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Prevalence of depression and anxiety in systemic lupus erythematosus: a systematic review and meta-analysis

BMC PsychiatryBMC series – open, inclusive and trusted201717:70

https://doi.org/10.1186/s12888-017-1234-1

Received: 30 August 2016

Accepted: 8 February 2017

Published: 14 February 2017

Abstract

Background

Systemic lupus erythematosus (SLE) patients are at high risk for depression and anxiety. However, the estimated prevalence of these disorders varies substantially between studies. This systematic review aimed to establish pooled prevalence levels of depression and anxiety among adult SLE patients.

Methods

We systematically reviewed databases including PubMed, Embase, PsycINFO, and the Cochrane database library from their inception to August 2016. Studies presenting data on depression and/or anxiety in adult SLE patients and having a sample size of at least 60 patients were included. A random-effect meta-analysis was conducted on all eligible data.

Results

A total of 59 identified studies matched the inclusion criteria, reporting on a total of 10828 adult SLE patients. Thirty five and thirteen methods of defining depression and anxiety were reported, respectively. Meta-analyses revealed that the prevalence of major depression and anxiety were 24% (95% CI, 16%-31%, I2 = 95.2%) and 37% (95% CI, 12%–63%, I2 = 98.3%) according to clinical interviews. Prevalence estimates of depression were 30% (95% CI, 22%–38%, I2 = 91.6%) for the Hospital Anxiety and Depression Scale with thresholds of 8 and 39% (95% CI, 29%–49%, I2 = 88.2%) for the 21-Item Beck Depression Inventory with thresholds of 14, respectively. The main influence on depression prevalence was the publication years of the studies. In addition, the corresponding pooled prevalence was 40% (95% CI, 30%–49%, I2 = 93.0%) for anxiety according to the Hospital Anxiety and Depression Scale with a cutoff of 8 or more.

Conclusions

The prevalence of depression and anxiety was high in adult SLE patients. It indicated that rheumatologists should screen for depression and anxiety in their patients, and referred them to mental health providers in order to identify effective strategies for preventing and treating depression and anxiety among adult SLE patients.

Trial registration

Current Meta-analysis PROSPERO Registration Number: CRD 42016044125. Registered 4 August 2016.

Keywords

Depression Anxiety Meta-analysis Systematic review

Background

Systemic lupus erythematosus (SLE) is a multisystem, autoimmune, connective-tissue disorder with frequent psychological comorbidities, of which depression and anxiety are two common manifestations [1, 2]. It has been reported that there were 2 times higher prevalence of depression in SLE patients compared to the general population [3]. In addition, previous study has reported that the anxiety disorders were twice as prevalent among SLE patients as compared to the controls [4]. Depression and anxiety often have profound impacts on SLE patients’ health and well-being including increased incidence of cardiovascular diseases [5], myocardial infarction [6], suicidal ideation [7], physical disability [8], decreased quality of life [9, 10], and a higher risk of premature mortality [11]. Therefore, depression and anxiety may be useful targets for interventions aimed at improving subjective health and quality of life in individuals with SLE. However, current epidemiological evidence found that the prevalence of depression and/or anxiety in SLE patients ranged widely from 2% to 91.7% in different studies [12, 13]. This vast inter-study difference was previously attributed to multiple factors, including study quality, unclear definition of depression or anxiety, diverse screening strategies used across studies [14]. Reliable estimates of depression and anxiety prevalence are important for informing efforts to prevent, treat, and identify causes of depression and anxiety among SLE patients. Recent meta-analyses have estimated the overall prevalence of depression and/or anxiety in rheumatoid arthritis and osteoarthritis patients [14, 15]. There has only been one previous systematic review of psychiatric symptoms in SLE [16]; however, no systematic review was conducted to quantify the prevalence of depression and anxiety in SLE using meta-analysis techniques. Our goal was to address this limitation. The objectives of this systematic review were (i) to establish pooled prevalence levels of depression and anxiety among adult SLE patients; (ii) to provide a summary of the methods used to define depression and anxiety in SLE; and (iii) to explore the impacts of study characteristics on prevalence estimates.

Methods

This systematic review was conducted within the Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) statement [17] and followed a predetermined registered protocol (PROSPERO: CRD42016044125).

Search strategy

A systematic review of published literature in scientific journals that reported on the prevalence of depression and/or anxiety among SLE patients was conducted by two independent reviewers using the following databases from their inception to August 2016: PubMed, Embase, PsycINFO, and the Cochrane database library. The computer-based searches combined terms related to SLE patients and study design with those related to depression or anxiety (see Additional file 1). We conducted citation chasing search strategy with all reference lists of included articles and relevant review papers were considered to identify potentially omitted articles. Finally, we corresponded with the authors for further information if we encountered articles just provided the mean and standard deviation of the depression and/or anxiety assessment scale.

Inclusion and exclusion criteria

Studies were included if they met the following criteria: (i) cross-sectional design, baseline cross-sectional data from a longitudinal study or baseline cross-sectional data from a trial, before group allocation; (ii) used validated methods (clinical interviews or self-report instruments) to assess depression or anxiety; and (iii) the sample size was no less than 60.

Case reports, review articles, animal studies, studies investigating neuropsychiatric syndromes, studies in languages other than English and papers not dealing with SLE patients were excluded. For this meta-analysis, studies using pediatrics sample or screening tools without stating the cut-off thresholds used to detect depression or anxiety were also excluded. Table 2 and Table 3 presented a full list of the eligible methods of detecting depression and anxiety, alongside the numbers of articles utilizing each method and the number of participants assessed.

Data extraction and quality assessment

Two researchers read the relative studies independently by the titles and abstracts to exclude the references which did not met the inclusion criteria. Then, they read full texts in the remaining studies as mentioned above, and determined whether these references included were final studies or not. When multiple publications spanned the years of longitudinal studies, baseline prevalence levels were reported. The following information was independently extracted from each article by other two trained investigators using a standardized form: year, country, mean disease duration, percentage of female participants, sample size, average age of participants, criteria for detection of depression and anxiety, and reported prevalence of depression and/or anxiety. If we encountered multiple publications from the same cohort, we used the data from the most recent or the paper reporting data from the largest number of participants. The methodological quality of each study included in the present meta-analysis was assessed using a modified version of the Newcastle-Ottawa Scale [18]. Studies were judged to be at low risk of bias (≥3 points) or high risk of bias (<3 points). Any disagreements in data extraction and quality assessment were resolved through discussion between the two reviewers or adjudication with a third reviewer.

Outcome measures

The outcomes were major/minor depression and affective/dysthymic/adjustment/anxiety disorder diagnosed with a structured clinical assessment [e.g., Diagnostic and Statistical Manual of Mental Disorders (DSM)-IV or International Classification of Diseases (ICD)-10] or depression and/or anxiety assessed with validated assessment tools [e.g., the Hospital Anxiety and Depression Scale (HADS), the Centre for Epidemiologic Studies Depression Scale (CES-D)] (see Additional file 2).

Statistical analyses

Because random-effects models tended to provide wider confidence intervals (CI) and were preferable in the presence of between-study heterogeneity, we used a random-effects meta-analysis to pool studies reporting the prevalence of depression and/or anxiety in SLE patients [19]. Between-study heterogeneity was assessed by the I2 with thresholds of ≥25%, ≥50% and ≥75% indicating low, moderate and high heterogeneity, respectively [20]. The influence of individual study on the overall prevalence estimate was explored by serially excluding each study in sensitivity analyses. Wherever possible, subgroup analyses were planned by overall study quality, sample size, country of origin and publication year, if there was more than one study in the subgroup. Pearson’s and Spearman’s correlation analyses were used to assess the association between variables and prevalence of depression and anxiety in people with SLE. Funnel plots and Egger’s test were combined to explore the potential publication bias in this meta-analysis [21, 22]. Statistical analyses were performed with STATA version 12.0. Statistical tests were 2-sided and used a significance threshold of P < 0.05.

Results

Search results

Fig. 1 provided the details of the study selection process. The initial search identified a total of 3347 potentially relevant articles. After removal of duplicates, titles and then abstracts were screened for potential eligibility. From this, 121 were considered in the full-text review, of which 59 articles met the inclusion criteria, and a full reference list was presented in Additional file 3. Inter-rater reliability of reviewers regarding study relevancy was high (Kappa = 0.87).
Fig. 1

Search results and study selection

Study characteristics

A summary of the included study characteristics was shown in Table 1. A total of 59 identified studies matched the inclusion criteria, reporting on a total of 10828 adult SLE patients. Twenty took place in North America, 18 in Asia, 12 in Europe, 6 in South America, 1 in Oceania, and 1 in Africa. The median of mean ages was 39 years (range, 30.0-50.1), and the median percentage of females represented in the sample was 93% (range, 75%–100%). In addition, the median number of participants per study was 100 (range, 60–1827), and the median of mean disease duration was 9 years (range, 0.22–16.3). Depression was defined in 35 different ways (Table 2). Seventeen studies assessed for depression using the 21 Item-Beck Depression Inventory (BDI), with sixteen different thresholds were presented in the articles. Thirteen articles used the CES-D; six different cut-off points were presented, and the most commonly used being 16. Twelve used the HADS with a cutoff of 8 or more, and 6 used other screening tools. Ten studies assessed for major depression using diagnostic criteria (DSM or ICD). The most commonly used screening questionnaire to assess anxiety was the HADS, with 10 studies using this screening tool with thresholds of 8. The methods employed to assess depression and anxiety and the frequency of their use were presented in Table 2 and Table 3. When evaluated by Newcastle-Ottawa quality assessment criteria, out of 5 possible points, 2 studies received 5 points, 7 received 4 points, 13 received 3 points, 36 received 2 points, and 1 received 1 point. The details of the assessment of individual studies were shown in Additional file 4.
Table 1

Overview of prevalence studies of mood in SLE patients (N ≥ 60)

Study ID

Country

Disease duration, mean ± SD/median (range)

Women, %

Sample size

Age, mean ± SD/median (range), years

Criteria for detection of anxiety (cutoff)

Anxiety prevalence, %

Criteria for detection of depression (cutoff)

Depression prevalence, %

NOS

Abdul-Sattar 2015

Egypt

10.0 ± 4.6 years

95%

80

30.9 ± 11.7

  

CES-D (>16.7)

43.75

2

Appenzeller 2009

Brazil

64.5 ± 48.5 months

94.6%

167

32.1 ± 11.0

  

21 Item-BDI (≥10)

20.9

2

Bachen 2009

USA

15.4 ± 9.7 years

100%

326

47.9 ± 11.3

DSM-IV

64

DSM-IV

Major depressive disorder: 42.4, dysthymic disorder: 2.9

5

Bogdanovic 2015

Serbia

6.8 ± 2.9 years

100%

60

43.4 ± 12.8

  

21 Item-BDI (≥16/≥20/≥30)

91.7/70/3.3

2

Calderon 2014

Chile

Median: 32.0 (0–243.0) months

100%

82

Median: 36.0 (17.0–64.0)

  

HADS (≥8)

37

2

Cho 2014

South Korea

NS

90.1%

201

41.3 ± 13.2

  

CES-D (≥16)

39.3

3

Chin 1993

Malaysia

4.1 ± 3.5 years

95%

79

31.1 ± 9.1

ICD-9 and DSM-III

7.6

ICD-9 and DSM-III

Major depressive disorder: 6.3, dysthymic disorder: 32.9

2

Da Costa 2005

Canada

13.8 ± 10.1 years

100%

100

45.4 ± 14.0

  

CES-D (≥16)

31

3

Doria 2004

Italy

9.9 ± 6.3 years

87.3%

126

38.9 ± 11.9

HAS (≥6/≥15)

74.6/27

HDS (≥8/≥16)

40.5/2.4

2

Duvdevany 2011

Israel

11.4 ± 9.1 years

88%

100

37.0 ± 11.8

HADS (≥8)

20

HADS (≥8)

37

4

García-Carrasco 2011

Mexico

106.5 ± 85.5 months

100%

106

40.5 ± 12.0

  

CES-D (≥16)

38.8

2

García-Carrasco 2013

Mexico

10.5 ± 7.4 years

100%

105

43.6 ± 11.3

  

CES-D (≥16)

33

2

Greco 2009

USA

16.3 ± 7.0 years

100%

161

50.1 ± 10.0

  

CES-D (≥16)

27

2

Hanly 2015

Canada

5.6 ± 4.8 years

88.9%

1827

35.1 ± 13.3

  

DSM-IV

12.7

4

Harrison 2006

USA

15.3 ± 3.2 years

100%

93

43.3 ± 13.7

  

CES-D (>27)

16.1

2

Huang 2007

China

7.5 ± 6.9 years

91.5%

129

37.4 ± 10.7

HADS (≥8)

32

HADS (≥8)

20

2

Iverson 2002

Canada

NS

NS

103

NS

  

21 Item-BDI (≥17)

39.8

1

Jarpa 2011

Chile

Median: 5.0 (0.1–40.0) years

90.8%

87

Median: 39.0 (16.0–27.0)

DSM-IV

18.1

DSM-IV

Major depressive disorder: 21.7, dysthymic disorder: 4.8

2

Julian 2011

USA

15.8 ± 9.3 years

93%

150

48.8 ± 12.3

  

ICD-10 and DSM-IV

Major depressive disorder: 17, dysthymic disorder: 4, minor depression: 6

3

Jung 2015

Korea

6.8 ± 4.4 years

93%

100

40.6 ± 10.3

  

21 Item-BDI (≥21)

13

2

Katz 2011

USA

13.6 ± 8.5 years

100%

716

48.1 ± 12.6

  

CES-D (≥24)

25

3

Karol 2013

USA

NS

93%

127

38.1 ± 12.3

  

21 Item-BDI (≥18)

41.7

2

Karimifar 2013

Iran

4.1 ± 0.5 years

80%

100

34.8 ± 10.9

  

21 Item-BDI (≥14)

60

2

Kheirandish 2015

Iran

9.0 ± 7.7 years

92.2%

166

33.1 ± 11.1

Cattell questionnaire (≥21)

84.9

21 Item-BDI (≥5/≥30)

64.5/9

2

Kotsis 2014

Greece

13.2 ± 9.1 years

84%

75

44.1 ± 13.3

  

PHQ-9 (≥10)

29.3

2

Kim 2015

USA

12.0 ± 8.0 years

93%

89

39.0 ± 15.0

  

CES-D (≥16)

63

3

Lapteva 2006

USA

13.8 ± 10.2 years

75%

60

41.0 ± 13.0

  

DSM-IV

Major depressive disorder: 16.6

2

Lisitsyna 2014

NS

134.9 ± 8.8 months

85.6%

180

34.6 ± 0.93

  

ICD-10

Major depressive disorder: 24.4, dysthymic disorder: 25.6, adjustment disorders: 18.9

2

Mak 2011

Singapore

54.9 ± 70.7 months

88%

60

40.5 ± 12.9

HADS (≥8)

38

HADS (≥8)

22

2

Maneeton 2013

Thailand

6.1 ± 4.8 years

98%

62

31.8 ± 9.0

HAS (≥14)

37.1

HDS (≥11)

45.2

2

Mirbagher 2016

Iran

8.3 ± 3.8 years

100%

77

36.5 ± 10.1

HADS (≥8)

71.4

HADS (≥8)

46.1

3

Monaghan 2007

Australia

10.2 ± 8.7 years

97%

60

44.4 ± 12.2

HADS (≥8)

44

HADS (≥8)

36

3

Montero-Lo’pez 2016

Spain

0.2 ± 0.7 years

100%

97

38.6 ± 9.3

SCL-90-R

4.1

SCL-90-R

5.2

2

Nery 2008

Brazil

9.8 ± 6.5 years

100%

71

34.8 ± 10.1

SCID for DSM-IV

46.5

SCID for DSM-IV

Major depressive disorder: 40.8

2

Neville 2014

Canada

10.2 ± 9.5 years

92.4%

612

46.8 ± 16.7

  

PHQ-2 (≥3)

28.1

4

Palagini 2014

Italy

15.0 ± 8.0 years

100%

81

43.6 ± 11.2

SAS (>44)

17.3

21 Item-BDI (≥11)

34.6

3

Panopalis 2010

USA

13.8 ± 8.9 years

91%

807

47.6 ± 13.1

  

CES-D (≥16)

38.5

5

Pettersson 2015

Sweden

Median: 12.0 years

92%

305

Median: 48

HADS (≥8)

34

HADS (≥8)

51

4

Postal 2016

Brazil

Median: 9.0 (0–33.0) years

96.7%

153

Median: 30.0 (10.0–62.0)

21 Item-BAI (≥8/≥16/≥26)

60.7/43.1/18.3

21 Item-BDI (≥14/≥20/≥29)

45.7/30.7/18.9

2

Radhakrishan 2011

India

NS

100%

100

18-60

SCID for DSM-IV

51

SCID for DSM-IV

Major depressive disorder: 46, adjustment disorder: 21, dysthymic disorder: 9

2

Roebuck-Spencer 2006

USA

13.8 ± 10.2 years

80%

60

41.3 ± 12.8

  

21 Item-BDI (≥14)

20

2

Segal 2012

USA

12.0 ± 2.3 years

93%

71

41.7 ± 1.5

  

CES-D (≥16)

39

2

Sehlo 2013

Saudi Arabia

6.9 ± 4.2 years

100%

80

34.8 ± 11.2

  

SCID for DSM-IV

Major depressive disorder: 11.25

2

Sfikakis 1998

Greece

7.8 ± 6.4 years

91.5%

71

37.0 ± 13.0

HAS (>17)

23.9

HDS (>17)

19.7

2

Shakeri 2015

Iran

NS

92.5%

160

30.1 ± 6.2

21 Item-BAI (≥8/≥16/≥26)

81.2/51.9/18.1

21 Item-BDI (≥21/≥31/>40)

69.3/38.7/20.6

2

Shen 2015

China

NS

91.2%

156

32.9 ± 10.2

Zung SAS (≥50)

20.51

Zung SDS (≥53)

33.33

3

Skare 2014

Brazil

8.2 ± 6.9 years

93%

100

39.2 ± 12.5

  

21 Item-BDI

(≥19/≥ 30)

21/2

2

Shorta1l 1995

England

11.0 ± 7.1 years

95%

80

41.0 ± 11.2

HADS (≥8)

39

HADS (≥8)

26

2

Stoll 2001

Switzerland

11.4 ± 9.0 years

90%

60

44.5 ± 15.4

  

HADS (≥8)

16

3

Tam 2008

China

9.7 years

95.9%

291

42.0 ± 12.0

HADS (≥8)

22

HADS (≥8)

18.2

3

Tay 2015

Singapore

72.3 ± 81.1 months

86.4%

110

38.7 ± 12.6

HADS (≥8)

40.9

HADS (≥8)

15.5

2

Tench 2000

England

Median: 36.0 (12.0–79.5) months

100%

120

Median: 38.0 (32.0–45.0)

HADS (≥8)

60

HADS (≥8)

37

2

Tjensvoll 2010

Norway

12.3 ± 8.6 years

87%

63

43.4 ± 13.3

  

21 Item-BDI

(≥13)

23.8

2

Utset 2014

USA

Median: 9 years

95%

344

>18

  

CES-D (>10)

54.5

4

van Exel 2013

Netherlands

7.8 ± 7.0 years

88.2%

102

44.4 ± 12.5

  

21 Item-BDI

(≥14)

27

3

Vina 2015

USA

143.2 ± 117.8 months

93%

343

44.4 ± 12.9

  

CES-D (≥17)

47.2

4

Weder-Cisneros 2004

USA

Mean: 97.0 (6–348) months

91.4%

81

31.2 ± 9.7

  

21 Item-BDI

(≥14)

40.7

3

Xie 2012

China

Median: 1.3 years

93.7%

285

34.0 ± 13.0

  

21 Item-BDI

(≥5/14/≥21)

59.3/40.7/19.3

4

Zakeri 2012

Iran

NS

90.5%

71

>18

  

21 Item-BDI

(≥16/≥32)

60/9.4

2

NS not stated, CES-D Centre for Epidemiological Studies Depression Scale, BDI Beck Depression Inventory, BAI Beck Anxiety Inventory, DSM-III/IV Diagnostic and Statistical Manual of Mental Disorders, Third/Fourth Edition, HADS Hospital Anxiety and Depression Scale, ICD International Classification of Diseases, HAS the Hamilton Anxiety Scale, HDS the Hamilton Depression Scale, PHQ Patient Health Questionnaire, SCID Structured Clinical Interview for Diagnostic and Statistical Manual, SCL-90-R Symptoms Checklist-90-Revised, Zung SAS Zung Self-rating Anxiety Scale, Zung SDS Zung Self-rating Depression Scale

Table 2

Methods of detecting depression and summary of prevalence and heterogeneity findings

Tool

Definition/cutoff

No. of studies

No. of participants

Prevalence, % (95% CI)

Heterogeneity I2, %

DSM and/or ICD

     

Major depressive disorder

 

10

2960

24 (16, 31)

95.2

Dysthymic disorder

 

6

922

12 (5, 18)

93.4

Adjustment disorder

 

2

280

20 (15, 24)

0.0

Minor depression

 

1

150

6 (2, 10)

-

HADS

≥8

12

1474

30 (22, 38)

91.6

CES-D

>10

1

344

55 (49, 60)

-

 

≥16

8

1640

38 (32, 44)

81.3

 

>16.7

1

80

44 (33, 55)

-

 

≥17

1

343

47 (42, 52)

-

 

≥24

1

716

25 (22, 28)

-

 

>27

1

93

16 (9, 24)

-

21 Item-BDI

≥5

2

451

61 (56, 66)

17.7

 

≥10

1

167

21 (15, 27)

-

 

≥11

1

81

35 (24, 45)

-

 

≥13

1

63

24 (13, 34)

-

 

≥14

6

781

39 (29, 49)

88.2

 

≥16

2

131

76 (45, 107)

95.4

 

≥17

1

103

40 (30, 49)

-

 

≥18

1

127

42 (33, 50)

-

 

≥19

1

100

21 (13, 29)

-

 

≥20

2

213

50 (12, 89)

96.8

 

≥21

3

545

34 (2, 65)

98.8

 

≥29

1

153

19 (13, 25)

-

 

≥30

3

326

5 (0, 9)

72.1

 

≥31

1

160

39 (31, 46)

-

 

≥32

1

71

9 (3, 16)

-

 

>40

1

160

21 (14, 27)

-

HDS

≥8

1

126

41 (32, 49)

-

 

≥11

1

62

45 (33, 58)

-

 

≥16

1

126

2 (0, 5)

-

 

>17

1

71

20 (10, 29)

-

PHQ-9

≥10

1

75

29 (19, 40)

-

PHQ-2

≥3

1

612

28 (25, 23)

-

SCL-90-R

 

1

97

5 (1, 10)

-

Zung SDS

≥53

1

156

33 (26, 41)

-

DSM Diagnostic and Statistical Manual of Mental Disorders, ICD International Classification of Diseases, HADS Hospital Anxiety and Depression Scale, CES-D Centre for Epidemiological Studies Depression Scale, BDI Beck Depression Inventory, HDS Hamilton Depression Scale, PHQ Patient Health Questionnaire, SCL-90-R Symptoms Checklist-90-Revised, Zung SDS Zung Self-rating Depression Scale

Table 3

Methods of detecting anxiety and summary of prevalence and heterogeneity findings

Tool

Definition/cutoff

No. of studies

No. of participants

Prevalence, % (95% CI)

Heterogeneity I2, %

DSM and/or ICD for anxiety disorder

 

5

663

37 (12, 63)

98.3

HADS

≥8

10

1332

40 (30, 49)

93.0

21 Item-BAI

≥8

2

313

71 (51, 91)

94

 

≥16

2

313

48 (39, 56)

59.2

 

≥26

2

313

18 (14, 22)

0

HAS

≥6

1

126

75 (67, 82)

-

 

≥14

1

62

37 (25, 49)

-

 

≥15

1

126

27 (19, 35)

-

 

>17

1

71

24 (14, 34)

-

Cattell questionnaire

≥21

1

166

85 (79, 90)

-

SCL-90-R

 

1

97

4 (0, 8)

-

Zung SAS

>44

1

81

17 (9, 26)

-

 

≥50

1

156

21 (14, 27)

-

DSM Diagnostic and Statistical Manual of Mental Disorders, ICD International Classification of Diseases, HADS Hospital Anxiety and Depression Scale, BAI Beck Anxiety Inventory, HAS Hamilton Anxiety Scale, SCL-90-R Symptoms Checklist-90-Revised, Zung SAS Zung Self-rating Anxiety Scale

Prevalence of depression among SLE patients

Prevalence estimates of depression ranged from 2% to 91.7% in individual studies (Table 1). Table 2 indicated the summary of meta-analyses and heterogeneity assessments. Meta-analyses revealed the prevalence of major depressive disorder to be 24% (95% CI, 16%–31%) according to the DSM and/or ICD diagnostic criteria, with high heterogeneity (I2 = 95.2%). Prevalence estimates of depression were 30% (95% CI, 22%–38%, I2 = 91.6%) for the HADS with thresholds of 8 and 38% (95% CI, 32%–44%, I2 = 81.3%) for the CES-D with thresholds of 16, respectively. Prevalence of depression according to the 21 Item-BDI with a cutoff of 14 or more was 39% (95% CI, 29%–49%), with high heterogeneity (I2 = 88.2%) (Fig. 2).
Fig. 2

Prevalence of depressive disorder in SLE

Prevalence of anxiety among SLE patients

Prevalence of anxiety alone ranged between 4% and 85% in individual studies (Table 1). Table 3 presented the summary of meta-analyses and heterogeneity assessments. Meta-analyses pooled the prevalence of anxiety to be 40% (95% CI, 30%–49%, I2 = 93.0%) and 37% (95% CI, 12%–63%, I2 = 98.3%) according to the HADS with thresholds of 8 and the DSM and/or ICD diagnostic criteria, respectively (Fig. 3).
Fig. 3

Prevalence of anxiety in SLE

Sensitivity and subgroup analyses

Table 4 suggested depression and anxiety prevalence estimates according to each sensitivity and subgroup analysis, in comparison with the primary analysis. Sensitivity analyses revealed that the exclusion of studies with less sample representativeness tended to decrease dysthymic disorder prevalence estimates according to DSM and/or ICD. The removal of studies with less comparable respondent and non-respondent comparability tended to increase depression prevalence estimates according to the HADS with a cutoff of 8 or more. According to DSM and/or ICD, anxiety prevalence estimates had a trend to decrease by exclusion of studies only using female sample. The subgroup analyses were conducted according to sample size, overall quality, publication year, and country of origin. The results showed that studies with sample size <200 had higher anxiety estimates [43% (95% CI, 31%–55%) vs 28% (95% CI, 16%–40%)] according to the HADS with a cutoff of 8 or more. When evaluated by Newcastle-Ottawa criteria, studies with lower total overall quality scores yielded higher dysthymic disorder estimates [18% (95% CI, 6%–29%) vs 3% (95% CI, 2%–25%)] according to DSM and/or ICD. In contrast with clinical interviews (DSM and/or ICD), more recent publications tended to yield higher depression and anxiety prevalence estimates according to self-report instruments. The subgroup analyses for country of origin showed no clear patterns. There was no particular trend or pattern in any other sensitivity analyses or subgroup analyses.
Table 4

Impact of study characteristics on prevalence estimates for depression and anxiety in SLE: sensitivity and subgroup analyses

Depression definition (cutoff)

Anxiety definition (cutoff)

 

Major depressive disorder (DSM and/or ICD)

Dysthymic disorder (DSM and/or ICD)

HADS (≥8)

CES-D (≥16)

21 Item-BDI (≥14)

21 Item-BDI (≥21)

21 Item-BDI (≥30)

HADS (≥8)

Anxiety disorder

(DSM and/or ICD)

Primary analysis

24 (16, 31)

I2 = 95.2%

10 studies

2960 patients

12 (5, 18)

I2 = 93.4%

6 studies

922 patients

30 (22, 38)

I2 = 91.6%

12 studies

1474 patients

38 (32, 44)

I2 = 81.3%

8 studies

1640 patients

39 (29, 49)

I2 = 88.2%

6 studies

781 patients

34 (2, 65)

I2 = 98.8%

3 studies

545 patients

5 (0, 9)

I2 = 72.1%

3 studies

326 patients

40 (30, 49)

I2 = 93.0%

10 studies

1332 patients

37 (12, 63)

I2 = 98.3%

5 studies

663 patients

Sensitivity analyses

 

Excluding studies with less sample representativeness

24 (6, 42)

I2 = 98.2%

3 studies

2303 patients

3 (2, 5)

I2 = 0%

2 studies

476 patients

29 (15, 44)

I2 = 82.7%

3 studies

220 patients

-

36 (27, 45)

I2 = 72.4%

3 studies

468 patients

-

-

31 (8, 55)

I2 = 90.1%

2 studies

160 patients

-

Excluding studies with less comparable respondent and non-respondent comparability

-

-

45 (37, 54)

I2 = 68.1%

3 studies

482 patients

44 (29, 59)

I2 = 91.9%

3 studies

996 patients

-

-

-

42 (17, 66)

I2 = 96.9%

3 studies

482 patients

-

Excluding studies

only using female sample

16 (11, 21)

I2 = 79.8%

6 studies

2383 patients

16 (4, 28)

I2 = 95.0%

4 studies

496 patients

27 (17, 36)

I2 = 92.9%

9 studies

1195 patients

44 (35, 54)

I2 = 85.6%

4 studies

1168 patients

39 (29, 49)

I2 = 88.2%

6 studies

781 patients

34 (2, 65)

I2 = 98.8%

3 studies

545 patients

5 (−2, 12)

I2 = 85.9%

2 studies

266 patients

33 (27, 39)

I2 = 79.4%

8 studies

1135 patients

12 (2, 23)

I2 = 76.5%

2 studies

166 patients

Subgroup analyses

 

Sample size

 

<200

22 (14, 31)

I2 = 90.5%

8 studies

807 patients

14 (5, 23)

I2 = 93.3%

5 studies

596 patients

29 (22, 36)

I2 = 81.1%

10 studies

878 patients

38 (28, 48)

I2 = 86.3%

6 studies

1008 patients

39 (25, 52)

I2 = 90.5%

5 studies

496 patients

41 (−14, 96)

I2 = 99.2%

2 studies

260 patients

5 (0, 9)

I2 = 72.1%

3 studies

326 patients

43 (31, 55)

I2 = 91.8%

8 studies

736 patients

30 (9, 52)

I2 = 96.0%

4 studies

337 patients

≥200

27 (2, 57)

I2 = 99.1%

2 studies

2153 patients

-

35 (2, 67)

I2 = 98.8%

2 studies

596 patients

39 (36, 42)

I2 = 0.0%

2 studies

632 patients

-

-

-

28 (16, 40)

I2 = 90.8%

2 studies

596 patients

-

Overall quality

 

<3 points (low quality)

23 (13, 34)

I2 = 91.8%

7 studies

657 patients

18 (6, 29)

I2 = 93.2%

4 studies

446 patients

26 (18, 33)

I2 = 77.5%

6 studies

581 patients

34 (28, 40)

I2 = 45.5%

4 studies

443 patients

42 (21, 63)

I2 = 93.8%

3 studies

313 patients

41 (−14, 96)

I2 = 99.2%

2 studies

260 patients

5 (0, 9)

I2 = 72.1%

3 studies

326 patients

42 (32, 52)

I2 = 82.5%

5 studies

499 patients

30 (9, 52)

I2 = 96.0%

4 studies

337 patients

≥3 points (high quality)

26 (6, 42)

I2 = 98.2%

3 studies

2303 patients

3 (2, 5)

I2 = 0%

2 studies

476 patients

34 (20, 48)

I2 = 95.0%

6 studies

893 patients

42 (33, 52)

I2 = 87.9%

4 studies

1197 patients

36 (27, 45)

I2 = 72.4%

3 studies

468 patients

-

-

38 (23, 53)

I2 = 95.5%

5 studies

833 patients

-

Publication year

 

1990s

-

-

-

-

-

-

-

-

-

2000s

33 (17, 50)

I2 = 91.0%

3 studies

457 patients

-

25 (17, 33)

I2 = 81.3%

5 studies

660 patients

28 (23, 34)

I2 = 0.0%

2 studies

261 patients

30 (10, 51)

I2 = 86.8%

2 studies

141 patients

-

-

39 (22, 57)

I2 = 95.0%

4 studies

600 patients

56 (39, 73)

I2 = 86.3%

2 studies

397 patients

2010-

21 (14, 29)

I2 = 91.5%

6 studies

2424 patients

11 (2, 19)

I2 = 92.0%

4 studies

517 patients

35 (22, 48)

I2 = 93.1%

6 studies

734 patients

42 (35, 48)

I2 = 78.6%

6 studies

1379 patients

43 (32, 55)

I2 = 88.5%

4 studies

640 patients

34 (2, 65)

I2 = 98.8%

3 studies

545 patients

5 (0, 9)

I2 = 72.1%

3 studies

326 patients

41 (26, 56)

I2 = 93.8%

5 studies

652 patients

34 (2, 67)

I2 = 96.1%

2 studies

187 patients

Country of origin

 

North America

22 (8, 37)

I2 = 97.3%

4 studies

2363 patients

3 (2, 5)

I2 = 0%

2 studies

476 patients

-

38 (31, 45)

I2 = 83.9%

7 studies

1439 patients

30 (10, 51)

I2 = 86.8%

2 studies

141 patients

-

-

-

-

Asia

21 (0, 41)

I2 = 96.0%

3 studies

259 patients

21 (−3, 44)

I2 = 93.7%

2 studies

179 patients

26 (18, 34)

I2 = 85.4%

6 studies

767 patients

-

50 (31, 69)

I2 = 91.3%

2 studies

385 patients

34 (2, 65)

I2 = 98.8%

3 studies

545 patients

-

37 (23, 51)

I2 = 94.4%

6 studies

767 patients

29 (−13, 72)

I2 = 98.2%

2 studies

179 patients

Europe

-

-

33 (17, 49)

I2 = 93.8%

4 studies

565 patients

-

-

-

-

44 (28, 61)

I2 = 91.9%

3 studies

505 patients

-

South America

31 (12, 50)

I2 = 85.3%

2 studies

158 patients

-

-

-

-

-

-

-

32 (4, 60)

I2 = 93.5%

2 studies

158 patients

The first line in each set of data is percentage prevalence (95% CI)

DSM Diagnostic and Statistical Manual of Mental Disorders, ICD International Classification of Diseases, HADS Hospital Anxiety and Depression Scale, CES-D Centre for Epidemiological Studies Depression Scale, BDI Beck Depression Inventory

Associated study variables

We used Pearson’s and Spearmen’s correlation analyses to assess the association between variables including mean/medium disease duration, proportion of female participants, mean/medium age, representativeness, sample size, comparability, overall quality, country of origin, publication year, and the prevalence of depression and anxiety. Table 5 indicated that more recent publications was significantly associated with increased depression prevalence (r = 0.26, P = 0.04). No study characteristics presented a significant association with anxiety prevalence estimate.
Table 5

Pearson's and Spearmen’s correlation between study characteristics and prevalence estimates

Study characteristic

Depression prevalence estimate

Anxiety prevalence estimate

No. of studies

r

P

No. of studies

r

P

Female, %

59

0.03

0.84

24

0.07

0.76

Mean/medium age, year

55

−0.13

0.35

23

−0.18

0.94

Mean/medium disease duration, year

53

−0.07

0.64

21

0.24

0.29

Representativeness

59

0.03

0.85

24

0.08

0.70

Sample size

59

0.12

0.38

24

0.01

0.97

Comparability

59

0.24

0.07

24

−0.11

0.61

Overall quality

59

0.13

0.33

24

−0.10

0.64

Country of origin

59

0.01

0.92

24

−0.10

0.63

Publication year

59

0.26*

0.04

24

−0.04

0.84

*Significant at a P <0.05 level

Assessment of publication bias

Assessment of publication bias indicated significant publication bias, according to the Egger’s test, in studies reporting depression according to HADS with thresholds of 8 and CES-D with a cutoff of 16 or more [Egger: bias = 0.81 (95% CI: 0.04, 1.58), P = 0.04, and Egger: bias = 2.79 (95% CI: 0.61, 4.97), P = 0.02, respectively]. There was no significant evidence of publication bias in any other analyses (see Additional file 5).

Discussion

This systematic review and meta-analysis of 59 studies involving 10828 adult SLE patients demonstrated that a few studies using gold standard clinical interviews (DSM and/or ICD) reported that major depression and anxiety were presented in 24% and 37% among SLE patients, respectively. The majority of studies using screening tools found that significant depression were presented in 30% using the HADS a cutoff of 8 or more and 39% using the 21 Item-BDI with thresholds of 14. This study also found that more recent publications was significantly associated with increased depression prevalence among SLE patients. Furthermore, the prevalence of anxiety was 40% according to the HADS with thresholds of 8. These prevalence estimates are significantly higher than those observed in the general population [23, 24] and other rheumatic and connective tissue diseases [15, 25, 26]. Furthermore, these findings demonstrated that SLE patients tended to have a higher prevalence of anxiety than depression, which was in line with previous studies [27, 28]. Such discrepancy could be explained by the differences in time frames when these studies were performed, disease characteristics, social and cultural contexts of the lupus patients and tools used for assessing depression or anxiety. Because the development of depression and/or anxiety could result in increased incidence of cardiovascular diseases [5], decreased quality of life [9, 10], and a higher risk of premature mortality [11] among SLE patients, these findings highlighted an important issue in health education for this population.

Neuropsychiatric (NP) disorders appeared in about 70% of the patients diagnosed with SLE [29]. Previous meta-analyses have assessed the prevalence of the 19 NP syndromes defined by the American College of Rheumatology (ACR) in 1999 among SLE patients [30]. However, there were a wide variety of neurologic and psychiatric manifestations of SLE, which extended beyond those identified in the 1999 ACR classification criteria for SLE [31]. Several attempts have been made to devise a classification of NP-SLE manifestations because there were controversies regarding the inclusion of mood disorders in the 1999 ACR NP-SLE criteria [31, 32]. That’s why we excluded the studies investigating neuropsychiatric syndromes among SLE patients in this meta-analysis.

Although studies varied widely in terms of quality, our sensitivity analyses suggested that depression and/or anxiety prevalence estimates (except dysthymic disorder estimates) were reasonably stable. Variation in study sample size contributed importantly to the observed heterogeneity in the data. Studies with sample size <200 had higher anxiety estimates according to the HADS with thresholds of 8. Furthermore, studies with lower total overall quality scores yielded higher dysthymic disorder estimates according to DSM and/or ICD. Country, publication year, age, and gender also contributed to the heterogeneity between studies.

In this meta-analysis, many methods were used for data extraction and synthesis. The gold standard method was diagnostic interviews using DSM or ICD criteria, which were often time consuming and expensive. Therefore, it was not ideal for examining patients in a busy hospital environment [33]. Alternatively, self-report screening tools might be used, because they were quick and easy to complete and cheaper to use than diagnostic interviews. However, prevalence estimates using screening tools were often overestimated, because such tools tended to prioritize sensitivity over specificity [33]. Furthermore, there have not been validation studies to determine the best cut-point for screening tools in SLE patients, and several cut-off scores on self-report tools were often used in many studies. It indicated that the rheumatologists should always report prevalence at conventional cut-points, and screen for depression and anxiety among SLE patients according to the social and cultural contexts of the rheumatologists and SLE patients in clinical practice.

There are, however, additional important shortcomings in the evidence on prevalence of depression in SLE that need to be addressed. First, a substantial amount of the heterogeneity among the studies remained unexplained by the variables examined. Unexamined factors, such as gender, age, disease duration, might contribute to the risk for depression and/or anxiety symptom among SLE patients. Second, the data were derived from studies that used different designs and involved different groups of patients (e.g., from different countries), which might result in heterogeneity among the studies. Third, we did not look for healthy subjects in each study reporting the prevalence of depression or anxiety in SLE patients, which should be addressed in future research.

Conclusions

The prevalence of depression and anxiety was high in adult SLE patients. It indicated that rheumatologists should screen for depression and anxiety in their patients, and they should refer them to mental health providers in order to identify effective strategies for preventing and treating depression and anxiety among SLE patients.

Declarations

Acknowledgments

We would like to thank Chenlin Zhang and Alick for their great assistance with this study.

Funding

This work was supported by the Natural Science Foundation of China (Grant no. 81401124); the Humanistic Nursing Care Foundation of China (Grant no. RW2016AM14); Preventive Medicine Projects from Bureau of Jiangsu Province (Y2012083); “Top Six Types of Talents” Financial Assistance of Jiangsu Province (Grant no. 10.WSN016); Jiangsu Provincial Commission of Health and Family Planning Foundation (Grant no. Z201622); Science Foundation of Nantong City (Grant no. MS22015003); the College graduate research and innovation of Jiangsu Province (KYZZ15_0353); and the Nantong University Graduate Innovation Program (YKC15075).

Availability of data and materials

The majority of data generated or analyzed during this study are included in this published article (and its Additional files). Remaining data not published here are available from the corresponding author on reasonable request.

Authors’ contributions

LZ and TF searched and checked the databases according to the inclusion and exclusion criteria, extracted the data and assessed their quality. LZ analyzed the data and wrote the draft of the paper. RY, QZ and BS gave advice on meta-analysis methodology and revised the paper. All authors contributed to reviewing or revising the paper. BS is the guarantor of this work and had full access to all the data in the study and takes responsibility for its integrity and the accuracy of the data analysis. All authors read and approved the final manuscript.

Competing interests

The authors declared that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Ethical approval and consent to participate are not required for this review.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Nursing, The Second Affiliated Hospital of Nantong University
(2)
School of Nursing, Nantong University

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Copyright

© The Author(s). 2017

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