Clinical Oral Investigations (2020) 24:2285–2294

https://doi.org/10.1007/s00784-019-03083-9

ORIGINAL ARTICLE

Is there association between stress and periodontitis?

Julita Maria F. Coelho 1 & Samilly S. Miranda 1 & Simone S. da Cruz 1,2 & Soraya C. Trindade 1 &
Johelle de S. Passos-Soares 1,3 & Eneida de M. M. Cerqueira 1 & Maria da Conceição N. Costa 4 &
Ana Claúdia M. G. Figueiredo 2 & Alexandre Marcelo Hintz 1 & Maurício L. Barreto 4 & Gregory J. Seymour 5 &
Frank Scannapieco 6 & Isaac Suzart Gomes-Filho 1

Received: 27 December 2018 / Accepted: 22 September 2019 / Published online: 25 October 2019
# Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
Objective This study estimated the association between stress and periodontitis.
Materials and methods A cross-sectional study was conducted with a sample of 621 individuals. Information about individuals was
obtained through a questionnaire. Stress was evaluated using the Perceived Stress Scale. The diagnosis of periodontitis was based on a
complete periodontal examination including clinical attachment level, probing depth, and bleeding on probing. Prevalence ratios
(PR), crude and adjusted, and their respective 95% confidence intervals (95%CI) were estimated by Poisson regression analysis.
Results In the final sample, 48.47% (301) of the individuals were classified as having stress, of which, 23.92% (72) had the
diagnosis of periodontitis. Association measurements between stress and probing depth ≥ 4 mm (PRadjusted = 1.28, 95%CI [1.04
to 1.58]), stress and clinical attachment level ≥ 5 mm (PRadjusted = 1.15, 95%CI [1.01 to 1.31]), and stress and periodontitis
(PRadjusted = 1.36, 95%CI [1.01 to 1.83]) showed that the frequency of these outcomes among those exposed to stress was 15–
36% higher than those without the condition of stress, after adjustment for age, sex, schooling level, current smoking habit,
pulmonary disease, and body mass index.
Conclusions The findings showed positive association between exposure to stress and the presence of periodontitis, reaffirming
the need to prevent and control stress.
Clinical relevance Although there are limitations in this study, the results showed that an association exists between stress and
periodontitis, signaling the necessity of a multidisciplinary attention when considering the psychological status in the manage-
ment of oral and general health conditions of the individual.

Keywords Epidemiology . Psychological stress . Mental health . Periodontitis . Chronic periodontitis . Oral health

Introduction individual’s ability to deal effectively with the situation. Due

to the changes brought about in the physical and psychologi-
Stress is related to emotional and physiological reactions cal adaptive dynamics, stress has been repeatedly associated
when there is a lifetime event conflict that exceeds the with increased susceptibility to the onset of disease [1–3].

Electronic supplementary material The online version of this article

(https://doi.org/10.1007/s00784-019-03083-9) contains supplementary
material, which is available to authorized users.

* Isaac Suzart Gomes-Filho 3

Department of Preventive Dentistry, Federal University of Bahia,
isuzart@gmail.com Salvador, Bahia, Brazil
4
1
Department of Epidemiology, Collective Health Institute, Federal
Department of Health, Feira de Santana State University, Avenida University of Bahia, Bahia, Brazil
Getúlio Vargas, 379, Centro, Feira de Santana, Bahia 44025-010, 5
Brazil Department of Periodontology, School of Dentistry, The University of
2
Queensland, Brisbane, Australia
Department of Epidemiology, Federal University of Recôncavo of 6
Bahia, Bahia, Brazil Department of Oral Biology, University of Buffalo, Buffalo, NY,
USA
2286
Some studies have shown that psychological stress or other
psychosomatic conditions can trigger immune responses that
favor the occurrence or exacerbation of changes in the oral
cavity, such as periodontitis [4, 5]. It can directly impair the
periodontal status through various biological mechanisms:
variation in the gingival fluid, production of interleukin IL-
1, IL-6, reduction of polymorphonuclear leukocytes and
phagocytosis, and decreased lymphocyte production, as well
as through changes in behavior related to health, such as oral
hygiene, smoking habit, and diet [3, 5, 6].
Stress is a prevalent problem in modern life [7]. The
American Psychological Association, USA (2013) [8], report-
ed that 20% of Americans have a high level of stress. Also,
according to the study Stress in Brazil (2013) [9], 34.26% of
Brazilians reported experiencing extreme stress. Likewise,
periodontitis presents a high prevalence worldwide [10]. It is
considered to be the second most prevalent oral disease in the
world, affecting people in developed countries—where the
prevalence of changes in periodontal tissues in adults in the
third decade of life can reach 85%—as well as in developing
countries [11].
Although previous studies have suggested that stress may
favor the occurrence of periodontitis [4, 6, 12–24], the evi-
dence is still fragile, due to variations in the method and lack
of standardization in the definition of exposure and outcome
factors, and as a result of a small sample size.
Thus, and given the importance of this issue for public
health, this study estimated the association between stress
and periodontitis, contributing to current knowledge, using a
sufficiently large sample size, which allowed for the explora-
tion of confounding covariables, and also different outcome
definitions.
Methods
A cross-sectional study approved by the Research Ethics
Committee of Feira de Santana State University
(Registration No. 025/2004) was conducted from a database
of a case-control study that had previously estimated the as-
sociation between periodontitis and acute myocardial infarc-
tion, developed at Santa Izabel Hospital and Ana Nery
Hospital in Salvador, Bahia, Brazil, over a period of 8 months.
Individuals who agreed to participate in the basic study
signed an informed consent form. The selection of the partic-
ipants consisted of individuals that looked for consultation in
the mentioned hospitals and of people living in the neighbor-
hood of these individuals. As inclusion criteria, they needed to
have at least four teeth to ensure the validity of periodontal
status measurements, not be pregnant, without cancer or HIV-
AIDS, not be using anti-inflammatory medication in the
2 months prior to the study, and no periodontal treatment in
the 6 months prior to the survey. Those with anterior
Clin Oral Invest (2020) 24:2285–2294
infarction, percutaneous coronary revascularization history
within the previous 6 months or surgical revascularization in
the 2 months prior to the study were excluded.
Information related to socioeconomic and demographic
characteristics, general and oral health condition, habits and
lifestyle, medical and dental history, and access to oral health
care was obtained through an interview questionnaire.
Furthermore, each participant completed a Perceived Stress
Scale survey.
Periodontal examination/periodontal parameters
Individuals underwent a complete periodontal examination by
a single examiner (JMSFC), who had been previously trained.
The degree of agreement of the collected clinical periodontal
data, through the Kappa coefficient (0.87 with difference of ±
1 mm), showed good agreement.
The following clinical periodontal parameters were evalu-
ated: probing depth, gingival recession, clinical attachment
level, bleeding on probing, visible plaque index, and number
of teeth. These were obtained at six sites per tooth except the
third molars, corresponding to the mesial buccal, medium-
buccal, disto buccal, mesial lingual, mid-lingual, and disto
lingual regions, through the use of a Williams periodontal
probe (Hu-Friedy, Chicago, IL, USA). The visible plaque in-
dex was evaluated in four regions per tooth (mesial, distal,
buccal, palatal/lingual).
The probing depth record was obtained by measuring the
gingival margin at the deepest region of penetration of the
probe [25]. The measurement of gingival recession was the
distance between the cementum-enamel junction and the gin-
gival margin. The clinical attachment level was obtained by
adding together the probing depth values and the gingival
recession measurements of each site [26]. The bleeding index
was established by observing its occurrence up to 10 s after the
examination of probing depth. The visible plaque index was
evaluated using the probe only to confirm the presence of
biofilm on the tooth surface [27].
The data on lipid and glycemic profile, body mass index
(BMI), and blood pressure were later obtained from the med-
ical records of study participants. These data and tests were
performed within 30 days of the oral exam.
Sample size
The calculation of the minimum sample size for this study
employed a 99% study power, confidence level of 99%, and
a ratio of 1:1 between exposure and non-exposure, with a
frequency of periodontitis of 38.2% for the unexposed group
and 61% in the exposed group [22]. The minimum estimated
number of individuals to compose the exposed group (indi-
viduals with exposure to stress) and not exposed was 235
each, totaling 470.
Clin Oral Invest (2020) 24:2285–2294
Exposure factor—stress
Stress was evaluated using the Perceived Stress Scale [28].
This instrument has 14 questions with response options rang-
ing from zero to four (0 = never, 1 = almost never, 2 = some-
times, 3 = often, 4 = always). The questions with positive con-
notation (4, 5, 6, 7, 9, 10, and 13) had a punctuation as fol-
lows: 0 = 4, 1 = 3, 2 = 2, 3 = 1, and 4 = 0. The remaining ques-
tions are negative and were added directly. Results varied
from zero to 56. Finally, an arithmetic average was obtained
to observe which individuals had stress greater than the aver-
age scores, thus defining the diagnosis of stress. As such, two
groups were formed: (1) individuals with perceived stress
score ≤ 24—not exposed to stress group; (2) individuals with
perceived stress score > 24—the group exposed to stress [29,
30].
Outcome—periodontitis
The participant was considered diagnosed with periodontitis
when 4 or more teeth were present, with 1 or more sites with
probing depth greater than or equal to 4 mm, with clinical
attachment level greater than or equal to 3 mm in the same
place, and the presence of bleeding on probing [31].
Furthermore, two clinical parameters were also employed as
surrogates for defining the presence of periodontitis: probing
depth ≥ 4 mm [15, 18] and clinical attachment level ≥ 5 mm
[12, 13, 23].
Data analysis
Descriptive analysis of the exposure variable (stress), outcome
variable (periodontitis), and all measured covariables was con-
ducted, obtaining the simple and relative frequencies for cat-
egorical covariables and measurements of central tendency
and dispersion, for the continuous covariables. To assess the
degree of homogeneity between the groups, the Pearson chi-
square test was used for categorical covariables and the Mann-
Whitney test for continuous covariables, according to their
distribution, with a 5% significance level. The cut-off points
used to categorize the covariables were established according
to their distribution in the sample or previous studies on the
topic.
Stratified analysis was performed to identify potential ef-
fect modifiers and confounders between the investigated
covariables. The presence of modifier effect was investigated
using the likelihood ratio test (P < 0.05) by comparing the
models with and without the product terms. For those
covariables in which the presence of effect modification was
not identified, the confounding role of these covariables was
assessed by backward strategy and the confounder identified
when the covariable produced a 10% relative difference in the
2287
association measurement in comparison to the saturated
model.
The association measurement between stress and periodon-
titis was performed by Poisson analysis, obtained by the prev-
alence ratio (PR) and 95% confidence interval (CI95%), both
crude and adjusted for each outcome definition criterion. In
the absence of confounders confirmed by statistical analysis,
some covariables were selected for the final adjusted model
due to the knowledge of their role in both the primary expo-
sure variable and the outcome variable.
To validate the analysis models used, the Hosmer-
Lemeshow test was employed to verify the goodness of fit
of the analysis model. Data analysis was performed using
the SPSS - Statistical Package for the Social Sciences, version
17.0 (SPSS Inc., Chicago, IL, USA) and STATA version 10.0.
Results
Characteristics of the sample according
to the diagnosis of stress
The study included 621 individuals, of which 300 were female
and 321 male, with a mean age of 59.42 ± 10.91 (± SD) years,
median of 59 years and a range of 40–91 years in the group
exposed to stress (301 individuals). In the unexposed group
(320 individuals without stress), the mean age was 59.40 ±
10 years (± SD), median of 58.5 years and a range of 40–
89 years.
Data for sample characterization, socioeconomic and
demographic covariables related to lifestyle habits, oral
health, and overall health conditions are distributed in
Table 1 in accordance with the diagnosis, or not, of stress.
The comparison groups proved to be homogeneous for
most characteristics with statistically significant difference
only for the covariables: gender (P < 0.01) and schooling
level (P < 0.01). The results showed that participants with
stress, compared to those not exposed to this condition,
were more frequently female (55.15% vs 41.88%), and
those with 4 years or less of study (82.67% vs 72.84%).
Covariables with few observations were not included in
the tables.
Characteristics of the sample according
to the occurrence of periodontitis
The study individuals were reclassified according to the diag-
nosis of periodontitis (Table 2) and those with periodontitis
(142 individuals) presented a mean age of 58.82 ± 10.90 (±
SD), median of 56.5 years and a range of 40–84 years. And,
for the group without periodontitis (479 individuals), they
presented a mean of 59.67 ± 10.89, median of 59 years and a
range of 40–91 years. The distribution of the investigated
2288 Clin Oral Invest (2020) 24:2285–2294

Table 1 Characteristics of the sample according to the diagnosis of stress. Salvador, Bahia, Brazil

Covariables Group exposed to stress (N = 301) Group not exposed to stress (N = 320) P

N % N %

Demographic covariables
Age (in years)
≥ 59 154 51.16 160 50.00 0.77
Race/skin color**
Black/brown/other 246 81.73 255 79. 69 0.52
Sex
Female 166 55.15 134 41.88 < 0.01
General health condition covariables
Body mass index (kg/m2)**
≥ 25 185 67.77 182 63.41 0.28
Diabetes
Yes 57 18.94 66 20.63 0.60
Hypercholesterolemia**
Yes 28 9.56 20 6.31 0.14
Hypertension
Yes 169 56.15 170 53.13 0.45
Pulmonary disease**
Yes 14 4.70 10 3.14 0.32
Renal disease**
Yes 25 8.39 35 11.01 0.28
Lifestyle habit covariables
Alcoholic beverage consumption**
Yes 134 44.52 147 46.23 0.67
Current smoking habit
Yes 37 12.29 49 15.31 0.28
Physical activity practice**
No 194 66.90 195 63.93 0.45
Oral health condition covariables
Consultation with a dentist (at least once a year)
Yes 194 64.45 203 63.44 0.79
Dental floss usage (at least once a day)**
No 242 82.59 261 84.19 0.60
Frequency of brushing**
< 3×/day 178 59.73 177 56.55 0.43
Participant received oral health guidance (at least once in a lifetime) **
No 150 50.00 160 50.00 1.00
Socioeconomic covariables
Family income1**
≤ 1 minimum salary 158 53.02 173 55.99 0.46
Home owner**
Yes 260 87.54 270 87.66 0.96
Household density**
> 3 persons 133 44.48 140 44.44 0.99
Marital status**
Married/other union 170 56.86 191 59.87 0.45
Occupation
No 181 60.13 191 59.69 0.91
Place of residence
Urban 283 94.02 300 93.75 0.89
Schooling level (in years of study)
Basic education (≤ 4 years) 248 82.67 228 72.84 < 0.01

*P value: significance level ≤ 0.05. 1Minimum salary value at the time of data collection: R$465,00. **Quantity of lost or not declared information

covariables showed that the groups are comparable, since only
current smoking habit showed a statistical difference between
comparison groups, with higher occurrence of individuals
with that habit in the group with periodontitis (19.01% vs.
12.32%).
In Table 3, the covariables related to periodontal status
were presented according to the diagnosis of stress. The
periodontal condition with greater alteration was observed
in the group exposed to stress, with statistically signifi-
cant differences in the number of teeth (P = 0.02), number
Clin Oral Invest (2020) 24:2285–2294 2289

Table 2 Characteristics of the sample according to the occurrence of periodontitis. Salvador, Bahia, Brazil

Covariables Group with periodontitis (N = 142) Group without periodontitis (N = 479)

N % N % P*

Demographic covariables
Age (in years)
≥ 59 62 43.66 252 52.61 0.06
Race/skin color
Black/brown/other 116 81.69 385 80.38 0.73
Sex
Male 79 55.63 242 50.52 0.28
General health condition covariables
Body mass index (kg/m2)**
≥ 25 84 65.62 283 65.51 0.98
Diabetes
Yes 24 16.90 99 20.67 0.32
Hypercholesterolemia**
Yes 15 10.79 33 7.01 0.14
Hypertension
Yes 82 57.75 257 53.65 0.39
Pulmonary disease**
Yes 05 3.57 19 3.99 0.82
Renal disease**
Yes 14 9.93 46 9.68 0.93
Lifestyle habit covariables
Alcoholic beverage consumption**
Yes 66 46.48 215 45.07 0.77
Current smoking habit
Yes 27 19.01 59 12.32 0.04
Physical activity practice**
No 84 60.87 305 66.74 0.20
Oral health condition covariables
Consultation with dentist
Yes 97 68.31 300 62.63 0.22
Dental floss usage (at least once a day)**
No 111 79.86 392 84.48 0.19
Frequency of brushing**
< 3×/day 73 52.90 282 59.62 0.16
Participant received oral health guidance (at least once in a lifetime)**
No 66 46.48 244 51.05 0.34
Socioeconomic covariables
Family income1**
≤ 1 minimum salary 78 56.93 253 53.83 0.52
Home owner**
Yes 117 85.40 413 88.25 0.37
Household density**
> 3 persons 54 38.57 219 46.20 0.11
Marital status**
Married/other union 80 56.74 281 58.91 0.65
Occupation
No 87 61.27 285 59.50 0.71
Place of residence
Urban 133 93.66 450 93.95 0.90
Schooling level (in years of study)
Basic education (≤ 4 years) 106 75.71 370 77.73 0.53

*P value: significance level ≤ 0.05. 1 Minimum salary value at the time of data collection: R$465.00. **Quantity of loss or not declared information

of sites with clinical attachment level of 3 to 4 mm
(P < 0.01), number of sites with clinical attachment level
of 5 mm (P = 0.04), number of sites with a probing depth
of 4 and 5 mm (P < 0.01), and number of sites with a
probing depth ≥ 6 mm (P = 0.02).
Association between stress and periodontitis
Association measurements, crude and adjusted, between
stress and periodontitis are presented in Table 4. According
to the unadjusted measurements, there was only association
2290 Clin Oral Invest (2020) 24:2285–2294

Table 3 Mean, median, and minimum and maximum values of covariables related to periodontal status according to the diagnosis of stress. Salvador,
Bahia, Brazil

Clinical periodontal parameters Group exposed to stress Group not exposed to stress P*
(N = 301) (N = 320)

Bleeding upon probing (%) 0.89

Mean ± sd 11.86 ± 18.05 11.30 ± 17.17
Median (interquartile range) 1.0 (0.0–19.0) 2.0 (0.0–17.5)
Minimum-maximum 0.0–96.0 0.0–91.0
Plaque index (%) 0.80
Mean ± sd 32.64 ± 15.03 31.86 ± 13.34
Median (interquartile range) 31.0 (25.0–40.0) 31.0 (25.0–38.0)
Minimum-maximum 0.0–84.0 0.0–90.0
Teeth present (n) 0.02
Mean ± sd 14.50 ± 8.13 15.81 ± 8.13
Median (interquartile range) 12.0 (8.0–22.0) 14.0 (9.0–22.25)
Minimum-maximum 2–32 4–32
Number of sites with a clinical attachment level of 1 to 2 mm (n) 0.22
Mean ± sd 0.83 ± 2.06 0.93 ± 2.17
Median (interquartile range) 0.0 (0.0–1.0) 0.0 (0.0–1.0)
Minimum-maximum 0.0–16.0 0.0–22.0
Number of sites with a clinical attachment level of 3 to 4 mm (n) < 0.01
Mean ± sd 6.33 ± 7.61 8.20 ± 8.34
Median (interquartile range) 3.0 (0.0–12.0) 6.0 (1.0–14.0)
Minimum-maximum 0.0–32.0 0.0–30.0
Number of sites with a clinical attachment level of 5 mm (n) 0.04
Mean ± sd 7.31 ± 4.54 6.65 ± 4.56
Median (interquartile range) 7.0 (5.0–10.0) 6.0 (3.0–9.0)
Minimum-maximum 0.0–29.0 0.0–23.0
Number of sites with a probing depth of 4 and 5 mm (n) < 0.01
Mean ± sd 4.22 ± 3.76 3.35 ± 3.68
Median (interquartile range) 4.0 (1.0–6.0) 2.0 (0.0–6.0)
Minimum-maximum 0.0–19.0 0.0–18.0
Number of sites with a probing depth of ≥ 6 mm (n) 0.02
Mean ± sd 2.33 ± 1.39 0.39 ± 1.54
Median (interquartile range) 1 (0–4.0) 0 (0–0)
Minimum-maximum 0–15.0 0–11.0

*P value: significance level ≤ 0.05; sd standard deviation

between stress and probing depth ≥ 4 mm: PRcrude = 1.26,
95% CI [1.03 to 1.55], demonstrating a likelihood of having
periodontitis, represented by probing depth ≥ 4 mm, 1.26
times higher among those diagnosed with stress in comparison
to those without the condition.
After the necessary adjustments for the following con-
founder covariables, age, sex, schooling level, current
smoking habit, pulmonary disease, and body mass index, all
models showed a positive association: PRadjusted = 1.28, 95%
CI [1.04–1.58] stress and probing depth ≥ 4 mm, PRadjusted =
1.15, 95% CI [1.01 to 1.31] stress and clinical attachment
level ≥ 5 mm, and PRadjusted = 1.36, 95% CI [1.01 to 1.83]
stress and periodontitis. These measurements showed that in
individuals exposed to stress the frequency of periodontitis
was 15 to 36% higher than those without the condition.
In the logistic regression model used, the Hosmer-
Lemeshow statistical test was employed to verify the good-
ness of fit for each model. The P value varied from 0.20 to
0.60, showing that the null hypothesis was rejected and indi-
cating the good quality of the regression models employed.
Discussion
According to the main findings of this study, there was a
positive association between exposure to stress and periodon-
titis, irrespective of the definition of periodontitis used, and
after adjustments for covariables recognized as potential con-
founders. These results corroborate previous studies that have
investigated this topic [4, 6, 12–24]. It is worth noting that the
magnitude of the observed association was larger in the model
which employed a robust periodontitis definition criteria [31],
in comparison to those which used a single periodontal clini-
cal parameter serving as a surrogate for defining the disease.
The biological plausibility for this association is based on
the knowledge that stress, as well as influencing the immune
Clin Oral Invest (2020) 24:2285–2294 2291

Table 4 Prevalence ratio (PR), crude and adjusted, for the association Given this diversity of criteria for classification of peri-
between stress and periodontal condition. Salvador, Bahia, Brazil (n =
odontal condition, this study evaluated three ways to define
621)
periodontitis. In most previous studies, it was common to
PR 95%CI P* employ a clinical parameter as a surrogate for a specific crite-
rion that defines periodontitis; in comparison, three outcome
MODEL 1 Stress and probing depth ≥ 4 mm
definitions were investigated in the present study. There is a
Crude_1 1.26 1.03–1.55 0.02
risk of obtaining a misdiagnosis of the disease when using
Adjusted_1§ 1.28 1.04–1.58 0.02
clinical parameters in isolation [35]; however, this study’s
MODEL 2 Stress and clinical attachment level ≥ 5 mm
results corroborated those studies which evaluated these pa-
Crude_2 1.13 0.99–1.28 0.06
rameters separately [15, 17, 18, 23], demonstrating that
Adjusted_2§ 1.15 1.01–1.31 0.03
stressed individuals have worse periodontal condition.
MODEL 3 Stress and periodontitis In order to use a criterion to define periodontitis as a spe-
Crude_3 1.22 0.92–1.63 0.17 cific disease, the diagnosis of periodontitis proposed by
Adjusted_3§ 1.36 1.01–1.83 0.04 Gomes-Filho et al. [31] was employed. Although no previous
*P: significance level ≤ 0.05; 95%CI 95% confidence interval. §Adjusted
study on the topic have used this criterion, it has been used in
for age, sex, schooling level, current smoking habit, pulmonary disease, studies that associated periodontal infection with systemic dis-
and body mass index eases and conditions [36–38]. It should be emphasized that
this criterion minimizes the risk of false-positive diagnosis of
response, triggers changes in health-related behaviors, periodontitis, which is important in investigations that seek to
resulting in infection and, therefore, destruction of the peri- evaluate the relationship between two events, which can be
odontal tissues. The stress promotes an increase in the produc- attributed to the use of a combination of three clinical peri-
tion of neuroendocrine hormones such as glucocorticoids and odontal parameters: probing depth, clinical attachment level,
catecholamines. The activation of these hormones causes ad- and bleeding on probing [31].
verse effects on immune functions, including the reduction of Moreover, it is worth highlighting the importance of
lymphocyte populations and natural killer cell activity, among performing a complete periodontal clinical examination, in-
others [2]. volving six sites on each tooth. Some previous studies used
Given some weaknesses in studies concerning the effect of a periodontal clinical examination, which did not involve six
exposure to stress and periodontitis, this research adds to the sites per tooth [13, 17, 18], and these tend to underestimate or
current knowledge, by discussing some important issues overestimate the presence of periodontitis and increase the
found in previous research in an attempt to strengthen the likelihood of misclassification of the disease [39].
hypothesis of this association, such as heterogeneity in the Regarding the sample size, of the previous studies identi-
diagnostic criteria of both exposure and outcome, the sample fied on the topic, only four had sufficient participants to guar-
size, and the exploration of confounding covariables for antee the reliability of the final findings (Genco et al. (1999)
adjustment. [12]—n = 1426, Hilgert et al. (2006) [15]—n = 235, Ng and
Only one study [4] that investigated the effect of stress on Leung (2006) [16]—n = 1000, Ishisaka et al. (2008) [18]—
non-surgical periodontal therapy used the perceived stress n = 624). In addition, all four presented adjusted association
scale to define the exposure, even though this instrument has measurements for the following confounders: age, sex, socio-
already been validated in different cultures and in more than economic factors, diabetes, oral hygiene, and smoking habit
20 countries and is considered the instrument of choice to [12, 15, 16, 18]. However, many previous studies did not
evaluate the perception of stress [32–34]. The authors con- perform this important adjustment, and as such, the reliability
cluded that those individuals under stress had a worse out- of their findings may be questioned [4, 6, 19, 20, 22–24].
come following periodontal therapy. Studies have also evalu- In the present study, due to a sufficiently large sample size,
ated other psychological factors together with stress, such as the following covariables were able to be included in the ad-
distress, anxiety, and depression [12, 14, 19, 21], which may justed analysis final model: age, sex, schooling level, current
have interfered in a more accurate definition of exposure. smoking habit, pulmonary disease, and body mass index, with
For the diagnosis of periodontitis, the differences between the aim of neutralizing the interference of these covariables, as
studies are quite meaningful because some used only the clin- they can influence both the exposure factor and the outcome.
ical attachment level [6, 12, 13, 16] and others only the prob- The frequency of stress and periodontitis is influenced by
ing depth [14, 20] as clinical parameters to define the groups age [4, 21, 22]. Individuals over 40 often face a greater num-
with and without periodontitis, whilst others classified the ber of negative life events, such as financial problems, work
disease when the individual presented changes in probing overload, death of a partner or family member, divorce, seri-
depth or in clinical attachment level [15, 17, 18, 23]. ous illness, and retirement, favoring the occurrence of
2292
increased stress levels. Similarly, the prevalence and severity
of periodontitis are higher from this age on [22].
Stress is more common among females [4, 40–42]. Men
and women tend to react differently to stress, psychologically
and biologically. In general, society imposes an overload of
activities on women. Personal, biological, hormonal, sexual,
and social demands are added on top of career demands [43,
44]. In contrast, periodontitis is more common among men
[45]. Some studies suggest that there may be an association
between sex hormones, especially high levels of testosterone
with periodontitis [46, 47].
Those with lower socioeconomic status, represented in this
study by schooling level, have the highest rates of morbidity,
psychological distress, stress, and periodontitis compared to
those in more advantaged socioeconomic positions [16, 22,
48]. Moreover, the tendency of individuals with lower social
support and high daily stress is to look for escapes to better
deal with those situations, smoking habit for example [12].
Smoking also represents a strong risk factor for periodontitis
[14, 49]. In addition, both stress and periodontitis have been
associated with higher incidence of pulmonary disease
[50–52], and high BMI levels [53, 54].
It is known that other factors could be associated with stress
and periodontitis, due to the multifactorial nature of both con-
ditions, which does not exclude the possibility of a spurious
association between the two diseases because of residual con-
founding represented by factors that were not evaluated in this
study. Another limitation is the cross-sectional design, pre-
cluding causal inferences between the exposure and the out-
come, as it does not ensure the temporality of the events. In
addition, the lack of radiographic examination, as well as the
inclusion of bleeding on probing in the definition of periodon-
titis, and the absence of information related to the minimum
daily amount of alcoholic beverage consumption and physical
activity practice may be limiting factors of the present study.
Nonetheless, these limitations do not weaken the relevance
of this research for public health, as it relates to two high-
prevalence conditions worldwide, which have systemic reper-
cussions for the affected individuals. However, the findings
suggest the need for more studies that can better clarify the
biological mechanisms that are involved in this association
and that can overcome the limitations signaled in this study.
They also suggest the need to undertake actions in the public
health service to prevent and control stress, since psycholog-
ical changes can trigger immune responses that favor the oc-
currence or exacerbation of many diseases, such as
periodontitis.
Acknowledgments Financial support for this research was provided by
the Research Support Foundation of the State of Bahia (FAPESB),
Salvador, Bahia, Brazil. And also by The National Council for
Scientific and Technological Development (CNPq), Brasilia, Brazil, and
Feira de Santana State University, Bahia, Brazil.
Clin Oral Invest (2020) 24:2285–2294
Authors’ contributions J. M. F. Coelho, S. S. Miranda, S. S. Cruz, S. C.
Trindade, J. S. Passos-Soares, E. M. M. Cerqueira, A. C. M. G.
Figueiredo, and Isaac S. Gomes-Filho contributed to the formulation of
the question under investigation, conception of the study, design, data
acquisition, data analysis, and interpretation and drafted and critically
revised the manuscript.
M. C. N. Costa, M. L. Barreto, G. J. Seymour, and F. Scannapieco
contributed to the analysis, interpretation, and critical revision the
manuscript.
A. M. Hintz contributed to the conception of the study, data acquisi-
tion, and critical revision of the manuscript.
All authors gave final approval and agreed to be accountable for all
aspects of the manuscript.
Funding information The work was supported by the Research Support
Foundation of the State of Bahia (FAPESB), Salvador, Bahia, Brazil. And
also by The National Council for Scientific and Technological
Development (CNPq), Brasilia, Brazil, and Feira de Santana State
University, Bahia, Brazil.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the institu-
tional and/or national research committee and with the 1964 Helsinki
Declaration and its later amendments or comparable ethical standards.
Informed consent Informed consent was obtained from all individual
participants included in the study.
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