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Periodontitis and respiratory diseases: A systematic review with meta‐analysis

Authors:

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 humans subjects were eligible for inclusion. Three independent reviewers performed the selection of articles and data extraction. 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: 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: ORadjusted: 1.78 (95%CI: 1.04 - 3.05), I2 = 37.9%, and with pneumonia: ORadjusted: 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.
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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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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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 Idenficaon
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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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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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
REFERENCES
Albandar, J. M., Brunelle, J. A., & Kingman, A. (1999). Destructive peri-
odontal disease in adults 30 years of age and older in the United
States, 1988–1994. Journal of Periodontology, 70(1) , 13–2 9. http s ://
doi.org/10.1902/jop.1999.70.1 .13
Armitage, G . C . (1999). Development of a classification system for peri-
odontal diseases and conditions. Annals of Periodontology, 4(1), 1–6.
htt ps ://doi.org /10.190 2/annals.1999.4.1.1
Atkins, D., Best, D., Briss, P. A ., Eccles, M., Falck-Ytter, Y., Flottorp, S.,
… GRADE Working Group (2004). Grading qualit y of evidence
and strength of recommendations. BMJ: British Medical Journal,
328(7454), 1490.
Azarpazhooh, A., & Leake, J. L. (2006). Systematic review of the as-
sociation between respiratory diseases and oral health. Journal
of Periodontology, 77(9), 1465–1482 . https ://doi.org/10.1902/
jop.2006.060010
Bansal, M., Khatri, M., & Taneja, V. (2013). Potential role of periodontal
infection in respirator y diseases - a review. Journal of Medicine and
Life, 6(3), 244–248.
Barros, S. P., Suruki, R., Loewy, Z. G., Beck, J. D., & Offenbacher, S. (2013).
A cohort study of the impact of tooth loss and periodontal disease
on res pirator y even ts am on g CO PD sub jec ts: Mod ula to r y rol e of sy s-
temic biomarkers of inflammation. PLoS ONE, 8(8), e68592. https ://
doi.org/10.1371/journ al.pone.0068592
Beasley, R., Semprini, A., & Mitchell, E. A. (2015). Risk factors for asthma:
Is prevention possible? Lancet, 386(9998) , 1075–1085. https ://doi.
org/10.1016/S0140-6736(15)00156-7
Cagnani, A., Barros, A. M. D. S., Sousa, L. L. A. D., Zanin, L., Bergamaschi,
C. D. C., Peruzzo, D. C., & Flório, F. M. (2016). Periodont al disease
as a risk f actor for aspiration pneumonia: A systematic review.
Bioscience Journal, 32(3), 813–821. https ://doi.org/10.14393/ BJ-
v32n3 a2016-33210
Chung, J. H., Hwang, H. J., Kim, S. H., & Kim, T. H. (2016). Associations
between periodontitis and chronic obstructive pulmonary disease:
The 2010 to 2012 Korean National Health and Nutrition Examination
Surv ey. Journal of Periodontology, 87(8), 864–871. https ://doi.
org/10.1902/jop.2016.150682
Din ne s, J., Deeks , J., Kir by, J., & Ro de ri ck , P. (20 05). A me th od ol ogical re-
view of how heterogeneity has been examined in systematic reviews
of diagnostic test accuracy. Health Technology Assessment, 9(12),
1–113. https ://doi.org/10.3310/hta9120
Egger, M.Davey Smit h, G., & Altman, D. G. (2001). Systematic reviews in
health care: Meta-analysis in context (2ed edn). London, UK: BMJ.
Egger, M., Davey Smith, G., Schneider, M., & Minder, C. (1997). Bias
in meta-analysis detected by a simple, graphical test. BMJ: British
Medical Journal, 315(7109), 629–634.
Eke, P. I., Page, R . C., Wei, L ., Thornton-Evans, G., & Genco, R. J. (2012).
Update of the case definitions for population-based surveillance of
periodontitis. Journal of Periodontology, 83(12), 1449–1454. https ://
doi.org/10.1902/jop.2012.110664
Endo, Y., Tomofuji, T., Ekuni, D., Irie, K., Azuma, T., Tamaki, N., … Morita,
M. (2010). Experimental periodontitis induces gene expression
of proinflammatory cytokines in liver and white adipose tissues
in obesity. Journal of Periodontology, 81(4), 520–526. https ://doi.
org/10.1902/jop.2009.090574
Ferreira, M. K. M., Ferreira, R. D. O., Castro, M. M. L., Magno, M. B.,
Almeida, A . P. C. P. S. C., Fagundes, N. C. F., … Lima, R. R. (2019). Is
there an association between asthma and periodontal disease among
adults? Systematic review and meta-analysis. Life Sciences, 223, 74
87. https ://doi.org/10.1016/j.lfs.2019.03.005
GINA (2012). Global initiative for asthma. Globa l strategy for asthma m an-
agement and prevention. Revised 2012. Vancouver.
Gomes-Filho, I. S., Cruz, S. S., Rezende, E. J. C., dos Santos, C .
A. S . T., Soledade, K. R., Mag alhães, M. A., Cerqueira, E.
M. M. (2007). Exposure measurement in the association be-
tween periodontal disease and prematurity/low birth weight.
Journal of Clinical Periodontology, 34(11), 957–963. https ://doi.
org /10.1111/j .1600 -051X .20 07.01141.x
Gomes-Filho, I. S., Soledade-Marques, K. R ., Seixas da Cruz, S., de
Santana Passos-Soares, J., Trindade, S. C., Souza-Machado, A., …
Freitas Coelho, J. M. (2014). Does periodont al infection have an
effec t on severe asthma in adults? Journal of Periodontology, 85(6),
e179–187. https ://doi.org/10.1902/jop.2013.130509
Gomes-Filho, I. S., Trindade, S. C., Passos-Soares, J. S., Figueiredo, A.
C. M. G., Vianna, M., & Cruz, S. S. (2018). Clinical diagnosis crite-
ria for periodontal disease: An update. Journal of Dental Health,
Oral Disorders & Therapy, 9(5), 354–356. https ://doi.org/10.15406/
jdhodt.2018.09.00408
Guan, S. M., Shu, L., Fu, S. M., Liu, B., Xu, X. L., & Wu, J. Z. (2009).
Prevotella intermedia upregulates MMP-1 and MMP-8 expression in
human periodontal ligament cells. FEMS Microbiology Letters, 299(2),
214–222. https ://doi.org/10.1111/j.1574-6968.2009.01748.x
Gueders, M. M., Ber tholet, P., Perin, F., Rocks, N., Maree, R ., Botta, V., …
Cata ldo, D. D. (200 8). A novel form ulation of inhaled doxycycline re-
duces allergen-induced inflammation, hyperresponsiveness and re-
modeling by matrix metalloproteinases and cytokines modulation in
a mouse model of asthma. Biochemical Pharmacology, 75(2), 514–526.
https ://doi.org/10.1016/j.bcp.2007.09.012
Harland, J., Furuta, M., Takeuchi, K., Tanaka, S., & Yamashita, Y. (2018).
Periodontitis modifies the association between smoking and chronic
obstructive pulmonary disease in Japanese men. Journal of Oral
Science, 60(2), 226–231. https ://doi.org/10.2334/josnu sd.17-0225
Higgins , J. P. (2008). Cochrane handbook para revisões sistemáticas de in-
tervenções versão 5.0.1.The Cochrane Collaboration.
Higgins , J. P., & Thompson, S. G . (20 02). Quantifying heterogeneity in a
meta-analysis. Statistics in Medicine, 21(11), 1539–1558. ht tps ://doi.
org /10.10 02/sim.118 6
Iwasaki, M., Taylor, G. W., Awano, S., Yoshida, A., Kataok a, S., Ansai, T., &
Nakamura, H. (2018). Periodontal disease and pneumonia mortality
in haemodialysis patients: A 7-year cohor t study. Journal of Clinical
Periodontology, 45(1), 38–45. https ://doi.org /10.1111/jcpe.12828
Khassawneh, B., Alhabashneh, R., & Ibrahim, F. (2019). The associa-
tion between bronchial asthma and periodontitis: A case-control
study in Jordan. Journal of Asthma, 56(4), 404–410. ht tps ://doi.
org/10.1080/02770 903.2018.1466315
Ledić, K., Marinković, S., Puhar, I., Spalj, S., Popović-G rle, S., Ivić-Kardum ,
M., … Plancak, D. (2013). Periodontal disease increases risk for
chronic obstructive pulmonary disease. Collegium Antropologicum,
37(3), 937–942.
Linden, G. J., Lyons, A., & Scannapieco, F. A. (2013). Periodontal systemic
associations: Review of the evidence. Journal of Periodontology, 84(4
Suppl), S8–S19. https ://doi.org/10.1902/jop.2013.1340010
McGowan, J., Sampson, M., Salzwedel, D. M., Cogo, E., Foerster, V., &
Lefebvre, C . (2016). PRESS peer review of elec tronic search strate-
gies: 2015 guideline statement. Journal of Clinical Epidemiology, 75,
40–46. https ://doi.org/10.1016/j.jclin epi.2016.01.021
Melo Neto, J. P., Melo, M. S. A. E., Santos-Pereira, S. A., Mar tinez, E. F.,
Okajima, L. S., & Saba-Chujfi, E. (2013). Periodontal infections and
community-acquired pneumonia: A case-control study. European
Journal of Clinical Microbiology and Infectious Diseases, 32(1), 27–32.
htt ps ://doi.o rg/10.1007/s10096- 012-1710-y
Mendes , V., Dos Santos, G. O., & Moraschini, V. (2018). Interrelation
of periodontal parameters between asthmatics and nonasthmatics
446 
|
   GOMES-FILHO E t aL.
subjects: A systematic review and meta-analysis. Journal of Dentistry,
69, 32–40. https ://doi.org/10.1016/j.jdent.2017.11.011
Modesti, P. A., Reboldi, G., Cappuccio, F. P., Agyemang, C., Remuzzi, G.,
Rapi, S., … Parati, G. (2016). Panethnic differences in blood pressure
in Europe: A systematic review and meta-analysis. PLoS ONE, 11(1) ,
e0147601. https ://doi.org/10.1371/journ al.pone.0147601
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & PRISMA Group
(2009). Preferred reporting items for systematic reviews and me-
ta-analyses: T he PRISMA st atement. PLoS Medicine, 6(7), e1000097.
0.1371/journ al.pmed.1000097
Moraschini, V., Calasans-Maia, J. A., & C alasans-Maia, M. D. (2018).
Association between asthma and periodontal disease: A systematic
review and meta-analysis. Journal of Periodontology, 89(4), 4 40–455.
htt ps ://doi.o rg /10.1902/ jop.2 017.170363
Page, R. C., & Eke, P. I. (20 07). Case definitions for use in popula-
tion-based surveillance of periodontitis. Journal of Periodontology,
78(7 Suppl), 1387–1399. https ://doi.org /10.1902/jop.20 07.060264
Pauwels, R. A., Buist, A. S., Calverley, P. M., Jenkins, C. R., Hurd, S. S.,
& Commit tee, G. S. (2001). Global strategy for the diagnosis, man-
agement, and prevention of chronic obstructive pulmonary disease.
NHLBI/WHO Global Initiative for Chronic Obstr uctive Lung Disease
(GOLD) Workshop summary. American Journal of Respirator y and
Critical Care Medicine, 163 (5), 1256–1276. https ://doi.org/10.1164/
ajrccm.163.5.2101039
Raghavendran, K ., Mylotte, J. M., & Scannapieco, F. A. (2007). Nursing
home-associated pneumonia, hospital-acquired pneumonia and ven-
tilator-associated pneumonia: The contribution of dental biofilms
and periodontal inflammation. Periodontology 2000, 44, 164–177.
https : //doi.org/10 .1111/j.16 00 -0757.20 06.0 0206.x
Rothman, K. J., Greeland, S., & Lash, T. L. (2011). Modern epidemiology
(3rd ed). Porto Alegre: Ar tmed.
Sabhar wal, A., Gomes-Filho, I. S., Stellrecht, E., & Scannapieco, F. A.
(2018). Role of periodo nta l therapy in man agement of common com-
plex systemic diseases and conditions: An update. Periodontology
2000, 78(1), 212–226. https ://doi.org/10.1111/prd.12226
Shi, Q., Zhang, B., Xing, H., Yang, S., Xu, J., & Liu, H. (2018). Patients with
chronic obstructive pulmonary disease suffer from worse periodon-
tal health-evidence from a meta-analysis. Frontiers in Physiology, 9,
33. https ://doi.org/10.3389/fphys.2018.0 0033
Si, Y., Fan, H., Song, Y., Zhou, X., Zhang, J., & Wang, Z. (2012). Association
between periodontitis and chronic obstructive pulmonary disease in
a Chinese population. Journal of Periodontology, 83(10), 1288–1296.
https ://doi.org/10.1902/jop.2012.110472
Soledade-Marques, K. R., Gomes-Filho, I. S., da Cruz, S. S., Passos-Soares,
J. D. S., Trindade, S. C., Cerqueira, E. D. M. M., Souza-Machado,
A. (2018). Association between periodontitis and severe as thma in
adults: A case-control study. Oral Diseases, 24(3), 442–448. https ://
doi .org/10.1111/odi .12737
START (2013). State of the art through systematic review - START. (Version
3.3). São Carlos - SP.
Takeuchi, K., Matsumoto, K., Furuta, M., Fukuyama, S., Takeshita, T.,
Ogata, H., … Yamashita, Y. (2019). Periodontitis is associated with
chronic obstructive pulmonary disease. Journal of Dental Research,
98(5), 534–540. htt ps ://doi.org/10.1177/00220 34519 833630
Tâlvan, E. T., Mohor, C., Chisnoiu, D., Cristea, V., & Câmpian, R . S.
(2017). E xpression of interleukin (IL)-1β, IL-8, IL-10 and IL-13 in
chronic adult. Archives of Medicine, 9(3), 4. https ://doi.org/10.21767/
1989-5216.100 0219
Tan, L., Wang, H., Pan, C., & Zhao, J. (2016). Periodontal health and
chronic obstructive pulmonar y disease stratified by smoking: A me-
ta-analysis. International Journal of Clinical and Experimental Medicine,
9(12), 23190–23197.
Terashima, T., Chubachi, S., Matsuzaki, T., Nakajima, T., Satoh, M., Iwami,
E., … Betsuyaku, T. (2017). The association between dental health and
nutritional status in chronic obstructive pulmonary disease. Chronic
Respiratory Disease, 14(4), 334–3 41. https ://doi.org/10 .1177/14799
7 2 3 1 6 6 4 3 0 7 6
Tonetti, M. S., Chapple, I. L ., Jepsen, S., & Sanz, M. (2015). Primary and
secondary prevention of periodontal and peri-implant diseases:
Introduction to, and objectives of the 11th European Workshop
on Periodontology consensus conference. Journal of Clinical
Periodontology, 42(Suppl 16), S1–S4. https ://doi.org/10.1111/
jcpe.12382
Vadiraj, S., Nayak, R., Choudhary, G. K., Kudyar, N., & Spoor thi, B. R.
(2013). Perio dontal pathogens and respirator y diseases- evaluating
their potential association: A clinical and microbiological study. The
Journal of Contemporary Dental Practice, 14 (4 ), 610 –61 5. h ttps ://doi.
org/10.5005/jp-journ als-10024-1373
Wells, G., Shea, B., O'Connell, D., Peterson, J., Welch, V., Losos, M., &
2014). The Newcastle-Ottawa Scale (NOS) for assessing the quality
of nonrandomised studies in meta-analyses. In. The Ottawa Hospital:
Research Institute.
WHO (2013). Oral health surveys: Basic methods (5th edn). School of
Dentistry, University of São Paulo, Brazil.
Zeng, X. T., Tu, M. L., Liu, D. Y., Zheng, D., Zhang, J., & Leng, W. (2012).
Periodontal disease and risk of chronic obstructive pulmonary dis-
ease: A meta-analysis of observational studies. PLoS ONE, 7(10) ,
e46508. https ://doi.org/10.1371/journ al.pone.0046508
Zhang, J., & Yu, K. F. (1998). W hat's the relative risk? A method of cor-
recting the odds ratio in cohor t studie s of common outcomes. JAMA,
280(19), 1690–1691. https ://doi.org/10.1001/jama.280.19.1690
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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
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Background and Objective: It is widely accepted that there is an association between chronic obstructive pulmonary disease (COPD) and periodontitis. However, whether the periodontal status of the COPD patients is worse than that of the non-COPD subjects is seldom assessed. The findings currently available are inconsistent, some even contradictory. Therefore, we performed this meta-analysis to compare the periodontal health status of COPD patients and non-COPD subjects. Methods: PubMed and Embase were searched for all of the eligible studies which comparing the periodontal status between COPD patients and non-COPD subjects. The results of periodontal parameters in each study were extracted and the mean differences and 95% confidence intervals (CIs) for each parameter were calculated to determine their overall effects. Results: In total, 14 studies involving 3348 COPD patients and 20612 non-COPD controls were included and 9 periodontal indexes were analyzed. The mean differences (95% CIs) between COPD and non-COPD subjects for probing depth, clinical attachment loss, level of alveolar bone loss, plaque index, oral hygiene index, bleeding index, bleeding on probing, gingival index, and remaining teeth were 0.261 (0.020–0.501), 0.480 (0.280–0.681), 0.127 (0.000–0.254), 0.226 (0.043–0.408), 0.802 (0.326–1.279), 0.241 (−0.106 to 0.588), 6.878 (5.489–8.266), 0.364 (0.036–0.692), and −3.726 (−5.120 to −2.331), respectively. Conclusion: In summary, this meta-analysis demonstrates that the COPD patients suffer from worse periodontal health status, indicated by deeper periodontal pockets, high level of clinical attachment loss, worse oral hygiene, more inflammation and bleeding in the gingival tissue, and lower number of remaining teeth. Nevertheless, considering the limitations in our meta-analysis, more high-quality, and well-designed studies focusing on the periodontal health of the COPD patients are required to validate our conclusion.
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Although they are known to share pathophysiological processes, the relationship between periodontitis and chronic obstructive pulmonary disease (COPD) is not fully understood. The aim of the present study was to test the hypothesis that periodontitis is associated with a greater risk of development of COPD, when smoking is taken into account. The analysis in a 5-y follow-up population-based cohort study was based on 900 community-dwelling Japanese adults (age: 68.8 ± 6.3 [mean ± SD], 46.0% male) without COPD aged 60 or older with at least 1 tooth. Participants were classified into 3 categories according to baseline periodontitis severity (no/mild, moderate, and severe). COPD was spirometrically determined by a fixed ratio of <0.7 for forced expiratory volume in 1 s (FEV 1 )/forced vital capacity (FVC) and by FEV 1 /FVC below the lower limit of normal. Poisson regression was used to calculate the relative risk (RR) of developing COPD according to the severity of periodontitis. The population attributable fraction (PAF) was also calculated. During follow-up, 22 (2.4%) subjects developed COPD. Compared with no/mild periodontitis subjects, a significantly increased risk of COPD occurred among severe periodontitis subjects (RR = 3.55; 95% confidence interval [CI], 1.18 to 10.67), but no significant differences were observed between the no/mild and moderate categories (RR = 1.48; 95% CI, 0.56 to 3.90). After adjustment for potential confounders, including smoking intensity, the relationship between severe periodontitis and risk of COPD remained significant (RR = 3.51; 95% CI, 1.15 to 10.74). Likewise, there was a positive association of periodontitis severity with risk of COPD (P for trend = 0.043). The PAF for COPD due to periodontitis was 22.6%. These data highlight the potential importance of periodontitis as a risk factor for COPD. © International & American Associations for Dental Research 2019.
Article
This systematic review and meta-analysis aimed to investigate a possible association between asthma and periodontal disease in adults. This study was conducted by Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) and the searches were performed on the following databases: PubMed, Scopus, Web of Science, Cochrane, LILACS, OpenGrey e Google Scholar. In this systematic review, observational studies with adult humans, which evaluated patients with and without asthma, were selected to verify the association between both diseases. To qualitative analysis, Fowkes and Fulton guidelines was used and for the quantitative analysis, it was used the mean and standard deviation from each group (with and without asthma), using confidence interval (CI) 95% and heterogeneity were tested using I ² index. Furthermore, a summary of the overall strength of evidence was presented using Grading of recommendations, assessment, development, and evaluation (GRADE). 3395 studies were identified, 11 were included on this systematic review to qualitative analysis and 6 of them to quantitative synthesis. Six meta-analyses were performed to the following clinical parameters: plaque index (PI), gingival index (GI), bleeding on probing (BOP), papillary bleeding index (PBI), calculus index (CI), clinical attachment loss (CAL). The meta-analysis results for CI was (p < 0.00001, I2 = 0%) PBI (p < 0.00001, I2 = 0%), CAL (p = 0,03, I ² = 98%) showed higher means for the asthmatic group. For BOP (p = 0.20 I2 = 83%), GI (p = 0.14 I2 = 97%) and PI (p = 0.53 I2 = 95%) non-statistical difference was found. The level of evidence analysis (GRADE) presented a low level of evidence among the clinical parameters. This systematic review and meta-analysis observed that asthmatic individuals present more periodontal disease, especially gingivitis, when compared to healthy individuals, but further studies with similar methods are necessary to evaluate interactions between both diseases.
Article
The goal of this review is to summarize the results of randomized trials reported since 2010 that assessed the effect of periodontal interventions on at least one systemic outcome in human subjects of any age, gender or ethnicity. Oral outcome measures included gingivitis, pocket depth, clinical attachment loss and/or radiographic bone loss and oral hygiene indices. Studies were excluded if the trial was not completed or if treatment was not randomized. The results suggest that nonsurgical periodontal intervention provided to pregnant women is safe and improves periodontal status without preventing adverse pregnancy outcomes. Nonsurgical periodontal intervention was also found to provide modest improvement in glycemic control in individuals with type 2 diabetes mellitus and periodontitis. Also, improving oral care through mechanical or chemical control of dental-plaque biofilm formation can contribute to the prevention of respiratory infections in differing clinical settings, including hospitals and nursing homes, and in patients with chronic obstructive pulmonary disease. No clinical trials were reported that tested the effect of periodontal interventions on medical outcomes of atherosclerosis, cardiovascular diseases, stroke, rheumatoid arthritis, Alzheimer's disease, chronic kidney disease or malignant neoplasia. © 2018 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Article
Objective: Our aim is to study the association between bronchial asthma (BA) and periodontitis in northern Jordan. Methods: A case-control study of 260 subjects; 130 with BA and 130 without BA (controls) were recruited from pulmonary clinics at a university hospital in northern Jordan. BA was physician diagnosed and on anti-asthma medications for ≥12 months. Periodontitis was defined as the presence of ≥ 4 teeth with ≥ 1 site with probing pocket depth (PPD) ≥ 4 mm and clinical attachment level (CAL) ≥ 3 mm. Results: Mean age for the participants was 45.3 years (range, 18–65) and 58.1% were females. Patients with BA had lower education and tended to live in rural areas. Periodontitis was present in 52 (40.0%) patients with BA and 26 (20.0%) in the control group, p<0.005. In binary logistic regression, patients with BA were more likely to have periodontitis than controls (adjusted odd ratio (OR) = 2.91, 95% CI (1.39-6.11), p = 0.005. Patients with BA had higher percentage of sites with: PPD ≥ 3, CAL ≥ 3, and CAL ≥ 4 than controls, p < 0.05. The risk (adjusted OR = 5.27, 95% CI (1.59-17.51) and CAL ≥ 3 were higher in patients on oral corticosteroids compared to inhaled corticosteroids, p<0.05. Conclusions: Bronchial asthma had a positive association with periodontitis, and treatment with oral corticosteroids increased the risk of periodontal disease. Large and longitudinal studies are needed to better identify this significant association.
Article
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.
Article
Aim: To evaluate the association between periodontal disease and pneumonia mortality in hemodialysis patients. Materials and methods: This prospective cohort study included 211 patients (mean age, 64.4 years) undergoing hemodialysis at a single medical center. The patients underwent a baseline clinical dental examination in 2008 and were then followed up until July 2015. Periodontal disease was defined as the presence of clinical attachment loss of ≥4 mm in ≥30% of the probed sites. The primary endpoint, i.e., death from pneumonia, was determined by reviewing death certificates, and was analyzed using the competing-risks regression model. Results: At baseline, 92 patients (43.6%) had periodontal disease. The median follow-up period was 84 months (interquartile range, 36-86 months). Of the 68 deaths that occurred, 21 were from pneumonia. The multivariable competing-risks regression model showed that periodontal disease was significantly associated with death from pneumonia (adjusted subhazard ratio, 3.49; 95% confidence interval, 1.14-10.64), after adjusting for other baseline health characteristics. Conclusions: The results of this study suggest that periodontal disease is independently associated with pneumonia mortality in hemodialysis patients. Future studies evaluating the potential effect of oral interventions for periodontal health improvement on pneumonia in hemodialysis patients would be of great interest. This article is protected by copyright. All rights reserved.
Article
Background: The aim of this systematic review is to evaluate the association between asthma and periodontal disease. Methods: An electronic search without date or language restrictions was carried out in MEDLINE, Cochrane, Web of Science, and LILACS until May 2016. 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. 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 systematic review strongly suggest the association of asthma with periodontal disease.