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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 38  |  Issue : 1  |  Page : 22-27

Association of psoriasis with asthma: A systematic review and meta-analysis of observational studies


1 Department of Respiratory Therapy, Chang Gung Memorial Hospital, Chiayi; Department of Respiratory Care, Chang Gung University of Science and Technology, Chiayi Campus, Taiwan
2 Department of Respiratory Care, Chang Gung University of Science and Technology, Chiayi Campus; Department of Pulmonary and Critical Care Medicine, Chang Gung Memorial Hospital, Chiayi; School of Medicine, College of Medicine, Chang Gung University, Taoyuan, Taiwan
3 School of Medicine, College of Medicine, Chang Gung University, Taoyuan; Department of Dermatology, Chang Gung Memorial Hospital, Linkou, Taiwan

Date of Submission09-May-2019
Date of Decision11-Jul-2019
Date of Acceptance06-Aug-2019
Date of Web Publication27-Feb-2020

Correspondence Address:
Ching-Chi Chi
Department of Dermatology, Chang Gung Memorial Hospital, Linkou, No. 5, Fuxing St, Guishan Dist, Taoyuan 33305
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ds.ds_33_19

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  Abstract 


Background: Psoriasis is a chronic inflammatory skin disease that has been associated with various inflammatory comorbidities such as cardiovascular disease and uveitis. Asthma involves inflammation of the airway. The two diseases share cytokine-mediated inflammatory mechanisms. Objectives: The main objective of the study was to examine the association of psoriasis with asthma. Methods: We conducted a systematic review and meta-analysis of observational studies that examined the association of psoriasis with asthma. We searched MEDLINE, Embase, and CENTRAL from inception to May 2, 2019 for relevant case–control, cross-sectional, or cohort studies. The risk of bias of included studies was assessed by using the Newcastle–Ottawa Scale. The random-effects model meta-analysis was used to calculate the odds ratio (OR) for case–control/cross-sectional studies and hazard ratio (HR) for cohort studies. Results: We included six case–control/cross-sectional (one case–control and five cross-sectional studies) and one cohort studies. Three studies were rated with a high risk of bias in case definition, representativeness of the cases, selection of controls, definition of controls, and ascertainment of exposure. Psoriasis was associated with significantly increased odds (OR 1.29; 95% confidence interval [CI] 1.20-'1.37) and risk (HR 1.38; 95% CI 1.23-'1.54) for asthma. A subgroup analysis revealed increased odds for asthma in both pediatric and adult patients with psoriasis (pooled OR being 1.24 [95% CI 1.10-'1.41] and OR 1.38 [95% CI 1.27-'1.50], respectively). Conclusion: The current evidence indicates a significant association of psoriasis with asthma. When psoriasis patients present with respiratory symptoms for shortness of breath, wheezing, and chest tightness, referral to pulmonologist may be considered.

Keywords: Asthma, meta-analysis, psoriasis, systematic review


How to cite this article:
Fang TP, Lin YC, Chi CC. Association of psoriasis with asthma: A systematic review and meta-analysis of observational studies. Dermatol Sin 2020;38:22-7

How to cite this URL:
Fang TP, Lin YC, Chi CC. Association of psoriasis with asthma: A systematic review and meta-analysis of observational studies. Dermatol Sin [serial online] 2020 [cited 2020 Apr 6];38:22-7. Available from: http://www.dermsinica.org/text.asp?2020/38/1/22/279603




  Introduction Top


Psoriasis is a chronic inflammatory skin disease that may affect both children and adults.[1],[2] Psoriasis is characterized by abnormal differentiation and hyperproliferation of keratinocytes,[3] which may vary in severity from mild localized plaques to generalized nearly the whole body.[4]

The prevalence of psoriasis was estimated as 0.5%-'11.4% in adults and 0%-'1.4% in children.[5] Psoriasis has been classified into two types according to the age of onset: type I (early-onset) psoriasis with age of onset before 40 years and peak age of onset being 16–22 years and type II (late-onset) psoriasis with age of onset at ≥40 years and peak age of onset at 57-'60 years.[6] The prevalence of psoriasis is higher in men than in women.[7],[8]

Psoriasis is no longer considered just a skin disease. Recent studies have demonstrated that psoriasis which has been associated with various inflammatory and immunologic comorbidities such as cardiovascular disease,[3] chronic kidney disease,[9] uveitis,[10] thyroid diseases,[11] inflammatory bowel disease,[12] vitiligo,[13] and multiple sclerosis.[14]

Asthma is a worldwide public health problem associated with chronic inflammation of the airways and characterized with airway hyperresponsiveness.[15] Both psoriasis and asthma have shared inflammatory cytokine-mediated mechanisms.[16] In addition, involvement of T-helper 17 (Th17) cells and Th17-associated cytokines, such as interleukin (IL)-17A and IL-17 receptor A, has been proposed as the common pathway in both psoriasis and asthma.[8],[17],[18] Psoriasis is a prototypic Th17-mediated disease with skin-infiltrating Th17 cells as the central players in the pathogenesis of psoriasis.[19] One previous Scottish population-based cross-sectional study found an increased prevalence of psoriasis in patients with asthma.[20] The objective of this study was to examine whether psoriasis is associated with asthma.


  Materials and Methods Top


Literature search

We conducted a systematic search of MEDLINE, Embase, and Cochrane Central Register of Controlled Trials from inception to May 2, 2019 for relevant studies. The search strategy is shown in [Table 1]. No language limitations were imposed. Case–control, cross-sectional, and cohort studies that examined the association of psoriasis with asthma were eligible for inclusion.
Table 1: Search strategy

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Study selection

Our inclusion criteria were: (1) study design being case–control, cross-sectional, or cohort study; (2) the case/exposure group comprised people diagnosed with psoriasis and the control group comprised individuals without psoriasis; and (3) the outcomes of interest was the odds of prevalent asthma or the risk of incident asthma. Two authors scanned the titles and abstracts of the search results and selected potentially eligible studies. We examined the full text to determine whether a study met our inclusion criteria. We excluded studies that employed the same data source or did not provide usable data for assessing the association of psoriasis with asthma. Disagreement was resolved by discussion.

Data extraction

For each included study, we extracted the following data determined a priori: first author, publication year, country, study design, case/exposure group, control group, characteristics of study participants (including age), and measures of association.

Risk of bias assessment

The risk of bias was assessed by using the Newcastle–Ottawa Scale (NOS).[21] The NOS applies three domains (selection of study groups, comparability, and outcome assessment) to evaluate the risk of bias of observational studies.

Statistical analysis

The association of psoriasis with asthma was expressed as odds ratio (OR) with 95% confidence interval (CI) in case–control and cross-sectional studies, and as hazard ratio (HR) with 95% CI in cohort studies. The Review Manager Version 5.3 (Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014) was used for conducting meta-analysis. Using the inverse variance method, we performed a random-effects model meta-analysis because we expected considerable clinical heterogeneity.

We also performed subgroup analyses according to the severity of psoriasis and age groups of study participants, i.e., those with severe psoriasis versus mild psoriasis and below 18 years (pediatric group) versus equal or above 18 years (adult group). The I2 statistic was calculated for assessing the statistical heterogeneity across the included studies. An I2 value of ≥ 50% represents substantial heterogeneity.[22]


  Results Top


Characteristics of included studies

As illustrated in [Figure 1], 802 records were identified from our search and 2 records were obtained from other sources (1 from a relevant review and 1 provided by an author [CC]). After removing duplicates, 651 records were available for screening. We excluded 642 records that did not meet our inclusion criteria. We included six case–control/cross-sectional (one case–control and five cross-sectional studies) and one cohort studies, with six providing usable data for meta-analyses. Two studies used overlapped study subjects, with one using data from March 1995 to the end of 2008 of the National Health Insurance Research Database[7] and the other using data between January 1, 2006 and December 31, 2007 of the same database.[23] Therefore, we excluded the latter study.[23]
Figure 1: PRISMA study flow diagram

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The characteristics of the included studies are summarized in [Table 2]. These studies were published between 2011 and 2017. The study subjects in five included studies were Caucasians,[1],[24],[25],[26],[27] while the study subjects of the other two studies were Asian populations.[3],[8] Two included studies reported data on pediatric populations,[1],[27] and three studies provided data on adults.[24],[25],[26] Three studies were rated with a high risk of bias in case definition, representativeness of the cases, selection of controls, definition of controls, and ascertainment of exposure [Figure 2]a. The one included cohort study was rated low risk of bias for all domains except for “adequacy of follow-up” where no relevant descriptions were provided [Figure 2]b. Asthma was identified by the use of ICD codes in five studies[1],[7],[8],[26],[27] and self-report in two studies.[24],[25]
Table 2: Characteristics of included studies

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Figure 2: Risk of bias of (a) the included case–control/cross-sectional studies and (b) the included cohort study

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Association of psoriasis with asthma

As illustrated in [Table 2], the prevalence of asthma in the psoriasis group ranged from 1.66% to 12.19% while that of the control group was 1.35%–9.50%. Only one cohort study examined the risk of asthma and the incidence of asthma was 6.41/1000 person-years in the psoriasis group and 4.38/1000 person-years in the control group.[8] As shown in [Figure 3], all six included case–control and cross-sectional studies found that people with psoriasis were associated with significantly increased odds of asthma (pooled OR 1.29; 95% CI 1.20-'1.37; studies = 6). The statistical heterogeneity was low (I2 = 33%). Consistently, the included cohort study showed an increased risk of asthma in people with psoriasis (HR 1.38; 95% CI 1.23-'1.54; study = 1).[8]
Figure 3: Odds of asthma in relation to psoriasis. CI: Confidence interval, SE: Standard error

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As illustrated in [Figure 4], the subgroup analysis based on age groups found increased odds of asthma in both the pediatric (pooled OR 1.24; 95% CI 1.10-'1.41; studies = 2) and adult populations (pooled OR 1.38; 95% CI 1.27-'1.50; studies = 3). No significant difference between the pediatric and adult subgroups in the odds of asthma was found (P = 0.180).
Figure 4: Subgroup analysis based on age groups. CI: Confidence interval, SE: Standard error

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  Discussion Top


Our study found a significant association of psoriasis with asthma. Compared to nonpsoriatic controls, psoriasis patients had 1.29-fold odds for prevalent asthma and 1.38-fold risk for incident asthma. Our stratified analysis based on age found significantly increased odds for asthma in both pediatric and adult psoriasis patients, with no significant difference between the two age groups.

Two case–control studies examined the respective OR for asthma in patients with mild and moderate-to-severe psoriasis.[7],[27] The Galili et al. 2017 study did not report the methods of classifying severity of psoriasis,[27] while the Tsai et al. 2011 study employed treatment pattern to identify the severity of psoriasis.[7] Therefore, we did not perform a meta-analysis based on the severity of psoriasis as the stratified data from the two studies might have not been comparable.

The exact mechanism of association of psoriasis with asthma is unclear but may be related to chronic inflammation. Pro-inflammatory cytokines, for example, IL-17 are released from active psoriatic plaques through the bloodstream and trigger inflammation of other organs. The “psoriatic march” has been proposed to explain the association of psoriasis and cardiovascular comorbidities driven by systemic inflammation.[28] The same mechanism may be applied to the respiratory comorbidities of psoriasis, including asthma found in this study.[29] Genetic factors may be another explanation for the association between psoriasis and asthma. A previous twin study indicated that the association between psoriasis and asthma may be explained in part by a shared genetic factor between the two diseases.[25]

There has been one similar systematic review that examined the association between psoriasis and asthma by Wang et al.[2] Both the studies of ours and Wang et al. found a significant association of psoriasis with asthma. However, our study has the following strengths compared to the study by Wang et al. First, we excluded the study by Yang et al.[23] because they used data overlapped with another study.[7] Therefore, our study avoids double counting of the same data and resultant overestimation of the association between psoriasis and asthma. Second, we reclassified the study of Tsai et al.[7] as a case–control study after reading its full text. We recalculated the OR values and improved the accuracy of effect estimates on the association of psoriasis with asthma. Third, we included one new study[26] and conducted a updated meta-analysis on the association of psoriasis with asthma.


  Conclusion Top


The current evidence indicates a significant association of psoriasis with asthma. Patients with psoriasis should be educated of potentially comorbid asthma. When psoriasis patients present with respiratory symptoms for example shortness of breath, wheezing, and chest tightness, referred to pulmonologist may be considered. On the other hand, further studies that provide specific data for groups of different ages, genders, or population are needed to clarify which subgroups of patients with psoriasis have an increased risk of asthma. Furthermore, additional prospective cohort studies are required to evaluate the causal relationship between psoriasis and asthma.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Augustin M, Radtke MA, Glaeske G, Reich K, Christophers E, Schaefer I, et al. Epidemiology and comorbidity in children with psoriasis and atopic eczema. Dermatology 2015;231:35-40.  Back to cited text no. 1
    
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Wang J, Ke R, Shi W, Yan X, Wang Q, Zhang Q, et al. Association between psoriasis and asthma risk: A meta-analysis. Allergy Asthma Proc 2018;39:103-9.  Back to cited text no. 2
    
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Tsai TF, Lee CH, Huang YH, Chi CC, Chang YT, Wong TW, et al. Taiwanese dermatological association consensus statement on management of psoriasis. Dermatol Sinica 2017;35:66-77.  Back to cited text no. 3
    
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Menter A, Gottlieb A, Feldman SR, Van Voorhees AS, Leonardi CL, Gordon KB, et al. Guidelines of care for the management of psoriasis and psoriatic arthritis: Section 1. Overview of psoriasis and guidelines of care for the treatment of psoriasis with biologics. J Am Acad Dermatol 2008;58:826-50.  Back to cited text no. 4
    
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Tsai TF, Wang TS, Hung ST, Tsai PI, Schenkel B, Zhang M, et al. Epidemiology and comorbidities of psoriasis patients in a national database in Taiwan. J Dermatol Sci 2011;63:40-6.  Back to cited text no. 7
    
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Fang HY, Liao WC, Lin CL, Chen CH, Kao CH. Association between psoriasis and asthma: A population-based retrospective cohort analysis. Br J Dermatol 2015;172:1066-71.  Back to cited text no. 8
    
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Chi CC, Wang J, Chen YF, Wang SH, Chen FL, Tung TH, et al. Risk of incident chronic kidney disease and end-stage renal disease in patients with psoriasis: A nationwide population-based cohort study. J Dermatol Sci 2015;78:232-8.  Back to cited text no. 9
    
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Chi CC, Tung TH, Wang J, Lin YS, Chen YF, Hsu TK, et al. Risk of uveitis among people with psoriasis: A nationwide cohort study. JAMA Ophthalmol 2017;135:415-22.  Back to cited text no. 10
    
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Wang SH, Wang J, Lin YS, Tung TH, Chi CC. Increased risk for incident thyroid diseases in people with psoriatic disease: A cohort study. J Am Acad Dermatol 2019;80:1006-12.  Back to cited text no. 11
    
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Yen H, Chi CC. Association between psoriasis and vitiligo: A systematic review and meta-analysis. Am J Clin Dermatol 2019;20:31-40.  Back to cited text no. 13
    
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Liu CY, Tung TH, Lee CY, Chang KH, Wang SH, Chi CC, et al. Association of multiple sclerosis with psoriasis: A systematic review and meta-analysis of observational studies. Am J Clin Dermatol 2019;20:201-8.  Back to cited text no. 14
    
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Ballardini N. The association between psoriasis and asthma. Br J Dermatol 2015;172:1485-6.  Back to cited text no. 15
    
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Li Y, Hua S. Mechanisms of pathogenesis in allergic asthma: Role of interleukin-23. Respirology 2014;19:663-9.  Back to cited text no. 16
    
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Egeberg A, Khalid U, Gislason GH, Mallbris L, Skov L, Hansen PR, et al. Risk of psoriasis in patients with childhood asthma: A Danish nationwide cohort study. Br J Dermatol 2015;173:159-64.  Back to cited text no. 17
    
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Amarnani A, Rosenthal KS, Mercado JM, Brodell RT. Concurrent treatment of chronic psoriasis and asthma with ustekinumab. J Dermatolog Treat 2014;25:63-6.  Back to cited text no. 18
    
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Eberle FC, Brück J, Holstein J, Hirahara K, Ghoreschi K. Recent advances in understanding psoriasis. F1000Res 2016;5. pii: F1000 Faculty Rev-770.  Back to cited text no. 19
    
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Weatherburn CJ, Guthrie B, Mercer SW, Morales DR. Comorbidities in adults with asthma: Population-based cross-sectional analysis of 1.4 million adults in Scotland. Clin Exp Allergy 2017;47:1246-52.  Back to cited text no. 20
    
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Wells G, Shea B, O'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. Ontario: Ottawa Hospital Research Institute; 2018.  Back to cited text no. 21
    
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Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions. Chichester: John Wiley and Sons; 2011.  Back to cited text no. 22
    
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Yang YW, Keller JJ, Lin HC. Medical comorbidity associated with psoriasis in adults: A population-based study. Br J Dermatol 2011;165:1037-43.  Back to cited text no. 23
    
24.
Hajdarbegovic E, Nijsten T, Westgeest A, Habraken F, Hollestein L, Thio B, et al. Decreased prevalence of atopic features in patients with psoriatic arthritis, but not in psoriasis vulgaris. J Am Acad Dermatol 2013;68:270-7.  Back to cited text no. 24
    
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Lønnberg AS, Skov L, Skytthe A, Kyvik KO, Pedersen OB, Meteran H, et al. Asthma in patients with psoriasis. Br J Dermatol 2015;172:1660-1.  Back to cited text no. 25
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

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