The Effects of Exercise On Muscle Strength, Body Composition, Physical Functioning and The Inflamatory Profile of Older Adults

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REVIEW

CURRENT
OPINION The effects of exercise on muscle strength, body
composition, physical functioning and the
inflammatory profile of older adults: a
systematic review
Keliane Liberman a,b, Louis N. Forti a,b, Ingo Beyer a,b,c, and Ivan Bautmans a,b,c

Purpose of review
This systematic review reports the most recent literature regarding the effects of physical exercise on muscle
strength, body composition, physical functioning and inflammation in older adults. All articles were
assessed for methodological quality and where possible effect size was calculated.
Recent findings
Thirty-four articles were included – four involving frail, 24 healthy and five older adults with a specific
disease. One reported on both frail and nonfrail patients. Several types of exercise were used: resistance
training, aerobic training, combined resistance training and aerobic training and others. In frail older
persons, moderate-to-large beneficial exercise effects were noted on inflammation, muscle strength and
physical functioning. In healthy older persons, effects of resistance training (most frequently investigated) on
inflammation or muscle strength can be influenced by the exercise modalities (intensity and rest interval
between sets). Muscle strength seemed the most frequently used outcome measure, with moderate-to-large
effects obtained regardless the exercise intervention studied. Similar effects were found in patients with
specific diseases.
Summary
Exercise has moderate-to-large effects on muscle strength, body composition, physical functioning and
inflammation in older adults. Future studies should focus on the influence of specific exercise modalities and
target the frail population more.
Keywords
elderly, exercise, inflammation, sarcopenia, skeletal muscle

INTRODUCTION endurance after 4–5 months. Also body weight


Reduced muscle mass (sarcopenia), muscle perform- and BFM can significantly be reduced after aerobic
ance and strength (dynapenia) and increased CLIP training in older adults [9]. Resistance training has
are typical characteristics of aging. Older adults with shown to increase muscle mass and muscle strength
higher CLIP show increased sarcopenia and dyna- already after 2–3 months [10]. Another study
penia [1]. Physical exercise can reduce CLIP, sarco- showed that resistance training at higher intensity
penia and dynapenia in older adults [2–4]. Aging is or combined medium intensity improved muscle
also accompanied by lower physical function and
activity as well as other changes in body compo-
sition such as osteoporosis and increased fat mass a
Frailty in Ageing Research Unit, bGerontology Department, Vrije Uni-
[5]. Exercise can slow down these processes and even versiteit Brussel and cGeriatrics Department, Universitair Ziekenhuis
reverse them [6]. In fact, exercise is one of the most Brussel, Brussels, Belgium
effective means to attenuate characteristics of aging Correspondence to Ivan Bautmans, PhD, Gerontology Department, Vrije
and many chronic diseases [7,8]. Universiteit Brussel (VUB), Laarbeeklaan 103, B-1090 Brussels,
In older adults, 30 min of aerobic training such Belgium. Tel: +32 2 477 42 07; e-mail: ivan.bautmans@vub.be
as walking, running or cycling three times per Curr Opin Clin Nutr Metab Care 2017, 20:30–53
week has significant effects on cardiorespiratory DOI:10.1097/MCO.0000000000000335

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The effects of exercise in older adults: a systematic review Liberman et al.

Only studies with an exercise intervention in older


KEY POINTS adults, with an outcome focused on inflammation,
 Thirty-four relevant articles were included: a muscle strength, body composition or physical
methodological quality assessment was performed and functioning were included; studies focusing on
effect size for outcome parameters was calculated the effects of nutritional supplementation or with-
where possible. out control group for exercise intervention were not
eligible. A total of 90 articles were excluded after
 Few articles involving limited types of interventions in
frail older adults showed improvements on muscle screening the titles and abstracts for the following
strength, physical functioning and CLIP. reasons: published before 2015, did not study older
adults, did not use an exercise intervention,
 In healthy nonfrail older adults, resistance training is measured other outcome parameters or for other
mostly used and showed improved CLIP, physical
reasons (e.g. study performed on animals). After
functioning, body composition and muscle strength.
reading full texts, 18 articles were excluded on
 Articles involving older adults with a specific disease the basis of study design (not RCTs), outcome
showed that exercise interventions are feasible and parameters or lack of exercise intervention. By
showed overall positive effects in all outcome screening the reference lists and citations of the
parameters, although reducing CLIP can be more
included articles, nine more relevant articles
challenging depending on the condition.
were identified and included in the review.
 Frail older patients are scarcely involved in exercise This finally resulted in 34 included articles
interventions, and more studies should focus on & && && & &
[12 ,13,14 ,15,16,17 ,18 ,19,20 ,21 ,22 – 25 ,
& && &&

comparing the effects of different types of exercise && & && &&
26,27 ,28– 30,31 ,32 ,33,34 ,35 – 38,39 – 41 ,42,
& &

interventions in this population. && &&


43 –45 ]. An overview of the literature search can
be found in Fig. 1.

strength more than resistance training at a low


intensity [11]. Quality assessment
The aim of this review is to provide an overview Articles were assessed by two reviewers (K.L. and I.B.,
of the most recent literature regarding the effects of Table 1) using the NICE guidelines for randomized
physical exercise on muscle strength, body compo- controlled trials [46].
sition, physical functioning and the inflammatory
profile in older adults.
Data extraction
For all articles, main characteristics of the partici-
METHODS pants and interventions were identified. Next, all
PubMed [search key: (Frail OR ‘Frail Elderly’[Mesh] outcome parameters regarding the inflammatory
OR ‘Aged’[Mesh]) AND (’Exercise’[Mesh] OR ‘Exer- profile, body composition, muscle strength and
cise Movement Techniques’[Mesh] OR ‘Exercise physical functioning were extracted. Data regarding
Therapy’[Mesh] OR ‘Resistance Training’[Mesh] these outcome parameters were identified, and
OR exercise) AND (Sarcopenia OR ‘Muscle Fibers, effect size was calculated using Cohen’s d (small
Skeletal’[Mesh] OR ‘Myoblasts, Skeletal’[Mesh] OR effect size d ¼ 0.2, medium effect size d ¼ 0.5 and
‘Muscle, Skeletal’[Mesh] OR ‘Inflammation’[Mesh] large effect size d ¼ 0.8) [47]. When insufficient data
OR ‘Cytokines’[Mesh] OR ‘Chemokines’[Mesh])] were available in the article, the authors were con-
and Web of Science [search key: (TS ¼ (Frail OR Frail tacted by e-mail to obtain supplementary data
Elderly OR Aged) AND TS ¼ (Exercise OR Exercise allowing us to calculate effect size. If authors did
Movement Techniques OR Exercise Therapy OR not respond, effect size was reported as ‘no data
Resistance Training OR exercise) AND TS ¼ (Sarco- available’ (n.d.a.). Effects of other interventions
(Sarcopenia OR Muscle Fibers, Skeletal OR Myo- (e.g. nutritional supplementation) were ignored in
blasts, Skeletal OR Muscle, Skeletal OR the data extraction and analysis.
Inflammation OR Cytokines OR Chemokines)]
were screened for articles published in 2015 or
2016 (last search on 26 May 2016). Filters were used RESULTS AND DISCUSSION
in PubMed, including studies when written in Eng- Thirty-four articles were included – four involving
lish, designed as randomized controlled trials or frail older adults (Table 2), 24 healthy, nonfrail older
controlled clinical trials (reviews were excluded) adults (Table 3) and five older adults with a specific
and included human patients aged at least 65 years. disease (Table 4). One article reported on both frail
This resulted in 108 and 26 articles, respectively. and nonfrail patients.

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Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


Ageing: biology and nutrition

Identification
Records identified through Additional records identified
database searching through other sources
(n = 108) (n = 36)

Records after duplicates removed


(n = 142)
Screening

Records screened Records excluded


(n = 142) (n = 90)

Full-text articles assessed


for eligibility Full-text articles excluded,
Eligibility

(n = 52) with reasons


(n = 18)

Studies included in
qualitative synthesis
(n = 34)
Included

Studies included in
quantitative synthesis
(meta-analysis)
(n = 34)

FIGURE 1. Overview of the literature search.

Exercise interventions exercise with horses (in which participants per-


Several types of exercises were identified in the 36 formed exercises on the floor interacting with the
included studies. These can be divided into four horse as well as exercises on the horse, n ¼ 1) [13],
categories. The first category, encompassing 16 stud- Pilates and Huber training (n ¼ 1) [28], (weighted) tai
chi (n ¼ 2) [16,40 ], soccer training [12 ] and balance
& &

ies, concerns resistance training ranging from mod- &&

erate (50–60% 1RM) to high (70–80% 1RM) intensity training [14 ].


& && && & & & && && &&
[12 ,14 ,17 ,18 ,20 ,21 ,23 ,29,30,32 ,34 ,36,
& & && &&
39 ,41 ,43 ,44 ]. Second, eight studies used aerobic
training, including mainly cycling and walking Exercise effects in frail older adults
&& && && && & &&
[15,17 ,23 ,25 ,27 ,31 ,35,45 ]. Third, six studies Five studies were identified, of which one reported
investigated the effects of combined training on the effects of exercise on inflammation [24 ],
&&

(combined resistance training and aerobic training) &&


four on body composition [24 ,34 ,41 ,45 ] and
&& & &&

&& && &&


[23 – 25 ,26,27 ,35]. Lastly, the remaining four on physical functioning and muscle strength
studies included other types of exercises including && && &
[19,24 ,34 ,41 ]. Frail elderly often present elev-
whole body vibration (WBV) (n ¼ 5) [19,33,37,38,42], ated CLIP [48], and physical frailty also implies –

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Table 1. Quality assessment of the included articles

(B) Performance bias


(systematic differences
(A) Selection bias between groups in the
(systematic differ- care provided, apart (D) Detection bias (bias in how
ences between the from the intervention (C) Attrition bias (systematic differences between the comparison outcomes are ascertained,
comparison groups) under investigation) groups with respect to loss of participants) diagnosed or verified)
References A1 A2 A3 Risk B1 B2 B3 Risk C1 C2a C2b C3a C3b Risk D1 D2 D3 D4 D5 Risk
&
Andersen et al. [12 ] U U Y U Y N U U Y ST: n ¼ 1; RT: n ¼ 0; U ST: n ¼ 1; RT: n ¼ 0; U L Y Y Y Y U L
Co: n ¼ 0 Co: n ¼ 0
Aranda-García et al. Y U N U Y N N U Y TE: n ¼ 1; HE: n ¼ 7; U TE: n ¼ 2; HE: n ¼ 10; U U Y Y Y Y U L
[13] Co: n ¼ 5 Co: n ¼ 5
&&
Beurskens et al. [14 ] U U Y U Y N U U Y HRT: n ¼ 0; BAL: n ¼ 0; N/A HRT: n ¼ 0; BAL: n ¼ 0; N/A L Y Y Y U U L
CO: n ¼ 0 CO: n ¼ 0
Camillo et al. [15] U U N/A L N/A N/A N/A U N/A n ¼ 0 N/A n ¼ 0 N/A U N/A Y Y N/A U L
Campo et al. [16] U U Y U Y N N U Y TCC: n ¼ 3; HEC: n ¼ 6 Y TCC: n ¼ 1; HEC: n ¼ 1 Y L Y Y Y U U U
Canuto Wanderley Y Y N U Y N N U Y AT: n ¼ 4; RT: n ¼ 8; U AT: n ¼ 3; RT: n ¼ 8; U L Y Y Y N U U
&&
et al. [17 ] WL: n ¼ 12 WL: n ¼ 0
&
Carneiro et al. [18 ] U U Y U Y N N U Y G2: n ¼ 4; G3: U G2: n ¼ 4; G3: U L Y Y Y U U U
n¼7 n¼7
Corrie et al. [19] Y Y N U Y Y N L Y SV: n ¼ 2; VV: n ¼ 2; Y / U L Y Y Y Y U L
Sham: n ¼ 2
&

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Dias et al. [20 ] Y U U U Y U U U Y ETG: n ¼ 4; CTG: n ¼ 3 U ETG: n ¼ 4; CTG: n ¼ 3 U U Y Y Y U U U
&
Emerson et al. [21 ] U U N H Y N U U Y n¼0 Y / N/A L Y Y Y N U U
&&
Forti et al. [22 ] Y Y Y L Y Y N L Y HIGH: n ¼ 0; LOWþ: N/A HIGH: n ¼ 1; LOWþ: Y L Y Y Y Y Y L
n ¼ 0; LOW: n ¼ 0 n ¼ 1; LOW: n ¼ 3
&&
Irving et al. [23 ] U U Y U N/A N N H Y CT: n ¼ 1 Y n¼0 Y L Y Y Y U U U
&&
Kim et al. [24 ] Y Y Y L Y Y Y L Y n¼0 Y n¼0 Y L Y Y Y Y Y L
&&
Lee et al. [25 ] U U U U Y U U U Y CT: n ¼ 5; AT: n ¼ 3 U CT: n ¼ 5; AT: n ¼ 3 U U Y Y Y U U U
Libardi et al. [26] Y U Y L Y U U U Y / N/A / N/A L Y Y Y U U U
&&
Lima et al. [27 ] U U N U Y U U U Y n¼0 N/A n ¼ 0 N/A L Y Y Y U U U
Markovic et al. [28] Y Y Y L Y N U U Y Huber: n ¼ 1; Pilates: U Huber: n ¼ 1; Pilates: U U Y Y Y Y Y L
n¼3 n¼3
Martins et al. [29] Y Y Y L Y N N U Y TG: n ¼ 5; CG: n ¼ 2 U TG: n ¼ 5; CG: n ¼ 2 U U Y Y Y U U U
Nicholson et al. [30] Y U N U Y N Y L Y RT: n ¼ 4; CON: n ¼ 3 U RT: n ¼ 0; CON: n ¼ 0 U L Y Y Y Y U L
&

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Nishida et al. [31 ] U U N U Y U N U Y EG: n ¼ 3; CG: n ¼ 4 U EG: n ¼ 3; CG: n ¼ 4 U U Y Y Y U U U
&&
Padilha et al. [32 ] U U Y U Y N N U Y G2: n ¼ 0; G3: N/A G2: n ¼ 0; G3: N/A L Y Y Y U U U
n¼0 n¼0

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Perchthaler et al. [33] U U U U Y U U U Y WBV: n ¼ 1; Co: n ¼ 5 U WBV: n ¼ 1; Co: n ¼ 5 U U Y Y Y U U U
&&
Reid et al. [34 ] U U Y U U N N U Y LO: n ¼ 1; HI: n ¼ 3 U LO: n ¼ 1; HI: n ¼ 3 U U Y Y Y Y Y L
The effects of exercise in older adults: a systematic review Liberman et al.

33
34
Table 1 (Continued)

(B) Performance bias


(systematic differences
(A) Selection bias between groups in the
Ageing: biology and nutrition

(systematic differ- care provided, apart (D) Detection bias (bias in how
ences between the from the intervention (C) Attrition bias (systematic differences between the comparison outcomes are ascertained,
comparison groups) under investigation) groups with respect to loss of participants) diagnosed or verified)

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References A1 A2 A3 Risk B1 B2 B3 Risk C1 C2a C2b C3a C3b Risk D1 D2 D3 D4 D5 Risk

Rossi et al. [35] U U Y U Y N U L Y CT: n ¼ 3; AT: n ¼ 20; U CT: n ¼ 3; AT: n ¼ 20; U U Y Y Y U U L


CON: n ¼ 16 CON: n ¼ 16
Ruiz et al. [36] Y Y Y L Y N N U Y IG: n ¼ 0; CG: n ¼ 0 N/A IG: n ¼ 0; CG: n ¼ 0 N/A L Y Y Y Y Y L
Salhi et al. [37] Y Y N U N N N H Y WBV: n ¼ : 5 RT: n ¼ 6 U WBV: n ¼ : 5 RT: n ¼ 6 U L Y Y Y U U L
Sitjà-Rabert et al. [38] Y Y Y L Y N U L Y WBV: n ¼ 14; RT: U WBV: n ¼ 7; RT: n ¼ 6 Y L Y Y Y Y U L
n ¼ 14
&
Strandberg et al. [39 ] Y U Y L Y N U U Y CON: n ¼ 3; RT: n ¼ 4 U CON: n ¼ 3; RT: n ¼ 4 U U Y Y Y U U L
&
Su et al. [40 ] U U N U Y U U U Y U U U U U Y Y U U U U
&
Tieland et al. [41 ] U U Y U Y N N U Y Ex: n ¼ 11; Co: n ¼ 8 U Ex: n ¼ 16; Co: n ¼ 17 U U Y Y Y U U L
Tseng et al. [42] Y Y N U Y N U L Y WBV: n ¼ 0; VFDWBV: Y WBV: n ¼ 0; VFDWBV: Y L Y Y Y U U L
n ¼ 0; CON: n ¼ 0 n ¼ 0; CON: n ¼ 0
&&
Villanueva et al. [43 ] U U U U Y N N U Y SS: n ¼ 0; SL: n ¼ 0 N/A SS: n ¼ 0; SL: n ¼ 0 N/A L Y Y Y N N L
Winters-Stone et al. Y U Y L U N N U Y POWIR: n ¼ 2; FLEX: N POWIR: n ¼ 5 FLEX: N U Y Y Y Y Y L
&&
[44 ] n¼3 n ¼ 10
&&
Yamada et al. [45 ] Y U U L Y N U U Y W: n ¼ 1; Co: n ¼ 2 U W: n ¼ 1; Co: n ¼ 2 U L Y Y Y U U L

A1: adequate method of randomization; A2: adequate concealment of allocation; A3: groups comparable at baseline; B1: groups received same care apart from intervention; B2: participants kept blind; B3: individuals
administering care kept blind; C1: groups followed up equal length of time; C2a participants did not complete treatment; C2b: groups comparable for treatment completion; C3a: participants with missing data; C3b:
groups comparable for availability in outcome data; D1: appropriate length of follow-up; D2: precise definition of outcome; D3: valid method to determine outcome; D4: investigators blinded to participants’ exposure;
D5: investigators blind to other important confounding factors. AT, aerobic training; BAL, balance training; CG, control group; CON, control; CT, combined training; CTG, conventional training group; ETG, eccentric-
focused training group; H, high risk; HE, horse exercise; HEC, health education classes; HRT, heavy-resistance strength training; L, low risk; N, no; N/A, not applicable; RT, resistance training; SV, side alternating
vibration; TCC, tai chi chih; U, unclear; VFDWBV, visual feedback-deprived and whole body vibration; VV, vertical vibration; WBV, whole body vibration; WL, waiting list; Y, yes.

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Volume 20  Number 1  January 2017
Table 2. Frail older adults

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Corrie et al. [19] Referred to an outpatient Usual falls prevention n.d.a. n.d.a.
falls prevention service program. 6/week.
1 h exercise class
and information
relevant to falls
Sham: n ¼ 20. Age 3/week. 12 weeks SV: leg power: $; SV: PASE: $; NEADL:
79.1  7.8 years vibration sessions maximal force $; TUG: $;
output: $ functional reach: $;
CST: $; 4SS: $
SV: n ¼ 20. Age 2–4 30 s bouts in VV: leg power: $ ^; VV: PASE: $; NEADL:
79.5  5.7 years week 1 and up to 6 maximal force $; TUG: $;
1 min by week 8 output: $ functional reach: $;
CST: $; 4SS: $
VV: n ¼ 21. Age VV versus SV versus Sham: leg power: $; Sham: PASE: $;
81.9  5.7 years Sham maximal force NEADL: z; TUG: z;
output: $ functional reach: $;
CST: "z; 4SS: $
&&
Kim et al. [24 ] Frail women. community- DEXA Smedley-type
dwelling dynamometer
CT: n ¼ 33. Age CT: 60 min. 2/week for CT: BDNF: "0.56z; CT: appendicular CT: grip strength: CT: n.d.a.: exhaustion:

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81.1  2.8 years 3 months. Warm-up. beta 2 microglobulin: skeletal MM: $0.10; $0.13; knee z#; low physical
30 min RT. 20 min of $0.06; myostatin: leg MM: $0.12 extension strength: activity: "z; WGS:
balance and gait $0.19; (IGFBP3/ $0.20 "0.37z; TUG:
training IGF1)  100: "0.36z; #0.98z~
GH: "0.6z
Placebo: n ¼ 32. Age Placebo: whole milk Placebo: BDNF: Placebo: appendicular Placebo: grip strength: Placebo: n.d.a.
80.3  3.3 years powder $0.19; beta 2 skeletal MM: $0.06; $0.07; knee WGS: $0.22; TUG:
microglobulin: leg MM: $0.08 extension strength: $0.07
$0.20; myostatin: $0.04
$0.15; (IGFBP3/
IGF1)  100: $0.40;
GH: $0.18
&&
Reid et al. [34 ] 52 participants RT: 2/week. Muscle size: computed 1RM SPPB
16 weeks tomography
n.d.a. n.d.a. n.d.a.

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LO: n ¼ 25. Age 78.3  5 LO group: 3  10 LO: $ LO: 1RM: "z; peak LO: "z
years repetitions at 40% power 408: $; peak
1RM power 708: $

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The effects of exercise in older adults: a systematic review Liberman et al.

35
36
Table 2 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

HI: n ¼ 27. HI group: 3  10 HI: $ HI: 1RM: "z; peak HI: "z
Age ¼ 77.6  4 years repetitions at 70% power 408: $; peak
Ageing: biology and nutrition

1RM power 708: $


Community-dwelling
Difficulty in a mobility-

www.co-clinicalnutrition.com
related task
&
Tieland et al. [41 ] Prefrail and frail DEXA 1RM SPPB
RT: n ¼ 62. Age RT: 2/week. RT: LBM: $0.09; RT: leg press: "8.82z; RT: "3.25~
78.4  1.0 years 24 weeks. appendicular LBM: leg extension:
3–4  10–15 $1.27 "8.24z~; dominant
repetitions at 50% HG: "1.04z;
1RM up to 8–10 nondominant HG:
repetitions at 75% "1.08z
1RM.
Control: n ¼ 65. Age Control: no intervention Control: LBM: $0.08; Control: leg press: Control: $1.70
79.5  1.0 years appendicular LBM: $2.79; leg
$0.18 extension: $2.67;
dominant HG:
"0.56z; nondominant
HG: "0.92z
&&
Yamada et al. [45 ] Age 65 years
Community-dwelling;
frail
W: n ¼ 15 W group: pedometer- W: SMI: "0,09z~
based walking
program. 6 months.
increase daily steps
by 10% each month
Control: n ¼ 25 Control: no program Control: SMI: #0.30z

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Results are given as prepost intervention: ", increase postintervention; #, decrease postintervention; $, no change; z, significant result in group; ~, significant difference between groups; ^, significance between first
group and last group; AT, aerobic training; CT, combined training; GH, growth hormone; n.d.a., no data available to calculate effect size; RT, resistance training; SV, side alternating vibration; VV, vertical vibration;
W, walk.

Volume 20  Number 1  January 2017


Table 3. Healthy nonfrail older adults

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Andersen et al. Healthy men 16 weeks. 2/week. DEXA


&
[12 ] 1 h/session
SG: n ¼ 9. Age SG: weeks 1–12: SG: FM: $0.72; LBM:
68.0  4.0 years 3  15 min; weeks 0.35^
13–52: 4  15 min
RT: n ¼ 9. Age RT: 3  16–20 RM RT: FM: $0.38;
69.1  3.1 years (weeks 0–4). 3  12 LBM:1.54 ~
RM (weeks 5–8).
3  10 RM (weeks
9–12) and 4  8 RM
(weeks 13–52)
CG: n ¼ 8. Age CG: no intervention CG: FM: $0.03; LBM:
67.4  2.7 years $0.23
Aranda-Garcı́a et 12 weeks. 60 min. 3/ Dynamometer:
al. [13] week
CT: n ¼ 17. Age CT: AT þRT 1/week: CT: KES 908: "0.53z; CT: WGS: $0.27; PA:
70.5  7.1 years 8–10 exercises. 8– KES: 608: $0.30; $ n.d.a.
12 repetitions handgrip: "1.02z
HE: n ¼ 10. Age HE: exercises on the HE: KES 908: "1.06z; HE: WGS: "0.72z; PA:
72.2  7.7 years ground interacting KES 608: $0.50; $n.d.a.

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with the handgrip: $0.17
horse þ exercises on
the horse
C: n ¼ 11. Age CON: no training CON: KES 908: C: WGS: $0.15; PA:
71.9  5.4 years $0.04; KES 608: $ n.d.a.
$0.16; handgrip:
$0.55
Beurskens et al. Healthy male adults 13 weeks. 3/week. BL, ULR and ULL
&&
[14 ] 60 min
HRT: n ¼ 19. Age Bilateral HRT: RT at HRT: BL: "0.46z^;
66.4  4.9 years 80% of 1RM. 3  10 ULR: "0.37z^; ULL:
repetitions "1.23z^
BAL: n ¼ 14. Age BAL: balancing tasks BAL: BL: "0.50z^;
66.3  5.3 years and exercises on soft ULR: "0.52z^; ULL:
mats. Wobble boards "0.99z^

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and uneven surfaces.
4  20 s
CON: n ¼ 20. Age CON: no training. CON: BL: #0.30z; ULR:

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66.7  4.0 years Follow regular #0.23z; ULL: #0.17z
routines
The effects of exercise in older adults: a systematic review Liberman et al.

37
38
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Canuto Wanderley Community-dwelling. 3/week. 8 months. DEXA Accelerometer


&&
et al. [17 ] physically session: 50 min
independent
AT: n ¼ 24. Age AT: 30 min walking/ RT: BFM: #0.73z^; RT: 6 MWT: $0.34;
70.0  5.7 years biking LBM: $0.09 stair ascent: #2.5z
^; 8 FUG: #1.5z^;
Ageing: biology and nutrition

sit-to-stand: #1.8 z^;


handgrip: $1; PA:
"0.46z

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RT: n ¼ 19. Age RT: month 1: 2  12– AT: BFM: #0.74z^; AT: 6 MWT: "0.56 z^;
67.3  4.9 years 15 repetitions at 50– LBM: $0.06 stair ascent: #5.00
60% of 1RM. Months z^; 8 FUG: 3.5 z^;
2–8: 2  12 sit-to-stand: #3.4z^;
repetitions at 80% of handgrip: $0.5; PA:
1RM "0.21z
WL: n ¼ 31. Age WL: call after 4 months. WL: BFM: $0.08; WL: 6 MWT: $0.03;
67.8  5.5 years No changing of LBM: $0.13 stair ascent: $0.5;
lifestyle 8 FUG: $0.5; sit-to-
stand: $1.25;
handgrip: $0; PA:
$0.04
&
Carneiro et al. [18 ] Older women RT: 1 set of 10–15 DEXA Training load (kg)
repetitions of 1RM
G2: n ¼ 28. Age G2: 2/week G3: G2: mm: n.d.a. "z G2: n.d.a. $
67.6  5.3 years 3/week
G3: n ¼ 25. Age G3: mm: n.d.a. "z G3: n.d.a. $~
67.0  5.6 years
&
Dias et al. [20 ] Healthy elderly women 12 weeks. 2/week. Maximal dynamic n.d.a.
Weeks 1 þ 2. 2  12 strength (1RM)
repetitions at 40% n.d.a.
1RM. Week 3 þ 4 at
50% 1RM. Weeks
5 þ 6. 2  10
repetitions at 55%

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1RM. Week 7 þ 8 at
60% 1RM. Week
9 þ 10 3  8
repetitions at 65%.
Week 11 þ 12 at
70% 1RM

Volume 20  Number 1  January 2017


Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

ETG: n ¼ 9. Age ETG: concentric 1.5 s. ETG: LP: $; knee CTG: 6 MWT: "z; TUG:
65.6  5.6 years Eccentric 4.5 s extension: "z #z; stair climbing: "z;
CST: #z
CTG: n ¼ 10. Age CTG: concentric 1.5 s. CTG: leg pres: $; knee ETG: 6 MWT: "z; TUG:
67.8  6.5 years Eccentric phases extension: "z #z; stair climbing: "z;
1.5 s CST: #z
&
Emerson et al. [21 ] Living independently DEXA 1RM
RT: n ¼ 11. Age RT: 2/week. 6 weeks. RT: FM: $0.03. LBM: RT: "0.82z~ RT: PWCFT: $0.49;
72.1  6.6 years 3 sets. 8–15 $0.01 CST: #1.23z; W:
repetitions at 70– #0.85z
85% of 1RM
C: n ¼ 12. Age CON: no training C: FM$. LBM: $0.01 C: $0.16 C: PWCFT: $0.03;
70.3  5.6 years CST: #0.42z; W:
$0.32
&&
Forti et al. [22 ] Community-dwelling RT: 3/week. 12
weeks
HIGH: n ¼ 18. Age HIGH group: 2  10– HIGH: IL-6: $0.47
67.9  4.4 years 15 repetitions at 80% sTNFR1: "0.13z
of 1RM IL-1RA: $0.16
IL-8: "0.26z

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LOW: n ¼ 19. Age LOW group: 1  60 LOW: IL-6: $0.16
68.9  5.3 years repetitions at 20% of sTNFR1: "0.21z
1RM IL-1RA: $0.31
IL-8: "0.59z
LOWþ: n ¼ 19. Age LOWþ: 1  60 LOWþ: IL-6: $0.07
67.6  6.0 years repetitions at 20% of sTNFR1: "0.14z
1RM immediately IL-1RA: $0.31
followed by 1  10– IL-8: "0.76z
20 repetitions at 40%
of 1RM
&&
Irving et al. [23 ] Older adults. Sedentary DEXA 1RM
CON/CT: n ¼ 12. Age
71  2 years
AT: n ¼ 11. Age 70  1 AT: cycling at 65% AT: BFM (%): $; BFM AT: CP (kg): $0.08; LP
years VO2 peak 1 h. 5/ (kg): #0.18z; LBM (kg): "0.41z

Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


week. 8 weeks (kg): "z; midthigh
skeletal muscle (cm2):
"0.16z

www.co-clinicalnutrition.com
The effects of exercise in older adults: a systematic review Liberman et al.

39
40
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

RT: n ¼ 10. Age 70  1 RT: 4 sets of 8–10 RT: BFM (%): $; BFM RT: CP (kg): "0.31z; LP
years repetitions. 4  / (kg): $; LBM (kg): (kg): "0.69z
week. 8 weeks $; midthigh skeletal
muscle (cm2): $0.23
CON: BFM (%): $; CON: CP (kg): $0.07;
BFM (kg): $; LBM LP (kg): $0.00
Ageing: biology and nutrition

(kg): $; midthigh
skeletal muscle (cm2):
$0.03

www.co-clinicalnutrition.com
CT: no exercise for 8 CT: CP (kg): n.d.a. "z;
weeks (CON). LP (kg): n.d.a."z
followed 8 weeks of
CT: cycling 30 min
5/week and 2/3
the RT volume 4
days/week
&&
Lee et al. [25 ] 27 women DEXA Isokinetic strength
65–75 years

CT: n ¼ 9 CT: AT. Walking at CT: CRP#1.45 z~ CT: body mass: #0.06z CT: left knee extension:
40–70% heart rate. IL-6: #1.11 z BFM: #0.66z "0.86z~
3/week þ RT 2/ TNF-a: #0.49z LBM: $0.33~ left knee flexion:
week. Elastic bands BF: #0.72z "0.43z~
15–20 repetitions. WHR: $0.09 right knee
intensity: 10–13 on extension: "0.97z~
Borg’s scale. 8 right knee flexion:
weeks $0.32
AT: n ¼ 10 AT: walking. 5/week. AT: CRP: #1.05 z AT: body mass: #0.34z AT: left knee extension:
8 weeks. Walking at IL-6: #0.59 z BFM: #0.51z $0.09
40–70% of HRR for TNF-a: #0.62 z LBM: $0.19 left knee flexion:
40 min BF: #0.67z $0.05
WHR: $0.23 right knee
extension: $0.06
right knee flexion:
$0.08

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Libardi et al. [26] 4 days/week. 12 CSA 1RM
weeks

Volume 20  Number 1  January 2017


Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

CT: n ¼ 8. Age ¼ 65 CT: W/run 40 min at CT: "0.26z CT: "0.92z


 3.7 years 60–85% VO2 peak.
After week 6:
50 min. 4  10
repetitions 70% 1RM.
After 6 weeks: 80%
1RM
BFR-CT: n ¼ 10. BFR-CT: BFR-RT and ET: BFR-CT: "0.27z BFR-CT: "0.46z
Age ¼ 64  4 years 1  30 repetitions
and 3  15
repetitions 20% 1RM.
After 6 weeks 30%;
ET same as other
group
CG: n ¼ 7. n ¼ 8. CG: no training CG: $0.07 CG: $0.25
Age ¼ 65  4 years
Sedentary. Not obese.
No CVD
Markovic et al. [28] 30 women 8 weeks. 3/week
Age: 70  4 years

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Huber group: n ¼ 16 Huber: combined core Huber group: body Huber group: isometric
and balance mass: $0.09; body trunk extension:
exercises 25–30 min. fat: #0.48z "0.98z; isometric
Interactive interface. trunk flexion: "1.19z;
Weeks 1–2: 50% of isometric trunk right
MVC. Weeks 3–5 lateral flexion:
over 65% MVC. "1.12z; isometric
Weeks 6–8 75% of trunk left lateral
MVC. 30–60 flexion: "1.17z;
contractions per upper body: "0.43z;
session lower body power:
"0.47z

Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


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The effects of exercise in older adults: a systematic review Liberman et al.

41
42
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Pilates group: n ¼ 14 Pilates: 3  1 h. Core Pilates: body mass: Pilates group: isometric
stability. Each $0.07; body fat: trunk extension:
exercise for 2–4 sets $0.05 $0.12; isometric
with 15–20 s trunk flexion: $0.14;
contraction time or isometric trunk right
15–20 repetitions lateral flexion:
$0.04; isometric
Ageing: biology and nutrition

trunk left lateral


flexion: $0.05;
upper body: "0.22z;

www.co-clinicalnutrition.com
lower body power:
$0.06
Martins et al. [29] DEXA
RT: n ¼ 20. Age RT: 2-week RT: ULFFM: $0.19 RT: handgrip strength:
69.1  6.3 years familiarization þ 8 LLFFM: $0.03 $0.10
week strength PT 608/s: $0.08
training 2/week PT 1208/s: "0.14z
CG: n ¼ 20. Age CG: did not receive CG: ULFFM: $0.00 CG: handgrip strength:
66.2  6.6 years any specific training LLFFM: $0.00 $0.03
or placebo condition PT 608/s: $0.02
PT 1208/s: $0.06
Nicholson et al. Healthy FM (DEXA) LP. Bench press (1RM)
[30] postmenopausal
women
RT: n ¼ 24. Age RT 2/week RT: $0.05 RT: LP: "0.51z
66  4.4 years bodypump class. BP: "0.6z
50 min/class. 6
months. 10 tracks.
each up to 6 min
CON: n ¼ 26. Age CON: no training CON: $0.05 CON: LP: $0.04
66  4.5 years BP: $0.00
&
Nishida et al. [31 ] Females

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Volume 20  Number 1  January 2017
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

AT: n ¼ 31. Age AT: bench step: height AT: IL-4: $0.05
70.4  5.8 years 15–20 cm. step IL-5: $0.03
rhythm at 40 steps/ IL-6: $0.09
min and increased by IL-8: $0.08
10 steps/min every IL-15: $0.21
4 min. separated by IFN-g: $0.21~
2-min rest intervals. TNF-a: $0.12
3/day 10–20 min TNF-b: $0.07
each session. For a
goal of 140 min/
week. At home for
12 weeks
CG: n ¼ 31. Age CG: normal lifestyle CG: IL-4: $0.18
69.7  6.6 years IL-5: $0.19
IL-6: $0.27
IL-8: $0.07
IL-15: $0.13
IFN-g: $0.36
TNF-a: $0.07
TNF-b: $0.18
&&
Padilha et al. [32 ] 27 older women 30 weeks: 12 weeks 1RM

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RT þ 12 weeks
detraining period þ 6
weeks data collection
G2: n ¼ 13. Age 1  10–15 repetitions G2: CP: "0.89z
68.9  5.0 years at 1RM KES: "0.83z
preacher curl: "1.80z
G3: n ¼ 14. Age RT 2/week (G2) G3: CP: "2.42z~
68.7  4.8 years KES: "0.67z~
preacher curl:
"2.10z~
Physically independent RT 3/week (G3)
Perchthaler et al. Healthy. Physically Maximal isokinetic
[33] active older adults muscle strength

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www.co-clinicalnutrition.com
The effects of exercise in older adults: a systematic review Liberman et al.

43
44
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

WBV: n ¼ 13; 5 men WBV: 12 training WBV: right leg


and 8 women; Age. sessions. 6 weeks. extension: $0.08
54.9  9.0 years Warm-up at 18 Hz. left leg extension:
Frequency of 30 Hz $0.14
combined with an right leg flexion:
amplitude of 3.9 mm $0.06
and a knee angle of left leg flexion:
Ageing: biology and nutrition

608. Rest time $0.13


between each
repetition was 60 s.

www.co-clinicalnutrition.com
120 s between
exercises
CO: n ¼ 8; 2 men and CG: no change in CO: right leg
6 women. Age physical activity extension: $0.09;
54.5  6.3 years left leg extension:
$0.21; right leg
flexion: $0.01; left
leg flexion: $0.25
Rossi et al. [35] Postmenopausal women AT: running track: 400, DEXA
800 and 1200 m
fastest possible
CT: n ¼ 35. Age CT: 57 min: 27 min AT: FM (kg): #0.34z;
60.3  6.1 years RT þ 30 min AT. RT: FM (%): #0.22z;
weeks 1–4: 3  15 FFM: "0.12z^
repetitions at 65% of
1RM; weeks 5–8:
3  12 repetitions at
70% of 1RM; weeks
9–12: 3–4  10
repetitions at 75%;
weeks 13–16: 3–
4  8 repetitions at
80% of 1RM
AT: n ¼ 35. Age CG: no intervention CT: FM (kg): #0.18z;
60.5  7.3 years FM (%): #0.31z^;

Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


FFM: "0.20z^
CG: n ¼ 34. Age CG: FM (kg): $0.03;
62.6  5.9 years FM (%): $0.01;
FFM: $0.07

Volume 20  Number 1  January 2017


Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Ruiz et al. [36] Planning to stay in the n.d.a. 1RM n.d.a.


same nursing home. n.d.a.
Ambulant
RT: n ¼ 20. Age RT: standard RT: ACE: $; sAPP: $; RT: LP: "z RT: 8 MWT: $; 4SS:
92.3  2.3 years care þ 8 weeks. BDNF: $; EGF: $; $; TUG: $; MMSE:
40–45-min TNF-a: $ $; GDS: $
intervention
3/week. 2–3 sets
of 8–10 repetitions
at 30% 1RM at the
start of the program
to 70% of 1RM at the
end. 4-week
detraining period
CON: n ¼ 20. Age CON: informed of CON: ACE: $; sAPP: CON: $ CON: 8 MWT: $;
92.1  2.3 years effects of PA. Daily $; BDNF: $; EGF: 4SS: $; TUG: $;
mobility exercises $; TNF-a: $ MMSE: $; GDS: $
Sitjà-Rabert et al. Healthy older adults 6 weeks. 3/week n.d.a.
[38]
WBV: n ¼ 59. Age WBV: static/dynamic WBV: TUG: $; 5 times

1363-1950 Copyright ß 2016 Wolters Kluwer Health, Inc. All rights reserved.
64.6  0.7 years exercise; 30–35 Hz sit-to-stand: "z
and amplitude
2–4 mm
RT: n ¼ 58. Age RT: static and dynamic RT: TUG: $; 5 times sit-
63.9  0.8 years exercise to-stand: "z
Strandberg et al. Recreationally DEXA 1RM Physical activity
&
[39 ] physically active (accelorometry)
women
RT: n ¼ 21. RT: 24 weeks. 2/ RT: CRP: $0.10; IL-6: RT: lean leg mass: RT: "0.96z~ RT: $0.20
Age 68  2 years week. 8–12 $0.02 $0.03; lean FM:
repetitions at $0.10; leg BMD:
75–85% of 1RM $0.12
CON: n ¼ 21. Age CON: no intervention CON: CRP: $1.12; IL- CON: lean leg mass: CON: $0.01 CON: $0.30
68  1 years 6: $0.00 $0.12; lean FM:
$0.12; leg BMD:

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$0.09

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The effects of exercise in older adults: a systematic review Liberman et al.

45
46
Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect
&
Su et al. [40 ] Older adults. Mean TC þ WTC: 4–5 60-min TC: 308/s: KES:
Age 65.3 years sessions/week of tai "0.32~; knee
chi training. flexors: $~;
4 months plantarflexors: $~;
dorsiflexors:
$0.63~^;1208/s:
KES: $0.12~; knee
Ageing: biology and nutrition

flexors: $0.36~
CON: n ¼ 16 WTC: wearing a WTC: 308/s: KES:
weighted vest "1.29z^; knee

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flexors: "0.24z^;
plantarflexors:
"0.83z^;
dorsiflexors: "1.0z^;
1208/s: KES:
"1.52z^; knee
flexors: "0.98z^
TC group: n ¼ 17 CON: no intervention CON: 308/s: KES:
$0.22; knee flexors:
$0.00;
plantarflexors:
$0.18; dorsiflexors:
$0.00; 1208/s:
KES: $0.04; knee
flexors: $0.15
WTC: n ¼ 16
Tseng et al. [42] Healthy n.d.a.
Age: 69.22  3.97
years
WBV: n ¼ 14 WBV: 3/week. 5 min. WBV: KES: "z; knee
Amplitude of 4 mm at flexor: $
20 Hz
VFDWBV: n ¼ 17 Visual feedback- VFDWBV: knee
deprived and WBV extensor: "z; knee

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(VFDWBV): blindfold flexor: "z
to block their visual
feedback during
WBV
CON: n ¼ 14 CON: 0 Hz. Eyes open CON: KESr: $; knee
flexor: $

Volume 20  Number 1  January 2017


Table 3 (Continued)

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Villanueva et al. Men RT: 36 sessions. DEXA Muscle strength (1RM)


&&
[43 ] 12 weeks: 4-week
AT (2  15 to 4  8
repetitions). Followed
by 8-week RT (2  6
to 3  4 repetitions)
SS: n ¼ 11. Age SS: short rest interval SS: LBM: "0.27z~; fat SS: CP: "1.14z~; LP: SS: margaria (time):
65.6  3.4 years length sets: 60 s mass: $0.17 "2.05z~ #1.90z; margaria
(power): "1.86~z;
400 m W: #1.81z
SL: n ¼ 11. Age SL: long rest interval SL: LBM "0.09z; fat SL: CP"1.07z; LP"1.40z SL: margaria (time):
70.3  4.9 years length sets: 4 min mass: $0.10 #1.90z; margaria
(power): "1.59z;
400 m W: #1.08z
Yamada et al. Age 65 years
&&
[45 ]
Community-dwelling;
nonfrail
W: n ¼ 55 W group: pedometer- W: SMI: #0.12~
based walking

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program. 6 months.
Increase daily steps
by 10% each month
CON: n ¼ 50 CON: no program CON: SMI: "0.00z

Results are given as prepost intervention: " ¼ increase postintervention; # ¼ decrease postintervention; $ ¼ no change; z ¼ significant result in group; ~ ¼ significant difference between groups; ^ ¼ significance between
first group and last group; n.d.a. ¼ no data available to calculate effect size. AT, aerobic training; BAL, balance training; BFR-CT, blood-flow restriction combined training group; BFR-RT, blood-flow restriction resistance
training group; BL, bilateral; CG, control group; CON, control; CP, chest press; CT, combined training; CTG, conventional training group; ET, eccentric-focused training; ETG, eccentric-focused training group; FFM, fat-
free mass; HE, horse exercise; HEC, health education classes; HRT, heavy-resistance strength training; LLFFM, lower limb fat-free mass; LP, leg press; MVC, maximum voluntary contraction; RT, resistance training; SG,
soccer group; TC, tai chi; TCC, tai chi chih; ULFFM, upper limb fat-free mass; ULL, unilateral left; ULR, unilateral right; VFDWBV, visual feedback-deprived and whole body vibration; W, walk; WBV, whole body
vibration; WHR, waist-to-hip ratio; WTC, weighted tai chi.

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The effects of exercise in older adults: a systematic review Liberman et al.

47
48
Table 4. Older adults with a specific disease

Inflammation Body composition Muscle strength Function


References Population Intervention effect effect effect effect

Camillo et al. COPD patients DW: negative inclination CK:


[15] of 10%
BMI < 30 kg/m2 DWL: addition of a vest. LW: $0.18
10% of weight
n ¼ 10. LW: without inclination DW: "0.66z
Age 67  7 years
Ageing: biology and nutrition

As long as possible up to DWL: "0.37z


20 min
Campo et al. Senior female cancer 60 min. 3/ week. n.d.a.

www.co-clinicalnutrition.com
[16] survivors 12 weeks
Diagnosis of solid tumor
cancer. Stages I–III,
3 months since
treatment completion
TCC: n ¼ 29. Age 65.9 TCC group: 19 TCC: cortisol: $ ~; IL-
years nonstrenuous 12: $; IL-6: $; TNF-
movements. 10 min of a: $; IL-10: $; IL-4:
closing movements $
HEC: n ¼ 25. Age 66.7 HEC: topics relevant to HEC: cortisol: $; IL-12:
years aging $; IL-6: $; TNF-a:
$; IL-10: $; IL-4: $
Lima et al. AH 10 weeks. 3/week
&&
[27 ]
AT: n ¼ 15. Age AT: 20 min in weeks 1–4. AT: IL-6: #1.36z^;
67.8  4.3 years 30 min in weeks 5–10 TNF-a: $0.26
CT: n ¼ 15. Age CT: 1 circuit lap (weeks CT: IL-6: $0.31; TNF-
67.8  5.2 years 1–4). 2 laps (weeks a: $0.33^
5–10) at 50–60% 1RM.
5 repetitions upper
limbs. 20 repetitions
trunk and lower limbs
CG: n ¼ 14. Age CG: no training CG: IL-6: $0.40; TNF-
69.9  5.5 years a: $0.09

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Salhi et al. [37] Patients with COPD. 3/week. 12 weeks QF 6 MWT
Referred to n.d.a. n.d.a.
rehabilitation
WBV: n ¼ 31. Age 58 WBV: 27 Hz. 2 mm peak WBV: $ WBV: "z~
(55–73) years amplitude. 30–1 min.
1–3 repetitions
RT: n ¼ 31. Age 63 RT: 3  10 repetitions at RT: "z RT: "z
(57–68) years 70% of 1RM

Volume 20  Number 1  January 2017


Winters-Stone et Men. Prostate cancer. 1RM
&&
al. [44 ] Currently receiving
ADT
The effects of exercise in older adults: a systematic review Liberman et al.

among others – characteristics as weakness, slow

Results are given as prepost intervention: " ¼ increase postintervention; # ¼ decrease postintervention; $ ¼ no change; z ¼ significant result in group; ~ ¼ significant difference between groups; ^ ¼ significance between
FLEX: CST: $0.50;

first group and last group; AH, arterial hypertension; AT, aerobic training; CT, combined training; DW, downhill walking; DWL, downhill walking þ load; LW, level walking; n.d.a., no data available to calculate effect
4 m usual WGS:
$0.34; 4 m fast
WGS: $0.47;
4 m fast WGS:
walking speed and reduced physical activity (see

walk: $0.60;
$0.28; PPB:

PPB: $0.36
$0.83; 4 m
POWIR: CST:
other articles in this issue for details about the frailty
phenotype). Aerobic training and resistance train-

$0.65
Function

ing can play an important role in reducing inflam-


effect

mation and increasing muscle strength and muscle


mass [49]. Sarcopenia is more pronounced in frail
elderly [50]. However, several studies showed that
"0.22z~; leg press:

despite frailty, physical functioning can be


POWIR: bench press:

$0.06; leg press:


FLEX: bench press:
improved after different kinds of exercises [51–53].
Muscle strength

After a combined training intervention, inflam-


"0.48z~

matory markers improved significantly, including


$0.03

increased BDNF (effect size ¼ 0.56), IGF-1 (effect


effect

size ¼ 0.36) and growth hormone (effect size ¼ 0.60)


&&
[24 ].
Investigating body composition after resistance
training at low, moderate or high intensity, none of
the studies showed significant changes in muscle
Body composition

&& && &


mass, LBM or muscle size [24 ,34 ,41 ]. However,
another study reported a small but significant
improvement of muscle mass (effect size ¼ 0.09)
effect

after a 1-year walking program compared with non-


exercising controls in whom muscle mass decreased
(effect size ¼ 0.30) [45 ].
&&

Muscle strength increased following resistance


training, with a large effect size for the leg press
(effect size ¼ 8.82) and leg extension (effect
Inflammation

size ¼ 8.24) as reported by Tieland et al. [41 ]; note-


&

&&
worthy, Reid et al. [34 ] found no significant differ-
ences in strength gains when comparing resistance
effect

training at high (70% 1RM, effect size ¼ n.d.a.) and


low (40% 1RM, effect size ¼ n.d.a.) intensity.
Four studies investigated the changes in daily
physical functioning. The SPPB was significantly
week. 12 months. RT:
home-based session/

improved after resistance training, regardless of


relaxation exercises
POWIR: 2 classes þ 1

FLEX: stretching and

&& &
the intensity [34 ,41 ]. In frail older adults, none
of the included studies investigated the effects of
free weights
Intervention

aerobic training on physical functioning, although


others suggest that aerobic training and especially
combined training can improve CLIP, muscle
strength and muscle mass of frail older adults
[49]. It should be noted that WBV significantly
improved muscle strength compared with sham
POWIR: n ¼ 29. Age

WBV, but not physical functioning [19].


69.9  9.3 years

70.5  7.8 years


FLEX: n ¼ 22. Age

Overall, only few articles were retrieved that


specifically reported on frail older persons, and future
Population

exercise trials should focus more on this important


population. Moreover, none of the included articles
compared different types of exercises, complicating
Table 4 (Continued)

size; RT, resistance training.

an overall recommendation on the preferred exercise


modality for frail older persons.
References

Exercise effects in healthy nonfrail older adults


Twenty-four studies including healthy, nonfrail
older adults performing an exercise intervention

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Ageing: biology and nutrition

were included. Six reported data on the inflamma- (effect size ¼ 0.26 and 0.27 following, respectively,
&& && & & &&
tory profile [22 ,25 ,31 ,36,39 ,45 ], 14 on body conventional combined training and combined
& && & & && &&
composition [12 ,17 ,18 ,21 ,23 ,25 ,26,28–30, training with blood flow restriction) [26].
& && && &&
35,39 ,43 ,45 ], 18 on muscle strength [13,14 , Out of the 18 articles reporting data on changes
& & & && && && & &
18 ,20 ,21 ,23 ,25 ,26,28– 30,32 ,33,36,39 ,40 , in muscle strength after an exercise intervention,
&&
42,43 ] and eight on physical functioning five compared different types of exercises, whereas
&& & & & &&
[13,17 ,20 ,21 ,36,38,39 ,43 ]. in seven articles different intensities of the same
Lee et al. showed that in older women, intervention were compared; 11 studies compared
proinflammatory cytokines such as CRP (effect the effects of exercise with a nonexercising control
size ¼ 1.45), TNF-a (effect size ¼ 0.49) and IL-6 group. Resistance training interventions signifi-
(effect size ¼ 1.11) decreased after 8 weeks of com- cantly improved both lower limb (leg extension
effect size ¼ 0.82 [21 ], effect size ¼ 0.96 [39 ]
& &
bined training. Interestingly, inflammatory markers
also decreased after aerobic training (effect and effect size ¼ 0.14 [29]; leg press effect
size ¼ 1.05 for CRP, effect size ¼ 0.59 for IL-6 and size ¼ 0.69 [23 ], effect size ¼ 0.51 [30] and effect
&&

effect size ¼ 0.62 for TNF-a). However, only for CRP size ¼ n.d.a. [20 ,36]; and bilateral leg strength
&

effect size ¼ 0.46 [14 ]) and upper limb (chest press


&&
a significant difference between the effects of com-
effect size ¼ 0.31 [23 ] and bench press effect
&&
bined training and aerobic training was reported
size ¼ 0.60 [30]) strength. Carneiro et al. [18 ] inves-
&& &
[25 ]. sTNFR1 and IL-8 significantly increased after
all three resistance training interventions in a study tigated different modalities of resistance training
investigating the effects of different intensities of and found significant differences in effects obtained
resistance training (HIGH, LOW and LOWþ; refer to between the group training twice and the group
&&
Table 3 for details) [22 ]. For sTNFR1, the effect size training three times in a week. Similar findings were
was rather small, though for IL-8, medium effect size reported in another study performed by Padilha
was obtained for the LOW group (effect size ¼ 0.59)
&& &&
et al. [32 ]. Interestingly, Villanueva et al. [43 ]
and a large effect size (effect size ¼ 0.76) for the showed that in older men significantly greater
LOWþ group. No significant differences between improvements can be obtained when performing
groups were observed, but training at HIGH external 4-week resistance training with a short (1 min) than
load also increased anti-inflammatory IL-1ra in male with a long (4 min) rest interval between the exercise
participants, which might be beneficial in combat- sets. These findings need to be confirmed in longer
&& &&
ing CLIP [22 ]. In addition, Yamada et al. [45 ] studies with larger sample size and might lead in the
found a significant increase in IGF-1 (effect future to adapted resistance training prescription
size ¼ 0.43) following aerobic training compared guidelines for older adults. Regarding the effects
with control (effect size ¼ 0.21). of combined training, significant improvements
Regarding the effect of exercise on body com- in muscle strength were reported by Irving et al.
[23 ] (effect size ¼ n.d.a.). It should be noted that
&&
position, most studies revealed a significant increase
&& &&
in LBM [23 ,43 ]. As shown in Table 3, changes in other studies showed that there were no significant
LBM were significantly different when comparing differences in effects obtained between concentric-
&
soccer with resistance training [12 ], combined focused or eccentric-focused resistance training
&& &
training with aerobic training [25 ] or short rest [20 ], between regular combined training or com-
interval with long rest interval during a resistance bined training with blood flow restriction [26] nor
&&
training intervention [43 ]. These studies confirm between Huber and Pilates exercise [28]. Another
that physical exercise positively influences LBM in study compared horse exercise and traditional com-
older adults and enforce previously published evi- bined training with a nonexercising control group.
dence [10]. BFM decreased significantly after exer- Their results suggest that muscle strength increases
cise. Following a Huber exercise intervention, a with large and medium effect sizes (effect size ¼ 1.06
medium effect was obtained (effect size ¼ 0.46) and 0.53, respectively) following horse and com-
[28], whereas larger effects were observed after bined training exercise, though without significant
combined training (effect size ¼ 0.66) [25 ], aerobic
&&
difference between both types of exercise [13]. The
training (effect size ¼ 0.51 [25 ] and effect
&& &
study by Su et al. [40 ] suggests that tai chi with
size ¼ 0.74 [17 ]) or resistance training (effect
&&
weighted vests can lead to significantly better
size ¼ 0.73) [17 ]. When looking at the effects of
&&
improvements of muscle strength compared with
exercise on muscle mass, a significant increase was regular tai chi, which might be explained by the
observed following resistance training (effect greater external load during training.
size ¼ n.d.a.) [18 ] as well as aerobic training (effect
&
Only eight included studies reported on changes
size ¼ 0.16) [23 ]. Combined training significantly
&&
in physical functioning after an exercise interven-
improved quadriceps muscle cross-sectional area tion. Overall, physical functioning was significantly

50 www.co-clinicalnutrition.com Volume 20  Number 1  January 2017

Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


The effects of exercise in older adults: a systematic review Liberman et al.

improved after exercise (resistance training, aerobic muscle strength after resistance training versus con-
training, WBV and horse exercise), and large effect trol in prostate cancer survivors and WBV versus
sizes (effect size 0.74) were obtained in parameters resistance training exercise in COPD patients,
measuring physical functioning such as chair stand muscle strength consistently showed a significant
increase (effect size ¼ 0.22–0.48 and n.d.a., respect-
&&
test, 400-m walk distance and other [13,17 ,
& & && &&
20 ,21 ,38,43 ] (Table 3). ively) [37,44 ]. This significant increase in muscle
We can conclude that most included articles strength is not so surprising, as baseline values
investigated resistance training. Those studies com- might be lower in these specific patients [56] and
paring different types of exercise reported no sig- demonstrates the necessity of intensive exercise for
nificant differences in the effects obtained on these patients to recover muscle weakness.
physical functioning. It seems that for the effects Two studies investigate the effects on physical
of resistance training on inflammation or muscle functioning and showed a significant improvement
strength, the exercise modalities (intensity and rest of 6-min walk test after both WBV and resistance
interval between sets) can influence the effects training in COPD patients (effect size ¼ n.d.a.) [37];
obtained, which warrants more exploration of the resistance training or flexibility training did not
underlying pathways in future research. As a final significantly influence physical function in prostate
&&
point, muscle strength seemed to be the most fre- cancer patients [44 ].
quently used outcome measure, regardless the exer- We can conclude that reducing the inflammatory
cise intervention studied. profile in patients with specific diseases via exercise
seems to be more challenging, although some
positive effects of aerobic training were reported.
Exercise effects in older adults with a None of the included studies investigated the effect
specific disease of resistance training on inflammation or body com-
Six studies were identified investigating the effects position, and therefore there is an urgent need for
of an exercise intervention in older adults with a intensifying research in this area. As a final remark, it
specific disease or disorder, including COPD, cancer must be noted that all studied exercise interventions
and arterial hypertension (AH) (Table 4). Three were feasible without major complications, and thus
studies looked at changes in the inflammatory pro- these specific conditions should not be considered as
&& & &&
file [15,16,27 ,54 ], two at muscle strength [37,44 ] contraindications for exercise interventions.
and two investigated changes in physical function-
&&
ing [37,44 ].
CONCLUSION
IL-6 was the only cytokine that showed signifi-
cant changes after an exercise intervention, which Few articles focused on exercise in frail older per-
decreased after 10 weeks of aerobic training (effect sons. Moderate-to-large exercise effects were noted
size ¼ 1.36) in older persons with AH [27 ]. One
&& on inflammation, muscle strength and physical
study focused only on creatine kinase in COPD functioning. As none of these articles compared
patients, which was significantly elevated after different types of exercise, an overall exercise recom-
downhill walking interventions, both with or with- mendation for frail older persons is difficult.
out carrying an external load (effect size ¼ 0.37 and In healthy older persons, the effects of resistance
0.66, respectively) [15]. The inflammatory outcomes training (most frequently investigated) on inflam-
in these studies showed similar effects as previously mation or muscle strength can be influenced by the
described in other studies, which suggest that exercise modalities (intensity and rest interval
physical exercise mediates an anti-inflammatory between sets). Muscle strength seemed to be the
response [55] and has positive effects on several most frequently used outcome measure, with mod-
diseases [8]. erate-to-large effects obtained regardless of the
No studies were found investigating exercise- exercise intervention studied. Similar effects were
induced changes in body composition. Of note, in found in patients with specific diseases.
patients after acute myocardial infarction, Oliveira
&
Acknowledgements
et al. [54 ] recently failed to detect significant effects
of 8 weeks of aerobic training on BFM nor on None.
inflammatory biomarkers. It must be mentioned
Financial support and sponsorship
that their participants were younger (aged
55  10.7 years for the aerobic training group), None.
and it cannot be excluded that older patients might
benefit more from exercise interventions compared Conflicts of interest
with younger ones. In both studies investigating There are no conflicts of interest.

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Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.


Ageing: biology and nutrition

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