Anda di halaman 1dari 9

ORIGINAL ARTICLE

Effects of yoga in adults with type 2 diabetes


mellitus: A meta-analysis
Jie Cui1,2, Jun-Hong Yan3, Li-Ming Yan4, Lei Pan5, Jia-Jin Le1, Yong-Zhong Guo6*
1
Glorious Sun School of Business and Management, Donghua University, 2Ruijin Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, Departments of 3Clinical
Medical Technology, 4Clinical Outpatient, 5Critical Care Medicine, Binzhou Medical University Hospital, Binzhou, and 6Department of Respiratory Medicine, Xuzhou Central Hospital,
The Affiliated Xuzhou Center Hospital of Nanjing University of Chinese Medicine, Xuzhou, China

Keywords ABSTRACT
Meta-analysis, Type 2 diabetes, Yoga Aims/Introduction: A meta-analysis was carried out to evaluate the efficacy of yoga in
adults with type 2 diabetes mellitus.
*Correspondence Materials and Methods: The PubMed, EMBASE and Cochrane databases were
Yong-Zhong Guo searched to obtain eligible randomized controlled trials. The primary outcome was fasting
Tel.: +86-1810-5208-862 blood glucose, and the secondary outcomes included glycosylated hemoglobin A1c, total
Fax: +86-0516-8395-6108 cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, triglyc-
E-mail address: tgsci2016@163.com
eride and postprandial blood glucose. Weighted mean differences and 95% confidence
intervals (CIs) were calculated. The I2 statistic represented heterogeneity.
J Diabetes Investig 2017; 8: 201–209
Results: A total of 12 randomized controlled trials with a total of 864 patients met the
doi: 10.1111/jdi.12548 inclusion criteria. The pooled weighted mean differences were -23.72 mg/dL (95% CI -
37.78 to -9.65; P = 0.001; I2 = 82%) for fasting blood glucose and -0.47% (95% CI -0.87
to -0.07; P = 0.02; I2 = 82%) for hemoglobin A1c. The weighted mean differences were -
17.38 mg/dL (95% CI -27.88 to -6.89; P = 0.001; I2 = 0%) for postprandial blood glucose,
-18.50 mg/dL (95% CI -29.88 to -7.11; P = 0.001; I2 = 75%) for total cholesterol, 4.30 mg/
dL (95% CI 3.25 to 5.36; P < 0.00001; I2 = 10%) for high-density lipoprotein cholesterol, -
12.95 mg/dL (95% CI -18.84 to -7.06; P < 0.0001; I2 = 37%) for low-density lipoprotein
cholesterol and -12.57 mg/dL (95% CI -29.91 to 4.76; P = 0.16; I2 = 48%) for triglycerides.
Conclusions: The available evidence suggests that yoga benefits adult patients with
type 2 diabetes mellitus. However, considering the limited methodology and the potential
heterogeneity, further studies are necessary to support our findings and investigate the
long-term effects of yoga in type 2 diabetes mellitus patients.

INTRODUCTION clinical studies as a cardinal non-pharmacotherapy5. Numerous


Type 2 diabetes mellitus is one of the most frequently encoun- training programs, such as jogging, walking, swimming, house-
tered metabolic syndromes worldwide1. The most recent meta- work and other outdoor exercises, have been developed. How-
analysis showed that the overall prevalence (9.1%) has been ever, taking into account the increasing prevalence of obesity,
increasing among inland residents in China since the 1970s, and the disabilities and complications associated with a seden-
and it increased rapidly with age2. Effective control of blood tary lifestyle6,7, few patients participate in conventional physical
glucose to reduce the risk of various complications, including exercise.
diabetic foot, diabetic neuropathy, cataract and cardiovascular Yoga originated in India over 4,000 years ago as a tradi-
disease, is especially important for type 2 diabetes mellitus tional form of mind–body training that seeks to unite the
management3,4. Medication, diet and physical activity or exer- individual self with the transcendental self8. Yoga asanas (pos-
cise are the major components of diabetes management. Train- tures) and pranayama (breath control) have recently become
ing exercises have been recommended by recent evidence-based very popular, and the role of yoga in several chronic diseases,
such as hypertension, asthma, chronic obstructive pulmonary
disease and diabetes, has been studied8–10. Several trials have
Received 24 March 2016; revised 22 May 2016; accepted 29 June 2016

ª 2016 The Authors. Journal of Diabetes Investigation published by Asian Association for the Study of Diabetes (AASD) and John Wiley & Sons Australia, Ltd J Diabetes Investig Vol. 8 No. 2 March 2017 201
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and
reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
ORIGINAL ARTICLE
Cui et al. http://onlinelibrary.wiley.com/journal/jdi

shown that yoga can reduce fasting blood glucose (FBG) and Statistical analysis
glycosylated hemoglobin A1c (HbA1c), as well as improve the All of the data were combined using Revman 5.3 (The
lipid levels and quality of life of type 2 diabetes mellitus Cochrane Collaboration, Oxford, UK). Weighted mean differ-
patients11–18. However, these studies present wide variations in ences (WMDs) with 95% confidence intervals (CIs) for contin-
sample size and even inconclusive results. Other studies uous variables were calculated and pooled using the random
applied a non-randomized study design that could affect the effects model23. Heterogeneity was tested using Cochrane’s Q-
final outcomes11–13. Thus, in the present study, we carried out test and the I2 statistic, and I2 values >50% were considered to
a meta-analysis of randomized controlled trials (RCTs) to show significant heterogeneity24. If I2 >50%, sensitivity analyses
determine the effectiveness of yoga in patients with type 2 was carried out to explore potential sources of heterogeneity
diabetes mellitus. and investigate the influence of a single study on the overall
pooled estimate. Combined with the demographic data of study
MATERIALS AND METHODS participants included in the present study, as well as to mini-
The current meta-analysis was carried out according to the rec- mize the risk of bias as a result of grouping criteria, subgroup
ommendations of the Cochrane Handbook for Systematic analyses were carried out to explore potential heterogeneity and
Reviews of Interventions19, and followed Preferred Reporting examine the influence of various exclusion criteria on the basis
Items for Systematic Reviews and Meta-Analyses guidelines20. of sample size (>60 vs ≤60), Jadad score (>2 vs ≤2), duration
(>3 months vs ≤3 months) and region (India vs non-India).
Data sources and searches Publication bias was assessed using Stata version 12.0 (Stata
The PubMed, Embase and Cochrane databases were searched Corporation LP, College Station, TX, USA), and results were
(until April 2016) for eligible RCTs using the key words ‘yoga’ analyzed using Begg’s and Egger’s test25. Finally, two-sided P-
and ‘diabetes’. Eligible trials were limited to adult human sub- values <0.05 were considered to show statistical significance.
jects, and only trials published with the full text and written in
English were included in this work. To ensure literature satura- RESULTS
tion, the bibliographies of all potentially eligible studies, includ- Search results and study characteristics
ing reference lists, citation searches and relevant systematic Initially, 189 potential studies were retrieved from the electronic
reviews, were searched by hand. databases. After reviewing their titles and abstracts, 164 studies
The available trials followed the PICOS criteria, including: were excluded because they were unrelated to the aims of the
(i) (P) patients: adult type 2 diabetes mellitus patients with or present study. Another 13 candidate studies were excluded for
without chronicity and diabetes-associated complications; (ii) various reasons (Figure 1). Finally, 12 RCTs were selected for
(I) intervention: yoga with or without other treatments; (iii) the present meta-analysis14–18,26–32.
(C) control: any type of control including usual care or stan- The main characteristics of 12 RCTs involving 864 patients
dard treatment; (iv) (O) outcomes: the primary outcome was are summarized in Table 1. All RCTs were made available in
FBG and the secondary outcomes included HbA1c, postpran- English between 1992 and 2014. The total sample size ranged
dial blood glucose (PPBG), total cholesterol (TC), high-density from 20 to 277. A total of 11 RCTs were carried out in four
lipoprotein cholesterol (HDL-C), low-density lipoprotein countries, including the UK15,27, India14,16,28–32, Cuba17,18 and
cholesterol (LDL-C) and triglyceride; and (v) (S) study design: Iran26. Two RCTs were carried out by Gordon et al.17,18 on the
RCT. same study population, and another two RCTs were carried
out by Shantakumari et al.16,30, also on the same study popula-
Data extraction tion. Follow-up periods varied from 15 days to 9 months. All
Two investigators (JC and JHY) independently extracted all of RCTs applied different yoga protocols with different exercise
the data, including the first author, publication year, country, times and times per session. Furthermore, Table S1 shows addi-
study population and grouping (sample size per group), age, tional information reported in all the randomized controlled
form or style of two groups, yoga protocol, duration, outcomes, trials.
study design, and Jadad scale, from the eligible RCTs. Disagree-
ments were resolved by a third investigator (LP). Quality and risk of bias assessment
Two investigators (JC and JHY) agreed on each item of the
Quality and risk of bias assessment Jadad score and Cochrane Risk of Bias Assessment tool. The
The quality of each trial was evaluated according to the Jadad mean Jadad score of the 12 RCTs was 2.8 (SD = 0.8). Risk-of-
scale21. Randomization (0–2 points), blinding (0–2 points), and bias assessment showed that all RCTs generated low risk in
dropouts and withdrawals (0–1 point) were identified in the terms of random sequence generation. None of the trials was
scale. A trial with a score ≤2 indicates low quality, whereas a double-blinded, and just three RCTs were single-blinded17,18,28.
score of ≥3 indicates high quality22. The risk of bias was Details of the quality and risk-of-bias assessment of all of the
assessed by the Cochrane Risk of Bias Assessment tool19. RCTs are shown in Table 1 and Figure S1, respectively.

202 J Diabetes Investig Vol. 8 No. 2 March 2017 ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd
ORIGINAL ARTICLE
http://onlinelibrary.wiley.com/journal/jdi Yoga for T2DM

Potential articles identified from


computerized database
(n = 189)

Studies excluded based on


the titles and abstracts
(n = 164)

Potentially relevant articles screened


(n = 25)
Reason for exclusion:
-insufficient data (n = 5)
-non-diagnosed patients (n = 3)
-repetitive trials (n = 3)
-written in non-English (n = 2)

Studies included in the


present meta-analysis
(n = 12)

Figure 1 | Search strategy and flow chart for this meta-analysis.

Meta-analyses of primary outcome P < 0.0001; P for heterogeneity = 0.18; I2 = 37%) for LDL-C
Nine RCTs reported FBG as a primary outcome . The 14,17,26–32
(Figure 4), -12.57 mg/dL (95% CI -29.91 to 4.76; P = 0.16; P
pooled WMDs were -23.72 mg/dL (95% CI -37.78 to -9.65; for heterogeneity = 0.12; I2 = 48%) for triglycerides (Figure 4)
P = 0.001; P for heterogeneity <0.00001; I2 = 82%) for FBG and 4.30 mg/dL (95% CI 3.25 to 5.36; P < 0.00001; P for
(Figure 2). Heterogeneity was clearly significant for the primary heterogeneity = 0.34; I2 = 10%) for HDL-C (Figure 5).
end-point. We carried out sensitivity analyses to investigate the
potential sources of heterogeneity. However, regardless of which Publication bias
study was excluded from our analysis, the source of heterogene- Publication bias is shown in Figure 6. The results of the Begg’s
ity was not observed and the overall combined WMDs, which and Egger’s tests suggested that no evidence of publication bias
ranged from -27.90 mg/dL (95% CI -41.84 to -13.96; was found from funnel plots and associated statistics for FBG
P < 0.0001) to -20.61 mg/dL (95% CI -33.99 to -7.23; (PBegg = 0.917; PEgger = 0.328).
P = 0.003), were not significantly altered. Next, we carried out
subgroup analyses to examine the influence of various exclusion DISCUSSION
criteria with respect to FBG according to sample size (>60 vs ≤ The aim of the present meta-analysis of the existing data is to
60), Jadad score (>2 vs ≤2), duration (>3 months vs quantitatively assess the role of yoga in patients with type 2
≤3 months) and region (India vs non-India). The detailed diabetes mellitus. The available evidence from 12 RCTs with a
results are shown in Table 2. We found that the overall com- total of 864 patients suggested that yoga can significantly
bined effects of the trials, regardless of their quality, sample size decrease patient FBG, PPBG, HbA1c, TC and LDL-C levels,
or follow-up period, were poor. Furthermore, non-Indian and increase their HDL-C.
patients might benefit from yoga more than Indian patients. Several systematic reviews focusing on yoga for adult patients
with type 2 diabetes mellitus have been published33–36.
Meta-analyses of secondary outcomes Although differences between our meta-analysis and these pre-
The aggregated results suggested that the WMDs were –0.47% vious studies can be noted, our principal findings are consistent
(95% CI -0.87 to -0.07; P = 0.02; P for heterogeneity with the published results. Three studies carried out by Innes
<0.00001; I2 = 82%) for HbA1c (Figure 3a), -17.38 mg/dL et al.33–35 were mainly narrative reviews. Although a recent sys-
(95% CI -27.88 to -6.89; P = 0.001; P for heterogeneity = 0.73; tematic review34 also meta-analyzed several clinical endpoints,
I2 = 0%) for PPBG (Figure 3b), -18.50 mg/dL (95% CI -29.88 including glucose control, lipid levels and body composition,
to -7.11; P = 0.001; P for heterogeneity = 0.003; I2 = 75%) for only studies reporting significant changes were included in that
TC (Figure 4), -12.95 mg/dL (95% CI -18.84 to -7.06; work. We believe that pooled results are not suitable for

ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd J Diabetes Investig Vol. 8 No. 2 March 2017 203
Table 1 | Characteristics of randomized controlled trials included in the meta-analysis

204
First author, Study population Study group Mean age, Form or style (I/C) Yoga protocol Duration Outcomes Study design/
Cui et al.

year and country (sample size) years (I/C) Jadad score


Intervention Control group
group

Gordon, 2008, 154 patients Yoga (77); 64.0/63.6 Hatha yoga Usual care (a 1 class/week, 6 months FBG, RCT/4
2008, Cuba without Control (77) (pranayamas, treatment plan 2-h class Lipid,
ORIGINAL ARTICLE

complications or dynamic warm-up as per their HbA1c


malnutrition, exercises, asanas, doctors, no
trained for T2DM and savasana) active exercise)
self-care; 81% F
Habibi, 2013, 26 female patients Yoga (16); Age range: Asana and Standard care 3 sessions/week, 3 months FBG RCT/2
Iran without taking Control (10) 45-60 pranayama 75 min/session

J Diabetes Investig Vol. 8 No. 2 March 2017


insulin exercise
Jyotsna, 2014, 120 patients with Yoga (64); 49.92/47.25 Sudarshan Kriya Standard 3-day group training 6 months FBS, RCT/3
India lifestyle Control (56) Yoga + standard treatment followed by PPBG,
modification and treatment classes 1x/week HbA1c
oral antidiabetic and daily home
medication practice with a
total of 25–35 min
Monro, 1992, UK 21 patients with Yoga (11); Age range: Yoga classes Standard care 1-2 classes/wk + 3 months FBG, RCT/2
taking Control (10) 45-67 (pranayama, (continuing 90 min, 1–5 times/ HbA1c
medication (13) shavasana and on medication, wk at home
or on diet control asanas) + standard diet)
alone (8) care
Nagarathna, 277 patients with Yoga (141); 53.46/51.38 Integrated yoga Physical 1 h/day, 5 days/week 9 months Lipid, FBG, RCT/4
2012, India stable dose of Control (136) (yogasanas, exercises and for 12 weeks, and PPBG,
oral hypoglycemic pranayama, life style then one 2 h HbA1c
agents or insulin meditation and education. class/week and 1 h
for at least 3 wks; lectures on yogic daily home
31% F life style) practice
Pardasany, 2010, 30 patients Yoga (15); Age range: Hatha yoga Oral 3 times/week 3 months FBG, RCT/2
India taking Control (15) 40-60 (asanas and hypoglycemic PPBG,
hypoglycemic pranayamas) medications Lipid,
medications; HbA1c
38% F
Shantakumari, 100 patients with Yoga (50); 45.51/44.46 Asana, pranayama Standard Daily for 1 h 3 months FBG, RCT/2
2013,2012, India hypertension and Control (50) and meditation + treatment (oral duration PPBG,
dyslipidemia; standard hypoglycemic Lipid,
48% F treatment drugs)
Subramaniyan, 20 adult males Yoga (10); Age range of Yogic exercises Brisk walking + 60 min daily 15 days FBG RCT/3
2012, India patients Control (10) 55% patients: routine between 6AM and
31-40 medicines 7AM for 15
consecutive days
http://onlinelibrary.wiley.com/journal/jdi

ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd
ORIGINAL ARTICLE
http://onlinelibrary.wiley.com/journal/jdi Yoga for T2DM

inclusion in the present study because, they can lead to selec-


Study design/

F, female; FBG, fasting blood glucose; FBS, fasting blood sugar; HbA1c, glycosylated hemoglobin A1c; I/C, intervention/control; RCT, randomized controlled trial; PPBG, postprandial blood
Jadad score
tion bias, and affect the objectivity and authenticity of our find-
ings. Additionally, another previous systematic review enrolling
RCT/3

RCT/3
just five RCTs with a total of 362 participants was published in
200836. In comparison with that review, the present meta-analy-
Outcomes

sis included 12 RCTs with a total of 864 patients. Considering

HbA1c
Lipid,
HbA1c

the limited data on the topic, we combined existing RCTs to

FBG,
increase the sample size, strengthen our analyses and produce
more robust results.

3 months
3 months

The present results showed that yoga significantly decreased


Duration

FBG, PPBG, HbA1c, TC and LDL-C levels, and increased


HDL-C in patients with type 2 diabetes mellitus. Significant
heterogeneity was noted during our analyses of FBG and
45–60 min/session

HbA1c. Given that we specified the primary end-point was


FBG, sensitivity and subgroup analyses were carried out to
6 days a week,
Yoga protocol

90-min class
Twice-weekly,

explore the potential sources of heterogeneity for FBG. We


found that exclusion of each of the RCTs considered in this
work did not resolve the heterogeneity issue or materially alter
the overall combined FBG. We thus believe that the hetero-
geneity observed across trials could be viewed as a result of
healthy lifestyle

clinical and methodological differences. Subgroup analyses were


and exercise)
Control group

Intervention

carried out to investigate the impact of various exclusion crite-


Educational

(general

ria according to sample size, Jadad score, duration and region.


Wait list

The overall combined effects of the trials, regardless of their


quality, sample size or follow-up period, were poor. Further-
more, non-Indian patients might benefit from yoga more than
gentle stretching

yoga asanas and


Form or style (I/C)

Indian patients. The exact reason is still unknown, and it might


pranayama +

be related to racial differences, and different diet and lifestyle


(pranayama,

intervention
Individualized
and asanas)

educational
Yoga classes
Intervention

habit, and also might be derived from the limited data or other
related bias, such as the existing heterogeneity. Thus, we believe
group

that robust, well-designed and larger-scale trials should be car-


ried out to substantiate the long-term effects of yoga in type 2
diabetes mellitus patients, especially those who are not from
India.
Total mean
Mean age,
years (I/C)

age: 60

65.8/64.4

Combining the present results with those reported in the


related literature, the following considerations might help direct
future clinical research on the effects of yoga on type 2 diabetes
mellitus management. First, exercise is a key factor for diabetes
(sample size)
Study group

Control (30)

Control (30)

management. As the optimal exercise form and appropriate


Yoga (29);

Yoga (27);

exercise parameters for type 2 diabetes mellitus patients are


unknown, the development of exercise regimens for these
patients seems to be warranted. Second, the aspects of yoga that
benefit patients with type 2 diabetes mellitus remain unknown,
glucose; T2DM, type 2 diabetes mellitus.
patients; 36.8% F
receiving advice
Study population

healthy lifestyle
and leaflets on

and objective outcome measurements, such as peripheral nerve


without taking

and exercise;

modulation, quality of life, blood pressure, overall survival,


insulin but
59 patients

57 elderly

inflammatory mediators and immune cell function, especially at


61% F

the cellular and molecular levels, are not carried out in most
studies. Therefore, further research should focus on improving
Table 1 (Continued)

measurement modalities to better address potential mechanisms


year and country

and obtain more reliable evidence of the role of yoga-based


Skoro-Kondza,

Vaishali, 2012,

training in type 2 diabetes mellitus patients. Third, the follow-


First author,

2009, UK

up periods of the RCTs included in the present study ranged


India

from 15 days to 9 months, and the long-term effects of yoga


remain unknown. Most of the RCTs included in the present

ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd J Diabetes Investig Vol. 8 No. 2 March 2017 205
ORIGINAL ARTICLE
Cui et al. http://onlinelibrary.wiley.com/journal/jdi

Yoga Control Mean Difference Mean Difference


Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Gordon 2008 –62.82 77.01 77 –15.84 72.11 77 10.9% –46.98 [–70.54, –23.42]
Habibi 2013 –29.38 51.2 16 13.5 39.3 10 8.0% –42.88 [–77.85, –7.91]
Jyotsna 2014 5.85 29.35 64 4.05 27.85 56 14.6% 1.80 [–8.44, 12.04]
Monro 1992 –10.8 28.8 11 21.6 32.4 10 10.2% –32.40 [–58.72, –6.08]
Nagarathna 2012 –9.64 43.35 141 –5.11 39.98 136 14.7% –4.53 [–14.35 ,5.29]
Pardasany 2010 –23 28.64 15 0.4 39.05 15 10.7% –23.40 [–47.91, 1.11]
Shantakumari 2012 –29.23 57.84 50 –5.2 69.58 50 10.5% –24.03 [–49.11, 1.05]
Subramaniyan 2012 –36.5 42.15 10 –19.3 61.37 10 5.8% –17.20 [–63.34, 28.94]
Vaishali 2012 –47.83 15.64 27 –10.8 21.97 30 14.7% –37.03 [–46.86, –27.20]

Total (95% Cl) 411 394 100.0% –23.72 [–37.78, –9.65]


Heterogeneity: Tau2 = 326.49; Chi2 = 45.26, df = 8 (P < 0.00001); I2 = 82%
–50 –25 0 25 50
Test for overall effect: Z = 3.30 (P = 0.0010)
Favors yoga Favors control

Figure 2 | Forest plots of evaluating the effect of yoga on fasting blood glucose.

Table 2 | Subgroup analyses based on various exclusion criteria for fasting blood glucose

Various exclusion criteria n (N) WMDs, mg/dL (95% CI) P-value I2 (%) Pheterogeneity

All included trials38–46 805 (9) -23.72 (-37.78 to -9.65) 0.001 82 <0.00001
Jadad scores ≥3 628 (5) -19.96 (-40.02 to 0.09) 0.05 90 <0.00001
Jadad scores ≤2 177 (4) -28.82 (-42.29 to -15.36) <0.0001 0 0.80
Sample sizes >60 651 (4) -15.16 (-32.37 to 2.04) 0.08 81 0.001
Sample sizes ≤60 154 (5) -34.73 (-42.97 to -26.50) <0.00001 0 0.77
Duration >3 months 551 (3) -13.19 (-32.99 to 6.60) 0.19 86 0.001
Duration ≤3 months 254 (6) -33.69 (-41.51 to -25.87) <0.00001 0 0.78
Region (India) 604 (6) -16.70 (-33.15 to -0.25) 0.05 86 <0.00001
Region (non-India) 201 (3) -40.97 (-56.66 to -25.28) <0.00001 0 0.72

CIs, confidence intervals; n, number of patients; N, number of trials; WMDs, weighted mean differences.

(a) Yoga Control Mean Difference Mean Difference


Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Gordon 2008 –0.14 2.07 77 0.86 1.79 77 13.7% –1.00 [–1.61, –0.39]
Jyotsna 2014 –0.02 1.23 64 –0.36 1.34 56 15.9% 0.34 [–0.12, 0.80]
Monro 1992 –1.56 1.8 11 0.2 1.6 10 5.5% –1.76 [–3.21, –0.31]
Nagarathna 2012 –1.21 2.79 141 –0.04 3.91 136 11.1% –1.17 [–1.97, –0.37]
Pardasany 2010 –0.24 0.44 15 0.01 0.31 15 18.5% –0.25 [–0.52, 0.02]
Skoro-Kondza 2009 –0.02 0.55 29 –0.07 0.3 30 19.0% 0.05 [–0.18, 0.28]
Vaishali 2012 –1.16 0.81 27 –0.38 0.88 30 16.3% –0.78 [–1.22, –0.34]

Total (95% Cl) 364 354 100.0% –0.47 [–0.87, –0.07]


Heterogeneity: Tau2 = 0.21; Chi2 = 33.30, df = 6 (P < 0.00001); I2 = 82%
–2 –1 0 1 2
Test for overall effect: Z = 2.32 (P = 0.02)
Favors yoga Favors control

(b) Yoga Control Mean Difference Mean Difference


Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Jyotsna 2014 –4.67 45.04 64 14.1 47.78 56 39.6% –18.77 [–35.45, –2.09]
Nagarathna 2012 –26.83 71.45 141 –15.42 66.42 136 41.8% –11.41 [–27.65, 4.83]
Pardasany 2010 –44.34 61.48 15 –11.54 69.76 15 5.0% –32.80 [–79.86, 14.26]
Shantakumari 2012 –31.57 69.82 50 –5.54 75.06 50 13.6% –26.03 [–54.44, 2.38]

Total (95% Cl) 270 257 100.0% –17.38 [–27.88, –6.89]


Heterogeneity: Tau2 = 0.00; Chi2 = 1.31, df = 3 (P = 0.73); I2 = 0%
–200 –100 0 100 200
Test for overall effect: Z = 3.25 (P = 0.001)
Favors yoga Favors control

Figure 3 | Forest plots of evaluating the effect of yoga on (a) glycosylated hemoglobin A1c and (b) postprandial blood glucose.

study were not blinded. Considering that blinding prevents bias Compared with previous reviews, our meta-analysis was car-
and protects the sequence after allocation37, appropriate blind- ried out in accordance with Preferred Reporting Items for Sys-
ing, such as blind-outcome assessments, should be carried out. tematic Reviews and Meta-Analyses guidelines and the

206 J Diabetes Investig Vol. 8 No. 2 March 2017 ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd
ORIGINAL ARTICLE
http://onlinelibrary.wiley.com/journal/jdi Yoga for T2DM

Yoga Control Mean Difference Mean Difference


Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
4.1.1 Total cholesterol
Gordon 2008 –2.32 53.97 77 28.62 48.32 77 17.4% –30.94 [–47.12, –14.76]
Nagarathna 2012 –20.66 41.85 141 –15.75 43.5 136 22.2% –4.91 [–14.97, 5.15]
Pardasany 2010 –11.67 17.84 15 4 20.34 15 19.4% –15.67 [–29.36, –1.98]
Shantakumari 2013 –25.32 33.09 50 9.49 36.36 50 19.4% –34.81 [–48.44, –21.18]
Vaishali 2012 –34.2 23.51 27 –23.9 17.57 30 21.6% –10.30 [–21.17, 0.57]
Subtotal (95% Cl) 310 308 100.0% –18.50 [–29.88, –7.11]
2 2 2
Heterogeneity: Tau = 125.57; Chi = 16.32, df = 4 (P = 0.003); I = 75%
Test for overall effect: Z = 3.18 (P = 0.001)

4.1.2 LDL-C
Gordon 2008 –0.08 52.04 77 0.17 44.61 77 11.7% –0.25 [–15.56, 15.06]
Nagarathna 2012 –11.27 34.76 141 –0.87 36.91 136 25.8% –10.40 [–18.85, –1.95]
Pardasany 2010 –8.53 12.72 15 5.13 16.18 15 20.2% –13.66 [–24.08, –3.24]
Shantakumari 2013 –24.23 34.72 50 0.49 29.85 50 15.5% –24.72 [–37.41, –12.03]
Vaishali 2012 –21.04 12.71 27 –7.44 18.39 30 26.8% –13.60 [–21.74, –5.46]
Subtotal (95% Cl) 310 308 100.0% –12.95 [–18.84, –7.06]
2 2 2
Heterogeneity: Tau = 16.37; Chi = 6.34, df = 4 (P = 0.18); I = 37%
Test for overall effect: Z = 4.31 (P <0.0001)

4.1.3 Triglycerides
Gordon 2008 –9.74 961.79 77 7.97 957.55 77 0.3% –17.71 [–320.85, 285.43]
Nagarathna 2012 –26.82 76.28 141 –29.48 94.62 136 32.4% 2.66 [–17.62, 22.94]
Shantakumari 2013 –21.77 41.15 50 25.17 119.25 50 17.3% –46.94 [–81.91, –11.97]
Vaishali 2012 –18.6 15.05 27 –8.07 19.97 30 50.0% –10.53 [–19.66, –1.40]
Subtotal (95% Cl) 295 293 100.0% –12.57 [–29.91, 4.76]
Heterogeneity: Tau = 134.72; Chi = 5.79, df = 3 (P = 0.12); I2 = 48%
2 2

Test for overall effect: Z = 1.42 (P = 0.16)

–50 –25 0 25 50
Favors yoga Favors control
Test for subgroup differences: Chi2 = 0.75. df = 2 (P = 0.69). I2 = 0%

Figure 4 | Forest plots of evaluating the effect of yoga on total cholesterol, low-density lipoprotein cholesterol (LDL-C), and triglyceride.

Yoga Control Mean Difference Mean Difference


Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Gordon 2008 0.03 16.97 77 –0.02 14.87 77 4.2% 0.05 [–4.99, 5.09]
Nagarathna 2012 3.13 14.13 141 –0.95 13.75 136 9.5% 4.08 [0.80, 7.36]
Shantakumari 2013 2.52 9.65 50 –1.1 11.3 50 6.2% 3.62 [–0.50, 7.74]
Vaishali 2012 5.85 1.08 27 1.24 1.59 30 80.0% 4.61 [3.91, 5.31]

Total (95% Cl) 295 293 100.0% 4.30 [3.25, 5.36]


Heterogeneity: Tau2 = 0.24; Chi2 = 3.33, df = 3 (P = 0.34); I2 = 10%
–4 –2 0 2 4
Test for overall effect: Z = 7.99 (P < 0.00001)
Favors control Favors yoga

Figure 5 | Meta-analysis of evaluating the effect of yoga on high-density lipoprotein cholesterol.

50 Cochrane Collaboration, which is one of its main strengths.


Another major strength is that we enrolled well-designed RCTs
with relatively large sample sizes and performed subgroup anal-
0
yses according to various exclusion criteria, including sample
size, Jadad score, duration and region, thereby improving the
WMD

critical significance of the present findings for clinical practice.


When interpreting the results, several limitations should be
–50 taken into account: (i) different characteristics of study partici-
pants, yoga forms and protocols, and exercise durations are the
most crucial confounders of the RCTs, and could result in risk
–100 of bias and heterogeneity; (ii) except for three RCTs17,18,28, all
0 10 20 30 other RCTs surveyed were not blinded, which could result in
SE of WMD performance and detection bias; (iii) considering that 12 RCTs
with a wide variation in sample size were incorporated into our
Figure 6 | Publication bias. Begg’s funnel plot of pseudo 95% confi- analysis, the effects of overestimation of treatment efficiency
dence intervals. SE, standard error; WMD, weighted mean differences.
may be significant; and (iv) missing and unpublished data, as

ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd J Diabetes Investig Vol. 8 No. 2 March 2017 207
ORIGINAL ARTICLE
Cui et al. http://onlinelibrary.wiley.com/journal/jdi

well as the exclusion of non-English language studies, could P3 event related evoked potential (ERP). Indian J Med Res
result in effect size bias. 2010; 131: 636–640.
In sum, based on the evidence, yoga significantly reduces 13. Popli U, Subbe CP, Sunil K. Research letter-the role of yoga
FBG levels and alters other significant clinical outcomes in as a lifestyle modification in treatment of diabetes mellitus:
patients with type 2 diabetes mellitus. These results support the results of a pilot study. Altern Ther Health Med 2014; 20: 24–
idea that yoga-based training is a possible alternative exercise 26.
for type 2 diabetes mellitus management. However, given the 14. Jyotsna VP, Dhawan A, Sreenivas V, et al. Completion
aforementioned limitations and potential bias of our analyses, report: Effect of Comprehensive Yogic Breathing program
more large-scale and robust RCTs must be carried out to verify on type 2 diabetes: A randomized control trial. Indian J
our current findings and substantiate the long-term effects of Endocrinol Metab 2014; 18: 582–584.
yoga in type 2 diabetes mellitus patients. 15. Skoro-Kondza L, Tai SS, Gadelrab R, et al. Community based
yoga classes for type 2 diabetes: an exploratory randomised
DISCLOSURE controlled trial. BMC Health Serv Res 2009; 9: 33.
The authors declare no conflict of interest. 16. Shantakumari N, Sequeira S, El deeb R. Effects of a yoga
intervention on lipid profiles of diabetes patients with
REFERENCES dyslipidemia. Indian Heart J 2013; 65: 127–131.
1. Ali S, Davies MJ, Brady EM, et al. Guidelines for managing 17. Gordon LA, Morrison EY, McGrowder DA, et al. Effect of
diabetes in Ramadan. Diabet Med 2016. doi: 10.1111/ exercise therapy on lipid profile and oxidative stress
dme.13080. indicators in patients with type 2 diabetes. BMC
2. Yang L, Shao J, Bian Y, et al. Prevalence of type 2 diabetes Complement Altern Med 2008; 8: 21.
mellitus among inland residents in China (2000–2014): a 18. Gordon L, Morrison EY, McGrowder DA, et al. Changes in
meta-analysis. J Diabetes Investig 2016; 7: 845–852. clinical and metabolic parameters after exercise therapy in
3. Joseph JJ, Golden SH. Type 2 diabetes and cardiovascular patents with type 2 diabetes. Arch Med Sci 2008; 4: 427–437.
disease: what next? Curr Opin Endocrinol Diabetes Obes 19. Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane
2014; 21: 109–120. Collaboration’s tool for assessing risk of bias in randomised
4. American Diabetes Association. Standards of medical care in trials. BMJ 2011; 343: d5928.
diabetes–2014. Diabetes Care 2014; 37(Suppl 1): S14–S80. 20. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA
5. Colberg SR, Sigal RJ, Fernhall B, et al. Exercise and type 2 statement for reporting systematic reviews and meta-
diabetes: the American College of Sports Medicine and the analyses of studies that evaluate healthcare interventions:
American Diabetes Association: joint position statement. explanation and elaboration. BMJ 2009; 339: b2700.
Diabetes Care 2010; 33: e147–e167. 21. Jadad AR, Moore RA, Carroll D, et al. Assessing the quality
6. Temelkova-Kurktschiev T, Stefanov T. Lifestyle and genetics of reports of randomized clinical trials: is blinding
in obesity and type 2 diabetes. Exp Clin Endocrinol Diabetes necessary? Control Clin Trials 1996; 17: 1–12.
2012; 120: 1–6. 22. Kjaergard LL, Villumsen J, Gluud C. Reported methodologic
7. Lin CC, Li CI, Liu CS, et al. Impact of lifestyle-related factors quality and discrepancies between large and small
on all-cause and cause-specific mortality in patients with randomized trials in meta-analyses. Ann Intern Med 2001;
type 2 diabetes: the Taichung Diabetes Study. Diabetes Care 135: 982–989.
2012; 35: 105–112. 23. DerSimonian R, Laird N. Meta-analysis in clinical trials.
8. Liu XC, Pan L, Hu Q, et al. Effects of yoga training in Control Clin Trials 1986; 7: 177–188.
patients with chronic obstructive pulmonary disease: a 24. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring
systematic review and meta-analysis. J Thorac Dis 2014; 6: inconsistency in meta-analyses. BMJ 2003; 327: 557–560.
795–802. 25. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-
9. Raub JA. Psychophysiologic effects of Hatha Yoga on analysis detected by a simple, graphical test. BMJ 1997; 315:
musculoskeletal and cardiopulmonary function: a literature 629–634.
review. J Altern Complement Med 2002; 8: 797–812. 26. Habibi N, Farsani Z, Yazdani B, et al. The influence of yoga
10. Chandler K. The emerging field of yoga therapy. Hawaii on risk profiles programs in women with diabetes type II.
Med J 2001; 60: 286–287. Adv Environ Biol 2013; 7: 550–555.
11. Singh S, Kyizom T, Singh KP, et al. Influence of pranayamas 27. Monro R, Power J, Coumar A, et al. Yoga therapy for NIDDM:
and yoga-asanas on serum insulin, blood glucose and lipid a controlled trial. Complement Med Res 1992; 6: 66–68.
profile in type 2 diabetes. Indian J Clin Biochem 2008; 23: 28. Nagarathna R, Usharani MR, Rao AR, et al. Efficacy of yoga
365–368. based life style modification program on medication score
12. Kyizom T, Singh S, Singh KP, et al. Effect of pranayama & and lipid profile in type 2 diabetes-a randomized control
yoga-asana on cognitive brain functions in type 2 diabetes- study. Int J Diabetes Dev Ctries 2012; 32: 122–130.

208 J Diabetes Investig Vol. 8 No. 2 March 2017 ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd
ORIGINAL ARTICLE
http://onlinelibrary.wiley.com/journal/jdi Yoga for T2DM

29. Vaishali K, Kumar KV, Adhikari P, et al. Effects of yoga-based 38. Rennard SI, Calverley PM, Goehring UM, et al. Reduction of
program on glycosylated hemoglobin level serum lipid exacerbations by the PDE4 inhibitor roflumilast–the
profile in community dwelling elderly subjects with chronic importance of defining different subsets of patients with
type 2 diabetes mellitus–a randomized controlled trial. Phys COPD. Respir Res 2011; 12: 18.
Occup Ther in Geriatr 2012; 30: 22–30. 39. Rabe KF, Bateman ED, O’Donnell D, et al. Roflumilast–an
30. Shantakumari N, Sequeira S, Eldeeb R. Effect of a yoga oral anti-inflammatory treatment for chronic obstructive
intervention on hypertensive diabetic patients. J Adv Intern pulmonary disease: a randomised controlled trial. Lancet
Med 2012; 1: 60–63. 2005; 366: 563–571.
31. Subramaniyan TG, Subramaniyan N, Chidambaram M. Brisk 40. Calverley PM, Sanchez-Toril F, McIvor A, et al. Effect of
walking and yoga as adjuvant therapy in management of 1-year treatment with roflumilast in severe chronic
type 2 diabetes mellitus. Int J Stud Res 2012; 2: 43–46. obstructive pulmonary disease. Am J Respir Crit Care Med
32. Pardasany A, Shenoy S, Sandhu JS. Comparing the efficacy 2007; 176: 154–161.
of tai chi chuan and hatha yoga in type 2 diabetes mellitus 41. Lee SD, Hui DS, Mahayiddin AA, et al. Roflumilast in Asian
patients on parameters of blood glucose control and lipid patients with COPD: a randomized placebo-controlled trial.
metabolism. Indian J Physiother Occup Ther 2010; 4: 11–16. Respirology 2011; 16: 1249–1257.
33. Innes KE, Vincent HK. The influence of yoga-based 42. Calverley PM, Rabe KF, Goehring UM, et al. Roflumilast in
programs on risk profiles in adults with type 2 diabetes symptomatic chronic obstructive pulmonary disease: two
mellitus: a systematic review. Evid Based Complement randomised clinical trials. Lancet 2009; 374: 685–694.
Alternat Med 2007; 4: 469–486. 43. Fabbri LM, Calverley PM, Izquierdo-Alonso JL, et al.
34. Innes KE, Selfe TK. Yoga for Adults with Type 2 Diabetes: A Roflumilast in moderate-to-severe chronic obstructive
Systematic Review of Controlled Trials. J Diabetes Res 2016; pulmonary disease treated with longacting
2016: 6979370. bronchodilators: two randomised clinical trials. Lancet
35. de GR Hansen E, Innes KE. The benefits of yoga for adults 2009; 374: 695–703.
with type 2 diabetes: a review of the evidence and call for 44. O’Donnell DE, Bredenbroker D, Brose M, et al. Physiological
a collaborative, integrated research initiative. Int J Yoga effects of roflumilast at rest and during exercise in COPD.
Therap 2013; 23: 71–83. Eur Respir J 2012; 39: 1104–1112.
36. Aljasir B, Bryson M, Al-Shehri B. Yoga Practice for the 45. Turk DC. Clinical effectiveness and cost-effectiveness of
Management of Type II Diabetes Mellitus in Adults: A treatments for patients with chronic pain. Clin J Pain 2002;
systematic review. Evid Based Complement Alternat Med 18: 355–365.
2010; 7: 399–408. 46. Manninen P, Riihimaki H, Heliovaara M, et al. Physical
37. Schulz KF, Grimes DA. Blinding in randomised trials: hiding exercise and risk of severe knee osteoarthritis requiring
who got what. Lancet 2002; 359: 696–700. arthroplasty. Rheumatology (Oxford) 2001; 40: 432–437.

SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Table S1| Additional information reported in all the randomized controlled trials.
Figure S1| Risk-of-bias analysis. (a) Risk-of-bias graph: the authors’ judgments about each risk-of-bias item presented as percent-
ages across all included studies. (b) Risk-of-bias summary: the authors’ judgments about each risk-of-bias item for the each
included studies.

ª 2016 The Authors. Journal of Diabetes Investigation published by AASD and John Wiley & Sons Australia, Ltd J Diabetes Investig Vol. 8 No. 2 March 2017 209