Interrelation of periodontal parameters between asthmatics and nonasthmatics subjects: a systematic review and meta-analysis

Abstract

Background

The aim of this systematic review (SR) is to evaluate the association between asthma and periodontal parameters.

Methods

An electronic search without date or language restrictions ​​was carried out in MEDLINE, Cochrane, Web of Science, and LILACS until May 2017. In addition, manual search and in the grey literature were also conducted. The search process, data analysis, and quality assessment were performed by two independent reviewing authors. Eligibility criteria included prospective and retrospective cohort studies, case-controls, and randomized clinical trials. For the meta-analysis, the inverse variance method was used in fixed or random effect models, which were chosen according to heterogeneity. The estimates of the intervention effects were expressed as the mean differences.

Results

The search and selection process yielded 21 studies, published between 1979 and 2017. The meta-analysis showed a statistically significant difference for the parameters of gingival bleeding, plaque index, and gingival index for asthmatic participants with P < 0.0001, P < 0.0001, and P = 0.0005, respectively.

Conclusions

The data from this SR suggest that asthmatic patients may be more susceptible to negative periodontal changes, althought further high-quality research wuold be welcome.

Introduction

Asthma is a chronic disease of the airways characterized by inflammation and bronchoconstriction that occurs in people of all ages. Asthma typically develops in childhood, with peak prevalence between 6 and 11 years old with wheeze being the most common symptom. The most recent revised global estimate of asthma suggests that as many as 334 million people have asthma with the burden of disability being high. Specifically, 14% of children and 8.6% of young adults globally experience asthma symptoms.

The historical view of asthma as a disease of high-income countries no longer holds true: most people affected are in low- and middle-income countries, and the prevalence of asthma is estimated to be increasing faster in the low- and middle-income countries. Children with chronic medical disorders, like asthma, who require long-term medication have an increased susceptibility to dental diseases in three ways: frequent use of sugar containing syrups, use of sedatives causing a decreased saliva secretion, and use of corticosteroids . In addition, immunoglobulins (IgE) found in allergic hypersensitivity are similar to those found in cases of gingivitis which suggests the immunological similarity between periodontal diseases and allergic reactions.

Previous studies indicate that children and adults with asthma have more gingivitis and periodontal disease than healthy controls. Although a number of studies have reported the association between asthma and periodontal disease, the exact relationship between these diseases has not yet been clarified. Differing from those results, other authors has shown that neither the asthma nor the disease severity affected periodontal health in asthmatic children, concluding that, if a relationship exists, it is weak and of little clinical significance. Friedrich et al. and Rivera et al. showed that there is an inverse association between periodontitis and asthma.

As observed, there is a lack of consensus in the literature regarding the relationship between periodontal risk and asthma in child and adult populations. In addition, to date, there is no SR searching for scientific evidence on this topic.

The objective of this SR was to evaluate the hypothesis that asthmatic subjects present more compromised periodontal parameters when compared to healthy subjects.

Materials and Methods

The protocol of this SR was based primarily on the PRISMA-P and registered in PROSPERO under number CRD42017069133. This SR’s methodology followed the recommendations of the Cochrane Handbook for Systematic Reviews of Interventions. PRISMA checklist was followed in order to increase the quality and transparency of the search. Clinical questionnaires were separated and organized using the PICOS strategy .

Focused question

Is there any relationship between asthma and periodontal disease?

Search strategy

An electronic search without date or language restriction ​​was carried out in PubMed/MEDLINE, Cochrane Central Register of Controlled Trials, Web of Science, and LILACS until May 2017. Furthermore, a specific electronic search was performed on the following journals’ websites: Journal of Periodontology , Journal of Clinical Periodontology , International Journal of Periodontics & Restorative Dentistry , and Journal of Periodontal Research. A search of the Grey Literature Report and OpenGrey databases revealed unpublished studies (grey literature). Searches in the ClinicalTrials.gov database and in references of the included studies (cross referencing) were also conducted.

MeSH terms, keywords, and other free terms related to “asthma[MeSH Terms]”; “periodontal disease[All Fields], periodontitis[MeSH Terms], gingivitis[MeSH Terms]”; gum disease[All Fields], gingival inflammation[All Fields], gum inflammation[All Fields], “dental health[MeSH Terms], and oral health[MeSH Terms]” were used with Boolean operators (OR, AND) to combine searches. The search strategy included appropriate changes in the keywords and followed the syntax rules of each database.

Inclusion criteria outlines according to the population, interventions/exposure, comparisons, outcomes, and study design (PICOS strategy)

Population: child or adult subjects (there was no age restriction).

Interventions or exposure: subjects with astma.

Comparison: healthy subjects.

Outcome: the primary outcome was the presence or absence of periodontal disease. The secondary outcome measures were periodontal parameters such as gingival index (GI), periodontal index status (PIS), plaque index (PI), calculus index (CI), gingival bleeding (GB), probing depth (PD), clinical attachment level (CAL), and marginal bone loss (MBL) between asthmatic and non-asthmatic participants.

Study design: clinicals trials, randomized clinical trials, prospective or retrospective cohorts, and case-controls.

Periodontal parameters definition

GI: The criteria are entirely confined to qualitative changes in the gingival soft tissue .

PIS: Used to assess the prevalence and severity of gingivitis and periodontitis within individual dentitions and in population groups .

PI: Based on quantifying and locating the amount of plaque adhering to the dental surface .

CI: This index assesses the presence or absence of calculus on the four surfaces of the four mandibular incisors .

GB: Records the presence or absence of gingival inflamation as determined by bleeding from interproximal gingival sulcus .

PD: Measurement of the depth of a sulcus or periodontal pocket determined by measuring the distance from a gingival margin to the base of the sulcus or pocket with a calibrated periodontal probe .

CAL: Distance between the cementoenamel junction to the pocket base .

MBL: Distance between the cementoenamel junction to the bone crest .

Exclusion criteria

This systemic review exlcuded studies of individuals with metabolic disorders, such as diabetes or immunological diseases. In addition, case series, case reports, and reviews were also excluded.

Screening process

The search and screening process was carried out by two independent reviewing authors (V.M.F. and J.A.C.M), starting with analysis of titles and abstracts. Next, full papers were selected for careful reading and analyzed according to eligibility criteria (inclusion/exclusion) for future data extraction. Disagreements between reviewing authors were resolved through careful discussion. When necessary, the authors of the included studies were contacted by email for clarification of eventual doubts.

Data extraction

When available, the following data were extracted from the included studies by two independent reviewing authors (V.M.F. and J.A.C.M): authors, participants, study design, analyzed parameters, outcomes, conclusions, and notes.

Assessments of the risk of bias and quality

Risk of bias and study quality analyses were performed independently by two reviewing authors (V.M.F. and M.D.C.M.). The Newcastle-Ottawa Scale (NOS) was used in the analysis of non-randomized studies (prospective and retrospective cohort studies or case-controls).

Studies could obtain one star/point per item in the selection and ascertainment categories, while two stars/points could be awarded in the comparability category. According to the NOS, the maximum score for a given study is nine stars/points. Studies scoring six or more stars were considered to have low risk of bias.

Statistical analysis

Only studies that search the same outcome with similar methodologies were included in the pairwise meta-analysis. For continuous outcomes (e.g., GI, PI, and GB), the estimation of intervention effects was expressed as mean difference (MD) with a confidence interval (CI) of 95%. The inverse variance method was used for the random effect or fixed effect models. Heterogeneity was assessed using chi-squared, and possible impact on the meta-analysis was quantified via I 2 . Values ≤ 25% were deemed as less heterogeneous, while values up to 50% and ≥ 70% were classified as medium and highly heterogeneous, respectively . When significant heterogeneity was found ( P < 0.10), the results of the random effect model were validated. When less heterogeneity was found, the fixed effect model was considered. The statistical significance level was determined as P < 0.05.

Data were analyzed using the Review Manager statistical software (version 5.2.8; The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark, 2014).

Materials and Methods

The protocol of this SR was based primarily on the PRISMA-P and registered in PROSPERO under number CRD42017069133. This SR’s methodology followed the recommendations of the Cochrane Handbook for Systematic Reviews of Interventions. PRISMA checklist was followed in order to increase the quality and transparency of the search. Clinical questionnaires were separated and organized using the PICOS strategy .

Focused question

Is there any relationship between asthma and periodontal disease?

Search strategy

An electronic search without date or language restriction ​​was carried out in PubMed/MEDLINE, Cochrane Central Register of Controlled Trials, Web of Science, and LILACS until May 2017. Furthermore, a specific electronic search was performed on the following journals’ websites: Journal of Periodontology , Journal of Clinical Periodontology , International Journal of Periodontics & Restorative Dentistry , and Journal of Periodontal Research. A search of the Grey Literature Report and OpenGrey databases revealed unpublished studies (grey literature). Searches in the ClinicalTrials.gov database and in references of the included studies (cross referencing) were also conducted.

MeSH terms, keywords, and other free terms related to “asthma[MeSH Terms]”; “periodontal disease[All Fields], periodontitis[MeSH Terms], gingivitis[MeSH Terms]”; gum disease[All Fields], gingival inflammation[All Fields], gum inflammation[All Fields], “dental health[MeSH Terms], and oral health[MeSH Terms]” were used with Boolean operators (OR, AND) to combine searches. The search strategy included appropriate changes in the keywords and followed the syntax rules of each database.

Inclusion criteria outlines according to the population, interventions/exposure, comparisons, outcomes, and study design (PICOS strategy)

Population: child or adult subjects (there was no age restriction).

Interventions or exposure: subjects with astma.

Comparison: healthy subjects.

Outcome: the primary outcome was the presence or absence of periodontal disease. The secondary outcome measures were periodontal parameters such as gingival index (GI), periodontal index status (PIS), plaque index (PI), calculus index (CI), gingival bleeding (GB), probing depth (PD), clinical attachment level (CAL), and marginal bone loss (MBL) between asthmatic and non-asthmatic participants.

Study design: clinicals trials, randomized clinical trials, prospective or retrospective cohorts, and case-controls.

Periodontal parameters definition

GI: The criteria are entirely confined to qualitative changes in the gingival soft tissue .

PIS: Used to assess the prevalence and severity of gingivitis and periodontitis within individual dentitions and in population groups .

PI: Based on quantifying and locating the amount of plaque adhering to the dental surface .

CI: This index assesses the presence or absence of calculus on the four surfaces of the four mandibular incisors .

GB: Records the presence or absence of gingival inflamation as determined by bleeding from interproximal gingival sulcus .

PD: Measurement of the depth of a sulcus or periodontal pocket determined by measuring the distance from a gingival margin to the base of the sulcus or pocket with a calibrated periodontal probe .

CAL: Distance between the cementoenamel junction to the pocket base .

MBL: Distance between the cementoenamel junction to the bone crest .

Exclusion criteria

This systemic review exlcuded studies of individuals with metabolic disorders, such as diabetes or immunological diseases. In addition, case series, case reports, and reviews were also excluded.

Screening process

The search and screening process was carried out by two independent reviewing authors (V.M.F. and J.A.C.M), starting with analysis of titles and abstracts. Next, full papers were selected for careful reading and analyzed according to eligibility criteria (inclusion/exclusion) for future data extraction. Disagreements between reviewing authors were resolved through careful discussion. When necessary, the authors of the included studies were contacted by email for clarification of eventual doubts.

Data extraction

When available, the following data were extracted from the included studies by two independent reviewing authors (V.M.F. and J.A.C.M): authors, participants, study design, analyzed parameters, outcomes, conclusions, and notes.

Assessments of the risk of bias and quality

Risk of bias and study quality analyses were performed independently by two reviewing authors (V.M.F. and M.D.C.M.). The Newcastle-Ottawa Scale (NOS) was used in the analysis of non-randomized studies (prospective and retrospective cohort studies or case-controls).

Studies could obtain one star/point per item in the selection and ascertainment categories, while two stars/points could be awarded in the comparability category. According to the NOS, the maximum score for a given study is nine stars/points. Studies scoring six or more stars were considered to have low risk of bias.

Statistical analysis

Only studies that search the same outcome with similar methodologies were included in the pairwise meta-analysis. For continuous outcomes (e.g., GI, PI, and GB), the estimation of intervention effects was expressed as mean difference (MD) with a confidence interval (CI) of 95%. The inverse variance method was used for the random effect or fixed effect models. Heterogeneity was assessed using chi-squared, and possible impact on the meta-analysis was quantified via I 2 . Values ≤ 25% were deemed as less heterogeneous, while values up to 50% and ≥ 70% were classified as medium and highly heterogeneous, respectively . When significant heterogeneity was found ( P < 0.10), the results of the random effect model were validated. When less heterogeneity was found, the fixed effect model was considered. The statistical significance level was determined as P < 0.05.

Data were analyzed using the Review Manager statistical software (version 5.2.8; The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark, 2014).

Results

Literature search

The initial search yielded 1,612 titles in MEDLINE/PubMed, 227 titles in the Cochrane Central Register of Controlled Trials, 861 in Web of Science, and 48 in LILACS. The first evaluation resulted in the selection of 23 full articles. Two studies were excluded after careful reading for failing to meet the eligibility criteria of the present review (not analyzing periodontal changes and review study, respectively). Thus, 21 studies published between 1979 and 2017 were included in this SR. Searching grey literature and the clinicaltrials.gov database yielded no further studies. Only studies in the English language were found. Fig. 1 presents the search and selection process of papers.

Fig. 1
Flow diagram (PRISMA format) of the screening and selection process.

Study characteristics

Table 1 presents the characteristics of included studies. Sixteen case-controls, four prospective cohort studies, and one retrospective 16 were included in the current SR.

Table 1
Main characteristics of included studies.
Authors (year) Participants Study design Analyzed parameters Outcomes Conclusions Potential confounders Notes
Hyyppä et al. 60 child participants (30 asthmatic and 30 nonasthmatic), age range 10–12 Case-control, PI and GI The GI was statistically higher ( P < 0.05) in the asthmatic group This study indicates that children with asthma have more gingivitis than their healthy controls Medications (no control information) Population/community-based (Finland)
Hyyppä 40 adult participants (20 asthmatic and 20 nonasthmatic), age range 20–58 Case-control, PI, GI, CI, PD and salivary analysis All periodontal parameters analyzed were significantly higher in the asthmatic group. The IgE concentrations in the saliva of asthmatic patients differed highly significantly (P < 0.001) when compared with the controls This study observed that asthmatic individuals present a higher prevalence of gingivitis and periodontitis. No potential confounders were reported Population/community-based (Finland)
Bjerkeborn et al. 116 child participants (61 asthmatic and 55 nonasthmatic), mean age 9.8 years Case-control, GB No statistically significant difference ( P > 0.05) was found between asthmatic children and the control group with respect to GB The study shows that neither the asthma per se nor the disease severity affected the gingival condition in asthmatic children. Medications (Controlled) Population/community-based (Sweden)
Laurikainen and Kauusisto 66 adult participants (33 asthmatic and 33 nonasthmatic), mean age 36 years Case-control, PI PI was statistically higher ( P < 0.0462) in the asthmatic group The results of this study support the hypothesis that adult asthmatics have a higher risk of periodontal disease than nonasthmatic participants. Smoking (Controlled), Medications (Controlled), Oral hygiene (Controlled) Population/community-based (Finland)
McDerra et al. 246 child participants (100 asthmatic and 146 nonasthmatic), age range 4-16 Case-control, PI and CI All periodontal parameters analyzed were significantly higher in the asthmatic group. Asthmatic children have poorer dental health than healthy children. They were also shown to have poorer periodontal status. Medications (Controlled) Population/community-based (England)
Shulman et al. 1,596 adolescent participants (238 asthmatic and 1,358 nonasthmatic), age range 13–17 Case-control, GB, CAL, PD, and CI None of the parameters analyzed were statistically significant between asthmatic and non-asthmatic participants The results do not support an asthma-periodontal health association. If one exists, it is weak and of little clinical significance. Smoking (Controlled) Medications (Controlled) Population/community-based (USA). This study was supported by National Health and Nutrition Examination Survey (USA)
Eloot et al. 140 asthmatic child participants, age range 3–17 Prospective cohort, GB and PI None of the parameters analyzed were statistically significant between asthmatic and non-asthmatic participants This analysis revealed that neither the period (of the disease and the medication) nor the severity of the asthma had a significant influence on the risk of gingivitis in asthmatic children Medications (no control information) Oral hygiene (Controlled) Population/community-based (Belgium)
Friedrich et al. 114 asthmatic participants, mean age 37.9 years Prospective cohort. CAL The study revealed a weak (P ≥ 0.05) inverse relation between periodontitis and asthma. There is an inverse association between periodontitis and asthma. Smoking (Controlled) Population/community-based (Germany)
Shashikiran et al. 211 child participants (105 asthmatic and 106 nonasthmatic), age range 6–14 Case-control, PIS Only the children taking antiasthmatic medication (baclamethasone, salbutamol inhaler, and salbutamol tablets) were found to have bad periodontal status compared to the control group It has been concluded that antiasthmatic medication has its effects on periodontal disease Medications (Controlled) Population/community-based (India)
Yaghobee et al. 100 adult participants (50 asthmatic and 50 nonasthmatic), mean age 39.6 years Case-control, PI, GI, GB, PIS, and CI There were significant differences ( P < 0.01) between asthmatics and non-asthmatic in PI, GI, GB, and PSI. However, there was no such differences in CI between the two groups ( P = 0.084) The results of the present study support a relationship between respiratory disease and periodontal health status. Medications (Controlled) Population/community-based (Tehran)
Mehta et al. 160 participants (80 asthmatic and 80 nonasthmatic), mean age 17.4 years Case-control, PI and GI The parameters were statistically higher ( P < 0.001) in the asthmatic group. There is a need to educate asthmatic subjects about their increased risk of gingival disease and the importance of proper plaque control Medications (Controlled) Population/community-based (India)
Stensson et al. 40 adolescent participants (20 asthmatic and 20 nonasthmatic), mean age 14 years Case-control, GB and PI The GB was statistically higher ( P < 0.01) in the asthmatic group. No statistically significant difference was found in the plaque index between the two groups. Adolescents with long-term asthma had more gingival bleeding than adolescents without asthma. Medications, (no control information), Oral hygiene (Controlled) Population/community-based (Sweden)
Stensson et al. 114 child participants (64 asthmatic and 50 nonasthmatic), age range 3-6 Case-control, GB Only asthmatic children with 3-year olds showed GB statistically higher ( P < 0.01) Children with asthma has a higher prevalence of bleeding gingivitis Medications (Controlled) Population/community-based (Sweden)
Stensson et al. 40 adult participants (20 asthmatic and 20 nonasthmatic), age range 18–24 Case-control, MBL, GB, PI, PD, and gingival crevicular fluid No statistically significant differences were found between the two groups in terms of MBL, PI, PD, and gingival crevicular fluid. The GB was statistically higher in the asthmatic participants (P = 0.03) Young adults with long-term controlled asthma had a higher prevalence of gingivitis Medications (Controlled) Population/community-based (Sweden)
Ferrazzano et al. 280 child participants (124 asthmatic and 156 nonasthmatic), mean age 9.11 years Case-control, PIS, PI, CI, GB None of the parameters analyzed were statistically significant between asthmatic and non-asthmatic participants Asthmatic children are similar to healthy participants for periodontal health status Medications (Controlled) Population/community-based (south Italy)
Gomez-Filho et al. 210 adult participants (113 asthmatic and 107 nonasthmatic), mean age 46.8 years Case-control, PD, CAL, GB, and PI All parameters analyzed were significantly higher in the asthma group. The frequency of periodontitis is higher in individuals with severe asthma than in those without a diagnosis of bronchial inflammation. Smoking (no control information), Oral hygiene (no control information) Population/community-based (Brazil)
Uppal et al. 100 adult participants (50 asthmatic and 50 nonasthmatic), mean age 40.1 years Case-control, PI, CI, GI, CAL, and GB All parameters analyzed were significantly higher in the asthma group. From the results of this study, it can be concluded that chronic periodontitis and asthma are associated to each other Smokers patients were excluded Population/community-based (India)
Real et al. 13,409 asthmatic adult participants, mean age 52 years Prospective cohort, A postal questionnaire including questions about respiratory and oral health (gum bleeding) was sent to general population samples in seven Northern European centres The association of gum bleeding with asthma symptoms appeared to be consistent in the different study centres (P < 0.001) A consistent link between gum bleeding and obstructive airways disease was observed, and not explained by common risk factors or metabolic factors Smoking (Controlled), Oral hygiene (Controlled) Population/community-based in seven Northern European centres (Aarhus, Reykjavik, Bergen, Gothenburg, Umeå, Uppsala, and Tartu). This study was supported by European Community Respiratory, Health Survey
Rivera et al. 1,315 asthmatic (191 active and 1124 controlled) obese adult participants, age range 40-65 Prospective cohort, PD, PI, GB, and CAL The proportion of persons with severe periodontitis was much lower among participants who reported active asthma compared with those controlled asthma. Similarly, median proportion GB and PI were also lower for participants with asthma than those without, especially for those taking asthma medication. Participants with severe periodontitis were less likely to have asthma. Stronger evidence of an inverse association was found when using asthma medication as outcome. Smoking (Controlled) Population/community-based (Puerto Rico)
Shen et al. 96,030 participants (19,206 asthmatic and 76,824 nonasthmatic), mean age 41.5 years Retrospective cohort, PIS and GI All parameters analyzed were significantly higher (P < 0.001) in the asthma group In the studied population, asthmatic patients are at an elevated risk of developing periodontal diseases Smoking (Controlled), Medications (Controlled) Population/community-based in National Health Insurance of Taiwan
Lee et al. 5,976 adult participants (89 asthmatic and 5,887 nonasthmatic), mean age 51.4 years Case-control, PIS and PD Patients with current asthma conditions were about 5 times more likely to be associated with periodontitis while adjusted by sociodemographic and lifestyle covariates The results of the study revealed that there is a positive association between asthma and periodontitis in patients having current asthma condition. Smoking (Controlled), Medications (Controlled) Population/community-based in results from Korean National Health and Nutrition Examination Survey
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Jun 17, 2018 | Posted by in General Dentistry | Comments Off on Interrelation of periodontal parameters between asthmatics and nonasthmatics subjects: a systematic review and meta-analysis
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