Download as docx, pdf, or txt
Download as docx, pdf, or txt
You are on page 1of 17

JournalofPsychosomaticRe

search126(2019)109823

Contents lists available at

Journal of Psychosomatic Research


journal homepage:

Review article

Effects of exercise on depression and anxiety in persons living with HIV: A


meta-analysis

Andreas Heissela, , Philipp Zecha, Michael A. Rappa, Felipe B. Schuchb, Jimmy B. Lawrencea,
Maria Kangasc, Stephan Heinzeld
a
SOCIAL AND Preventive Medicine, DEPARTMENT Exercise AND HEALTH Sciences, University of POTSDAM, GERMANY
b
DEPARTAMENTO de métodos e TÉCNICAS DESPORTIVAS, UNIVERSIDADE FEDERAL de SANTA MARIA, BRAZIL
c
Centre for EMOTIONAL HEALTH, DEPARTMENT of Psychology, MACQUARIE University, Sydney, AUSTRALIA
d
CLINICAL Psychology AND PSYCHOTHERAPY, DEPARTMENT of EDUCATION AND Psychology, Freie Universität Berlin, GERMANY

ARTICLEINFO
ABSTRACT
Keywords:
HIV Objective: The purpose of this systematic review and meta-analysis was to examine the effects of exercise on
Exercise depression and anxiety in people living with HIV (PLWH), and to evaluate, through subgroup analysis, the effects
Depression of exercise type, frequency, supervision by exercise professionals, study quality, and control group conditions on
Anxiety these outcomes.
Meta-analysis Method: A literature search was conducted through four electronic databases from inception to February
Supervision
2019. Considered for inclusion were randomized controlled trials (RCTs) investigating exercise interventions
and depression or anxiety as outcomes in people living with HIV (≥ 18 years of age). Ten studies were
included (n = 479 participants, 49.67% females at baseline), and the standardized mean difference (SMD)
and hetero- geneity were calculated using random-effect models. An additional pre-post meta-analysis was
also conducted. Results: A large effect in favor of exercise when compared to controls was found for
depression (SMD = −0.84, 95%CI = [−1.57, −0.11], p = 0.02) and anxiety (SMD = −1.23, 95%CI
= [−2.42, −0.04], p = 0.04).
Subgroup analyses for depression revealed large effects on depression for aerobic exercise only (SMD =
−0.96, 95%CI = [−1.63, −0.30], p = 0.004), a frequency of ≥3 exercise sessions per week (SMD =
−1.39, 95%CI = [−2.24, −0.54], p < 0.001), professionally supervised exercise (SMD = −1.40, 95%CI
= [−2.46,
−0.17], p = 0.03]), and high-quality studies (SMD = −1.31, 95%CI = [−2.46, −0.17], p = 0.02).
Conclusion: Exercise seems to decrease depressive symptoms and anxiety in PLWH, but other larger and
high- quality studies are needed to verify these effects.

1. Introduction
cardiovascular, kidney, and neurological diseases, as well as metabolic
In 2016, the number of individuals living with the human im- risk factors [4–6]. Moreover, sleep problems and depression in PLWH
munodeficiency virus (HIV) as reported by the World Health have been associated with higher disability [7].
Organization (WHO) was estimated to range between 30.8 and 42.9 The prevalence of PLWH experiencing depression and anxiety has
million people worldwide [1]. People living with HIV (PLWH) face been reported to be two- to fourfold higher than in non-infected in-
challenges related to social inclusion, uncertainty, and worrying about dividuals [8]. Among other things, both HIV itself and HAART con-
their future, which are linked, to some extent, to mental and physical tribute to this elevated prevalence of depression when compared to
impairments associated with HIV, including depressive and anxiety HIV-negative individuals. Depression has been shown to decrease
disorders [2,3]. quality of life (QOL) and negatively affect the HIV disease progression
Although highly active antiretroviral therapy (HAART) has ex- [9], and can lead to a higher risk of suicide in PLWH than in HIV-
tended the lifespan of individuals with HIV, it is not without its risks. negative individuals [10,11]. Therefore, the improvement of mental
Notably, studies have shown that HAART increases the risk of health and QOL in PLWH has become a priority in HIV research [12].
Cluster of differentiation 4 (CD4) cell count and viral load play a key


Corresponding author at: Social and Preventive Medicine, Department Exercise and Health Sciences, University of Potsdam, Am Neuen Palais 10, Potsdam 14469,
Germany.
E-MAIL ADDRESS: andreas.heissel@uni-potsdam.de (A. Heissel).

https://doi.org/10.1016/j.jpsychores.2019.109823
R00e2ce2i-v3e9d992/6 ©Fe2b0ru1a9ryEl2se0v1i9e;rRInecc.eAivleldriignhtrsevreisseedrvfeodr.m 30 August 2019; Accepted 31 August 2019
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823
PERO).
role for PLWH and help estimate individuals' overall health status.
There is evidence for a relationship between CD4 cell count and de-
creased mental health and well-being. A lower CD4 cell count in
PLWH could be an indicator of untreated depression [13]. In other
words, chronic depression could negatively affect the disease process
and lead to a decreased CD4 cell count and an increased viral load
[9,14]. Fur- thermore, a meta-analysis by Gonzales et al. [15] showed
that depres- sion was significantly associated with non-adherence to
HIV-treat- ments. While adherence to HIV medication treatment is
essential for a stable viral load, mental health status is not adequately
treated by medication alone. Research has shown that psychotherapy
treatments such as cognitive behavioral therapy (CBT) increase
adherence to HAART and improve depressive symptoms [16].
However, most coun- tries lack adequate resources for psychotherapy
[17].
Physical activity, defined as any bodily movement produced by
skeletal muscles and which requires energy expenditure [18] has be-
come a topic of great interest for mental health promotion, since
people with higher levels of physical activity are less likely to develop
de- pression [19] and anxiety [20]. Moreover, exercise, a structured
subset of physical activity, has proven to be an effective low-threshold
treat- ment in individuals suffering from depression and other mental
dis- orders [21,22]. Additionally, people with HIV spend more time in
se- dentary behavior and less in physical activity when compared to
other chronic populations [23,24]. In recent years, a growing number
of systematic and meta-analytic reviews have investigated the effects
of exercise in PLWH [23–30]. Although the antidepressant effects of
ex- ercise have been demonstrated in people with mental disorders,
pre- vious reviews of exercise in PLWH have focused mainly on
physiolo- gical outcomes [25–30], with minimal attention given to
mental health outcomes.
In a recent Cochrane review in which the authors investigated the
effectiveness of aerobic exercise for PLWH [31], only two studies
were included which reported the impact of exercise on depressive
symp- toms. Although in another recent study [32] the aim was to
evaluate the effects of various types of interventions on depression for
PLWH in Africa, only one study was included based on an exercise
intervention. Additionally, in a separate recent systematic review [33],
although the aim was to evaluate the effects of exercise and mental
health outcomes for PLWH (which included depression and anxiety
outcomes), the re- sults were restricted to a qualitative analysis of
studies evaluating aerobic and/or resistance exercise; yet, the authors
did not conduct a meta-analysis on any mental health outcomes. A
further shortcoming yet to be addressed in previous meta-analytic
reviews on this topic includes investigating the impact of other forms
of physical exercise (beyond aerobic and resistance exercise), such as
yoga, on mental health outcomes in PLWH. Additionally, none of the
meta-analytic re- views to date have evaluated whether the effects of
exercise for PLWH are influenced by training frequency or
professional supervision, and whether the exercise intervention
condition was compared to a struc-
tured versus non-structured control condition.
Accordingly, the objective of the present systematic and meta-ana-
lytic review is to address these gaps and limitations in this field. In
particular, the aims of this review are twofold: 1) to investigate the
effect of exercise (including other forms of exercise, e.g., yoga, tai chi)
on depression and anxiety in PLWH; and 2) to investigate whether the
effects of exercise are moderated by exercise type, training frequency,
supervision by exercise professionals, study quality, and different con-
trol group conditions (structured and non-structured control groups).

2. Methods

We conducted a systematic review and meta-analysis focusing on


randomized controlled trials (RCTs) according to the Cochrane
Collaboration protocol [34]. The procedure was previously registered
on the international prospective register of systematic reviews (PROS-

2
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823
Studies-Depression Scale (CES-D)).
(http://www.crd.york.ac.uk/PROSPERO/display_record.asp?ID=
CRD42016035798) and refers to the Preferred Reporting Items for 2.3. SEARCH STRATEGY intervention intensity, type of
Systematic Reviews and Meta-Analyses (PRISMA) guidelines [35]. control group, anti-depressants
The literature search was and HAART medication intake,
conducted by two reviewers (PZ supervision of participants, and
2.1. Included studies AND types of interventions
and JL) who first independently peer review or thesis. In the case
screened each title for potential of missing data or unconvertible
Studies were considered for inclusion if they: 1) were RCTs and
relevance as set by the eligibility measuring units in a study, the
exercise interventions were compared to any concurrent structured
criteria described above. If an authors were contacted via email
control condition (defined as any assigned activity except exercise)
article met the title- screening and the missing data or an
and/or non-structured control condition (defined as no assignment, as
process, the abstracts were then adequate conversion of a
usual daily activity or on a waiting list), 2) included at least one ex-
fully screened. For poten- tially measuring unit were requested.
ercise intervention ≥1 time per week, 3) investigated depression and/
eligible studies, full-text papers If two weeks passed with no
or anxiety symptoms pre- to post-intervention using a validated mea-
were obtained and assessed by reply, the author was then kindly
sure, 4) were published in English or German, 5) included adult parti-
the same two independent reminded of the request. When
cipants ≥18 years old, and 6) included people with an HIV-positive
reviewers. In the case of the corresponding author did not
status. For the purposes of this review, exercise was defined as any
disagreement, both authors reply, the co-authors were
“planned, structured and repetitive bodily movement done to improve
discussed their differences until contacted via email as well.
or maintain one or more components of physical fitness” [18]. Ac-
they reached an agreement. If When no email address was
cording to this definition, beyond traditional forms of exercise such as
this was not possible, a third reported, the author was searched
aerobic exercise or strength training, other forms of exercise modes
author (AH) was consulted for via Google and Research Gate,
such as yoga or tai chi were also included, as they qualify as effective
the final decision. and contacted if possible. In
exercise treatments [36,37].
To identify relevant cases where none of the authors
To examine the differences in effects between PLWH who
published trials, as well as replied to any attempts to make
exercised compared to those who did not (i.e., non-exercisers), the
existing systematic reviews, the contact, the study was excluded
control group was defined as performing no exercise at all. Control
following electronic databases from the quantitative synthesis.
groups exercising at different intensity levels or performing any type
were searched to include studies In order to determine the risk of
of exercise were strictly excluded to prevent falsification of the
published up to February 2019: bias of the included studies, the
results regarding the comparison of non-exercising and exercising
Pubmed, Physiotherapy Physiotherapy Evidence
participants because moderate-intensity exercise can have similar
Evidence Database (PEDro), Database (PEDro) scale was
effects on mental health when compared to more intense exercise.
PsycNet, and the Cochrane used. The PEDro scale is based
Therefore, comparing ex- ercise versus exercise may lead to an
Central Register of Controlled upon the Delphi list described
underestimation of the effect size [38]. For trials which included more
Trials (CENTRAL). Search by Verhagen et al. [40].
than one intensity of exercise, we used the exercise arm with the
parameters and syntax were The criteria of the PEDro scale
greatest clinical effect in the review. Similarly, when trials provided
adapted to the requirements of (eligibility criteria (EC))
more than one type of exercise, we used the type of exercise with the
each database. Combined MeSH determine: if the eligibility
greatest clinical effect. However, because this may overestimate the
terms and text words were criteria were specified, 1.
effect of exercise, we used the exercise arm which provides the
related to HIV, exercise, and whether subjects were ran- domly
biggest ‘dose’ of exercise, and performed a sensi- tivity analysis to
depression/ anxiety. In addition, allocated to groups, 2. whether
explore the effect of using the smallest ‘dose’. Control groups were
systematic reviews and cohort the allocation was concealed, 3.
separated into structured and non-structured control conditions. Any
studies were cross- referenced. whether the groups were similar
activity except exercise, e.g. heat therapy, reading a book, were
To identify unpublished or on- at baseline regarding the most
defined as structured control conditions, and non-structured
going studies, clinicaltrials. gov im- portant prognostic indicator,
control conditions were defined as not being involved in any
was searched. Reference lists 4. whether there was blinding of
organized form of activity and free of any form of intervention, e.g.
and tables of contents in relevant all sub- jects, 5. whether there
continuing daily activity or being on a waiting list. A trial was
publications, reviews, and books was blinding of all therapists who
considered an RCT if the allocation of participants was reported as
were also screened. The search administered the therapy, 6.
randomized, and the eligibility criteria had to be specified.
stra- tegies represent the method whether there was blinding of all
used for all databases using the assessors who mea- sured at least
2.2. Outcomes Boolean operators AND/OR and one key outcome, 7. whether the
can be found in detail in the measures of at least one key
The primary outcome was the post-intervention results for depres- Appendix (Table A.1). outcome were obtained from >
sion, and the secondary outcome was anxiety. In cases where a study 85% of the subjects initially allo-
investigated depression or anxiety with more than one assessment tool 2.4. DATA EXTRACTION cated to groups, 8. whether all
[39], separate meta-analyses were conducted. In this review, the spe- subjects for whom outcome
cific focus was on evaluating the effects of exercise on depression and Data were extracted by two measures were available received
anxiety symptoms. Thus, ‘depression’ and ‘anxiety’ was defined in independent reviewers (PZ and the treatment or control condition
terms of symptom severity, not in terms of a clinical diagnosis of a JL) using a standardized data as allocated or, where this was
depressive or anxiety disorder. Studies that only used broad measures abstraction digital form sheet, not the case, data for at least one
of mental health and health-related quality of life (HRQOL) were and included the following: key outcome were analyzed with
excluded, as they were deemed too generic. Any study that used a author, year and country of an “intention to treat,” 9. whether
validated quan- titative self-report measure assessing depression and publication, investigated the results of between- group
anxiety symptoms was considered for inclusion (e.g. State-Trait outcome, exercise method, statistical comparisons are
Anxiety Inventory (STAI), Beck Depression Inventory (BDI), number of participants (% reported for at least one key
General Health Questionnaire (GHQ), Profile of Mood State- women), pre-and post-outcome outcome, and 10. whether the
Depression/Anxiety (POMS-D/A), Hospital An- xiety and Depression measures at baseline for study provided both point
Scale-Depression/Anxiety (HADS-D/A), Centre for Epidemiological intervention and control groups, measures and measures of

3
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823
variability for at least one key all groups to determine the cognitive beha- vioral stress
outcome. Two reviewers (PZ as a high-quality study [41,42]. differences. Additionally, a management intervention [58],
and JL) independently assessed pooled standard one study did not include
the risk of bias using the PEDro 2.5. DATA ANALYSIS difference to adjust the exercise in the individual or
scale. Dis- crepancies between differences was used [44], as family activity intervention [59],
the two reviewers were resolved Review Manager 5.3 was was the post-in- tervention and one study had no exercise
by consulting two other authors used for the data analysis. sample size. For both groups, included in the positive-affect
(AH and SH). A study with a Different in- struments were these three values were used for skills intervention [60]. For
PEDro score ≥ 5 was graded pooled for data analysis if they statistical calculation in Review further information about the
measured the same Manager 5.3. We interpreted study selection process, see Fig.
psychological construct for SMD ranges 0.00–0.39 as 1.
depression and anxiety. For the small, 0.40–0.70 as moderate,
meta-ana- lysis, the main and above 0.70 as large [45]. A
outcome of the means, standard p value of < 0.05 was
differences, and number of considered statistically
participants allocated to each significant. Heterogeneity was
group were used. If different determined by calculating the I2
measuring units were used in statistics [46]. We considered
the studies, such as mean ± three ranges of heterogeneity: a)
2
standard error or mean ± I ≤ 25% for low hetero-
change/difference (post minus geneity, b) I2 > 25–75% for
pre); these were converted into moderate heterogeneity, and c)
the common measuring unit of 2
I > 75% for considerably high
mean ± standard difference. heterogeneity [46]. The
Random-effect models were conducted pre-post analyses
used when calculating the were then compared to the post
standardized mean differences analyses to identify possible
(SMD) of the post-treatment differences [44,47]. Assessing
measures comparing exercise publication bias, Egger's Test
and other forms of exercise was pre- ferred to Begg's Test
with control groups across all due to its higher sensitivity
in- cluded trials [43]. Subgroup [48,49].
analyses for the different types
of exercise, number of sessions, 3. Results
professional supervision, and
structured and non- structured 3.1. CHARACTERISTICS of excluded
control conditions were studies
performed whenever possible.
High- quality studies with a low As shown in Fig. 1, 4850
risk of bias (PEDro score ≥ 5) studies were identified. After
were analyzed separately four dupli- cates were removed,
[41,42]. In line with the 4814 studies were excluded by
standard analysis procedure in assessing the title. Nine records
the Cochrane meta-analyses, needed to be excluded after
SMDs were calculated using reading the abstract. Seven
means, standard differences, records did not investigate
and sample sizes post- depression or anxiety, one study
intervention (post-treatment had a non- exercising control
effect sizes). Due to the group by investigating two
possibility that no different intervention groups,
parallelization pre-intervention and one study did not assess
between intervention and exercise as an intervention.
(structured) control groups was The full texts of the
assured in the main outcomes at remaining 23 studies were
the starting points, especially in assessed. Twelve additional
small sample sizes despite studies were then excluded:
randomization or due to high Eight studies did not measure
dropout rates, we used an depression or anxiety [36,50–
additional method to compare 56], four studies had no
the two methods with one exercise inter- vention or had an
another. Therefore, we exercise intervention that did
conducted additional meta- not meet the inclusion criteria,
analyses (pre-post analyses). one study had only two groups
For the main outcomes, we differing in their intensity levels
calculated new means by of exercise (moderate and high
subtracting the post- intensity) but no non-exercising
intervention means from the control group [57], in one study
pre-intervention means between there was no exercise in the

4
Fig. 1. PRISMA flow diagram.

3.2. CHARACTERISTICS of studies excluded from the QUANTITATIVE synthesis


3.4. CHARACTERISTICS of PARTICIPANTS
One study was excluded due to missing or incomplete data [61]
(see also Appendix Table A.2). The author was contacted twice but the A total of 479 participants for baseline (49.67% females) and 429
re- quested data were not made available. Hence, a total of 10 studies participants for post-intervention measures (10.44% withdrawal rate)
were included in the quantitative analysis. were investigated. Four studies reported a nil dropout rate
[63,65,68,70].
Six studies reported ART medication for all participants
3.3. CHARACTERISTICS of studies included in the QUANTITATIVE synthesis [62,64,65,68–70]. One of these six studies that reported ART medica-
tion also made a distinction between the antiretroviral medications
Of the 10 included trials, four studies investigated aerobic exercise concerning the drug classification [69]. The other four studies did not
(AE) [39,62–64], four investigated aerobic exercise and resistance report whether participants were on HAART medication [39,63,66,67].
training (AERT) [65–69], and two studies investigated a yoga inter- Two studies reported anti-depressant or anti-anxiety medication use
vention (Y) [68,70]. The duration of the interventions ranged from 4 to [39,69]. In Neidig et al. [39], twelve out of 60 participants used anti-
12 weeks, the duration of each exercise session ranged from 45 to depressants (16.70% in the intervention group (IG) and 23.30% in the
75 min, the sessions per week ranged from 2 to 6 times per week. control group (CG)) and 10% of the 60 participants used anxiolytics
Follow-up data were presented in none of the included studies. Parti- (10% in the IG and 10% in the CG) at entry. 16.70% of the participants
cipants were supervised in six trials, and in five of these studies parti- used antidepressants and 10% of the participants used anti-anxiety
cipants were professionally supervised by a yoga trainer [68,70], a agents. Shah et al. [69] only mentioned in the exclusion criteria that
personal trainer [39] or a physiotherapist [64,66]. Two studies did not participants with untreated depression were excluded. Detailed in-
report on supervision [62,63]. In two studies the participants were in- formation about the study characteristics are summarized in Table 1.
structed to exercise privately in their own at home not being Six studies investigated participants who were not diagnosed
supervised [65,69]. Participants in 8 studies performed their exercise with depressive symptoms [39,62–64,66,67]. In four studies, the
intervention stationary. Two studies were conducted in Africa [62,65], authors reported details for depression conditions in the inclusion or
three studies in India [66,68,70], two studies in the USA [39,63], and exclusion criteria. Participants in the studies of Naoroibam et al.
one study in Germany [64]. Five studies assessed structured control [70] n = 14 (n = 9/22 participants in the intervention group and n =
groups [62,63,65–67] and five assessed non-structured control groups 5/22 parti- cipants in the control group) and Daniels et al. [65] n =
[39,64,68–70]. No study assessed two different intensity levels for the 8/60 partici- pants were partly diagnosed with depressive
intervention group. Detailed information about supervision, control symptoms. 20 participants (n = 12/22 participants in the
group conditions and other study characteristics are available in intervention group and n = 8/22 in the control group) in the study
Table 1. by Naoroibam et al. [70] were diagnosed with anxiety symptoms.
The study by Kiloor et al. [68] excluded par- ticipants with
psychiatric illnesses or use of antipsychotic medications.
A.
Table 1 Heis
Characteristic of studies included in the meta-analysis. sel,
et
Author, Year, AL.

Country Outcome Method/ Participants n n, post (n), Baseline (SD); post (SD); within Intervention Control group Anti- Super-vision Location of Peer
Parameter Intervention (% women) WR%/ group difference post minus condition depressant/ exercise reviewed/
pre, post intention baseline (SD) ART intervention thesis
to treat medication
yes/no Intervention Control M/S S/Wk Wks M/Wk

1 Aweto, 2016,
Nigeria BDI-D: aerobic pre: 40 40, 33, depression: depression: 45 3 6 135 structured: group not mentioned/ not mentioned stationary peer
depression exercise vs. (62.50%), 17.5%/ no 10.33 (6.48); 10.06 (5.96); counselling for on ART reviewed
CG post: 33 3.50 (1.27); 8.33 (5.80); 30 min. Once in two
2 Daniels, 2018, (69.70%) −6.83 (3.88) −1.73 (5.88) weeks.
South Africa BDI-D: aerobic and pre: 60 60, 60, depression: depression: N.A. 2 6 N.A. structured: read the not mentioned/ not supervised home based peer
depression resistance (100%) post: 0%/ no 6.17 (3.97); 4.64 (2.79); prescribed material on ART reviewed
exercise vs. 60 (100%) 4.85 (2.85); 2.75 (2.10);
CG −1.32 (3.41) −1.89 (2.45)
3 Dianatinasab, GHQ- aerobic pre: 40 40, 30, depression: depression: 65 3 12 195 structured: receiving not mentioned/ professionally stationary peer
2018, 28:depression and (100%), post: 25%/ no 4.84 (2.76); 6.60 (4.25); routine educational not mentioned supervised reviewed
Iran anxiety resistance 30 (100%) 2.69 (1.44); 7.60 (5.38); and medical service
exercise vs. −2.15 (2.10) 1.00 (4.82)
CG anxiety: 5.92 anxiety: 6.30
(4.46); (4.19);
3.61 (2.33); 6.20 (4.29);
−2.31 (3.40) −0.1 (4.24)
4 Jaggers, 2014, POMS-D: aerobic and pre: 49 49, 44, depression: depression: 75 2 6 120 structured: sedentary not mentioned/ supervised stationary peer
USA depression resistance (26.50%), 10.2%/ no 14.38 (12.15); 9.39 (9.08); activities not mentioned reviewed
exercise vs. post: 44 (NA) 6.21 (7.35); 8.20 (9.30);
CG −8.17 (9.75) −1.19 (9.19)
5 Kiloor, 2018, HADS-D/A: yoga vs. CG pre: 60 (65%) 60, 60, depression: depression: 60 5 8 300 non-structured: wait not mentioned/ professionally stationary peer
India depression, post: 60 0%/ no 9.16 (2.15); 9.19 (2.04); list, usual activity on ART supervised reviewed
anxiety (65%) 4.74 (1.12); 10.23 (1.93);
−4.42 (1.64) 1.04 (1.99)
anxiety: 11.29 anxiety: 11.45
(2.15); 5.45 (2.17); 12.48
(1.34); −5.84 (2.20); 1.03
(1.75) (2.19)
6 LaPerriere, POMS-D/A: aerobic pre: 17 (0%), 17, 17, depression: depression: 10 45 3 12 135 structured: not mentioned/ not mentioned stationary peer
1990, depression, exercise vs. post: 17 (0%) 0%/ yes 10.90 (1.70); (1.60); 23.80 assessment only not mentioned reviewed
USA anxiety CG 14 (3.70); 3.1 (7.90); 13.80
(2.7) anxiety: (4.75) anxiety:
12.80 (2); 11.30 (1.60);
Jou
12.90 (2.50); 16.30 (3.80); 5 rNAl
0.10 (2.25) (2.70) ofPs
7 Naoroibam, HADS-D/A: yoga vs. CG pre: 44 44, 44, depression: depression: 60 6 4 360 non-structured: not mentioned/ professionally stationary peer ych
2016, India depression, (45.50%), 0%/ no 9.18 (2.95); 9.55 (3.01); routine daily on ART supervised reviewed
oso
activity mAt
anxiety post: 44 7.95 (1.78); 9.59 (3.03);
icRe
(45.50%) −1.23 (2.37) 0.04 (3.02) seAr
anxiety: 10.82 anxiety: 10.14 ch1
(3.86); 9.91 (3.16); 11.45 26(
(3.35); −0.91 (3.36); 1.31 201
(3.61) (3.26) 9)1
098
8 Neidig, 2003, POMS-D, BDI- aerobic pre: 60 60, 48, POMS-D: POMS 60 3 12 180 non-structured: wait (n) 12/60 anti- professionally stationary peer 23
USA D: depression exercise vs. (13%), post: 20%/yes depression: depression: list, usual activity depressants, supervised reviewed
CG 48 (8.30%) 10.90 (11.80); 10.90 (8.50); (n) 9/60 anti-
6.10 (8.90); 10.90 (11.20); anxiety agents/
−4.80 (10.35) 0 not mentioned
BDI-D: (9.85) BDI
depression: depression:
8.90 (5.90);
(continued on next
PAGE)
description of control group condition. Standard deviation (SD), antiretroviral therapy (ART), withdrawal rate (WR), State-Trait Anxiety
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823

Note. Study characteristics presented as author/year of publication, investigated outcome, specific intervention investigated, (n) participants (percentage women) at pre- and post-intervention, withdrawal rate (WR) in percent,
Peer reviewed/ thesis The study of Shah et al. [69] explicitly excluded participants with un-

intention to treat yes/no, baseline measures mean ± SD intervention group, baseline measure mean ± SD control group, minutes per session (M/S), sessions per week (S/Wk), weeks (Wks), minutes per week (M/Wk),
treated depressive symptoms.

peer reviewed
thesis

(GHQ), Profile of Mood State-Depression/Anxiety (POMS-D/A), Hospital Anxiety and Depression Scale-Depression/Anxiety (HADS-D/A), intervention group (IG), control group (CG), not available (N.A.).
3.5. Outcomes of included studies
Location of exercise intervention

home based
Nine studies reported the effects of exercise on depression

stationary
outcomes [39,62,63,65–70], while only five studies reported
anxiety outcomes [63,64,66,68,70]. A summary of the outcome
measures for these stu- dies are summarized in the Appendix (Table

not supervised
professionally supervised

A.3).
Super-vision

3.6. Risk of BIAS

Five studies were graded as having good methodological quality


and low risk of bias with a PEDro score ≥ 5 [39,62,63,68,69]. The
not mentioned/ (n) 15/34

re- maining five studies were rated as low-quality studies (high risk
Anti- depressant/ ART

of bias) [64–67,70]. The risk of bias analysis according to the


PEDro scale is available in the Appendix, Table A.4.

3.7. META-ANALYTIC results


non- structured:routine daily activity
Control group condition

3.7.1. Depression
Nine studies investigated depression (n = 194 in the exercise
group, n = 201 in the control group) and five were of high quality.
An overall standardized mean difference SMD = −0.84 (95% CI
-1.57 to −0.11) in favor of the exercise group was found in the
M/Wk

random-effect model for post-intervention values. There was a


N.A.
120

significant overall effect (Z = 2.27, p = 0.02) of exercise


Wks

compared to the control group at post- treatment. Statistical


10

12

2 2
heterogeneity was high (I = 91%, X = 87.82, df = 8, p < 0.001).
S/Wk
Intervention

N.A.

Measuring tools used from the included studies were: BDI-D, GHQ-
2

28, POMS-D, HADS-D, see Appendix, Table A.3. Table 2 shows all
N.A.
M/S

statistical results of the subgroup analyses for de- pression. The


60

forest plot of the main analysis of depression is shown in Fig. 2.


Control
group difference post minus baseline (SD)

3.7.2. Anxiety
Five studies investigated anxiety (n = 92 in the exercise group,
8.70 (7.10);

n = 93 in the control group), two of which were of high quality. An


overall standardized mean difference SMD = −1.23 (95% CI -2.42
Intervention

to
−0.04) in favor of the exercise group was found in the random-
effect model for post-intervention values. There was a significant
overall ef- fect (Z = 2.03, p = 0.04) of exercise compared to the
control group at post-treatment. Statistical heterogeneity was
high (I2 = 92%, X2 = 48.90, df = 4, p < 0.001). Measuring tools
WR%/

for anxiety used from the included studies were: GHQ-28, POMS-
42 no 42, 34,

11.90%/ 67, 59,


within

A, HADS-A, STAI, see Appendix, Table A.3. Table 2 shows the


post (n),

results of the meta-analysis for anxiety; no subgroup analysis was


(SD);

conducted due to the low number of studies identified. The forest


19%/
post

plot of the main analysis for anxiety is shown in Fig. 3.


postn,

(19%), post: pre:


(SD);pre,
(% women)

3.7.3. Pre-post ANALYSES


The SMD difference in the depression post analysis (−0.84) and
nBaseline

pre-post analysis (−0.91) was 0.07 favoring the pre-post analysis. A


Intervention

aerobic exercise vs. CG

minimal difference in SMD post minus pre-post was found for anxiety
Participants

(0.04) favoring the pre-post analyses. Thereby no substantial differ-


ences between the results and heterogeneity between post and pre-post
Method/

analyses exist. Post analysis vs. pre-post analysis for the outcomes are
STAI: anxiety

presented in Table 3.
depression BDI-D:
Outcome Parameter

3.7.4. Sensitivity ANALYSES


Sensitivity analyses where performed after the main analyses. A
Table 1 (continued)

sensitivity analysis for depression was conducted, excluding the


Schlenzig, 1992,

studies of Daniels et al. [65] and Jaggers et al. [67]; a large


significant effect was found (SMD = −1.19 (95% CI -1.97 to
2 2
−0.40), Z = 2.95 p = 0.003, X = 0.98, df = 6, p < 0.001, I =
89%). The two afore-

6
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823
mentioned studies were excluded due to the continuously unequal

10
(large differences) baseline measures in the intervention and control

9
groups ((Daniels et al. [65] IG 6.17 (3.97), CG 4.64 (2.79) at baseline;
Jaggers et al. [67]: IG 14.40 (12.20), CG 9.40 (9.10) at baseline). further meaningful evidence to this field.
Conducting a second sensitivity analysis for depression Given the moderately high methodological heterogeneity between
(excluding the studies of Shah et al. and Daniels et al. [65,69]), a studies, these findings need to be considered in this context. The
large significant effect was found (SMD = −1.21 (95% CI -1.97 to studies were conducted in different countries, such as the USA, Africa,
Germany, and India. Different prevalence rates for depression in
−0.45), Z = 3.12 (p < 0.01), X2 = 46.95, df = 6, p < 0.01, I2 =
PLWH are reported in China (50.8%) [72], Vietnam [73] (44%),
87%). The reason for excluding these studies was due to the
Africa (9% -
missing information about ex- ercise minutes per session and/or
32%) [74] and India (67.3%) [75]. Also, two studies [63,64] were
sessions per week, and the circum- stance that participants were
conducted in the pre-ART era before the year 1995. Depression and
instructed to perform the instructed ex- ercise at home on their
anxiety prevalence and levels for PLWH during the pre-ART era
own.
were higher. In the study of LaPerriere [63], the values for
Conducting a third sensitivity analysis for depression by
depression and anxiety in the exercising group (+3.1/ +0.1) did not
excluding the study of LaPerriere [63], a moderate significant effect
decrease com- pared to the non-exercising control group (+13.8/
was found for depression (SMD = −0.76 (95% CI -1.53 to −0.01).
+5) but was just increasing less.
Excluding the study of Schlenzig et al. [64], a large significant
The study of LaPerriere [63] did not report HAART. In the partici-
effect for anxiety was found (SMD = −1.49 (95% CI -2.98 to
pant description in the paper, it was mentioned that the participants did
−0.01).
not know about their HIV status at study entry, which implies that they
were not on HAART at all. In the study by Schlenzig [64], 15 of 34
3.7.5. PUBLICATION BIAS participants were under anti-retroviral medication and the participants
According to Egger's test, a publication bias was found for presented different HIV-specific disease progressions. The circum-
depres- sion (bias = −8.24, CI 95% 16.41 to −0.06), p = 0.048). stances for developing depression or anxiety are different compared
However, no publication bias was found for anxiety (bias = −9.66, with participants of a study conducted in more recent years with a
CI 95% -36.97 to 17.64), p = 0.34. stable infection and HAART. The two studies in the sub-analysis for
depression investigating yoga only were the same as in the sub-
4. Discussion analysis for HADS only. The comparison between the (commonly
used) post- analyses and the pre-post analyses revealed no differences
To our knowledge, this is the first meta-analysis evaluating the ef- in the results and heterogeneity indicating that drop-out after
fects of exercise (both traditional and non-traditional forms of activity) randomization espe- cially in small samples sizes did not lead to
on depression and anxiety outcomes in PLWH. Notably, the results of significant differences in the main outcomes pre- to post intervention.
the meta-analysis for depression revealed a high and significant effect The present findings are in accordance with previous studies de-
of exercise on depressive symptoms (SMD = −0.84). When analyzing monstrating the beneficial effects of exercise in reducing depressive
only low-risk-of-bias studies, this effect was found to be even greater symptoms [22], which is also evident for PLWH.
(SMD = −1.31). Importantly, in subgroup analyses testing only ex- A large and significant effect (SMD = −1.23) for anxiety was
ercise trials with three or more sessions per week (SMD = −1.39) and found at post-treatment. However, this finding was based on a
professional supervision (SMD = −1.40), significant and large effects conservative number of studies (n = 5); therefore, these results are
were evident. Although the meta-analysis of O'Brien et al. [31] already provisional, as more RCTs are clearly needed in this field.
found a significant improvement in depression scores favoring the ex- Nonetheless, this effect is also in accordance with previous studies that
ercisers compared to the non-exercisers, the analysis was limited to have shown the anxiolytic effects of exercise [76]. The current
two studies (LaPerriere [63] and Smith [71], n = 65; with the study of findings further indicate that ex- ercise is also beneficial in reducing
La- Perriere [63] being conducted in the pre-ART era). We now can anxiety symptoms in PLWH.
add

Table 2
Meta-analytic results – depression, anxiety for post-intervention values.
2 2 2
Effect foci n trials (n participants) SMD (95% CI) Z (p) I (Tau ), Chi , df (p)

Depression
Random-effect model 9 (395) −0.84 [−1.57, −0.11] 2.27 (0.02) 91% 1.11, 87.82, 8 (< 0.001)

Subgroup analysis
1. AE 3 (98) −0.96 [−1.63, −0.30] 2.86 (0.004) 52% 0.18, 4.15, 2 (=0.13)
2. AERT 4 (193) −0.12 [−0.86, 0.62] 0.32 (0.75) 84% 0.47, 18.68, 3 (< 0.001)
3. Yoga 2 (104) −2.03 [−4.76, 0.70] 1.46 (0.15) 97% 3.75, 28.96, 1 (< 0.001)
4. ≥ 3 sessions/week 6 (232) −1.39 [−2.24, −0.54] 3.20 (< 0.001) 87% 0.97, 38.94, 5 (< 0.001)
5. Professional supervision 4 (182) −1.40 [−2.64, −0.17] 2.24 (0.03) 92% 1.45, 38.39, 3 (< 0.001)
6. PEDro score ≥ 5 5 (217) −1.31 [−2.46, −0.17] 2.24 (0.02) 92% 1.56, 52.14, 4 (< 0.001)
7. POMS-D - only 3 (109) −0.60 [−1.23, 0.02] 1.88 (0.06) 55% 0.16, 4.41, 2 (=0.11)
8. BDI - only 4 (200) −0.18 [−0.96, 0.59] 0.46 (0.64) 86% 0.53, 21.00, 3 (=0.001)
9. HADS-D - only 2 (104) −2.03 [−4.76, 0.70] 1.46 (0.15) 1.46 (0.15) 97% 28.96, 1 (< 0.001) 3.75, 28.96, 1 (< 0.001)
10. structured control 5 (184) −0.62 [−1.53, −0.30] 1.32 (0.19) 88% 0.93, 32.59, 4 (< 0.001)
11. non-structured control 4 (211) −1.11 [−2.38, 0.15] 1.73 (0.08) 94% 1.55, 50.16, 3 (< 0.001)

Anxiety
Random-effect model 5 (185) −1.23 [−2.42, −0.04] 2.03 (0.04) 92% 1.67, 48.90, 4 (< 0.001)

Note. Panel includes n trials (n participants), standardized mean difference (SMD), 95% confidence interval (95% CI), Z-score (Z) and significance (p) of
exercise vs. control conditions. Statistical heterogeneity (I2) is tested using the Chi2 statistics, including degree of freedom (df) and significance (p) and Tau2. A

7
A. Heissel, et AL. JourNAlofPsychosomAticRes
eArch126(2019)109823
negative SMD favors the exercise group. Aerobic exercise (AE), aerobic exercise combined with resistance training (AERT), Physiotherapy Evidence Database
(PEDro), Beck Depression Inventory (BDI), Profile of Mood State (POMS), Hospital Anxiety and Depression Scale (HADS).

8
Fig. 2. Forest plot using random effect model of studies examining the impact of exercise on depression.

Fig. 3. Forest plot using random effect model of studies examining the impact of exercise on anxiety.

Table 3
Pre-post comparison of depression and anxiety.

Outcome Studies (n) Participants (n) Post-analysis


2 2
Random effect model I Pre-post analysis I Post minus pre-post
2
Random effect model Diff. random Diff. I

Depression 9 395 −0.84 [−1.57, −0.11] 91% −0.91 [−1.51, −0.32] 86% 0.07 5%
Anxiety 5 185 −1.23 [−2.42, −0.04] 92% −1.27 [−2.49, −0.04] 92% 0.04 0%

Note. Panel includes study outcome, studies (n), participants (n), random effect of post analysis, heterogeneity of post analysis (I2), random effect of pre-post analysis,
heterogeneity of pre-post analysis (I2), difference of post minus pre-post analysis of random effect models and heterogeneity (I2).

In this investigation, only two studies [68,69] explicitly excluded


participants with a psychiatric illness, which includes depression and total sample range of 17 to 67 participants. This wide sampling
anxiety. For all other included studies, diagnosed depression was not a varia- bility increases the risk of sample bias among the studies and
reason for exclusion. Effectively, the baseline scores of the depression can lead to high statistical heterogeneity. Furthermore, across the
and anxiety measures were under the cut-off values for depression or ten studies, the participant dropout rate was 10.44% (n = 50). Six
anxiety in six studies [39,62–64,66,67]. Overall, 42 (8.8%) of the 479 of these studies had a high withdrawal rate according to the quality
participants at baseline were diagnosed with depression or anxiety. In assessment from the PEDro scale (≥ 15% of participants dropped
the review by Chaudhury et al. [77], the prevalence of depression was out) [39,62,64,66,67,70]. However, due to the proportionate
36% and of anxiety 16% in PLWH. Also, they reported that the pre- dropout rates in the intervention and control groups in these trials,
valence of depression and anxiety in PLWH ranged from 7.2% to the migration bias within the studies of participants who dropped
71.9% and from 4.5% to 82.3%, respectively. Given the fact that the out is minimized. Taken together, this pattern of findings highlights
pre- valence for depression and anxiety is underrepresented in the the need for future RCTs in this field to use larger sample sizes that
included studies compared to the general HIV population, the effect of comply with the criteria of high-
exercise could also be underestimated. quality studies, including the blinding of assessors and intention-to-
treat analysis, and involve clinically standardized outcome measures.
5. Limitations As outlined in the participants' characteristics, two of the included
studies included samples taking anti-depressants or anti-anxiety medi-
This review was based explicitly on depression and anxiety out- cations [39,69]. The inclusion of these studies may have partially in-
comes. Hence, the findings may not generalize to broader QOL out- fluenced the current results of the meta-analyses, as medication use in
comes that are more multidimensional. The results from the current combination with exercise may have a potential synergistic effect in
review need to also be interpreted in the context of several limitations. improving well-being. It is unclear, however, whether participants in
First, the findings from the pre-post analysis may have in part been the remaining eight studies used anti-depressants or anxiolytics, as
influenced by the small sample sizes, given that the majority (i.e., these studies did not report on medication usage. This merits further
60%) of included trials was comprised of samples < 50, with a investigation in future, larger scale RCTs in this field. Furthermore, it
combined is known that HAART medication affects physiological parameters
such as muscle tissue, body composition, cardiovascular parameters,
and also
psychological parameters [5,78–80].
Although the medication intake in the studies that reported indeed a synergistic effect when exercise is combined with medication
HARRT use was similar, the risk of medication bias is still possible use. Third, the effect of age regarding the impact of exercise on de-
since dif- ferent types of HAART were analyzed. The duration of pression and anxiety status has not been investigated systematically.
HAART intake and the number of therapy changes may also be Finally, the number of studies investigating exercise beyond the tradi-
different for every HIV- positive participant. These factors may tional forms of aerobic and resistance training is small, with only two
influence the effect of any type of exercise method investigated. studies identified for PLWH. Hence, it is too early to determine
Further research in a more homo- genous classification for medication whether the benefits of exercise are equivalent across different forms
intake is needed. of physical activity for PLWH. Further research is clearly needed to
In addition, the current meta-analysis excluded any control groups extend this line of research.
exercising at different intensity levels or performing other forms of With regard to the higher effect in the subgroup analysis of pro-
exercise. However, we considered the strict differentiation between fessional supervision (SMD = −1.40 [−2.64, −0.17]), these results
exercising and non-exercising participants as a strength of this study. are similar to those of Schuch et al.'s [87] meta analyses investigating
The inclusion of an exercising control group would lead to confounded exercise in the context of depressed patients also finding large and
results regarding the comparison of exercising and non-exercising higher effects for exercise led by exercise professionals. Another study
PLWH. in the context of exercise and aging with nearly 500 participants found
This current meta-analysis excluded studies investigating quality of that the perceived need support from the exercise professional predicts
life. It must be mentioned that the MOS-HIV or the SF-36 are primary depressive symptoms and satisfaction with life [88]. Therefore, further
tools of investigation in several excluded studies, e.g. Mutimura et al. studies need to control for the effect of the supervision suggesting that
[81], Maharaj et al. [82], Ogalha et al. [83], and Mkandla et al. [84]. e.g. the competence and empathy of the supervisor influences the
These questionnaires also include domains of anxiety and depression outcomes positively. Also exercising with a training partner or in a
as part of the mental health summary score. The current findings are group can have positive effects on the outcomes and therefore should
re- latively comparable to the findings of Nosrat et al. [33], although be controlled and might promote an even greater decrease in
they found positive effects of exercise when comparing exercise to depressive and anxiety symptoms.
control groups. The limitation of Nosrat's review [33] is that the results
are not based on meta-analytical findings. In the current meta-analysis, 5.2. IMPLICATIONS for PRACTICE
we used validated specific measures for depression and anxiety.
Regarding the control group conditions, the meta-analysis for PLWH have a higher risk of developing depressive or anxiety
de- pression showed a higher effect in favor of the intervention symptoms when compared to HIV negatives. This meta-analysis
group when comparing non-structured vs. structured control showed the benefits of performing exercise for reducing depressive
conditions (SMD = 1.11 vs. SMD = −0.62), even though both and anxiety symptoms beyond the well investigated benefits for
analyses are not significant (p = 0.08 vs. p = 0.19). Furthermore, physical health in PLWH. Additionally, exercise is generally a fast
within a non-struc- tured control condition such as “maintaining reachable and easy accessible option that should be recommended by
daily activity,” it remains unclear what exactly the participants did physicians to PLWH. Moreover, the results further showed that a high
during this time. frequency of training sessions (3 or more per week) may be beneficial
specifically for the reduction of depressive symptoms. Supervision by
5.1. IMPLICATIONS for RESEARCH qualified exercise professionals also led to greater effects for
depression. This psycho-so- cial component of the involvement of an
It is noteworthy that there was an equal gender distribution in the exercise professional that might be further increased by exercising
included studies, with women comprising 49.7% of the sample within a group or a partner should be considered in the
average. This indicates that the findings are applicable across both recommendations of physicians and out- reach clinics.
genders. This is particularly relevant given that research has shown
that the pre- valence rates for anxiety and depression may be higher in 6. Conclusion
women versus men [85,86]. However, given that all of included
studies in the current review did not report the depression and anxiety The present meta-analytic outcomes indicate large effects for the
results sepa- rately for each gender, unfortunately this precluded efficacy of exercise interventions in reducing both depression and an-
conducting sub- analyses according to whether or not the effects of xiety symptoms in PLWH. Although these findings are based on a
exercise for de- pression and anxiety were influenced by gender. small number of RCTs, these results suggest that exercise seems to be
Accordingly, future research is needed to specifically test whether mod- erately to largely beneficial for reducing depression and anxiety
women and men benefit equally from the positive effects of exercise in PLWH. Taken together, the results suggest that highly frequent (3 or
interventions. more per week), professionally supervised, and aerobic exercise may
The outcomes of this review identified some additional gaps that lead to the greatest improvements in depressive symptoms for PLWH.
need to be addressed in future research. First, PEDro scale criteria:
blinding subjects (n = 0), and blinding researchers/evaluators (n =
Dclaration of Competing Interests
0) were not met from any study. Blinding subject and blinding re-
searchers/evaluators are hardly realizable due to the nature of the
The authors have no competing interests to report.
ex- ercise intervention. Some criteria for high methodological
quality were not met by many studies, such as blinding assessors (n
= 7), measuring at least one key outcome obtained from > 85% of Funding
subjects initially al- located to groups (n = 6), and intention-to-treat
analysis (n = 8). Therefore, the methodological quality of studies This research did not receive any specific grant from funding
needs to be improved in future trials. Second, medication intake, agencies in the public, commercial, or not-for-profit sectors.
especially antidepressants, was not specified in the majority of
trials. This information is important to detail in future studies in
order to establish whether or not there is
Appendices

Table A.1
Systematic search strategy.

Database Date Combined terms and text words

Pubmed 13.02.2019 (((((((((HIV[MeSH Terms]) AND physical exercise[MeSH Terms]) OR physical activity[MeSH Terms]) OR yoga[MeSH Terms]) OR tai chi[MeSH
Terms]) OR qigong[MeSH Terms]) AND psychological [MeSH Terms] depression[MeSH Terms]) OR dysthymia[MeSH Terms]) OR anxiety[MeSH
Terms]
Cochrane Cen- 13.02.2019 HIV, exercise, physical activity, depression, anxiety
tral
PsycNet 13.02.2019 “HIV” OR “human immunodeficiency virus”) AND (“exercise” OR “physical activity” OR “aerobic” OR “resistance” OR “strength “OR “fitness “OR
“yoga “OR “tai chi “OR “qigong“) AND (“depression” OR “psychological” OR “depressive” OR “dysthymic” OR “dysthymia” OR “anxiety”)
PEDro 13.02.2019 HIV, exercise, physical activity, depression, anxiety
Clinicaltrials. 13.02.2019 (HIV exercise OR physical activity OR resistance OR aerobic OR yoga OR tai chi OR qigong AND depression OR anxiety or dysthymia)
gov

Note. Scientific databases consulted for the systematic review, with search term combinations and search dates as day, month and year.

Table A.2
Study characteristics of studies excluded from quantitative synthesis.
Author,
Outcome Method Participants Baseline Intervention Control Reason for Supervision Peer re-
Year,
Parameters /Intervention group exclusion viewed/
Country Intervention Control M/ S/ Wks M/ thesis
S Wk Wk

1 Galantino,
ML., 2005 POMS aerobic exer- (n) = 38, AE 2 8 non-struc- no baseline not men- peer re-
USA cise vs. tai chi n = 13,TC tured: usual or post tioned viewed
vs. control n = 13, CG daily activity measures
n = 12

Note. Study characteristics presented as author/year of publication, investigated outcome, specific intervention investigated, (n) participants, baseline measures
mean ± SD intervention group, baseline measure mean ± SD control group, minutes per session (M/S), sessions per week (S/Wk), weeks (Wks), minutes per
week (M/Wk), description of control group condition. Profile of Mood State (POMS), aerobic exercise (AE), tai chi (TC), control group (CG).

Table A.3
Outcome measures.

Studies Outcome Measuring tool Number of stu-


dies (%)

(Aweto et al., 2016; Daniels & Van Niekerk 2018; Dianatinasab et al., 2018; Jaggers et al., 2014; Kiloor et al., 2018;
Depression BDI-D, GHQ-28, POMS- 9 (90%)
LaPerriere et al., 1990; Naoroibam et al. 2016; Neidig et al. 2003; Shah et al., 2016)
D, HADS-D
(Dianatinasab et al. 2018; Kiloor et al., 2018; LaPerriere et al., 1990; Naoroibam et al., 2016, Schlenzig et al., 1992) Anxiety (GHQ-28, POMS-A, 5 (50%)
HADS-A, STAI)

Note. Studies: author/year of publication, Outcome: investigated parameter, measuring tool, number of investigating studies (percentage), Beck Depression Inventory-
Depression (BDI-D), General Health Questionnaire −28 (GHQ-28), Profile of Mood State-Depression/Anxiety (POMS-D/A), Hospital Anxiety and Depression Scale
(HADS), State-Trait Anxiety Inventory (STAI), percentage (%).

Table A.4
Risk of bias analysis according to the PEDro scale.

Study E I I III I V VI VII VIII IX X Tota


C I V l

Aweto HA. 2016 Y 1 1 1 0 0 0 0 0 1 1 5


Daniels AK. 2018 Y 1 0 0 0 0 0 1 0 1 1 4
Dianatinasab M. 2016 Y 1 0 1 0 0 0 0 0 1 1 4
Jaggers FR. 2014 Y 1 0 0 0 0 0 0 0 1 1 3
Kiloor A. 2018 Y 1 1 1 0 0 0 1 0 1 1 6
LaPerriere A. 1990 Y 1 0 1 0 0 0 1 1 1 1 6
Naoroibam R. 2016 Y 1 0 1 0 0 0 0 0 1 1 4
Neidig JL. 2003 Y 1 0 1 0 0 1 0 1 1 1 6
Schlenzig C. 1992 Y 1 0 1 0 0 0 0 0 1 1 4
Shah KN. 2016 Y 1 1 1 0 0 1 1 0 1 1 7

Note. EC: eligibility criteria, I: allocated randomization of subjects to groups, II: concealed allocation, III: similarities of groups at baseline, IV: blinding of
subjects, V: blinding of researchers/evaluators, VI: blinding of assessors, VII: measure of at least one key outcome obtained from > 85% of subjects initially
allocated to groups, VIII: intention to treat, IX: statistical comparison of between-group results, X: measured at least one key outcome at two time points, 1:
criteria is present, 0: criteria is missing. *EC does not contribute to the total score, Y: Yes, eligibility criteria present.

References [1] World Health Organization, Number of People (All Ages) Living with HIV Estimates by WHO
Region [Internet], Available from, 2017. http://apps.who.int/gho/data/
view.main.22100WHO?lang=en.
[2] Bayoumi A.M. O'Brien, C. Strike, N.L. Young, K. King, A.M. Davis, How do
existing HIV-specific instruments measure up? evaluating the ability of instruments [27]
to de- scribe disability experienced by adults living with HIV, Health Qual. Life
Outcomes
8 (1) (2010) 88.
[3] Bayoumi A.M. O'Brien, C. Strike, N.L. Young, A.M. Davis, Exploring disability
from the perspective of adults living with HIV/AIDS: development of a conceptual
fra- mework, Health Qual. Life Outcomes 6 (1) (2008) 76.
[4] S.G. Deeks, S.R. Lewin, D.V. Havlir, The end of AIDS: HIV infection as a chronic
disease, Lancet 382 (9903) (2013) 1525–1533.
[5] K.M. Erlandson, J.A. Schrack, C.M. Jankowski, T.T. Brown, T.B. Campbell,
Functional impairment, disability, and frailty in adults aging with HIV-infection,
Curr HIV/AIDS Rep. 11 (3) (2014 Sep) 279–290.
[6] A.T. Rodriguez-Penney, J.E. Iudicello, P.K. Riggs, K. Doyle, R.J. Ellis, S.L.
Letendre, et al., Co-morbidities in persons infected with HIV: increased burden with
older age and negative effects on health-related quality of life, AIDS Patient Care
STDs 27 (1)
(2013 Jan) 5–16.
[7] J.O. Mugisha, E.J. Schatz, M. Randell, M. Kuteesa, P. Kowal, J. Negin, et al.,
Chronic disease, risk factors and disability in adults aged 50 and above living with
and without HIV: findings from the wellbeing of older people study in Uganda,
Glob.
Health Action 9 (1) (2016 Dec) 31098.
[8] G. Tesfaw, G. Ayano, T. Awoke, D. Assefa, Z. Birhanu, G. Miheretie, et al.,
Prevalence and correlates of depression and anxiety among patients with HIV on-
follow up at Alert Hospital, Addis Ababa, Ethiopia, BMC Psychiatry [Internet] 16
(368) (2016) 1–7 Dec [cited 2017 Jan 3];16(1). Available from: http://
bmcpsychiatry.biomedcentral.com/articles/10.1186/s12888-016-1037-9.
[9] J. Leserman, Role of depression, stress, and trauma in HIV disease progression,
Psychosom Med 70 (5) (2008 Jun) 539–545.
[10] L. Schlebusch, R.D. Govender, Elevated risk of suicidal ideation in HIV-positive
persons, Depress. Res. Treat. 2015 (2015) 1–6.
[11] Y.-L. Wu, H.-Y. Yang, J. Wang, H. Yao, X. Zhao, J. Chen, et al., Prevalence of sui-
cidal ideation and associated factors among HIV-positive MSM in Anhui, China, Int.
J. STD AIDS. 26 (7) (2015 Jun 1) 496–503.
[12] S.A. Nixon, J. Hanass-Hancock, A. Whiteside, T. Barnett, The increasing chronicity
of HIV in sub-Saharan Africa: re-thinking" HIV as a long-wave event" in the era of
widespread access to ART, Glob. Health 7 (1) (2011) 41.
[13] S. Amanor-Boadu, M.S. Hipolito, N. Rai, C.K. McLean, K. Flanagan, F.T.
Hamilton, et al., Poor CD4 count is a predictor of untreated depression in human
im-
munodeficiency virus-positive African-Americans, World J. Psychiatr. 6 (1) (2016)
128.
[14] G. Ironson, C. O'Cleirigh, M.A. Fletcher, J.P. Laurenceau, E. Balbin, N. Klimas, et
al., Psychosocial factors predict CD4 and viral load change in men and women
with
human immunodeficiency virus in the era of highly active antiretroviral treatment,
Psychosom Med. 67 (6) (2005 Nov) 1013–1021.
[15] J.S. Gonzalez, A.W. Batchelder, C. Psaros, S.A. Safren, Depression and HIV/AIDS
treatment nonadherence: a review and meta-analysis, JAIDS J. Acquir. Immune
Defic. Syndr. 58 (2) (2011 Oct) 181–187.
[16] S.A. Safren, C. O'Cleirigh, J.Y. Tan, S.R. Raminani, L.C. Reilly, M.W. Otto, et al.,
A randomized controlled trial of cognitive behavioral therapy for adherence and
de-
pression (CBT-AD) in HIV-infected individuals, Health Psychol. 28 (1) (2009) 1–10.
[17] A. Larisch, G. Heuft, S. Engbrink, E. Brähler, W. Herzog, J. Kruse, Behandlung
psychischer und psychosomatischer Beschwerden-Inanspruchnahme, Erwartungen
und Kenntnisse der Allgemeinbevölkerung in Deutschland, Z Für Psychosom Med
Psychother. 59 (2) (2013) 153–169.
[18] C.J. Caspersen, K.E. Powell, G.M. Christenson, Physical activity, exercise, and
physical fitness: definitions and distinctions for health-related research, Public
Health Rep. 100 (2) (1985) 126.
[19] F.B. Schuch, D. Vancampfort, J. Firth, S. Rosenbaum, P.B. Ward, E.S. Silva, et al.,
Physical activity and incident depression: a Meta-analysis of prospective cohort
studies, Am. J. Psychiatry 175 (7) (2018 Jul) 631–648.
[20] F.B. Schuch, B. Stubbs, J. Meyer, A. Heissel, P. Zech, D. Vancampfort, et al.,
Physical activity protects from incident anxiety: A meta-analysis of prospective
cohort stu- dies: SCHUCH ET AL. Depress Anxiety [Internet], 17 [cited 2019 Jul 17];
Available
from: http://doi.wiley.com/10.1002/da.22915.
[21] G.M. Cooney, K. Dwan, C.A. Greig, D.A. Lawlor, J. Rimer, F.R. Waugh, et al.,
Exercise for depression, The Cochrane Collaboration, Cochrane Database of
Systematic Reviews [Internet], John Wiley & Sons, Ltd, Chichester, UK, 2013, ,
https://doi.org/10.1002/14651858.CD004366.pub6 [cited 2017 Jul 4]. Available
from:.
[22] F.B. Schuch, D. Vancampfort, J. Richards, S. Rosenbaum, P.B. Ward, B. Stubbs,
Exercise as a treatment for depression: a meta-analysis adjusting for publication
bias, J. Psychiatr. Res. 77 (2016 Jun) 42–51.
[23] D. Vancampfort, J. Mugisha, M. De Hert, M. Probst, J. Firth, P. Gorczynski, et al.,
Global physical activity levels among people living with HIV: a systematic review
and meta-analysis, Disabil. Rehabil. 40 (4) (2018 Feb 13) 388–397.
[24] D. Vancampfort, J. Mugisha, M. De Hert, M. Probst, B. Stubbs, Sedentary behavior
in people living with HIV: a systematic review and Meta-analysis, J. Phys. Act.
Health 14 (7) (2017 Mar 14) 571–577.
[25] M. Gomes Neto, C.S. Conceição, V.O. Carvalho, C. Brites, Effects of combined
aerobic and resistance exercise on exercise capacity, muscle strength and quality of
life in HIV-infected patients: a systematic review and meta-analysis. Sacchetti M,
editor, PLOS ONE 10 (9) (2015 Sep 17) e0138066.
[26] M. Gomes-Neto, C. Conceicao, V. Carvalho, C. Brites, A systematic review of the
effects of different types of therapeutic exercise on physiologic and functional
measurements in patients with HIV/AIDS, Clinics. 68 (8) (2013 Aug 30) 1157–
1167.
L.L. Leach, S.H. Bassett, G. Smithdorf, B.S. Andrews, A.L. Travill, Suppl 1: M3: a Nurses AIDS Care. 14 (2) (2003 Mar) 30–40.
systematic review of the effects of exercise interventions on body composition in [40] A.P. Verhagen, H.C.W. de Vet, R.A. de Bie, A.G.H. Kessels, M. Boers, L.M.
HIV+ adults, Open AIDS J. 9 (2015) 66. Bouter, et al., The Delphi list: a criteria list for quality assessment of randomized
[28] K.K. O'Brien, A.M. Tynan, S.A. Nixon, R.H. Glazier, Effectiveness of clinical
Progressive Resistive Exercise (PRE) in the context of HIV: systematic trials for conducting systematic reviews developed by Delphi consensus, J. Clin.
review and meta-analysis using the Cochrane Collaboration protocol, Epidemiol. 51 (12) (1998 Dec 1) 1235–1241.
BMC Infect Dis. 17 (1) (Apr 12 2017) [41] A.M. Moseley, R.D. Herbert, C. Sherrington, C.G. Maher, Evidence for phy-
268, https://doi.org/10.1186/s12879-017-2342-8. siotherapy practice: a survey of the physiotherapy evidence database (PEDro),
[29] C.G.A. Pérez Chaparro, P. Zech, F. Schuch, B. Wolfarth, M. Rapp, A. Aust. J. Physiother. 48 (1) (2002) 43–49.
Heiβel, Effects of aerobic and resistance exercise alone or combined on [42] C. Sherrington, R.D. Herbert, C.G. Maher, A.M. Moseley, PEDro. A database of
strength and hormone outcomes for people living with HIV. A meta- randomized trials and systematic reviews in physiotherapy, Man. Ther. 5 (4) (2000
analysis. Parmenter B, editor, PLOS ONE 13 (9) (2018 Sep 4) Nov) 223–226.
e0203384. [43] M. Borenstein, L. Hedges, H. Rothstein, Meta-analysis: Fixed effect vs. random ef-
[30] Zech P, Pérez-Chaparro C, Schuch F, Wolfarth B, Rapp M, Heissel A. fects, Meta-Anal Com [Internet] (2007) 1–162 [cited 2017 Jan 3]; Available from
Effects of aerobic and resistance exercise on cardiovascular parameters https://www.meta-analysis.com/downloads/Meta-analysis%20fixed%20effect
for people living with %20vs%20random%20effects%20072607.pdf.
HIV. J. Assoc. Nurses AIDS Care. e-pub ahead; [44] S.V. Faraone, Interpreting estimates of treatment effects: implications for managed
[31] K.K. O’Brien, A.-M. Tynan, S.A. Nixon, R.H. Glazier, Effectiveness care, Pharm Ther. 33 (12) (2008) 700.
of aerobic ex- ercise for adults living with HIV: systematic review and [45] H.J. Schünemann, A.D. Oxman, G.E. Vist, J.P. Higgins, J.J. Deeks, P. Glasziou, et
meta-analysis using the Cochrane Collaboration protocol, BMC Infect al., Interpreting results and drawing conclusions, in: J.P. Higgins, S. Green (Eds.),
Dis. [Internet] 16 (182) (2016 Dec) 1–56 [cited 2017 Mar 29];16(1). Cochrane Handbook for Systematic Reviews of Interventions [Internet], John Wiley
Available from: http://bmcinfectdis. & Sons, Ltd, Chichester, UK, 2008, , https://doi.org/10.1002/9780470712184.ch12
biomedcentral.com/articles/10.1186/s12879-016-1478-2. [cited 2017 Jul 14]. p. 359–87. Available from:.
[32] S.M. Lofgren, N. Nakasujja, D.R. Boulware, Systematic review of [46] J.P. Higgins, S.G. Thompson, J.J. Deeks, D.G. Altman, Measuring inconsistency in
interventions for depression for people living with HIV in Africa, AIDS meta-analyses, Bmj. 327 (7414) (2003) 557–560.
Behav. 22 (1) (2018 Jan) 1–8. [47] S.B. Morris, Estimating effect sizes from Pretest-Posttest-control group designs,
[33] S. Nosrat, J.W. Whitworth, J.T. Ciccolo, Exercise and mental health of people living Organ. Res. Methods 11 (2) (2008 Apr) 364–386.
with HIV: a systematic review, Chronic Illn. 13 (4) (2017 Dec) 299–319. [48] X. Shi, C. Nie, S. Shi, T. Wang, H. Yang, Y. Zhou, et al., Effect comparison
[34] The Cochrane Public Health Group, Guide for developing a Cochrane between Egger's Test and Begg's Test in publication bias diagnosis in meta-analyses:
protocol [Internet], Available from, 2011. evidence
http://ph.cochrane.org/sites/ph.cochrane.org/ from a pilot survey, Int. J. Res. Stud. Biosci. [Internet] 5 (5) (2017) 14–20 [cited
files/public/uploads/Guide%20for%20PH%20protocol_Nov 2019 Jul 17];5(5). Available from: https://www.arcjournals.org/pdfs/ijrsb/v5-i5/
%202011_final%20for 3.pdf.
%20website.pdf. [49] K.L. Soeken, A. Sripusanapan, Assessing publication bias in meta-analysis, Nurs.
[35] D. Moher, L. Shamseer, M. Clarke, D. Ghersi, A. Liberati, M. Res. 52 (1) (2003 Jan) 57–60.
Petticrew, et al., Preferred reporting items for systematic review [50] J. Baigis, D.M. Korniewicz, G. Chase, A. Butz, D. Jacobson, A.W. Wu,
and meta-analysis protocols Effectiveness of a home-based exercise intervention for HIV-infected adults: a
(PRISMA-P) 2015 statement, Syst Rev. 4 (1) (2015) 1. randomized trial, J.
[36] N.L. McCain, D.P. Gray, R.K. Elswick, J.W. Robins, I. Tuck, J.M. Assoc. Nurses AIDS Care. 13 (2) (2002) 33–45.
Walter, et al., A randomized clinical trial of alternative stress [51] S. Fillipas, L.B. Oldmeadow, M.J. Bailey, C.L. Cherry, A six-month, supervised,
management interventions in persons with HIV infection, J. Consult. aerobic and resistance exercise program improves self-efficacy in people with
Clin. Psychol. 76 (3) (2008) 431–441. human immunodeficiency virus: a randomised controlled trial, Aust. J. Physiother.
[37] N. Falsafi, A randomized controlled trial of mindfulness versus yoga: 52 (2006) 185–190.
effects on depression and/or anxiety in college students, J. Am. [52] C.L. Lox, E. McAuley, R.S. Tucker, Exercise as an intervention for enhancing sub-
Psychiatr. Nurses Assoc. 22 jective well-being in an HIV-1 population, J. Sport Exerc. Psychol. 17 (4) (1995)
(6) (2016) 483–497. 345–362.
[38] P. Ekkekakis, Honey, I shrunk the pooled SMD! Guide to critical [53] R.D. MacArthur, S. Levine, T. Birk, Supervised exercise training improves cardio-
appraisal of sys- tematic reviews and meta-analyses using the pulmonary fitness in HIV-infected persons, Med. Sci. Sports Exerc. 25 (6) (1993 Jun
Cochrane review on exercise for de- pression as example, Ment. 1) 684–688.
Health Phys. Act. 8 (2015 Mar) 21–36. [54] B.T. Mausbach, S.J. Semple, S.A. Strathdee, J. Zians, Effectiveness of a Behavioral
[39] J.L. Neidig, B.A. Smith, D.E. Brashers, Aerobic exercise training for depressive Intervention for Increasing Safer Sex Behaviors in HIV-positive MSM
symptom Management in Adults Living with HIV infection, J. Assoc. Methamphetamine Users: Results from the EDGE Study, 16 (2008).

[55] A. McDermott, L. Zaporojan, P. McNamara, C.P. Doherty, J. Redmond, C. Forde, CD4 count and mental health among HIV infected women: a randomized control trial, J.
et al., The effects of a 16-week aerobic exercise programme on cognitive function in Exerc. Sci. Fit. 16 (1) (2018 Apr) 21–25.
people living with HIV, AIDS Care 29 (6) (2017 Jun 3) 667–674. [67] J. Jaggers, G. Hand, W. Dudgeon, S. Burgess, K. Phillips, J. Durstine, et al., Aerobic and
[56] W.W. Stringer, M. Berezovskaya, W.A. O'Brien, C.K. Beck, R. Casaburi, The effect resistance training improves mood state among adults living with HIV, Int. J.
of exercise training on aerobic fitness, immune indices, and quality of life in HIV+ Sports Med. 36 (02) (2014 Oct 16) 175–181.
patients, Med. Sci. Sports Exerc. 30 (1) (1998) 11–16. [68] A. Kiloor, Metri K. Sonykumari, Impact of yoga on psychopathologies and QoLin persons with
[57] L. Terry, E. Sprinz, J.P. Ribeiro, Moderate and high intensity exercise training in HIV: A randomized controlled study, J. Bodyw. Mov. Ther. [Internet]. 23 (2) (2018) 278–283
HIV-1 seropositive individuals: a randomized trial, Int. J. Sports Med. 20 (02) Oct [cited 2018 Nov 7]; Available from: https://linkinghub.
(1999) 142–146. elsevier.com/retrieve/pii/S1360859218304467.
[58] S.E. Jensen, D.B. Pereira, N. Whitehead, I. Buscher, J. McCalla, M. Andrasik, et al., [69] K.N. Shah, Z. Majeed, Y.B. Yoruk, H. Yang, T.N. Hilton, J.M. McMahon, et al., Enhancing physical
Cognitive–behavioral stress management and psychological well-being in HIV+ function in HIV-infected older adults: a randomized controlled
racial/ethnic minority women with human papillomavirus, Health Psychol. 32 (2) clinical trial, Health Psychol. 35 (6) (2016) 563–573.
(2013 Feb) 227–230. [70] R. Naoroibam, K.G. Metri, R. Nagaranta, H.R. Nagendra, Effect of integrated yoga (IY) on
[59] L. Li, G. Ji, L.-J. Liang, C. Lin, J. Hsieh, C.-W. Lan, et al., Efficacy of a multilevel psychological states and CD4 counts of HIV-1 infected patients: a rando- mized controll pilot
intervention on the mental health of people living with HIV and their family study, Int. J. Yoga. 9 (1) (2016) 57–61.
members in rural China, Health Psychol. 36 (9) (2017 Sep) 863–871. [71] B.A. Smith, J.L. Neidig, J.T. Nickel, G.L. Mitchell, M.F. Para, R.J. Fass, Aerobic exercise:
[60] J.T. Moskowitz, A.W. Carrico, L.G. Duncan, M.A. Cohn, E.O. Cheung, A. effects on parameters related to fatigue, dyspnea, weight and body com- position in HIV-
Batchelder, et al., Randomized controlled trial of a positive affect intervention for infected adults, Aids. 15 (6) (2001) 693–701.
people newly diagnosed with HIV, J. Consult. Clin. Psychol. 85 (5) (2017) 409– [72] T. Wang, H. Fu, A.C. Kaminga, Z. Li, G. Guo, L. Chen, et al., Prevalence of de- pression or
423. depressive symptoms among people living with HIV/AIDS in China: a systematic review and
[61] M.L. Galantino, K. Shepard, L. Krafft, A. Laperriere, J. Ducette, A. Sorbello, et al., meta-analysis, BMC Psychiatr. [Internet] 18 (160) (2018)
The effect of group aerobic exercise and t'ai chi on functional outcomes and quality
of life for persons living with acquired immunodeficiency syndrome, J. Altern.
Complem. Med. Res. Paradigm Pract. Policy. 11 (6) (2005) 1085–1092.
[62] H.A. Aweto, A.I. Aiyegbusi, A.J. Ugonabo, T.A. Adeyemo, Effects of aerobic
exercise on the pulmonary functions, respiratory symptoms and psychological status
of people living with HIV, J. Res. Health Sci. 16 (1) (2016) 17–21.
[63] A.R. LaPerriere, M.H. Antoni, N. Schneiderman, G. Ironson, N. Klimas, P. Caralis,
et al., Exercise intervention attenuates emotional distress and natural killer cell
decrements following notification of positive serologic status for HIV-1,
Biofeedback Self-Regul. 15 (3) (1990) 229–242.
[64] C. Schlenzig, Reaktionen des Immunsystems und der Psyche HIV-Infizierter und
AIDS-Patienten auf kontrollierte sporttherapeutische Langzeitbehandlung,
[Heidelberg]: Ruprecht-Karls-Universität Heidelberg (1992).
[65] A.K. Daniels, R.L. Van Niekerk, The impact of a therapeutic exercise intervention
on depression and body self-image in HIV-positive women in sub-Saharan Africa,
HIVAIDS – Res. Palliat. Care. 10 (2018 Jul) 133–144.
[66] M. Dianatinasab, M. Fararouei, V. Padehban, A. Dianatinasab, Y. Alimohamadi,
S. Beheshti, et al., The effect of a 12-week combinational exercise program on
1–14 Dec [cited 2019 Jul 17];18(1). Available from:
https://bmcpsychiatry.
biomedcentral.com/articles/10.1186/s12888-018-1741-8.
[73] S.N. Levintow, B.W. Pence, T.V. Ha, N.L. Minh, T. Sripaipan, C.A.
Latkin, et al., Prevalence and predictors of depressive symptoms
among HIV-positive men who
inject drugs in Vietnam. Moitra E, editor, PLOS ONE 13 (1) (2018
Jan 24) e0191548.
[74] C. Bernard, F. Dabis, N. de Rekeneire, Prevalence and factors
associated with de- pression in people living with HIV in sub-Saharan
Africa: A systematic review and meta-analysis. Seedat S, editor, PLOS
ONE 12 (8) (2017 Aug 4) e0181960.
[75] P. Rai, B.L. Verma, A study on depression in people living with
HIV/AIDS in south- west part of Uttar Pradesh, India, South East Asia
J. Public Health. 5 (1) (2015 Sep
13) 12–17.
[76] B. Stubbs, D. Vancampfort, S. Rosenbaum, J. Firth, T. Cosco, N.
Veronese, et al., An examination of the anxiolytic effects of exercise
for people with anxiety and stress- related disorders: a meta-analysis,
Psychiatry Res. 249 (2017 Mar 1) 102–108.
[77] S. Chaudhury, A. Bakhla, R. Saini, Prevalence, impact, and
management of de- pression and anxiety in patients with HIV: a
review, Neurobehav. HIV Med. 15 (2016 May).
[78] J. Price, J. Hoy, E. Ridley, I. Nyulasi, E. Paul, I. Woolley, Changes in
the prevalence of lipodystrophy, metabolic syndrome and
cardiovascular disease risk in HIV-in-
fected men*, Sex Health [Internet] 12 (3) (2015) 240–248 [cited
2017 Jan 3]; Available from: http://www.publish.csiro.au/?
paper=SH14084.
[79] J.R. Kingery, Y. Alfred, L.R. Smart, E. Nash, J. Todd, M.R. Naguib, et
al., Short-term and long-term cardiovascular risk, metabolic syndrome
and HIV in Tanzania, Heart.
102 (15) (2016 Aug 1) 1200–1205.
[80] D.H. Akena, S. Musisi, E. Kinyanda, A comparison of the clinical
features of de- pression in HIV-positive and HIV-negative patients
in Uganda, Afr. J. Psychiatr. [Internet] 13 (2010) 43–51 [cited 2017
Jan 3];13(1). Available from: http://www.
ajol.info/index.php/ajpsy/article/view/53429.
[81] E. Mutimura, A. Stewart, N.J. Crowther, K.E. Yarasheski, W.T. Cade, The
effects of exercise training on quality of life in HAART-treated HIV-
positive Rwandan subjects
with body fat redistribution, Qual. Life Res. 17 (3) (2008 Apr) 377–385.
[82] S.S. Maharaj, V. Chetty, Rehabilitation program for the quality of life
for individuals on highly active antiretroviral therapy in KwaZulu-
Natal, South Africa: a short re- port, Int. J. Rehabil. Res. 34 (4) (2011
Dec) 360–365.
[83] C. Ogalha, E. Luz, E. Sampaio, R. Souza, A. Zarife, M.G. Neto, et al.,
A randomized, clinical trial to evaluate the impact of regular physical
activity on the quality of life, body morphology and metabolic
parameters of patients with AIDS in Salvador,
Brazil, JAIDS J. Acquir. Immune Defic. Syndr. 57 (2011) S179–S185.
[84] K. Mkandla, H. Myezwa, E. Musenge, The effects of progressive-
resisted exercises on muscle strength and health-related quality of life
in persons with HIV-related poly- neuropathy in Zimbabwe, AIDS
Care 28 (5) (2016 May 3) 639–643.
[85] K. Aljassem, J.M. Raboud, T.A. Hart, A. Benoit, D. Su, S.L.
Margolese, et al., Gender differences in severity and correlates of
depression symptoms in people living with
HIV in Ontario, Canada, J. Int. Assoc. Provid. AIDS Care JIAPAC. 15
(1) (2016 Jan) 23–35.
[86] N.P. Caballero-Suárez, E. Rodríguez Estrada, M. Candela-Iglesias, G. Reyes-Terán,
Centro de Investigación de Enfermedades Infecciosas (CIENI),
Instituto Nacional de Enfermedades Respiratorias (INER). Comparison
of levels of anxiety and depression
between women and men living with HIV of a Mexico City clinic,
Salud Ment. 40 (1) (2017 Jan 31) 15–22.
[87] F.B. Schuch, D. Vancampfort, J. Richards, S. Rosenbaum, P.B.
Ward, B. Stubbs, Exercise as a treatment for depression: a meta-
analysis adjusting for publication
bias, J. Psychiatr. Res. 77 (2016 Jun) 42–51.
[88] A. Heissel, A. Pietrek, M. Rapp, S. Heinzel, G. Williams, Perceived
health care cli- mate of older people attending an exercise program:
validation of the German short version of the modified health care
climate questionnaire, J Aging Phys Act. (2019) [epub ahead].

You might also like