ELISA, enzyme-linked immunoso ben
assay; IG, in e en ion g oup; MMSE, Mini Men al S a e Examina ion; MOCA, Mon eal
3
Cogni i e Assessmen ; MPE, mul icomponen physical exe cise; RAVLT, Rey Audi o y-Ve bal
Lea ning Tes ; SPPB, Sho Physical Pe o mance Ba e y; WAIS-IV, Wechsle Adul
In elligence Scale, Fou h Edi ion; 1RM, 1 epe i ion maximum
4
1. In oduc ion
Cogni i e unc ion ends o decline wi h aging, a phenomenon o en e e ed o as cogni i e
aging [1]. Cogni i e aging in ol es a li elong p ocess o g adual, ongoing, and highly a iable
changes in cogni i e unc ion ha occu as people ge olde [1]. In addi ion, aging is ela ed o
de e io a ing a ec i e unc ion [2].
In addi ion o he physical bene i s o pa icipa ing in an exe cise p og am, in e en ional
s udies demons a e ha physical exe cise imp o es ce ain domains o cogni i e and a ec i e
unc ions in olde adul s [3,4]. Howe e , hese obse a ions ha e mainly ocused on
communi y-dwelling olde adul s. Physical exe cise in e en ions may be pa icula ly impo an
o olde adul s who li e in nu sing homes, as hey ypically ha e wo yingly low le els o
physical ac i i y compa ed o cu en ecommenda ions o communi y-dwelling olde adul s
[5]. Few in e en ions implemen ed in nu sing homes ha e assessed he e ec s o physical
exe cise p og ams on he cogni i e and a ec i e domains o indi iduals li ing in hese se ings
[6,7]. The in ensi y o in e en ions is ypically no epo ed in nu sing home s udies [8-10] bu
appea s low in mos cases. The e is also high a iabili y in he ype o in e en ion [6,7] and in
many s udies, he leng h o he in e en ion is sho , limi ing he impac ha he in e en ion
migh ha e [6-8]. Fu he , p io s udies ha e no demons a ed clea e ec s on a ec i e
unc ions in nu sing home esiden s, wi h some s udies epo ing imp o emen s [6,7,9] ha
we e no con i med in o he s [10]. The e is an u gen need o quali y esea ch in ol ing
nu sing home esiden s, wi h longe in e en ions and la ge sample sizes, o help de e mine he
op imal physical exe cise in e en ions needed o make signi ican imp o emen s o and/o
simply main ain cogni i e and a ec i e unc ions [8].
B ain-de i ed neu o ophic ac o (BDNF) p omo es he g ow h and di e en ia ion o neu ons
and synapses while suppo ing he su i al o exis ing neu ons and is an impo an molecule
in ol ed in cogni i e and a ec i e unc ions [11,12]. BDNF also media es imp o emen s in
5
execu i e unc ion ollowing physical exe cise [12]. Howe e , he impac o physical exe cise
on se um concen a ions o BDNF is equi ocal [13]. While some s udies desc ibe inc eases in
his neu o ophic ac o , o he s do no ind any changes a e physical exe cise p og ams [13].
To u he explo e he connec ion be ween BDNF and exe cise and o gene ally es ablish
guidelines o physical exe cise among nu sing home esiden s, we conduc ed an explo a o y
s udy e alua ing he e ec s o a six-mon h indi idualized, p og essi e, mul icomponen
physical exe cise (MPE) p og am on cogni i e and a ec i e unc ions among olde adul s li ing
in nu sing homes. Pa icipan s’ se um BDNF le els we e analyzed be o e and a e he
in e en ion.
2. Me hods
2.1. S udy design
This s udy was a six-mon h mul icen e , andomized, con olled, single-blind s udy among en
nu sing homes in Gipuzkoa, Spain (ACTRN12616001044415) [14]. This a icle p esen s he
esul s o an explo a o y seconda y analysis whose main ou come was he Sho Physical
Pe o mance Ba e y (SPPB) [15]. The in e en ion was conduc ed be ween Oc obe 2016 and
July 2017. The ial was app o ed by he Commi ee on E hics in Resea ch a he Uni e si y o
he Basque Coun y, UPV/EHU (Humans Commi ee Code M10/2016/105; Biological Samples
Commi ee Code M30/2016/106). W i en in o med consen was p o ided by each pa icipan .
2.2. Pa icipan s
The s udy included 112 men and women li ing in nu sing homes who me he ollowing
c i e ia: ≥70 yea s old, sco ed ≥50 on he Ba hel Index (0–100), sco ed ≥20 on he MEC-35 es
(0–35) [an adap ed and alida ed e sion o he Mini Men al S a e Examina ion (MMSE) in
Spanish], and who we e capable o s anding up and walking independen ly o a leas en
me e s (Figu e 1) [14]. Pa icipan s we e andomized in a 1:1 a io using sealed opaque
en elopes o ei he he con ol (CG) o in e en ion g oup (IG) by coin- ossing sequence
6
gene a ion. Assessmen s we e done in each cen e by he esea ch eam, who we e blinded o
g oup alloca ion.
2.3. Con ol g oup
Pa icipan s assigned o he CG pa icipa ed in ou ine ac i i ies ha he nu sing homes o e ed
o esiden s: memo y wo kshops, eading, singing, and o he simila ac i i ies.
2.4. In e en ion g oup
In addi ion o ou ine ac i i ies, he IG pe o med a p e iously desc ibed indi idualized and
p og essi e MPE in e en ion [14]. The in e en ion consis ed o a one hou supe ised g oup
session wice a week, sepa a ed by a leas wo days, o a six-mon h pe iod. The MPE p og am
included s eng h, balance, and walking ecommenda ions. Each session began wi h i e
minu es o wa m-up pe o ming ange-o -mo ion exe cises. S eng h aining was indi idually
adap ed o each pa icipan and ocused on uppe and lowe ex emi y s eng h. The B zycki
equa ion was applied o calcula e one epe i ion maximum (1RM) and adap he adequa e load
p og ession o a m-cu l, knee lexion, and knee ex ension exe cises o e e y pa icipan a
baseline and e e y wo mon hs. Chai -s and, hip abduc ion, and hip adduc ion exe cises we e
pe o med wi hou ex e nal loads, and he in ensi y was ailo ed o he capabili ies o each
pa icipan by adjus ing he numbe o epe i ions and eloci y. The in ensi y anged om 40%
a i s o 70% 1-RM in he six h mon hs o he p og am. Balance exe cises we e also
indi idually adap ed and included exe cises p og essing in di icul y, s a ing by dec easing a m
suppo along wi h dec easing he base o suppo o challenge pa icipan s’ balance as hey
p og essed. Some exe cises a ied h oughou he pe iod, including weigh ans e om one leg
o ano he , p op iocep i e exe cises, and s epping p ac ice. Sessions ended wi h i e minu es o
deep b ea hing exe cises and elaxa ion. Physical exe cise sessions we e conduc ed in a p i a e
gym o p i a e ooms adequa e o hese ac i i ies so as o a oid any sha ed expe iences wi h
he con ol g oup. The ooms whe e he exe cises we e conduc ed we e sui able o
7
app oxima ely nine people a a ime. Inside he oom we e pa allel ba s, i m chai s o a la ge
able o use as a suppo o s eng h and balance exe cises. All sessions we e conduc ed by a
p o essional ins uc o wi h a deg ee in physical ac i i y and spo s sciences and aining in
adap ed physical ac i i y in olde adul s. A endance was de e mined by pa icipan s’ p esence
a physical exe cise sessions. Walking ecommenda ions we e also indi idually ailo ed based
on pa icipan s’ pe o mance on he baseline six-minu e walking es and s a ed wi h pa hs ha
las ed i e minu es pe day a he beginning o he in e en ion, wi h he goal o comple ing 20
minu es pe day (se en days/week) by he end o he six-mon h pe iod. The ecommenda ions
we e based on a speci ic numbe o laps on a ce ain ack (based on he ae obic capaci y o
each pa icipan as measu ed by he six-minu e walk es ). The numbe o laps pe o med by he
pa icipan s in each day was collec ed daily he las week o he second and ou h mon hs by
each nu sing home p incipal nu se. Those nu ses moni o ed he comple ion o he
ecommenda ions checking he pe o mance by hemsel es, asking he assis an nu ses o he
s udy pa icipan s acco ding o he in e nal o ganiza ion om each cen e .
2.5. P ocedu es
All en olled pa icipan s we e assessed be o e he in e en ion pe iod (mon h 0) and a e he
six-mon h in e en ion pe iod. All measu emen s we e collec ed by he same in es iga o s. All
ou come measu emen s we e e alua ed in he pa icipan s' place o esidence.
2.6. Ou comes
We p e iously desc ibed he bene i s o he in e en ion on SPPB (p ima y ou come) in nu sing
homes esiden s [15]. Global cogni ion was assessed by he Mon eal Cogni i e Assessmen
(MOCA) [16], which included isuospa ial/execu i e unc ion, naming, a en ion, language,
abs ac ion, delayed ecall, o ien a ion, and global measu es o cogni i e unc ioning. To al
lea ning measu e o he Spanish alida ed e sion o he Rey Audi o y-Ve bal Lea ning Tes
(RAVLT) [17] was used o e alua e e bal memo y and capaci y o ecall and accumula e
8
wo ds h ough lea ning ials. T ail making es A [18] was adminis e ed o e alua e execu i e
unc ion. The Coding and Symbol Sea ch es was used o measu e p ocessing speed on he
Wechsle Adul In elligence Scale, Fou h Edi ion (WAIS-IV) [19]. Ve bal luency was
measu ed by he numbe o wo ds lis ed beginning wi h a gi en le e in 60 seconds [20].
Seman ic luency was measu ed h ough he numbe o wo ds p oduced in he es ic ed
"animal" ca ego y in 60 seconds [20]. Highe sco es on hese scales indica e be e cogni i e
unc ioning, excep o he T ail making es A, in which highe sco es indica e wo se
pe o mance.
Anxie y and dep ession we e measu ed wi h he Goldbe g Anxie y and Dep ession Scale, in
which high sco es indica e mo e symp oms o anxie y and dep ession [21]. Loneliness was
measu ed wi h he De Jong-Gie eld Loneliness Scale, whe e high sco es indica e a highe
pe cep ion o loneliness [22]. Quali y o li e was measu ed wi h he Quali y o Li e in
Alzheime ’s Disease a ing scale, whe e he o al sco e anges om 13 (wo s ) o 52 (bes )
poin s [23].
Blood samples we e collec ed in he mo ning a e an o e nigh as and a leas 24 hou s a e
he las exe cise session. A e collec ion, ubes we e cen i uged a 5,000 pm o 10 min.
Se um ob ained o each pa icipan was s o ed in aliquo s a –80ºC un il analysis. Se um BDNF
(ng/mL) was quan i ied using a sandwich enzyme-linked immunoso ben assay (ELISA).
Human BDNF Quan ikine Immunoassay (R&D Sys ems, Minneapolis, MN) was pe o med
acco ding o he manu ac u e ’s ins uc ions. Analyses, blinded o g oup alloca ion and in
duplica e, we e a e aged. While he manu ac u e epo s <20 pg/mL o sensi i i y, <6.2%
in a-assay and <11.3% in e -assay co-e icien o a iabili y (CV), he sensi i i y o he
expe imen s has been o <3.1% in a-assay and <9.2% in e -assay CV.
2.7. S a is ical analyses
9
A sample size o 114 pa icipan s was equi ed o de ec minimal signi ican e ec s on he
SPPB, he main ou come o he app o ed ial, accep ing an alpha isk o 0.05 and a be a isk o
0.20 in a bila e al con as assuming a 25% loss o ollow-up [14]. No mal dis ibu ion o he
da a was checked using he Kolmogo o -Smi no es . When no no mally dis ibu ed, da a
we e squa e oo ans o med. S a is ical compa isons a baseline we e pe o med using an
unpai ed s uden ’s es . Be ween-g oup di e ences we e assessed using mixed design analysis
o co a iance (ANCOVA; wo ime poin s x wo g oups) con olling o baseline alues. A
pos -hoc Bon e oni es was used o de e mine di e ences wi hin g oups. Pa ial η2 was
calcula ed o es ima e e ec size. Values o η 2 o ≤0.02, ≤0.13, and ≥0.26 we e conside ed
small, medium, and la ge, espec i ely. The signi icance le el o all es s was se a P < 0.05.
S a is ical analysis was pe o med using IBM SPSS S a is ics 24 s a is ical so wa e package
(SPSS Inc., Chicago, IL).
3. Resul s
The mean age o he pa icipan s was 84.9 yea s (age ange = 70–102 yea s) and pa icipan s
we e p edominan ly women (70.5%). The e we e no di e ences be ween baseline alues o CG
and IG desc ip i e cha ac e is ics (Table 1).
O he 112 pa icipan s who began he s udy, 88 comple ed he six-mon h assessmen (Figu e 1).
A endance a es o he physical exe cise sessions we e 90.8%, and compliance wi h he
walking ecommenda ions was 79.0%. No ad e se e en s associa ed wi h he physical exe cise
p og am we e obse ed.
A e six mon hs o MPE in e en ion, a g oup by ime in e ac ion in a o o he IG was
obse ed on he MOCA (P = 0.003; η 2 = small) and symbol sea ch es s (P = 0.049; η 2 = small)
(Table 2). When di e ences we e analyzed wi hin g oups, he CG showed poo e esul s o
MOCA, WAIS-IV (coding and symbol sea ch), e bal luency, and seman ic luency es s a e
16
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19
31 L.N. Fo i, R. Njemini, I. Beye , E. Eelbode, R. Meeusen, T. Me s, I. Bau mans, S eng h
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h ps://doi.o g/10.1007/s11357-014-9704-6.
20
Figu e 1
S udy low diag am.
21
Table 1
Desc ip i e cha ac e is ics o pa icipan s a baseline
Con ol g oup (n = 55)
In e en ion g oup (n = 57)
P alue
Age (yea s), mean ± SD
84.7 ± 6.1
85.1 ± 7.6
0.812
Sex, n (%)
Female
37 (67.3)
42 (73.7)
0.461
Male
18 (32.7)
15 (26.3)
BMI (kg/m2), mean ± SD
28.2 ± 5.3
28.2 ± 5.1
0.991
WHR, mean ± SD
0.97 ± 0.08
0.98 ± 0.07
0.697
Ba hel Index, mean ± SD
82.8 ± 13.1
79.2 ± 12.9
0.153
MEC-35 es , mean ± SD
28.0 ± 3.5
27.0 ± 4.0
0.157
SD, s anda d de ia ion; BMI, body mass index; WHR, wais - o-hip a io; MEC-35 es , adap ed
and alida ed e sion o he Mini Men al S a e Examina ion in Spanish
22
Table 2
Cogni i e and a ec i e unc ion among con ol and in e en ion g oup pa icipan s.
Con ol g oup (n = 45)
In e en ion g oup (n = 43)
Baseline,
mean (SD)
6 mon hs,
mean (SD)
Baseline,
mean (SD)
6 mon hs, mean
(SD)
P a
Pa ial
η 2 b
Cogni i e unc ion
MOCA (0–30)
14.3 (3.7)
13.0 (5.1)*
14.2 (4.5)
14.9 (5.1)
0.003
0.121
RAVLT ( o al ep.) (0–75)
19.2 (8.4)
20.7 (11.5)
18.0 (8.7)
19.9 (12.1)
0.140
0.028
TMT-A
124 (54)
136 (72)
120 (45)
107 (40)
0.836
0.001
Coding (WAIS-IV)
13.8 (9.5)
10.9 (8.8)*
11.7 (7.8)
10.1 (8.4)*
0.439
0.011
Symbol sea ch (WAIS-IV)
9.0 (4.4)
6.6 (5.4)*
7.0 (5.3)
6.7 (5.9)
0.049
0.063
Ve bal luency es
7.3 (3.9)
6.5 (4.1)*
6.7 (3.5)
6.4 (3.7)
0.489
0.006
Seman ic luency es
8.7 (3.1)
7.4 (4.2)*
7.9 (3.2)
7.2 (3.3)
0.638
0.003
A ec i e unc ion
Goldbe g anxie y
1.3 (1.3)
1.4 (1.5)
1.5 (1.8)
1.3 (1.6)
0.817
0.001
Goldbe g dep ession
0.8 (1.8)
1.2 (1.8)
1.0 (2.1)
0.9 (1.8)
0.478
0.007
DJGLS
5.3 (2.8)
4.3 (3.4)
5.8 (3.1)
3.2 (2.6)*
0.030
0.062
QoL-AD
34.1 (4.9)
33.1 (5.3)
34.3 (6.6)
35.4 (7.1)
0.051
0.049
BDNF (ng/mL)
33.6 (14.2)
32.8 (15.7)
34.2 (15.0)
33.5 (13.2)
0.899
<0.001
SD, s anda d de ia ion; MOCA, Mon eal Cogni i e Assessmen ; RAVLT, Rey Audi o y-Ve bal
Lea ning Tes ; ep, epe i ions; TMT-A, T ail Making Tes A; WAIS-IV, Wechsle Adul
In elligence Scale, Fou h Edi ion; DJGLS, De Jong-Gie eld Loneliness Scale; QoL-AD, quali y
o li e in Alzheime ’s disease; BDNF, b ain-de i ed neu o ophic ac o
a P o g oup x ime in e ac ion.
b Es ima ion o e ec size o g oup x ime in e ac ion.
*P < 0.05, signi ican ly di e en om baseline.
