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Oral Diseases. 2020;26:439–446.
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439wileyonlinelibrary.com/journal/odi
Received: 23 Septem ber 2019
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Revised: 8 Oc tober 2 019
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Accepted: 27 Oc tober 2019
DOI: 10.1111/odi.13228
ORIGINAL ARTICLE
Periodontitis and respiratory diseases: A systematic review
with meta-analysis
Isaac Suzart Gomes-Filho1 | Simone Seixas da Cruz2,1 | Soraya Castro Trindade1 |
Johelle de Santana Passos-Soares3,1 | Paulo Cirino Carvalho-Filho4 |
Ana Cláudia Morais Godoy Figueiredo5 | Amanda Oliveira Lyrio6 |
Alexandre Marcelo Hintz1 | Mauricio Gomes Pereira6 | Frank Scannapieco7
© 2019 John Wiley & Sons A /S. Published by Jo hn Wiley & Sons Ltd. A ll right s rese rved
1Depar tment of Health , Feira de Santana
State Universit y, Bahia, B razil
2Depar tment of Epidemi ology, Federal
University of Recôncavo of Bahia, B ahia,
Brazil
3Department of Preventive Dentistry,
Federal Univer sity of Bahia, Salvado r, Brazil
4Bahiana School of Medicine and Public
Health , Salva dor, Brazil
5Epidemi ology Surve illance, Feder al District
Health State Dep artment, Brasília, Brazil
6Faculty of Health Sciences, Universit y of
Brasí lia, Br asília, Distrito Fede ral, Brazil
7Depar tment of Oral Biology, Uni versit y of
Buffalo, Buf falo, NY, USA
Correspondence
Isaac Su zart G omes-F ilho, Department of
Health , Feira de Santana State Un iversity,
Avenida Ge túlio Vargas, 379, Centro, Feira
de Santana, Bahia, Brazil.
Email: isuzart@gmail.com
Abstract
Objective: To conduct a systematic review and meta-analysis to evaluate the recent
scientific literature addressing the association between periodontitis and asthma,
chronic obstructive pulmonary disease (COPD), and pneumonia.
Materials and Methods: The search for studies was carried out using MEDLINE/
PubMed, EMBASE, Lilacs, Web of Science, Scopus, and SciELO databases, including
the gray literature (ProQuest). Reference lists of selected articles were also searched.
Studies having varying epidemiological designs assessing the association between
periodontitis and respiratory diseases in human subjects were eligible for inclusion.
Three independent reviewers performed the selection of articles and data extrac-
tion. Fixed and random effects meta-analysis were performed for the calculation of
the association measurements (Odds Ratio—OR) and 95% confidence intervals (95%
CI).
Results: A total of 3,234 records were identified in the database search, with only
13 studies meeting the eligibility criteria and 10 studies contributed data for meta-
analysis. Using a random effects models periodontitis was associated with asthma:
ORadjusted: 3.54 (95% CI: 2.47–5.07), I2 = 0%; with COPD: OR adjusted: 1.78 (95%
CI: 1.04–3.05), I2 = 37.9%; and with pneumonia: OR adjusted: 3.21 (95% CI: 1.997–
5.17), I2 = 0%.
Conclusions: The main findings of this systematic review validated an association
between periodontitis and asthma, COPD and pneumonia.
KEY WORDS
asthma, chronic obstructive pulmonar y disease, periodontitis, pneumonia, respiratory
diseases
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GOMES-FILHO E t aL.
1 | INTRODUCTION
The association between periodontitis and several respirator y
diseases has been investigated in the last decades. While several
systematic reviews have suggested an association between respi-
ratory diseases and poor oral health (Cagnani et al., 2016; Ferreira
et al., 2019; Mendes, Dos Santos, & Moraschini, 2018; Moraschini,
Calasans-Maia, & C alasans-Maia, 2018; Shi et al., 2018; Tan, Wang,
Pan, & Zhao, 2016; Zeng et al., 2012), one recent systematic review
on the subject, which included studies from 2002 to 2012, con-
cluded that the findings showed a weak association bet ween peri-
odontitis and pulmonary diseases (Linden, Lyons, & Scannapieco,
2013). Although several studies have shown that improvements in
oral hygiene prevent several respiratory diseases, this question re-
mains unresolved.
Respiratory diseases and periodontitis are among the most com-
mon diseases of humans worldwide (Beasley, Semprini, & Mitchell,
2015; Tonetti, Chapple, Jepsen, & Sanz, 2015). Pneumonia, a com-
mon infectious disease of the lung parenchyma, is more prevalent
among the elderly, and the oral microbiota plays an important role
in the natural history of some forms of the disease (Raghavendran,
Mylotte, & Scannapieco, 20 07; Sabharwal, Gomes-Filho, Stellrecht,
& Scannapieco, 2018).
Asthma is a chronic inflammatory disease affecting both young
and old (Beasley et al., 2015). An increasing number of studies have
observed an association with periodontal disease (Gomes-Filho et
al., 2014; Khassawneh, Alhabashneh, & Ibrahim, 2019; Soledade-
Marques et al., 2018). The same has been seen for chronic obstruc-
tive pulmonary diseases (COPD), a chronic condition comprised of
both bronchitis and emphysema characterized by airflow obstruc-
tion due to increased chronic inflammatory response within the air-
way. A number of investigations have suggested that periodontitis
and COPD share common underlying processes, for example, neu-
trophil-rich inflammation with subsequent proteolytic destruction
of connective tissues (Barros, Suruki, Loewy, Beck, & Offenbacher,
2013; Chung, Hwang, Kim, & Kim, 2016; Harland, Furuta, Takeuchi,
Tanaka, & Yamashita, 2018; Ledić et al., 2013; Takeuchi et al., 2019).
However, the precise pathophysiological mechanisms to explain the
underlying nature of the association are still uncertain.
The course of the pulmonary diseases can be affected by
both infectious and inflammatory process, such as periodontitis
(Azarpazhooh & Leake, 2006; Vadiraj, Nayak, Choudhary, Kudyar,
& Spoor thi, 2013). The microorganisms present in the periodontal
pocket, specially anaerobic bacteria, can be aspirated into the lower
airway (Bansal, Khatri, & Taneja, 2013). Epithelial sensitization and
the hematogenous spread of the proinflammatory mediators such
as cytokines and metalloproteinases produced in the diseased peri-
odontal tissue (Guan et al., 2009; Tâlvan, Mohor, Chisnoiu, Cristea,
& Câmpian, 2017) can incr ease the inflammator y burden, exacerbat-
ing disease activity to diminish airflow (Gueders et al., 2008). This
inflammatory burden can be amplified by stimulation of the liver,
eliciting the production of acute-phase proteins, such as C-reactive
protein, interleukin-6, transferrin, apolipoprotein b, and amyloid A
protein, which in turn potentiate the inflammatory response by lung
tissues (Endo et al., 2010).
Seven recent systematic reviews assessing the association be-
tween poor oral health and pulmonary diseases have been published
to date: 3 related to the association between periodontal clinical
parameters and asthma (Ferreira et al., 2019; Mendes et al., 2018;
Moraschini et al., 2018), 3 focused on the relationship between
worse periodontal condition and COPD (Shi et al., 2018; Tan et al.,
2016; Zeng et al., 2012), and 1 regarding the association between
periodontal disease and pneumonia (Cagnani et al., 2016). All these
reviews concluded that periodontal disease is associated with the
target respiratory disease. However, the findings were presented
only based on the association between periodontal clinical param-
eters, such as probing depth (PD), clinical attachment level (C AL),
bleeding on probing (BOP) or plaque index (PI), and the respirator y
disease, instead of the association bet ween periodontitis, as a clini-
cal entit y, and asthma, COPD, or pneumonia.
Therefore, the present systematic review with meta-analysis of
observational or interventional investigations in humans aimed to re-
view the most recent scientific evidence on the association between
periodontitis and the three aforementioned respiratory diseases.
2 | METHODS
2.1 | Registration and protocol
A search for systematic reviews on the topic was conducted in
the International Prospective Register of Systematic Reviews—
PROSPERO database, and no records were found. The systematic
review was registered in PROSPERO: CRD42019126056.
The PRISMA state ment wa s used to guide the writ ing of th is sys-
tematic review (Moher, Liberati, Tetzlaff, Altman, & PRISMA Group,
200 9).
2.2 | Eligibility criteria for the studies
Cross-sectional, case–control, cohort or randomized, controlled
clinical trials, conducted with human subjects’ age ≥18 years, were
included in this review to investigate the association between peri-
odontitis and asthma, COPD, and pneumonia, without restriction
of the language used, over the period of January 1, 2010 to June
19, 2019. Case studies and reviews, investigations with sample size
<100 individuals, and those without clear description of the diag-
nostic criteria for periodontitis and/or respirator y disease or self-
referred by participants were excluded.
2.3 | Information sources
Studies were accessed using the following electronic databases;
MEDLINE through PubMed, EMBASE, LIL ACS, Web of Science,
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GOMES -FILHO E t aL.
Scopus, and SciELO. Reference lists of articles selected for the sys-
tematic review were examined, as well as specific databases con-
taining texts from the gray literature (ProQuest), such as master's
dissertations, doctoral theses.
2.4 | Search strategies
The descriptors used and their synonyms were identified in the
Medical Subject Headings—MeSH. The uniterms employed in English
for the search strategies were Periodontitis, Periodontal Disease,
Gingivitis, Asthma, Pneumonia, and Chronic Obstructive Pulmonary
Disease. The Boolean operators were AND and OR. This search
strateg y was adapted for the other electronic databases (Appendix
S1). Peer Review Electronic Search Strategy—PRESS evaluated the
quality of search strategies (McGowan et al., 2016).
2.5 | Study selection
Following exclusion of duplicates, studies were selected by reading
titles and abstracts using the State of the Art through Systematic
Review program version 3.4. (START, 2013) by three reviewers
(I.S.G.F., S.S.C., and P.C.C.F.) that were unaware of the decisions
made by their peers during the article selection process. Three
investigators (I.S.G.F., S.S.C., and A.C.M.G.F.) independently read
the ful l te xt of the sele cted article s an d th ose th at met t he eligib il-
ity criteria were included in the systematic review. In cases where
there was a divergence between the researchers, the inclusion
or exclusion of the articles was adjudicated through a consensus
among them.
2.6 | Extraction of data
The investigators (I.S.G.F., J.S.P.S., and S.C.T.) performed and organ-
ized the extraction of data from the included articles using the fol-
lowing fields: author's name, year of publication, place and year of
study, objective, study design, sample size, criteria for the diagnosis
of the periodontitis and respiratory diseases (asthma, COPD, and
pneumonia), association measurement, confounding covariables,
and the main findings. When data were not available, the authors of
the studies were contacted (Appendix S1).
2.7 | Evaluation of study quality
To evaluate the quality of the selected studies, the Quality Access
Scale instrument—Newcastle–Ottawa was used (Modesti et al.,
2016; Wells et al., 2014). The researchers (I.S.G.F., A.O.L., and
A.M.H.) also performed the quality evaluation of all studies, and
then, the information was confronted with consensus among them.
2.8 | Data analysis
Data analysis was performed using the statistical package STATA®
version 15 (StataCorp LLC), Serial number: 301506206729. To
evaluate the statistical heterogeneity of the data used for the meta-
analysis, the chi-square test (p < .10) and the Higgins and Thompson
I-square (I2) were used. In order to identif y the magnitude of data in-
consistency, the I2 score was used. I2 values above 50% represented
high inconsistency, values of 25% to 50%, moderate inconsistency
and I2 value less than 25%, low inconsistency (Higgins & Thompson,
2002).
Global association measurements between periodontitis and
th e main res pi rator y disease ou tc om es (a sth ma , COP D, an d pne u-
monia), the Odds Ratio (OR), and 95% confidence interval (95%
CI) were obtained with fixed and random effects meta-analysis
using the DerSimonian–Laird method and the forest plot graph.
Cohort study findings reported as relative risk or cross-sectional
study findings reported as prevalence ratio were converted to an
odds ratio according to criteria defined by Zhang (Zhang & Yu,
1998).
The inspection of the Begg's funnel plot and Egger's test, with
a statistical significance of p < .10 (Egger & Altman, 2001; Egger,
Davey Smith, Schneider, & Minder, 1997), to evaluate the publication
bias were also done, along with the Galbraith graphic for evaluation
of heterogeneit y among the studies in accordance with their distri-
bution (Dinnes, Deeks, Kirby, & Roderick, 20 05), acknowledging the
limitations of this meta-analytic measurement.
2.9 | Quality of evidence of the present study—
GRADE system
GRADE system (Atkins et al., 2004) was used to evaluate the qual-
ity of the evidence of the present study. It has five items that may
decrease its quality, as follows: risk of bias, inconsistency, indirect
evidence, inaccuracy, and publication bias. Other three items may
impact the quality of evidence: magnitude of the effect, dose–re-
sponse gradient, and possible confounding adjustment. The final
quality of evidence may be scored as follows: high qualit y ≥4 points,
moderate quality—3 points, low quality—2 points, and very low evi-
dence—1 point.
3 | RESULTS
A total of 3,234 records were identified. After duplicates were
removed, the titles and abstract s were read. Of the 92 articles
that were selected for complete reading, only 13 texts met the
eligibility criteria of this systematic review related to the asso-
ciation between periodontitis and respiratory diseases, with
3 studies targeting asthma, 7 on COPD, and 3 on pneumonia
(Figure 1).
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GOMES-FILHO E t aL.
3.1 | General characteristics and quality of studies
The 13 studies considered for this review included 22,327 participants
(with 740 indi vidua ls with asthma, 20,921 with COPD studie s, and 66 6
with pneumonia). Of the 13 studies identified, 8 were case–control,
3 were cohort and 2 were cross-sectional design. Most of them were
conducted in Asia (53.85%—7 studies, of which 4 were conducted in
Ja pan), foll ow e d by Sout h Ame r ic a (3 0.7 7%— 4 stu die s , al l con duc ted in
Brazil), North America (7.69%—1 study), and Europe (7.69%—1 study).
There was a diversity of diagnostic definitions for periodontitis
used in the studies. Among them, 15,38% used criteria of the Center
for Disease Control/American Association of Periodontology (Eke,
Page, Wei, Thornton-Evans, & Genco, 2012; Page & Eke, 2007).
About 15.38% used the Community Periodontal Index—CPI (WHO,
2013). About 15.38% used the United States Third National Health
and Nutrition Examination Survey (Albandar, Brunelle, & Kingman,
1999). About 15,38% used Armitage classification system for peri-
odontal diseases (Armitage, 1999). And 23.10% used Gomes-Filho
et al. (2007, 2018) criterion. The remaining studies, one (7.69%) used
CAL >4 mm at 60% of the measured sites and the other (7.69%) used
the case definition of ≥4 teeth with ≥1 site with PD ≥4 mm and CAL
≥3 mm (Appendix S1).
Regarding the diagnosis of the respiratory diseases, from the 3
studies that evaluated the association between periodontitis and
asthma, 2 followed the recommendation of the Global Initiative of
Asthma (GINA, 2012). Similarly, from the 7 studies on the relation-
ship between periodontitis and COPD, 6 followed the statement of
the Global Initiative for Chronic Obstructive Lung Disease (Pauwels
et al., 2001). Regarding pneumonia, each study employed different
criteria to diagnose the disease.
Over all, the study quality assessment s were high—76.91% with a
mean of 7.46, and no article was found to have low quality (Appendix
S1).
Of the total number of studies included in the review, 3
(Appendix S1) evaluated the relationship between periodontitis
and respiratory diseases but, one had only crude association mea-
surement between periodontitis and COPD (Chung et al., 2016),
and in the other, two did not co ntain the association meas urement
or mea ns to obt ai n it (Si et al. , 2012 ; Ter as hima et al. , 2017). Of the
10 remaining studies that presented the adjusted association mea-
surement , only 3 investigations were included in the meta-analy-
sis to generate the summary association measurement between
periodontitis and asthma (Gomes-Filho et al., 2014; Khassawneh
et al., 2019; Soledade-Marques et al., 2018). Four studies between
periodontitis and COPD (Barros et al., 2013; Harland et al., 2018;
Ledić et al., 2013; Takeuchi et al., 2019). And 3 articles between
periodontitis and pneumonia (Gomes-Filho et al., 2014; Iwasaki
et al., 2018; Melo Neto et al., 2013). In these investigations, the
FIGURE 1 Flowchart of the search,
selection, and inclusion of the studies
related to the association between
periodontitis and respiratory diseases
[Colour figure can be viewed at
wileyonlinelibrary.com]
Records identified through database searching
MEDLINE/PubMed: 493 EMBASE: 667
Lilacs: 34 Web of Science: 580
Scopus: 820 SciELO: 13
(n = 2,607)
Screening
Included Eligibility Idenficaon
Additional records identified
through other sources
ProQuest: 527
(n = 527)
Records after duplicates removed
(n = 1,995)
Records screened
(n = 1,995)
Records excluded
(n = 1,926)
Full-text articles assessed
for eligibility
(n = 69)
Full-text articles excluded,
with reasons
(n = 56)
Studies included in
qualitative synthesis
(n = 13)
Studies included in
quantitative synthesis
(meta-analysis)
(n = 11)
Asthma: 03 studies;
COPD: 07 studies;
Pneumonia: 03 studies.
Asthma: 03 studies;
COPD: 05 studies;
Pneumonia: 03 studies.
Duplicates
(n = 1,139)
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GOMES -FILHO E t aL.
covariables most frequently considered in the adjustment of
the association measurements were age (92.31% of the studies),
smoking habit (76.92%), body mass index (53.85%), sex (46.15%),
schooling level (38.46%), and alcoholic beverage consumption
(23.08%). Articles excluded from the systematic review are pre-
sented in Appendix S1.
3.2 | Periodontitis and respiratory diseases
To obtain the global association measurement, analysis of the unad-
justed (Figure S1) and adjusted OR were performed according to the
type of respiratory disease.
For the association between periodontitis and asthma, the me-
ta-analysis yielded an adjusted OR of 3.54 (95% CI: 2.47–5.07), with
an I2 as 0% (95% CI: 0%–90%), representing a strong global associa-
tion, and low heterogeneity among the studies (Figure 2).
In relation to COPD, the met a-analysis yielded an adjusted OR
of 1.78 (95% CI: 1.04–3.05), with an I2 as 37.9% (95% CI: 0%–79%),
representing a moderate summary association between peri-
odontitis and COPD, and moderate variation among the studies
(Figure 2).
Regarding pneumonia, the meta-analysis yielded an adjusted
OR of 3.21 (95% CI: 1.99–5.17 ), with an I2 as 0% (95% CI: 0%–90%),
representing a strong global association between periodontitis and
pneumonia, and low inconsistency among the studies (Figure 2).
The Galbraith graphic (Figure S2) showed the distribution of
studies, responsible for the heterogeneity in this meta-analysis. This
finding reinforced the impossibility of using the sensitivity and me-
ta-regression analysis. The funnel graphic (Figure S3) indicates the
existence of publication bias for this final association measurement,
since the studies are diffusely distributed, confirmed with Egger's
test (p = .08).
4 | DISCUSSION
The main findings of this systematic review showed a moderate to
strong association between periodontitis and respiratory diseases,
with high methodological quality among most of the studies and low
to moderate heterogeneity of the selected investigations. Previous
systematic reviews related to the association between periodon-
tal clinical parameters and asthma (Ferreira et al., 2019; Mendes
et al., 2018; Moraschini et al., 2018); worse periodontal condition
and COPD (Shi et al., 2018; Tan et al., 2016; Zeng et al., 2012); and
periodontal disease and pneumonia (Cagnani et al., 2016) showed
a positive relationship between periodontal clinical parameters and
the respiratory disease of interest.
Another relevant aspect of this systematic review is the het-
erogeneity observed among the studies. Although the heteroge-
neity appears low, some inconsistency among the studies exists
and it can be attributed not only to the diversity of the criteria for
defi nin g the expo su re an d the ou tcome , but also due to po pu lat io n
differences including socioeconomic–demographic conditions,
lifestyle, access to healthcare services, and other health-related
characteristics. For these reasons, a recent classification of het-
erogeneity was not used for the present study since it indicates
I2 close to 0% as no heterogeneity (Higgins, 2008). For the calcu-
lation of the summary association measurement, some additional
an aly ses we re no t poss ib l e to per form, su ch as th e sens it i vit y anal-
ysis, meta-regression, and subgroup analysis, since the number of
observations was less than 10 studies. These analyses would favor
the identification of possible variables that influenced the final
global association measurement.
Among the general characteristics of the systematic review in-
vestigations, the sample size varied greatly among the 13 selected
studies, with 8 presenting samples smaller than 500 participants,
with 3 having samples smaller than 200 subjects (Ledić et al., 2013;
Melo Neto et al., 2013; Terashima et al., 2017). Comparison groups
with small numbers of individuals in each group can influence the
final measurement, presenting spurious associations (Rothman,
Greeland, & Lash, 2011). Therefore, for the present systematic re-
view, the eligibility criteria employed the exclusion of studies with
sample sizes less than 100 subject s. For the calculation of the me-
ta-analysis, this measure was also used in an attempt to reduce the
possibility of the influence of cross-sectional analysis on the final
findings, although there were only two studies with this design: one
conducted with a sample of 5,878 subjec ts (Chung et al., 2016) and
the other with 1,474 subjec ts (Harland et al., 2018). Thus, the exis-
tence of a causal association is favored and reinforced by the consis-
tency of similar findings from several empirical, independent studies
on a given topic (Rothman et al., 2011).
The use of confounding covariables in the association analysis
was also evaluated in the selected studies. The vast majority in-
cluded in their final models a confounder analysis using covariables
that were related to the exposure and outcome factors, considered
important factors in the investigation. This measure helps to neu-
tralize the influence of other factors on the association between the
periodontitis and the respiratory diseases, reinforcing the impor-
tance of the epidemiological concept of multicausality (Rothman et
al., 2011).
It should be noted that the objective of this systematic review
was not to evaluate studies that associate the periodontal clinical
parameters, such as PD, CAL, BOP, or PI, separately with the respi-
ratory disease. Periodontitis is an impor tant public health problem
and needs to be measured and evaluated as a clinical entity, that is,
the role of periodontitis in asthma, COPD, or pneumonia. Many pre-
vious systematic reviews (Cagnani et al., 2016; Ferreira et al., 2019;
Mendes et al., 2018; Moraschini et al., 2018; Shi et al., 2018; Tan et
al., 2016; Zeng et al., 2012) presented their conclusions only on the
basis of the relationship between one or more periodontal clinical
parameter with the abovementioned respiratory diseases, which is
different from the main objective of this review.
Among the limitations of this systematic review, potential pub-
lication bias stands out, regardless of the use of many databases,
in addition to publications from the gray literature and contacting
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GOMES-FILHO E t aL.
authors of published ar ticles that did not present enough data.
Another significant limitation was the small number of studies used
in the meta-analysis that employed the final summary association
measurements, which prevented further analysis for the identifica-
tion of interfering covariables, and the exclusive positive association
between the exposure and the outcome among the investigations
related to periodontitis and asthma, as well as periodontitis and
pneumonia.
Another limitation was the multiple diagnostic for pneumonia
among the studies that related it to periodontitis (Gomes-Filho et
al., 2014; Iwasaki et al., 2018; Melo Neto et al., 2013). For obtain-
ing the meta-analytic measurement, a study was included where
the outcome was mortality due to pneumonia, considered a prox y
variable for diagnosis of this respirator y disease (Iwasaki et al.,
2018). These is su es impacted the qualit y of evidence ( At ki ns et al.,
2004), because it was rated overall as low or very low (Appendix
S1).
The strengths of this review include the use of research tech-
niques and validated instruments. PRESS was used to evaluate the
quality of search strategies (McGowan et al., 2016). START was
employed for exclusion of duplicates studies (START, 2013). The
Newcastle–Ottawa Quality Survey Scale (Modesti et al., 2016;
Wells et al., 2014) to assess the quality of the investigations and the
PRISMA statement (Moher et al., 2009) to guide selection of studies
were included for analysis.
Additionally, other strengths were the inclusion of studies with
moderate and high methodological quality, usage of adjusted asso-
ciation measurement to calculate the global measurement, employ-
ment of investigations that use clinical periodontitis case definition
for diagnosis of the participants, and finally, several number of data-
bases for screening of the studies.
5 | CONCLUSIONS
The findings of this systematic review validated previous studies
reporting associations between periodontitis and asthma, COPD,
and pneumonia. This evidence should be interpreted with caution.
There is a need for further research to minimize methodological and
clinical heterogeneity between studies, particularly concerning the
characteristics of the samples and the definition of the most relevant
outcomes.
In addition, both periodontitis and the respiratory diseases are
relevant public health problems and these findings argue for addi-
tional meas ures to implement oral health prevention and health pro-
motion measures for these respirator y diseases.
CONFLICT OF INTEREST
The author s also de clare no conflict s of interes t related to the stud y.
AUTHOR CONTRIBUTION
I. S. Gomes-Filho, S. S. Cruz, S. C. Trindade, J. S. Passos-Soares,
P. C. Carvalho-Filho, A. C. M. G. Figueiredo, A. O. Lyrio, A. M.
Hintz,M. G. Pereira, F. Scannapieco declare that we have made
substantial contributions to the research design, or the acquisi-
tion, analysis or interpretation of data; to drafting the paper or
revising it critically; and that we all have approved the submitted
version.
FIGURE 2 Forest plot of the meta-
analysis with adjusted association
measurements between periodontitis and
respiratory diseases, such as pneumonia,
chronic obstruc tive pulmonar y disease,
and asthma, and 95% confidence intervals
of all the evaluated studies
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445
GOMES -FILHO E t aL.
ORCID
Isaac Suzart Gomes-Filho https://orcid.
org/0000-0002-4270-8491
Soraya Castro Trindade https://orcid.org/0000-0001-7125-9114
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How to cite this article: Gomes-Filho IS, da Cruz SS, Castro
Trindade S, et al. Periodontitis and respiratory diseases:
A systematic review with meta-analysis. Oral Dis.
2020;26:439–446. https ://doi.org/10.1111/odi.13228
