Meta-analysis of Circulating Adiponectin, Visfatin, and Ghrelin Levels in Patients with Systemic Lupus Erythematosus

Young Ho Lee; Gwan Gyu Song

doi:10.4078/jrd.2017.24.2.99

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Lee and Song: Meta-analysis of Circulating Adiponectin, Visfatin, and Ghrelin Levels in Patients with Systemic Lupus Erythematosus

Original Article

J Rheum Dis 2017;24(2):99-107.

Published online: 31 October 2017

DOI: https://doi.org/10.4078/jrd.2017.24.2.99

Meta-analysis of Circulating Adiponectin, Visfatin, and Ghrelin Levels in Patients with Systemic Lupus Erythematosus

Young Ho Lee, Gwan Gyu Song

Division of Rheumatology, Department of Internal Medicine, Korea University Medical Center, Korea University College of Medicine, Seoul, Korea

Corresponding to: Young Ho Lee, Division of Rheumatology, Department of Internal Medicine, Korea University Medical Center, Korea University College of Medicine, 73, Inchon-ro, Seongbuk-gu, Seoul 02841, Korea. E-mail: lyhcgh@korea.ac.kr

Received 6 January 201724 February 2017 Accepted 12 April 2017

This is a Free Access article, which permits unrestricted non-commerical use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Objective

To evaluate the association between circulating adiponectin, visfatin, and ghrelin levels and systemic lupus erythematosus (SLE).

Methods

We conducted a meta-analysis to compare serum/plasma adiponectin, visfatin, and ghrelin levels in patients with SLE to those of healthy controls.

Results

Eleven articles (822 patients with SLE and 676 controls) were included in the meta-analysis. The meta-analysis showed that the adiponectin level was significantly higher in the SLE group than in the control group (standardized mean difference [SMD]=0.360, 95% confidence interval [CI]=0.025∼0.695, p=0.035). Stratification according to region showed that high adiponectin levels were associated with SLE in the Western population (SMD=0.225, 95% CI=0.024∼0.426, p=0.028), but not in the South American population. A subgroup analysis that adiponectin level is significantly higher in the SLE group than in the control after adjustment for age, sex, body mass index, large sample size (n>100); and mean age>40 years (SMD=0.492, 95% CI=0.065∼0.920, p=0.024; SMD=0.492, 95% CI=0.065∼0.920, p=0.024; SMD=0.429, 95% CI=0.124∼0.733, p=0.006, respectively). Stratification by region showed significantly increased visfatin and ghrelin levels in the SLE group in Western and South American populations.

Conclusion

Our metaanalysis demonstrated that circulating adiponectin, visfatin, and ghrelin levels are significantly higher in SLE.

Keywords: Adiponectin, Visfatin, Ghrelin, Systemic lupus erythematosus

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Figure 1.

Meta-analysis of the relationship between adiponectin and systemic lupus erythematosus (SLE) in all study subjects (A) and each study region (B). Std diff: standardized difference, CI: confidence interval.

Figure 2.

Meta-analysis of the relationship between visfatin (A) or ghrelin (B) levels and systemic lupus erythematosus (SLE) in each study region. Std diff: standardized difference, CI: confidence interval.

Figure 3.

Funnel plot of studies that examined the relationship between adiponectin and systemic lupus erythematosus (Egger regression p-value=0.894). Std diff: standardized difference, Std err: standardized error.

Table 1.

Characteristics of individual studies included in the meta-analysis

Study	Country	Patient		Age, yr		BMI, kg/m²		Disease duration, yr	Adipokines	Adjustment^*	Quality score
Study	Country	SLE	Control	SLE	Control	SLE	Control	Disease duration, yr	Adipokines	Adjustment^*	Quality score
Barbosa, 2015 [12]	Brazil	52	33	33.4±9.4	32.5± 10.5	23.8+3.5	21.8+2.5	7.5	A	Age	8
McMahon-1, 2014 [13]	USA	142	72	39.6±13.5	40.5±11.8	25.7+5.9	23.7+5.1	11.4 + 8.0	A	Age	7
McMahon-2, 2014 [13]	USA	61	28	51.9±10.2	54.6± 10.1	28.0+7.1	25.3+5.8	14.9+11.4	A	Age	7
Vadacca, 2013 [14]	Italy	60	29	42.26±40.54	45.69± 11.57	25.2+4	24+4.6	10+5	A	Age, gender, BMI	9
Reynolds, 2010 [15]	USA	119	71	42.6±41.3	41.3 + 11.9	25.9+6.3	24.8+5.3	NA	A	Age, gender, BMI	8
De Sanctis, 2009 [16]	Venezuela	60	60	36±6	32±12	24+2.7	22+2.0	NA	A, V, G	NA	6
Chung, 2009 [17]	USA	109	78	40.2±11.5	40.5 + 12.0	29.2+7.5	27.0+6.0	8.2+7.3	A, V	Age, gender	9
Al-1, 2009 [18]	Canada	21	21	14.43±2.20	10.04 + 3.48	24.07+3.57	NA	NA	A, G	Gender	7
Al-2, 2009 [18]	Canada	84	56	14.32±2.67	10.04 + 3.48	23.76+5.30	NA	NA	A, G	Gender	7
Sada, 2006 [19]	Japan	37	80	44±15	44±6	22.1+3.5	22.2+3.2	9.4+7.1	A	Age, gender, BMI	8
Rovin-1, 2005 [20]	USA	18	39	47.9±7.21	33.5 + 10.6	32.6 + 6.36	25.9 + 5.09	NA	A	NA	6
Rovin-2, 2005 [20]	USA	18	39	34.6±7.64	33.5 + 10.6	29.5 + 10.62	25.9 + 5.09	NA	A	NA	6
Ozgen, 2011 [21]	Turkey	26	29	34.2±11.0	38.0+10.3	23.2+4.4	25.9+4.7	3.8 + 3.9	V	BMI	7
Kim, 2010 [22]	Korea	15	80	34.6±6.7	27.4+6.6	NA	NA	47.41 +33.66^*	G	Gender, BMI	8

Values are presented as number and mean±standard deviation. SLE: systemic lupus erythematosus, BMI: body mass index, NA: not available, A: adiponectin, V: visfatin, G: ghrelin, USA: United States of America.

^* Matched or similar factors, or no statistical difference in variables between the SLE and control groups

^† months.

Table 2.

Meta-analysis of the adiponectin levels in patients with SLE compared to healthy controls

Group	Population	Number of study	Test of association			Test of heterogeneity
Group	Population	Number of study	SMD^*	95% CI	p-value	Model	p-value	I²
All	Overall	12	0.360	0.025∼0.695	0.035	R	0.000	88.1
Region	Western	9	0.225	0.024∼0.426	0.028	R	0.018	56.6
	South American	2	0.746	−1.571∼3.062	0.528	R	0.000	98.2
	Asian	1	0.993	0.583∼1.403	2.1×10⁻⁶	NA	NA	NA
Matched variables^†	Yes	9	0.273	0.015∼0.531	0.008	R	0.000	71.4
	No	3	0.632	−0.808∼2.072	0.390	R	0.000	95.6
Sample size, n	<100	4	0.082	−0.386∼0.550	0.731	R	0.010	73.3
	≥100	8	0.492	0.065∼0.920	0.024	R	0.000	90.6
Mean age, yr	<40	6	0.307	−0.336∼0.950	0.349	R	0.000	93.0
	≥40	6	0.429	0.124∼0.733	0.006	R	0.003	72.1

SLE: systemic lupus erythematosus, SMD: standard mean difference, CI: confidence interval, R: random effects model, NA: not available.

^* Magnitude of the Cohen's d effect size (SMD) (0.2∼0.5, small effect; 0.5∼0.8, medium effect; and ≥0.8, large effect)

^† age, sex, or body mass index.

Table 3.

Meta-analysis of visfatin and ghrelin levels in patients with SLE compared to healthy controls

Group	Population	Number of study	Test of association			Test of heterogeneity
Group	Population	Number of study	SMD^*	95% CI	p-value	Model	p-value	I²
Visfatin	Overall	3	0.451	−0.000∼0.903	0.050	R	0.018	75.2
	Western	1	0.365	0.072∼0.658	0.015	NA	NA	NA
	South American	1	0.892	0.517∼1.267	3.2×10⁻⁶	NA	NA	NA
	Middle Eastern	1	0.025	−0.505∼0.554	0.927	NA	NA	NA
Ghrelin	Overall	4	0.611	−0.383∼1.605	0.228	R	0.000	94.3
	Western	2	0.560	0.258∼0.861	2.7×10⁻⁴	F	0.170	46.9
	South American	1	2.000	1.562∼2.438	<1.0×10⁻⁸	NA	NA	NA
	Asian	1	−0.478	−1.034∼0.077	0.091	NA	NA	NA

SLE: systemic lupus erythematosus, SMD: standard mean difference, CI: confidence interval, R: random effects model, F: fixed effects model, NA: not available.

^* Magnitude of the Cohen's d effect size (SMD) (0.2∼0.5, small effect; 0.5∼0.8, medium effect; and ≥0.8, large effect).

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