Edited by: Stefano Piaserico, University of Padova, Italy
Reviewed by: Andreas Recke, Universität zu Lübeck, Germany; Irina Khamaganova, Pirogov Russian National Research Medical University, Russia
This article was submitted to Dermatology, a section of the journal Frontiers in Medicine
†These authors have contributed equally to this work
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.
As a long-lasting autoimmune disorder affecting the skin, psoriasis is characterized by scaly, red, and well-demarcated skin plaques resulting from keratinocyte hyperproliferation and altered differentiation, the presence of an inflammatory cell infiltrate, and neovascularization (
Periodontitis is a chronic infectious disease of the tooth-supporting tissues, and its main clinical manifestations are gingival bleeding, periodontal pocket formation, the destruction of connective tissue attachment, and alveolar bone loss (
Several epidemiological studies have noted that patients with psoriasis have a significantly elevated risk of periodontitis compared with nonpsoriasis controls; this is especially true in patients with severe psoriasis and psoriatic arthritis (
We hypothesized that psoriasis patients suffer from worse periodontal health. Therefore, we performed the current meta-analysis to identify all related clinical studies comparing periodontal status indexes between psoriasis patients and nonpsoriasis subjects and then to evaluate whether the periodontal status of psoriasis patients is worse than that of the nonpsoriasis subjects by comparing the clinical periodontal parameters. Through this research, we hope to facilitate a better understanding of the association between psoriasis and periodontal health as well as to provide better evidence-based evaluations and recommendations to clinicians and patients.
For this meta-analysis, we searched PubMed and EMBASE with no language or publication date restrictions on May 20, 2019, to obtain all of the relevant clinical studies for inclusion in our study. The following combination of key words was used: (“periodontitis” OR “periodontal disease”) AND (psoriasis). We additionally searched the reference lists of the included studies, relevant reviews and meta-analyses for additional potential studies.
Following the searches of the electronic databases, studies were selected based on the pre-established inclusion criteria. A study could be included in this meta-analysis if all of the following conditions were met: (1) the study compared the periodontal status between the psoriasis patients and nonpsoriasis subjects; (2) the psoriasis patients were described clearly; (3) data regarding the periodontal indexes were available and could be extracted; and (4) the studies used validated methods to perform the periodontal examinations. However, the articles were excluded if (1) they were reviews, comments, letters or case reports; (2) they were
Study screening was performed by two independent investigators (QP and SQ) based on the criteria above, and a third investigator (WJ) arbitrated when any conflict occurred regarding the suitability of a study for inclusion. At first, the investigators screened all titles and abstracts independently to exclude the duplicates and obviously irrelevant articles. Second, we examined the full texts of all the remaining papers and assessed them for their adherence to prespecified inclusion criteria. Finally, only the articles meeting the inclusion criteria were included in this meta-analysis.
The following information was independently extracted from the included studies by two investigators (ZR and EL): the name of the first author; year of publication; study location (country); numbers, ages, and sexes of participants in psoriasis group and nonpsoriasis group; periodontal parameters; and the results, including the level of alveolar bone loss (ABL), bleeding index (BI), bleeding on probing (BOP), clinical attachment loss (CAL), gingival index (GI), probing depth (PD), plaque index (PI), and the number of remaining or missing teeth.
Study quality was assessed with the Newcastle-Ottawa Quality Assessment Scale in the current meta-analysis (
The data analyses were performed with STATA software (Version 12.0; Stata Corp, College Station, Texas, USA). Because each available periodontal index in the current study was continuous, the weighted mean difference (WMD) with 95% confidence intervals (CIs) was calculated by pooling the means and standard deviations (SD) of each index from all studies, by which we aimed to explore the difference in the periodontal status between the psoriasis group and the nonpsoriasis group. In addition, we assessed the heterogeneity across studies using the
In total, 300 potentially relevant articles were identified after our initial search of PubMed, EMBASE and the references of relevant articles. After excluding the duplicated records, 238 studies were left for screening. Next, 215 records that were irrelevant to our topic were excluded after the titles and abstracts were screened, leaving 23 articles for a further full text review. Finally, 8 studies fulfilled the eligibility criteria and were included in this meta-analysis (
Flow chart for the study selection process.
The publication dates of the 8 included studies ranged from 2013 to 2019. In total, 812 psoriasis patients and 772 nonpsoriasis subjects were studied. Two studies (
Characteristics of the included studies.
Mendes et al. ( |
Brazil | 397 (159/238) | 46.03 ± 8.34 | 359 (119/240) | 47.47 ± 5.06 | Remaining teeth; BOP; PD; CAL | 8 |
Woeste et al. ( |
Germany | 100 (59/41) | 47.4 ± 14.7 | 101 (43/58) | 46.9 ± 16.8 | BOP; missing teeth | 6 |
Sezer et al. ( |
Turkey | 80 (43/37) | 42.88 ± 11.50 | 40 (20/20) | 42.28 ± 11.86 | PD; CAL; PI; BOP | 6 |
Sharma et al. ( |
India | 33 (19/14) | 34.58 ± 3.47 | 35 (18/17) | 34.34 ± 3.11 | PD; CAL | 6 |
Skudutyte-Rysstad et al. ( |
Norway | 50 (38/12) | 44.4 ± 10.2 | 121 (61/60) | 48.6 ± 9.4 | Missing teeth; BOP | 7 |
Üstün et al. ( |
Turkey | 51 (24/27) | 41.73 ± 11.27 | 50 (24/26) | 37.90 ± 11.16 | CAL; PD; PI; GI | 6 |
Fadel et al. ( |
Sweden | 89 (46/43) | 59 ± 10 | 54 (21/33) | 60 ± 11 | Remaining teeth; BOP; ABL | 6 |
Mayer et al. ( |
Israel | 12 (5/7) | 48.7 ± 10.4 | 12 (5/7) | 51.5 ± 9.97 | PD; GI; PI;BOP | 5 |
For the study quality assessment, two studies had ≥7 points (
Six of the included studies reported BOP data in the psoriasis and nonpsoriasis group (
Forest plot of the weighted mean difference in bleeding on probing between the psoriasis and nonpsoriasis groups.
Summary of the periodontal indexes analyzed in this meta-analysis.
BOP | 6 | 9.188 | 4.046 to 14.330 | <0.001 | 73.6 |
PD | 5 | 0.524 | 0.183 to 0.865 | 0.003 | 86.8 |
CAL | 4 | 0.408 | 0.051 to 0.765 | 0.025 | 81.0 |
PI | 3 | 0.186 | −0.170 to 0.543 | 0.306 | 72.1 |
GI | 2 | 0.458 | −0.413 to 1.328 | 0.303 | 92.3 |
Remaining teeth | 2 | −1.709 | −2.106 to −1.312 | <0.001 | 0 |
Missing teeth | 2 | 1.130 | 0.275 to 1.985 | 0.010 | 0 |
ABL | 1 | 0.400 | 0.102 to 0.698 | 0.008 | – |
Five included studies reported PD data for the psoriasis and nonpsoriasis groups (
Forest plot of the weighted mean difference in probing depth between the psoriasis and nonpsoriasis groups.
Four included studies reported the CAL index for the psoriasis and nonpsoriasis groups (
Forest plot of the weighted mean difference in clinical attachment loss between the psoriasis and nonpsoriasis groups.
Three studies reported the results of the PI in both groups (
Forest plot of the weighted mean difference in plaque index between the psoriasis and nonpsoriasis groups.
Two studies reported the results of the GI for the psoriasis and nonpsoriasis groups (
Forest plot of the weighted mean difference in gingival index between the psoriasis and nonpsoriasis groups.
Two studies each reported the results for remaining teeth (
Forest plot of the weighted mean difference in remaining teeth and missing teeth between the psoriasis and nonpsoriasis groups.
Only one study (
There has been increasing interest in the association between periodontal disease and chronic inflammatory diseases or systemic diseases, although the underlying nature of the association is not fully understood (
In total, we included 8 studies in this meta-analysis (
Several prospective studies have explored the relationship between periodontitis and psoriasis, some of which also had similar results to those in our current study. Egeberg et al. investigated the association between psoriasis and periodontitis in a nationwide cohort study, and they found a significant increase in the risk of periodontitis that was associated with psoriasis, especially in patients with severe psoriasis and psoriatic arthritis (
Our meta-analysis results supported our hypothesis, namely, psoriasis patients suffer from worse periodontal health. Based on previous reports, despite the uncertainty regarding the specific mechanism by which periodontitis and psoriasis interact, several factors may contribute to the worse periodontal status of psoriasis patients. First, infection may play a role. Periodontitis is a chronic infectious disease of the tooth-supporting tissues. Some types of microbes play important roles in the occurrence and development of the disease (
In order to give a clear and reliable answer to the periodontal status difference between the psoriasis and nonpsoriasis patients, it is crucial to control confounding factors. As we have mentioned above, many factors, such as smoking, age, gender, drinking and some disease such as diabetes, obesity, COPD, are the common risk factors between periodontitis and psoriasis. It is undeniable that these confounding factors may affect the occurrence, development and treatment of these two disease. For example, smoking could not only affect the periodontal status, but also affect oxidative stress, interaction with active signaling pathways in psoriasis and vascular influences (
Unfortunately, despite our meta-analysis and related clinical studies revealing that psoriasis patients suffer from worse periodontal health, whether active treatment of periodontal disease contributes to improved outcomes for psoriasis patients has not yet been studied. Keller et al. found that treatment for periodontitis could attenuate the risk for subsequent psoriasis but could not eliminate the risk completely (
To the best of our knowledge, this is the first meta-analysis to specifically compare the periodontal statuses of psoriasis patients and nonpsoriasis subjects, by which we aimed to provide more evidence regarding the association between psoriasis and periodontal disease. However, we must acknowledge that there are limitations in our meta-analysis. First, the number of studies that reported each periodontal index was limited. For four indexes (GI, remaining teeth, missing teeth, ABL), there were fewer than 3 studies. Second, the comprehensive analysis revealed high levels of heterogeneity for some indexes; therefore, random effects models were adopted. Third, because of the limited study number included in our meta-analysis, we did not perform subgroup analyses or meta-regression analysis to explore related risk factors. Therefore, the findings should be interpreted with caution, and well-designed studies are needed in the future.
In summary, our meta-analysis supports the hypothesis that psoriasis patients suffer from worse periodontal health compared with nonpsoriasis subjects, mainly including worse gingival inflammation, more alveolar bone loss, fewer remaining teeth and more missing teeth. These results indicate that we must pay more attention to periodontal health during the prevention, occurrence, and treatment of psoriasis. In addition, we call for further research about the effect of the treatment of periodontal disease on psoriasis. Considering the limitations of this meta-analysis, more high-quality and well-designed studies are needed to validate our conclusion in the future.
All datasets generated for this study are included in the manuscript/
PQ and QS: literature search, study selection, and risk of bias evaluation. RZ, LE, and PW: data extraction and data analysis. PQ, QS, RZ, and JW: manuscript drafting and revision. HL and JW are the corresponding authors, and they undertook the work of designing this meta-analysis. All authors read and approved the final manuscript.
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.
The Supplementary Material for this article can be found online at:
Egger's publication bias plot of bleeding on probing.
Egger's publication bias plot of probing depth.