Skip to main content

SYSTEMATIC REVIEW article

Front. Med., 27 February 2020
Sec. Dermatology

A Meta-Analysis of Observational Studies on the Association of Chronic Urticaria With Symptoms of Depression and Anxiety

\nYuzhou Huang,,Yuzhou Huang1,2,3Yi Xiao,,Yi Xiao1,2,3Xingyu ZhangXingyu Zhang4Jie Li,,
Jie Li1,2,3*Xiang Chen,,
Xiang Chen1,2,3*Minxue Shen,,,
Minxue Shen1,2,3,4*
  • 1Department of Dermatology, Xiangya Hospital, Central South University, Changsha, China
  • 2Hunan Engineering Research Center of Skin Health and Disease, Central South University, Changsha, China
  • 3Hunan Key Laboratory of Skin Cancer and Psoriasis, Central South University, Changsha, China
  • 4Department of Social Medicine and Health Management, Xiangya School of Public Health, Central South University, Changsha, China

Background: Chronic urticaria (CU) is a frequently occurring skin condition associated with many psychological factors, but the effect size of associations varied in literature.

Objectives: To perform a systematic review and meta-analysis on the associations of CU with the symptoms of depression and anxiety.

Methods: According to a pre-specified protocol, we systematically searched articles published in PubMed, Web of Science, CNKI, and CQVIP databases between January 2000 and January 2019. Pooled estimates in terms of odds ratios (ORs) or standardized mean differences (SMDs) were calculated according to outcome measures. Subgroup analysis by disease subtypes and tool of measurement, and sensitivity analysis were performed. Risk of bias and quality of studies were evaluated.

Results: Twelve studies were selected for the systematic review. The ORs were 3.99 [95% confidence interval (CI): 3.24–4.91, P < 0.001] for anxiety and 2.94 (95% CI: 2.42–3.58, P < 0.001) for depression. The SMDs of severity were 0.98 for anxiety (95% CI: 0.76–1.200, P < 0.001) and 0.84 for depression (95% CI: 0.59–1.10, P < 0.001). Subgroup analysis by disease subtypes and tool of measurement showed variations in effect size, where chronic spontaneous urticaria showed greater effects on anxiety (OR = 6.62, 95% CI: 3.67–11.95, P < 0.001) and depression (OR = 6.13, 95% CI: 2.31–16.31, P < 0.001). Sensitivity analysis demonstrated consistent results.

Conclusion: CU is associated with higher risks of anxiety and depression.

Introduction

Chronic urticaria (CU) is one of the most common skin disorders characterized by the rapid appearance of wheals, angioedema, or both, for more than 6 weeks (1). The symptoms of CU are caused by the activation of skin mast cells and subsequent histamine release and other inflammatory mediators. The annual prevalence of CU is estimated to be 0.5–5% in the general population (2, 3). CU is divided into chronic spontaneous urticaria (CSU) and chronic inducible urticaria (CIndU) (1, 4). CSU occurs spontaneously with no identifiable triggers, while CIndU is characterized by the need for specific triggers (4).

It is estimated that at least 30% of patients with skin disease have significant psychiatric or psychological morbidities (5, 6). Previous studies consistently showed that anxiety and depression are common psychological comorbidities of itching-related skin diseases (79). Many studies have shown that patients with CU often develop psychiatric complications (10, 11). The most common diagnoses of mental disorders observed in patients with CU are depression, anxiety, and somatoform disorders (11). Patients with CSU even have more psychiatric co-morbidities than patients with psoriasis and atopic dermatitis (12). The effect of CSU on the quality of life was reported as similar to that of cardiovascular diseases (13). Psychological complications are often one of the most important indicators of overall disability associated with skin conditions.

Globally, urticaria was estimated to contribute to 4.7 million age-standardized disability-adjusted life years (14). However, the disability weights used to estimate the burden of non-communicable skin diseases are primarily determined by disfigurement and cutaneous symptoms. Psychological impacts and health-related quality of life are neglected but import aspects of skin disorders. Unfortunately, the number of people suffering from anxiety and depression in skin diseases in European countries is largely underestimated by dermatologists (15). In addition, the effect size of associations shows large variations owing to the heterogeneities in population, setting, tools of measurement, criteria of diagnosis, sample size, etc.

The current systematic review of published data aimed to assess the association of CU with the symptoms of anxiety and depression in observational studies, and to further provide a synthesis of reported effect sizes of associations. The protocol of this meta-analysis has been registered on PROSPERO (CRD42018117095), and the study is reported based on the Preferred Reporting Items for Systemic Reviews and Meta-Analysis (PRISMA) guidelines.

Methods

Search Strategy

We searched articles published in PubMed, Web of Science, Chinese National Knowledge Infrastructure (CNKI), and Chinese Scientific Journals Full Text Database (CQVIP), including full-text articles in both English and Chinese. The Chinese literature was searched using Chinese keywords. The searching strategy applied in PubMed is shown below:

  (1) Urticaria

  (2) Chronic urticaria

  (3) 1 or 2

  (4) Psychopathology

  (5) Stress

  (6) Depression

  (7) Anxiety

  (8) psychiatry*

  (9) Or/4–8

(10) 3 and 9.

We searched the articles between January 2000 and March 2019, in English or Chinese (Figure 1). The search strategy adjusts to a controlled vocabulary for each database. Gray literature and conference abstracts have not been searched.

FIGURE 1
www.frontiersin.org

Figure 1. Selection process for study inclusion in the systematic review and meta-analysis.

Study Selection

Studies are considered to meet the eligibility criteria if (1) hospital-based or population-based observational study, including cross-sectional study, case-control study, and cohort study; (2) there is a clear diagnosis of CU; (3) they are published in either English or Chinese; (4) there is a clear diagnosis or standardized measurement of anxiety or depression, such as a doctor's diagnosis or medical history; (5) effect size is reported as odds ratio (OR) or mean difference with 95% confidence intervals (CIs). The exclusion criteria were (1) CU is not diagnosed in detail or is measured by unvalidated tools; (2) no control group; (3) local and/or federal government reports that are not peer reviewed, as well as summaries and presentations of meetings; (4) publication in languages other than English or Chinese.

The articles were evaluated by two investigators independently using pre-specified qualification forms based on eligibility criteria and were forward looking. Any inconsistency between the investigators was resolved by consensus.

Data Extraction

Relevant information was extracted and recorded on a data collection form (e.g., name of the first author, year of publication, country of origin, study duration, number and characteristics of participants, and identification of depression and anxiety).

Study Quality Assessment

The quality of included observational studies was assessed using the Newcastle-Ottawa Scale (NOS) (16). The NOS includes a series of questions that are used to assess the choice of study participants, the comparability of the population, and the determination of exposure or outcomes with a maximum score of 9. Studies with scores ≥5 were classified as high-quality studies. Using these checklists, two reviewers evaluated each of the included articles for their quality. Divergent views were resolved by consultation with a third reviewer.

Statistical Analysis

For dichotomous outcomes (anxiety and depression), the odds ratios (ORs) with 95% confidence intervals (CIs) were estimated. For continuous data (severity of symptoms), standardized mean differences (SMDs) with 95% CIs were calculated. To generate the pooled estimates of the outcomes, fixed effect models or random effect models were used according to the heterogeneity between studies. To assess the extent to which statistical heterogeneity in meta-analysis is due to differences between studies rather than accidental, we used I2 statistic and Cochran's Q (with corresponding P-values) (17). The forest plots were used for a visual representation of the presence and nature of statistical heterogeneity. In the subgroup analysis, subtypes of CU (including CSU, CIndU, and unspecified CU) and tools to measure (ascertain) anxiety and depression were evaluated. In sensitivity analysis, one study was eliminated at a time, and the pooled estimate was calculated. Egger's test was used to assess publication bias (18). A value of P < 0.05 was considered statistically significant. All statistical analyses were performed using the STATA software, version 14.0 (StataCorp, College Station, TX, USA).

Results

Data Sources and Selection Process

A total of 1,292 articles were selected in our screening. Of these, 296 duplicated articles were excluded and 948 articles were excluded after initial screening because they were not observational studies, or the subjects were not related to our topic. Of the full-text articles, 48 were retained for further screening. Of these, 35 were excluded for various reasons (Figure 1). Thirteen studies with a total of 3,627 study participants were included in the final meta-analysis (1931).

Characteristics of Included Studies

The characteristics of the included studies are summarized in Table 1. There were three cross-sectional studies and nine case-control studies. There were a total of 1,116 CU patients and 2,511 controls, with a mean age of participants ranging from 28.2 to 46.3 years, except the study in children.

TABLE 1
www.frontiersin.org

Table 1. Characteristics of the included studies.

Main Analysis

As shown in Figure 2, the pooled OR was 3.99 (95% CI: 3.24–4.91, P < 0.001) for anxiety and 2.94 (95% CI: 2.42–3.58, P < 0.001) for depression. If excluding the study in children, the pooled ORs were 4.08 (95% CI: 3.20–5.21, P < 0.001) for anxiety and 2.94 (95% CI: 2.41–3.58, P < 0.001) for depression. In studies that measured the symptoms of anxiety and depression as severity scores, the pooled SMDs was 0.98 for anxiety (95% CI: 0.76–1.200, P < 0.001) and 0.84 for depression (95% CI: 0.59–1.10, P < 0.001).

FIGURE 2
www.frontiersin.org

Figure 2. Pooled estimates of the associations of chronic urticaria with symptoms of anxiety and depression. (A) Anxiety, in terms of odds ratio. (B) Anxiety, in terms of standardized mean difference. (C) Depression, in terms of odds ratio. (D) Depression, in terms of standardized mean difference.

Subgroup Analysis

Subgroup analysis by disease subtypes is shown in Figure 3. The ORs of CSU, CIndU, and unspecified CU were 6.62 (95% CI: 3.67–11.95, P < 0.001), 3.53 (95% CI: 1.43–8.74, P < 0.001), and 3.79 (95% CI: 2.91–4.94, P < 0.001) for anxiety, respectively. The ORs of CSU, CIndU, and unspecified CU were 6.13 (95% CI: 2.31–16.31, P < 0.001), 4.32 (95% CI: 1.97–9.49, P < 0.001), and 2.77 (95% CI: 2.26–3.41, P < 0.001) for depression, respectively. As shown in Figure S1, the SMDs of CSU and unspecified CU were 1.15 (95% CI: 0.83–1.47, P < 0.001) and 0.82 (95% CI: 0.51–1.12, P < 0.001) for anxiety, and 0.99 (95% CI: 0.75–1.24, P < 0.001) and 0.61 (95% CI: 0.16–1.06, P = 0.001) for depression, respectively.

FIGURE 3
www.frontiersin.org

Figure 3. Subgroup analysis of the associations of chronic urticaria with symptoms of anxiety and depression in terms of odds ratio, by subtypes of chronic urticaria. (A) Anxiety and subtypes of chronic urticaria. (B) Depression and subtypes of chronic urticaria. CU, chronic urticaria; CSU, chronic spontaneous urticaria; CIndU, chronic-induced urticaria.

Subgroup analysis by tools of measurement is shown in Figure S2. The ORs varied from 3.53 (95% CI: 2.88–4.34, P < 0.001) to 7.11 (95% CI: 3.60–14.02, P < 0.001) for anxiety and from 2.36 (95% CI: 0.86–6.44, P < 0.001) to 4.85 (95% CI: 2.32–10.14, P < 0.001) for depression. The SMDs varied from 0.78 (95% CI: 0.27–1.28, P = 0.003) to 1.25 (95% CI: 0.77–1.72, P < 0.001) for anxiety and from 0.63 (95% CI: 0.19–1.07, P < 0.001) to 1.13 (95% CI: 0.66–1.60, P < 0.001) for depression. All pooled estimates were statistically significant.

Sensitivity Analysis

We performed sensitivity analyses and assessed the relative impact of each study by excluding the studies one by one. The results showed no significant changes (Figure 4).

FIGURE 4
www.frontiersin.org

Figure 4. Sensitivity analysis of the pooled estimates by excluding the studies one by one. (A) Anxiety, in terms of odds ratio. (B) Depression, in terms of odds ratio.

Assessment on Quality of Studies

The risk of bias appraised among the included studies is shown in Table 2. Study quality scores ranged from 6 to 9, and all of them were of good quality.

TABLE 2
www.frontiersin.org

Table 2. Quality assessment of the included studies.

Publication Bias

Egger's regression test (P = 0.050 for anxiety and P = 0.020 for depression) indicated significant publication bias, where the effect size (OR) was positively associated with study sample size.

Discussion

In this meta-analysis, we analyzed 3,627 participants in 13 studies over the past 18 years, and investigated the associations of CU with the symptoms of anxiety and depression. We found that patients with CU had significantly higher risks and severities of anxiety and depression than health controls. Patients with CU had 3-fold risk of anxiety or depression, and patients with CSU had 6-fold risk of anxiety or depression, compared to the controls. The magnitude of associations varied moderately among the tools of measurement, but the conclusions remained consistent.

Many research studies support the association of mast cell activation with emotional problems. In a recent a study, depression levels in patients with mastocytosis were found to be significantly associated with tryptophan (TRP) levels (32). TRP metabolism changes in mastocytosis and is associated with stress and depression, suggesting that mast cells participate in the inflammatory pathway associated with depression. Mast cell activation also increases anxiety-like behavior (33), while anxiety and depression are associated with increased mast cell counts and degranulation (34). There is growing evidence that mast cells are critical for the pathogenesis of inflammatory diseases (32, 35). Studies show that depression can develop, in part, based on inflammatory changes, including interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-a), IL-1β, IL-2, and C-reactive protein (CRP) (3638). In a meta-analysis of severe depressive cytokines, patients with depression had increased TNF-α and interleukin-6 levels compared to health controls (37). Therefore, mast cells play an important role in inflammation-induced depression (32, 39). We speculated that the relationship between CU and anxiety and depression was partly mediated by the release of inflammatory factors and the degranulation of mast cells.

In this meta-analysis, five studies included patients with CSU, three included CIndU, and five did not specify the subtype of CU. We observed a stronger correlation between CSU and anxiety/depression than CIndU or unspecified CU. A survey in 2013, however, reported that patients with inducible urticaria had more symptoms of anxiety and depression than those with CSU (40). Owing to the heterogeneities across included studies, it is difficult to conclude that the magnitude of association is larger in CSU than that in CIndU from this meta-analysis.

The measurement or diagnosis of anxiety and depression might serve as another important source of heterogeneity. In the subgroup analysis by the tool of measurement, the ORs varied from 3.53 to 7.11 for anxiety and from 2.36 to 54.85 for depression. The Hospital Anxiety and Depression Scale (HADS) has been widely used to assess the presence and severity of anxiety and depression in patients with physical illness (41). The HADS demonstrates high reliability with a Cronbach's alpha coefficient of 0.884 and test–retest correlation of 0.944 (42). However, in primary care settings, the HADS performs less well than the other instruments, such as the Beck Depression Inventory (43). Some authors suggest that the potential structure of the HADS in the sample is inconsistent and is highly dependent on the structure of establishing statistical methods (44, 45). The Self-Rating Anxiety Scale (SAS) developed by Zung has been widely used in the research and clinical practice of anxiety testing (46). The Cronbach's alpha of SAS is 0.897, and the test–retest reliability is 0.913 (47). The Zung Self-Rating Depression Scale (SDS) is designed to measure depression (48) and related symptoms with an alpha coefficient of 0.79 (49). However, some studies did not recommend to rely too much on the total score of SDS, since the various characteristics of heterogeneous symptoms are contained in a single dimension of severity (50, 51). In this meta-analysis, two studies by Balp et al. used a self-reported measure of anxiety and depression (26, 30), yet the reliability and validity were not mentioned by the authors. As a result, the variations in effect size were partly attributable to the tools of measurement.

The study has limitations. First, despite the strong association of CU with anxiety and depression, the causality could not be confirmed since all the included studies were cross-sectional or case-control studies. Eligible prospective cohort studies were not identified in the literature. A reversed causal relationship may exist, where CU might be triggered by changes in emotional status, possibly through mechanisms involving the hypothalamic–pituitary–adrenal axis or brain–gut–microbiome axis. Second, the variations in diagnosis and measurement of anxiety and depression may lead to substantial between-study heterogeneities. In addition, there was significant publication biases, which may be due to the fact that negative results were less likely to appear in published papers. The study also has strengths. First, this is the first meta-analysis and systematic review for the association of CU with symptoms of anxiety and depression. We confirmed the association through the synthesis of evidence, and the result has significant clinical implication for dermatologists. Second, we established strict inclusion and exclusion criteria, resulting in a relatively uniform data set. Including quality assessment was also a valuable asset of this assessment, allowing readers to judge the strength of evidence. In addition, research options and data extraction were completed by two independent reviewers, which help to ensure the comprehensiveness and accuracy of the review.

In conclusion, our present meta-analysis demonstrated that CU is associated with higher risks of anxiety and depression, and CSU might be associated with a larger effect on the risks.

Data Availability Statement

All datasets generated for this study are included in the article/Supplementary Material.

Author Contributions

YH, YX, and XZ searched the literature and extracted the data. YH and MS performed the systematic review, analyzed the data, and drafted the manuscript. JL and XC reviewed and revised the manuscript. XC obtained the funding. All authors gave final approval to the version submitted for publication.

Funding

This work was supported by the National Key Research and Development Project of China Precision Medicine Initiative (2016YFC0900802) and the National Natural Science Foundation of China (81974476, 81673065). The funder did not participate in this study.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmed.2020.00039/full#supplementary-material

Figure S1. Subgroup analysis of the associations of chronic urticaria with symptoms of anxiety and depression in terms of standardized mean difference, by subtypes of chronic urticaria. (A) Anxiety and subtypes of chronic urticaria. (B) Depression and subtypes of chronic urticaria. CU, chronic urticaria; CSU, chronic spontaneous urticaria; CIndU, chronic-induced urticaria.

Figure S2. Subgroup analysis of the associations of chronic urticaria with symptom of anxiety and depression, by tool of measurement. (A) Tool of measurement by anxiety, in terms of odds ratio. (B) Tool of measurement by anxiety, in terms of standardized mean difference. (C) Tool of measurement by depression, in terms of odds ratio. (D) Tool of measurement by depression, in terms of standardized mean difference.

References

1. Zuberbier T, Aberer W, Asero R, Abdul Latiff AH, Baker D, Ballmer-Weber B, et al. The EAACI/GA(2)LEN/EDF/WAO guideline for the definition, classification, diagnosis and management of urticaria. Allergy. (2018) 73:1393–414. doi: 10.1111/all.13397

PubMed Abstract | CrossRef Full Text | Google Scholar

2. Bernstein JA, Lang DM, Khan DA, Craig T, Dreyfus D, Hsieh F, et al. The diagnosis and management of acute and chronic urticaria: 2014 update. J Allergy Clin Immunol. (2014) 133:1270–7. doi: 10.1016/j.jaci.2014.02.036

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Zuberbier T, Balke M, Worm M, Edenharter G, Maurer M. Epidemiology of urticaria: a representative cross-sectional population survey. Clin Exp Dermatol. (2010) 35:869–73. doi: 10.1111/j.1365-2230.2010.03840.x

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Magerl M, Altrichter S, Borzova E, Gimenez-Arnau A, Grattan CE, Lawlor F, et al. The definition, diagnostic testing, and management of chronic inducible urticarias - The EAACI/GA(2) LEN/EDF/UNEV consensus recommendations 2016 update and revision. Allergy. (2016) 71:780–802. doi: 10.1111/all.12884

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Gupta MA, Gupta AK. Psychodermatology: an update. J Am Acad Dermatol. (1996) 34:1030–46. doi: 10.1016/S0190-9622(96)90284-4

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Picardi A, Abeni D, Melchi CF, Puddu P, Pasquini P. Psychiatric morbidity in dermatological outpatients: an issue to be recognized. Br J Dermatol. (2000) 143:983–91. doi: 10.1046/j.1365-2133.2000.03831.x

PubMed Abstract | CrossRef Full Text | Google Scholar

7. Boehm D, Schmid-Ott G, Finkeldey F, John SM, Dwinger C, Werfel T, et al. Anxiety, depression and impaired health-related quality of life in patients with occupational hand eczema. Contact Dermatitis. (2012) 67:184–92. doi: 10.1111/j.1600-0536.2012.02062.x

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Dalgard FJ, Gieler U, Tomas-Aragones L, Lien L, Poot F, Jemec GBE, et al. The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries. J Invest Dermatol. (2015) 135:984–91. doi: 10.1038/jid.2014.530

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Tey HL, Wallengren J, Yosipovitch G. Psychosomatic factors in pruritus. Clin Dermatol. (2013) 31:31–40. doi: 10.1016/j.clindermatol.2011.11.004

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Hashiro M, Okumura M. Anxiety, depression, psychosomatic symptoms and autonomic nervous function in patients with chronic urticaria. J Dermatol Sci. (1994) 8:129–35. doi: 10.1016/0923-1811(94)90007-8

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Staubach P, Eckhardt-Henn A, Dechene M, Vonend A, Metz M, Magerl M, et al. Quality of life in patients with chronic urticaria is differentially impaired and determined by psychiatric comorbidity. Br J Dermatol. (2006) 154:294–8. doi: 10.1111/j.1365-2133.2005.06976.x

PubMed Abstract | CrossRef Full Text | Google Scholar

12. Gupta MA, Gupta AK, Schork NJ, Ellis CN. Depression modulates pruritus perception: a study of pruritus in psoriasis, atopic dermatitis, and chronic idiopathic urticaria. Psychosom Med. (1994) 56:36–40. doi: 10.1097/00006842-199401000-00005

PubMed Abstract | CrossRef Full Text | Google Scholar

13. Berrino AM, Voltolini S, Fiaschi D, Pellegrini S, Bignardi D, Minale P, et al. Chronic urticaria: importance of a medical-psychological approach. Eur Ann Allergy Clin Immunol. (2006) 38:149–52.

PubMed Abstract | Google Scholar

14. Karimkhani C, Dellavalle RP, Coffeng LE, Flohr C, Hay RJ, Langan SM, et al. Global skin disease morbidity and mortality: an update from the global burden of disease study 2013. JAMA Dermatol. (2017) 153:406–12. doi: 10.1001/jamadermatol.2016.5538

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Dalgard FJ, Svensson A, Gieler U, Tomas-Aragones L, Lien L, Poot F, et al. Dermatologists across Europe underestimate depression and anxiety: results from 3635 dermatological consultations. Br J Dermatol. (2018) 179:464–70. doi: 10.1111/bjd.16250

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Wells G, Shea BO, Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-analyses. Ottawa, ON: Ottawa Hospital Research Institute (2000). Available online at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

Google Scholar

17. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. (2002) 21:1539–58. doi: 10.1002/sim.1186

PubMed Abstract | CrossRef Full Text | Google Scholar

18. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. (1997) 315:629–34. doi: 10.1136/bmj.315.7109.629

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Wu YP, Chang JM, Fu Y, Bao YQ, Feng HP, Yang M, et al. Study on the correlation between depression, anxiety and chronic urticaria. Chin J Dermatol. (2003) 36:30–2. doi: 10.3760/j.issn:0412-4030.2003.02.009

CrossRef Full Text

20. Pasaoglu G, Bavbek S, Tugcu H, Abadoglu O, Misirligil Z. Psychological status of patients with chronic urticaria. J Dermatol. (2006) 33:765–71. doi: 10.1111/j.1346-8138.2006.00178.x

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Brzoza Z, Kasperska-Zajac A, Badura-Brzoza K, Matysiakiewicz J, Hese RT, Rogala B. Decline in dehydroepiandrosterone sulfate observed in chronic urticaria is associated with psychological distress. Psychosom Med. (2008) 70:723–8. doi: 10.1097/PSY.0b013e31817bcc8d

PubMed Abstract | CrossRef Full Text | Google Scholar

22. Engin B, Uguz F, Yilmaz E, Ozdemir M, Mevlitoglu I. The levels of depression, anxiety and quality of life in patients with chronic idiopathic urticaria. J Eur Acad Dermatol Venereol. (2008) 22:36–40. doi: 10.1111/j.1468-3083.2007.02324.x

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Uguz F, Engin B, Yilmaz E. Axis I and axis II diagnoses in patients with chronic idiopathic urticaria. J Psychosom Res. (2008) 64:225–9. doi: 10.1016/j.jpsychores.2007.08.006

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Herguner S, Kilic G, Karakoc S, Tamay Z, Tuzun U, Guler N. Levels of depression, anxiety and behavioural problems and frequency of psychiatric disorders in children with chronic idiopathic urticaria. Br J Dermatol. (2011) 164:1342–7. doi: 10.1111/j.1365-2133.2010.10138.x

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Zhang QL, Hou SC. Investigation on the correlation between artificial urticaria and depressive symptoms. J Clin Dermatol. (2011) 40:475–6. doi: 10.3969/j.issn.1000-4963.2011.08.011

CrossRef Full Text

26. Balp MM, Vietri J, Tian H, Isherwood G. The impact of chronic urticaria from the patient's perspective: a survey in five European countries. Patient. (2015) 8:551–8. doi: 10.1007/s40271-015-0145-9

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Zhang QL, Hou SC, Zhan SX, Wang Y, Giu WL. Study on the correlation between artificial urticaria and mental depression and anxiety symptoms. Chinese J Lepr Dermatol. (2016) 32:556–8.

28. Ograczyk A, Miniszewska J, Pietrzak A, Zalewska-Janowska A. Sense of coherence as a protective factor in chronic urticaria. Postepy Dermatol Alergol. (2017) 34:168–73. doi: 10.5114/ada.2017.67084

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Tat TS. Higher levels of depression and anxiety in patients with chronic urticaria. Med Sci Monit. (2019) 25:115–20. doi: 10.12659/MSM.912362

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Balp MM, Lopes da Silva N, Vietri J, Tian H, Ensina LF. The burden of chronic urticaria from Brazilian patients' perspective. Dermatol Ther. (2017) 7:535–45. doi: 10.1007/s13555-017-0191-4

CrossRef Full Text | Google Scholar

31. Barbosa F, Freitas J, Barbosa A. Chronic idiopathic urticaria and anxiety symptoms. J Health Psychol. (2011) 16:1038–47. doi: 10.1177/1359105311398682

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Georgin-Lavialle S, Moura D, Salvador A, Chauvet-Gelinier J, Launay J, Damaj G, et al. Mast cells' involvement in inflammation pathways linked to depression: evidence in mastocytosis. Mol Psychiatry. (2016) 21:1511–6. doi: 10.1038/mp.2015.216

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Nautiyal KM, Ribeiro AC, Pfaff DW, Silver R. Brain mast cells link the immune system to anxiety-like behavior. Proc Natl Acad Sci USA. (2008) 105:18053–7. doi: 10.1073/pnas.0809479105

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Yuan HP, Li Z, Zhang Y, Li XP, Li FK, Li YQ. Anxiety and depression are associated with increased counts and degranulation of duodenal mast cells in functional dyspepsia. Int J Clin Exp Med. (2015) 8:8010–4.

PubMed Abstract | Google Scholar

35. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, Zhang B, et al. Mast cells and inflammation. Biochim Biophys Acta. (2012) 1822:21–33. doi: 10.1016/j.bbadis.2010.12.014

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Dantzer R. Cytokine, sickness behavior, and depression. Immunol Allergy Clin North Am. (2009) 29:247–64. doi: 10.1016/j.iac.2009.02.002

PubMed Abstract | CrossRef Full Text | Google Scholar

37. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, et al. A meta-analysis of cytokines in major depression. Biol Psychiatry. (2010) 67:446–57. doi: 10.1016/j.biopsych.2009.09.033

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Liu Y, Ho RC, Mak A. Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J Affect Disord. (2012) 139:230–9. doi: 10.1016/j.jad.2011.08.003

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Conti P, Caraffa A, Ronconi G, Conti C, Kritas S, Mastrangelo F, et al. Impact of mast cells in depression disorder: inhibitory effect of IL-37. Immunol. Res. (2018) 66:323. doi: 10.1007/s12026-018-9004-9

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Weller K, Koti I, Makris M, Maurer M. Anxiety and depression seem less common in patients with autoreactive chronic spontaneous urticaria. Clin Exp Dermatol. (2013) 38:870–3. doi: 10.1111/ced.12190

PubMed Abstract | CrossRef Full Text | Google Scholar

41. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. (1983) 67:361–70. doi: 10.1111/j.1600-0447.1983.tb09716.x

PubMed Abstract | CrossRef Full Text | Google Scholar

42. Michopoulos I, Douzenis A, Kalkavoura C, Christodoulou C, Michalopoulou P, Kalemi G, et al. Hospital Anxiety and Depression Scale (HADS): validation in a Greek general hospital sample. Ann Gen Psychiatry. (2008) 7:4. doi: 10.1186/1744-859X-7-4

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Williams JW Jr, Pignone M, Ramirez G, Perez Stellato C. Identifying depression in primary care: a literature synthesis of case-finding instruments. Gen Hosp Psychiatry. (2002) 24:225–37. doi: 10.1016/S0163-8343(02)00195-0

PubMed Abstract | CrossRef Full Text | Google Scholar

44. Brennan C, Worrall-Davies A, McMillan D, Gilbody S, House A. The Hospital Anxiety and Depression Scale: a diagnostic meta-analysis of case-finding ability. J Psychosom Res. (2010) 69:371–8. doi: 10.1016/j.jpsychores.2010.04.006

PubMed Abstract | CrossRef Full Text | Google Scholar

45. Coyne JC, van Sonderen E. No further research needed: abandoning the Hospital and Anxiety Depression Scale (HADS). J Psychosom Res. (2012) 72:173–4. doi: 10.1016/j.jpsychores.2011.12.003

PubMed Abstract | CrossRef Full Text | Google Scholar

46. Zung WW. A rating instrument for anxiety disorders. Psychosomatics. (1971) 12:371–9. doi: 10.1016/S0033-3182(71)71479-0

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Samakouri M, Bouhos G, Kadoglou M, Giantzelidou A, Tsolaki K, Livaditis M. [Standardization of the Greek version of Zung's Self-rating Anxiety Scale (SAS)]. Psychiatriki. (2012) 23:212–20.

PubMed Abstract | Google Scholar

48. Zung WW. A self-rating depression scale. Arch Gen Psychiatry. (1965) 12:63–70. doi: 10.1001/archpsyc.1965.01720310065008

PubMed Abstract | CrossRef Full Text | Google Scholar

49. Knight RG, Waal-Manning HJ, Spears GF. Some norms and reliability data for the State–Trait Anxiety Inventory and the Zung Self-Rating Depression scale. Br J Clin Psychol. (1983) 22:245–9. doi: 10.1111/j.2044-8260.1983.tb00610.x

PubMed Abstract | CrossRef Full Text | Google Scholar

50. Newmann JP, Engel RJ, Jensen JE. Age differences in depressive symptom experiences. J Gerontol. (1991) 46:P224–35. doi: 10.1093/geronj/46.5.P224

PubMed Abstract | CrossRef Full Text | Google Scholar

51. Tennen H, Hall JA, Affleck G. Depression research methodologies in the Journal of Personality and Social Psychology: a review and critique. J Pers Soc Psychol. (1995) 68:870–84; discussion 885–91. doi: 10.1037/0022-3514.68.5.870

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: chronic urticaria, depression, anxiety, meta-analysis, observational study

Citation: Huang Y, Xiao Y, Zhang X, Li J, Chen X and Shen M (2020) A Meta-Analysis of Observational Studies on the Association of Chronic Urticaria With Symptoms of Depression and Anxiety. Front. Med. 7:39. doi: 10.3389/fmed.2020.00039

Received: 22 October 2019; Accepted: 27 January 2020;
Published: 27 February 2020.

Edited by:

Ivan V. Litvinov, McGill University, Canada

Reviewed by:

Irina Khamaganova, Pirogov Russian National Research Medical University, Russia
Isabelle Vallerand, University of Calgary, Canada

Copyright © 2020 Huang, Xiao, Zhang, Li, Chen and Shen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Jie Li, xylijie@csu.edu.cn; Xiang Chen, chenxiangck@126.com; Minxue Shen, shenmx1988@csu.edu.cn

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.