Available via license: CC BY 4.0
Content may be subject to copyright.
Received: 14 April 2023
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Revised: 16 September 2023
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Accepted: 20 September 2023
DOI: 10.1002/cre2.794
REVIEW ARTICLE
Serum level of vitamin D in patients with recurrent aphthous
stomatitis: A systematic review and meta‐analysis
of case control studies
Roya Safari‐Faramani
1
|Mohsen Salehi
2
|Saman Ghambari Haji Shore
2
|
Neda Omidpanah
3
1
Research Center for Environmental
Determinants of Health, School of Public
Health, Kermanshah University of Medical
Sciences, Kermanshah, Iran
2
Students Research Committee, Kermanshah
University of Medical Sciences,
Kermanshah, Iran
3
Department of Oral and Maxillofacial
Medicine, School of Dentistry, Kermanshah
University of Medical Sciences,
Kermanshah, Iran
Correspondence
Neda Omidpanah, Department of Oral and
Maxillofacial Medicine, School of Dentistry,
Kermanshah University of Medical Sciences,
Dental School, Shariati Ave, Kermanshah, Iran.
Email: n.omidpanah20000@gmail.com
Funding information
Research Committee of Kermanshah
University of Medical Sciences
Abstract
Objectives: Recurrent aphthous stomatitis (RAS) is an ulcerative condition with
unknown etiology. The effect of vitamin D in the etiology of RAS is still a matter of
controversy. In this study, we aimed at review the available evidence on the role of
vitamin D deficiency in RAS etiology.
Material and Methods: PubMed, Cochrane Library for Systematic Reviews, ISI Web of
Science, Scopus, and EmBase were systematically searched for evidence on RAS and
vitamin D up to January 2020. Retrieved records were screened and assessed by two
of the authors independently. Newcastle−Ottawa scale was used to assess the quality
of individual studies. AMSTAR tool was used for assessing the quality of the study.
Results: Eight studies including 383 healthy control and 352 patients with RAS were
eligible for the meta‐analysis. Serum vitamin D levels were significantly lower in RAS
patients. The weighted mean difference was −7.90 (95% CI: −11.96 to −3.85).
Conclusions: The results highlighted the importance of vitamin D deficiency in the
etiology of RAS. However, more studies are needed to reach a robust decision. The
observed association between vitamin D and RAS is probably due to the effect of
vitamin D on the immune system.
KEYWORDS
recurrent aphthous stomatitis, vitamin D
1|BACKGROUND
Recurrent aphthous stomatitis (RAS) is the most common lesion
of the oral mucosa, with a prevalence of from 5% to 66% in the
general population (Akintoye & Greenberg, 2005; Scully, 2006). RAS
is diagnosed by ruling out other possible causes of stomatitis
(Krisdapong et al., 2012; Tabolli et al., 2009). RAS is morphologically
divided into three categories: minor, major, and herpetiform, the most
common form of which is minor and accounts for 85% of RAS lesions
and it does not leave scars. The major type is more widespread and
its size is larger than 10 mm, and its recovery is accompanied by the
creation of scars. The herpetic type is a form of multiple deep
wounds with irregular edges (Feng et al., 2015).
Although the underlying causes of RAS are unclear, some
research has shown that systemic factors, including genetics,
immunological, and hematological abnormalities, as well as other
Clin Exp Dent Res. 2023;1–7. wileyonlinelibrary.com/journal/cre2
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This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
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© 2023 The Authors. Clinical and Experimental Dental Research published by John Wiley & Sons Ltd.
factors such as trauma, smoking, stress, nutritional deficiencies, and
allergies, are among the potential causes (Rivera‐Hidalgo et al., 2004;
Slebioda et al., 2014). These initiating factors cause the secretion of
preinflammatory cytokines by infiltration of leukocytes against a
specific area of the oral mucosa depending on the extent and severity
of the disease (Rivera‐Hidalgo et al., 2004; Slebioda et al., 2014;
Tabolli et al., 2009).
Hydroxyvitamin D (25‐OHD), also known as vitamin D, is a type
of fat‐soluble vitamin. It is produced in the skin through exposure to
sunlight and can also be obtained from certain foods and supple-
ments. Vitamin D deficiency can occur due to insufficient sunlight
exposure, reduced availability, or certain medications such as
glucocorticoids, antiretroviral drugs, or anticonvulsants (Straube
et al., 2015). Vitamin D receptors (VDR) are present in many tissues
throughout the body, and a lack of 25‐OHD has been associated with
various health conditions, including musculoskeletal disorders,
metabolic and autoimmune diseases, respiratory and cardiovascular
issues, cancer, psychiatric disorders, chronic pain, and hypo-
thyroidism (Adorini, 2005; Taheriniya et al., 2021).
Recently, the role of vitamin D in the etiopathogenesis of RAS
has been highlighted, (Ali, 2019; Bahramian et al., 2018).
1,25 Dihydroxyvitamin D, a bioactive form of vitamin D3, a
steroid hormone, has a crucial role in calcium and bone metabolism
(Adorini, 2005). Vitamin D endocrine system has the property of
regulating immune and inflammatory responses. The cells of the
innate and adaptive immune system, such as macrophages, T cell,
B cell, express the dendritic cells that receive vitamin D (VDR) and are
involved in the production and response to vitamin D. The net effect
of vitamin D on the immune system is to increase intrinsic immunity
with multiple adaptive immune systems (Adorini et al., 2004).
The role of vitamin D in the development of RAS has been a
subject of debate in recent studies. Several investigations have
examined the potential connection between low levels of vitamin D
and the occurrence of RAS, yielding conflicting findings. While certain
studies have indicated a correlation between vitamin D deficiency
and the onset of RAS, (Ali, 2019; Bahramian et al., 2018; Khabbazi
et al., 2015; Öztekin & Öztekin, 2018) others have not definitively
established the role of vitamin D deficiency in RAS lesions (Krawiecka
et al., 2017; Suhail et al., 2019). The objective of the current study
was to conduct a systematic review of the available evidence
concerning the influence of vitamin D deficiency on the pathogenesis
of RAS.
2|METHODS
2.1 |Protocol and registration
The Preferred Reporting Items for Systematic Review and Meta‐
Analyses (PRISMA) guideline followed to report the results of this
systematic review (Liberati, 2009) and was registered on the
International prospective register of systematic reviews, PROSPERO
(CRD42019138725).
2.2 |Focused question (based on PICO criteria)
The study was designed to answer if the level of serum vitamin D is
different between patients with RAS and healthy controls. The study
question was clarified based on the PICO categories (i.e., population,
intervention [exposure in this study], comparison group, and
outcomes).
2.3 |Search strategy
A systematic search was conducted in electronic databases (Scopus,
Web of Science, PubMed, Embase, and Cochrane Library) up to January
2020, without language restrictions. The search terms used “Aphthous”
or “Oral ulcer”or “Sutton's disease”or “recurrent aphthous were
Stomatitis”and “25‐hydroxy vitamin D”or “vitamin D.”
2.4 |Eligibility criteria and study selection process
Inclusion criteria were observational studies that reported levels
vitamin D in saliva or serum, between the RAS patients and healthy
controls. Exclusion criteria included commentaries, letters to the
editor, editorials, case reports, reviews/systematic reviews, confer-
ence abstracts, book chapters, and studies with irrelevant data.
Based on the inclusion criteria, the eligibility of each article was
evaluated by reviewing their titles and abstracts. Two reviewers
independently evaluated the titles and abstracts for this purpose.
Disagreements were resolved following discussion with a third
reviewer. Next, the full‐texts of the suggested potential eligible
articles were retrieved and screened. The reasons for exclusion of
articles were documented.
2.5 |Data extraction
Two reviewers independently extracted the data from the full‐texts
of articles based on a predetermined form and a third reviewer
checked the extracted data. The following details were extracted:
authors, publication year, sample size in each group, mean age of the
participants, male percent, laboratory method, and serum or saliva
level of vitamin D in each group.
2.6 |Risk of bias assessment
Newcastle−Ottawa quality assessment scale for case control
studies was used to assess the risk of bias in the individual studies
(Wells et al., 2014).
The Newcastle−Ottawa scale is based on three main domains
including selection, comparability, and exposure. This tool also served
to classify the quality of each study as either high (7 or above), fair
(between 4 and 7), or low (less than 4). One of the authors performed
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SAFARI‐FARAMANI ET AL.
this quality assessment. The quality assessment was conducted by
one author. To assess the quality of the present systematic review,
AMSTAR 2 (Assessing the Methodological Quality of Systematic
Reviews) tool was used (Shea et al., 2017).
2.7 |Statistical methods
The standard mean difference and its 95% confidence interval (CI)
were calculated for each study using Review Manager 5.3 (RevMan
5.3; Cochrane Collaboration). These values were used to assess the
difference in salivary and serum vitamin D levels between patients
with RAS and healthy controls. A p‐value less than .05 was
considered statistically significant. To evaluate the heterogeneity
among the studies, the I
2
statistic was used. A p‐value less than .1
(I
2
> 50%) indicated significant heterogeneity, leading to the use of a
random‐effects model for the analysis.
Funnel plot analysis was performed using the Comprehensive
Meta‐Analysis version 2.0 (CMA 2.0) software. Both Egger's and
Begg's tests were used to assess publication bias, with a p‐value less
than .05 (two‐tailed) indicating significant publication bias.
The unit of measurement for salivary and serum vitamin D levels
in this meta‐analysis was ng/mL.
The study protocol was funded and registered in the Research
Committee of Kermanshah University of Medical Sciences.
3|RESULTS
3.1 |Study selection
After removing the duplicates literature search yielded 120 records.
After excluding the irrelevant title and abstracts, 17 studies were
chosen to be potentially eligible for the review. Of which, three did
not report vitamin D levels; one did not have a control group and in
the other five, RAS was the manifestation of the other disease.
Finally, eight studies were included for the final review. Details of the
study selection are depicted in Figure 1.
FIGURE 1 Flow diagram of literature search.
SAFARI‐FARAMANI ET AL.
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3.2 |Study characteristics
The characteristics of the included case‐control studies are presented
in Table 1.
Eight studies including 383 healthy control and 352 patients with
RAS were eligible for the meta‐analysis. The mean age of the
participants ranged from 8.7 to 36.4 in RAS patients and 7.6 to 40.8
in healthy controls.
Out of eight studies included in the meta‐analysis, two studies
were from Iran (Bahramian et al., 2018; Khabbazi et al., 2015),
three from Turkey (Nalbantoğlu & Nalbantoğlu, 2019; Öztekin &
Öztekin, 2018; Tamer & Avcı,2019), one from Poland (Krawiecka
et al., 2017), one from United Arab Emirates (Suhail et al., 2019), and
one from Iraq (Ali, 2019).
One study (Bahramian et al., 2018) reported vitamin D levels on
saliva and serum and the rest of studies on serum. Five studies assessed
the association between serum levels of vitamin D and RAS variables
such as duration, severity, and frequency (Ali, 2019; Khabbazi
et al., 2015; Krawiecka et al., 2017; Liberati, 2009; Suhail et al., 2019).
The measurement method of serum levels of vitamin d in three
(Ali, 2019; Khabbazi et al., 2015;Nalbantoğlu & Nalbantoğlu, 2019)
studies was ELISA (enzyme‐linked immunosorbent assay) and four
(Bahramian et al., 2018; Krawiecka et al., 2017; Öztekin & Öztekin, 2018;
Suhail et al., 2019) studies was ECLAI (electro‐chemiluminescencbinding
assay) and one study did not report (Tamer & Avcı,2019).
Mean age, male percent, rest of the data are shown in Table 1.
3.3 |Risk of bias assessment
Results of the risk of bias assessment for individual studies are presented
in Table 2. The total score for all the included studies was more than 5.
3.4 |Meta‐analysis reports
Figure 2shows serum levels of vitamin D in RAS and healthy controls.
Out of the eight included studies, two studies didn't find significant
differences between serum vitamin D levels in patients with RAS and
healthy controls (Bahramian et al., 2018; Krawiecka et al., 2017). One
study demonstrated a significant association between serum levels of
vitamin D and number ulcer in patients with RAS (Bahramian et al., 2018).
In general, serum vitamin D levels were significantly lower in RAS
patients. The weighted mean difference was −7.90 (95% CI: −11.96 to
−3.85) which was significantly differ from zero, (z= 3.82, p<.0001).
Heterogeneity χ
2
was 45.7 (degree of freedom = 7, p< .0001) (Figure 2).
3.5 |Publication bias
The symmetrical funnel plot using the Begg's and Egger's tests
showed low risk of publication bias (the pvalues for the Begg' and
Egger's tests were .536 and .851, respectively).
TABLE 1 Characteristics of studies included in the systematic review on comparing the level of vitamin D levels in RAS patients and the healthy controls.
Author Year of publication, country
Mean age, male percent (%)
Method RAS type
Sample size
Mean ± SD of serum vitamin D
(ng/mL)
RAS patients Healthy controls RAS patients Healthy controls RAS patients Healthy controls
Funda Tamer 2018, Turkey 34−25 33.9−30 NR Minor 20 20 13.6 ± 6.5 20.9 ± 10
Al‐Amad Suhail 2019, United Arab Emirates 34−66 31−66 ECLIA Idiopathic minor 52 52 53.6 ± 24.6 51.1 ± 26.9
Ayla Bahramian 2018, Iran 38.8−61.5 40.8−65.4 ECLIA Idiopathic minor 26 26 33.07 ± 12.41 50.89 ± 9.3
Alireza Khabbazi 2014, Iran 33.4−60.8 34.1−61.2 ELISA Idiopathic minor 46 49 12.1 ± 7.7 27.4 ± 9.7
Ewa Krawiecka1 2017, Poland 34.15−36.4 32.05−24.2 ECLIA Minor, major, herpetiform 66 66 16.81 ± 8.45 19.22 ± 10.44
Aynure Öztekin 2018, Turkey 31.2−37.5 27.4−45.7 ECLIA Idiopathic minor 40 70 11 ± 7.03 16.4 ± 10.19
Nalbantoğlu, A. 2019, Turkey 8.7−46.1 7.6−51.4 ELISA Idiopathic minor 72 70 16.4 ± 8.6 23.1 ± 11.5
Ali, N. S. M. 2019, Iraq 36.4−0 33.64−0 ELISA Idiopathic minor 30 30 13.9 ± 12.72 22.08 ± 17.779
Abbreviations: ELISA, enzyme‐linked immunosorbent assay; RAS, recurrent aphthous stomatitis.
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SAFARI‐FARAMANI ET AL.
3.6 |Sensitivity analysis
Sensitivity analysis was performed by omitting one study in turn, with
the pooled weighted mean difference varied between −9.04 (95% CI:
−10.72 to −7.37) and −5.97 (95% CI: −7.62 to −4.34), supporting the
stability of the results.
3.7 |The quality of the systematic review
The quality of evidence was evaluated using the second version of
AMSTAR tool. A score of 15 out of 16 was obtained.
4|DISCUSSION
In the present study published evidence on the role of vitamin D
deficiency in the occurrence of RAS has been systematically
reviewedandtheresultshavebeensummedupviameta‐
analysis. Based on the results, the serum level of vitamin D was
significantly lower in patients suffering RAS compared to the
healthy controls. However, we did not find an association between
a vitamin D deficiency and frequency of ulcers in RAS patients.
Previous research has often associated multivitamin deficiency in
RAS patients with hematinic deficiencies such as vitamin B12, folic
acid, and iron (Chen et al., 2015). However, our systematic review
indicates that vitamin D levels appear to be lower in RAS patients
compared to controls.
RAS is a painful condition that negatively impacts eating, speech,
and oral hygiene. The frequent and severe relapses can significantly
reduce the quality of life. The exact cause of RAS is not completely
understood (Lopez‐Jornet et al., 2014; Saikaly et al., 2018). The
results of the current study consistent with many previous studies
that demonstrated Low levels of vitamin D in autoimmune diseases
such as rheumatoid arthritis, systemic lupus erythematosus, MS, type
1 diabetes, inflammatory bowel disease, and psoriasis (Bergler‐Czop
& Brzezińska‐Wcisło, 2016; Cutolo et al., 2006; Hyppönen
et al., 2001; Teichmann et al., 1999).
How vitamin D affects RAS is not yet well understood. Given
that the immunological context for RAS has been determined. The
VDR and the vitamin D activating enzyme (1‐α‐hydroxylase)
TABLE 2 Risk of bias assessment of primary studies based on
Newcastle−Ottawa scale for case control studies.
Author Selection Comparability Exposure
Total
score
Funda Tamer 2 1 2 5
Al‐Amad Suhail 3 1 2 6
Ayla Bahramian 3 1 2 6
Alireza Khabbazi 3 1 2 6
Ewa Krawiecka1 3 1 2 6
Aynure Öztekin 3 1 2 6
Nalbantoğlu, A. 3 1 3 7
Ali, N. S. M. 2 1 2 5
FIGURE 2 Weighted mean difference (WMD) of vitamin D levels between RAS patients and the healthy controls. Random effects model
was applied. RAS, recurrent aphthous stomatitis.
SAFARI‐FARAMANI ET AL.
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are expressed in various immune cells found, including T cells,
macrophages, and dendritic cells and in the epithelial tissue of the
oral mucosa. Low levels of vitamin D in RAS patients were associated
with the VDR, proinflammatory cytokines, strong immunomodulatory
effects, and T helper cells. T helper cells induce proinflammatory
cytokines, leading to epithelial damage or ulcers (Adorini, 2002; Chen
et al., 2015).
Vitamin D deficiency in RAS‐related diseases such as Behcet's
syndrome and PFAPA (priodic fever, aphthous stomatitis, pharangits,
and cervical adenitis) that one of the main symptoms of which is RAS,
has been proven (Aslan et al., 2017; Faydhi et al., 2022). According to
Ainure Oztekin study, patients with RAS could benefit from taking
vitamin D as a supportive treatment (Öztekin & Öztekin, 2018).
Therefore, reducing vitamin D levels might play a role in the
development of RAS, for the reasons mentioned above.
Limitations: (1) Studies did not have a similar method for
measuring vitamin D levels. (2) Patients with different types of RAS
were included in the studies. (3) varying male‐to‐female ratios.
(4) The geographical location of the studies, which were seven
conducted in Asia. These factors contributed to high heterogeneity
between the studies.
Strengths: (1) we had no publication bias across studies. (2) One
study being of high quality and seven studies being of moderate
quality according to the NOS tool. (3) Most studies were matched
by sex and age. (4) Sensitivity analysis supported the stability
of the results.
5|CONCLUSION
There was a relationship between low vitamin D in serum and RAS.
Therefore, it may be worthwhile to check vitamin D levels in patients
with RAS.
AUTHOR CONTRIBUTIONS
Roya Safari‐Faramani, Mohsen Salehi, and Saman Ghambari Haji
Shore conceived and designed the study, formulated the research
question, helped in the design of the study, including the screening of
the retrieved records, interpretation of the results as well as the draft
of this paper. Neda Omidpanah, Mohsen Salehi, and Saman Ghambari
Haji Shore screened the retrieved records, extracted the data for this
study, and performed the statistical analysis and interpretation of the
results as well as the draft of this paper. All three authors have given
final approval for this study to be published.
ACKNOWLEDGMENTS
This study is a part of dissertation for Doctoral degree in dentistry
approved in Kermanshah University of Medical Sciences by Mohsen
Salehi. The work was supported by the research deputy of
Kermanshah University of Medical Sciences. This study is a part of
Mohsen Salehi's thesis and has been approve and funded by the
Research Committee of Kermanshah University of Medical Sciences.
The grant number was 980874.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflict of interest.
DATA AVAILABILITY STATEMENT
The data will be avaible upon the request.
ETHICS STATEMENT
This article does not contain any studies with human participants or
animals performed by any of the authors.
ORCID
Neda Omidpanah http://orcid.org/0000-0003-4300-8785
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How to cite this article: Safari‐Faramani, R., Salehi, M.,
Ghambari Haji Shore, S., & Omidpanah, N. (2023). Serum level
of vitamin D in patients with recurrent aphthous stomatitis: A
systematic review and meta‐analysis of case control studies.
Clinical and Experimental Dental Research,1–7.
https://doi.org/10.1002/cre2.794
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