Received: 17 February 2020 Revised: 21 April 2020
DOI: 10.1002/JPER.20-0105
ORIGINAL ARTICLE
Influence of psychological stress on non-surgical
periodontal treatment outcomes in patients with severe
chronic periodontitis
Catherine Petit1,2,3 Victor Anadon-Rosinach1,2
Catherine Schmidt-Mutter4 Nicolas Tuzin5
Olivier Huck1,2,3
1Periodontology, University of Strasbourg,
Dental Faculty, Strasbourg, France
2University Hospital of Strasbourg,
Strasbourg, France
3 UMR 1260 Regenerative Nanomedicine,
INSERM (French National Institute of
Health and Medical Research),
Strasbourg, France
4Clinical Investigation Center, INSERM
U1434, University Hospital of Strasbourg,
Strasbourg, France
5Methodology and Biostatistics Group,
Public Health Department, University
Hospitals of Strasbourg, Strasbourg,
France
Correspondence
Pr Olivier Huck, Department of Periodon-
tology, Dental Faculty, University of Stras-
bourg, 8 rue Sainte-Elisabeth, 67000 Stras-
bourg, France.
Email: o.huck@unistra.fr
Funding information
University Hospital of Strasbourg,
Grant/Award Number: AAPJC 2013 HUS
N◦ 5502
J Periodontol. 2020;1–10.
Accepted: 7 June 2020
Laurence Rettig4
Jean-Luc Davideau1,2
Abstract
Background: The aim of this study was to evaluate the influence of psychologi-
cal stress on non-surgical periodontal treatment (SRP) outcomes in patients with
severe chronic periodontitis (stage 3/4 generalized periodontitis) at 6 months in
the French population.
Methods: Patients diagnosed with severe generalized chronic periodontitis
(periodontitis stage 3/4) were included in this study. At baseline, psychologi-
cal status was evaluated by self-administered questionnaire (Depression Anxiety
Stress Scale 42 [DASS-42] and Toulouse coping scale [TCS]). Plasma levels of cor-
tisol and chromogranin-A were determined. Patients were then managed by oral
hygiene instructions, scaling and root planing of sites with PD >3 mm and fol-
lowed at 3 and 6 months. Quantitative and qualitative variables were described
and interactions were determined by linear and logistic regressions.
Results: Seventy-one patients were included in this study and 54 were followed
up to 6 months. An average probing depth (PD) reduction of 0.73 ± 0.11 mm
and decrease of diseased sites (PD >3 mm) were measured at 6 months illus-
trating SRP efficacy. Multivariable analysis showed that increased DASS-stress
score was associated to worsened SRP outcomes in terms of bleeding on probing
(BOP) (OR = 1.02, P <0.05) and mean PD (P <0.05) reduction. An increase of
DASS-depression score negatively influenced PD >5 mm (OR = 1.06, P <0.05),
PD >7 mm (OR = 1.17, P <0.01), CAL >5 mm (OR = 1.03, P <0.05), and
CAL >7 mm (OR = 1.07, P <0.05) reduction. Negative coping strategies were
also associated with worsened SRP outcomes.
Conclusions: Patients with increased stress, anxiety, and depression scores as
well as those exhibiting negative coping strategies demonstrate worsened SRP
outcomes. DASS-42 and TCS were useful to determine psychological status and
their use could be incorporated to assess treatment prognosis.
KEYWORDS
chromogranin-A, coping, cortisol, depression, periodontitis, stress
wileyonlinelibrary.com/journal/jper © 2020 American Academy of Periodontology 1
2 PETIT et al.
1 INTRODUCTION
Periodontitis is a multifactorial inflammatory disease of
infectious origin with high prevalence worldwide charac-
terized by clinical attachment loss (CAL) and increased
probing depth (PD).1 Severe periodontitis affects around
11% of the population worldwide with a peak incidence
at around 38 years of age2 impacting significantly the
oral health‒related quality of life and the rate of tooth
loss.3,4
Periodontal treatment aims to reduce bacterial load
and to suppress inflammation. It mainly consists of non-
surgical periodontal therapy (SRP) including oral hygiene
instructions (OHI) and subgingival debridement.5 Peri-
odontal treatment exhibits a high rate of success character-
ized by improvement of clinical parameters such as plaque
index (PI), bleeding on probing (BOP), PD, clinical attach-
ment level, and, at long-term, reduced tooth loss.6‒8 Treat-
ment outcomes could be influenced by risk factors includ-
ing unmodifiable conditions such as genetic or acquired
diseases, and modifiable factors such as smoking, obesity,
inadequate oral hygiene techniques, compliance, or tooth-
related parameters, for instance, unadapted crowns.8‒11
Amongst them, psychological status and related disor-
ders, especially chronic stress, anxiety, and depression
have also been proposed. However, only a few studies
focusing on their influence on SRP outcomes have been
conducted.12‒14
Stress is regarded as a cognitive perception of uncon-
trollability or unpredictability that is expressed in a phys-
iological and/or behavioral response.15 It could be clas-
sified as either acute or chronic. Acute stress lasts for
a period of minutes to hours while chronic stress per-
sists for several weeks or even months. In case of acute
stress, stress response may prepare the immune system for
challenges such as an infection that may be imposed by
the stressor. At contrary, when stress becomes chronic, it
may influence inflammatory processes leading to devel-
opment of chronic diseases such as rheumatoid arthri-
tis, diabetes, cardiovascular diseases, or even periodontal
diseases.16,17 In vitro and in vivo studies evaluating the
involvement of stress associated mediators such as corti-
sol, chromogranin-A, or beta-endorphin have shown that
these markers, present in the blood and in the gingival
crevicular fluid, are linked to the inflammatory response.17
Moreover, stress molecules have been identified as poten-
tially influencing the bacterial ecology of oral biofilms
and, thus, promoting the periodontal pathogens growth
as observed for Porphyromonas gingivalis.18,19 The mech-
anisms by which stress could affect periodontal disease
progression and wound healing have been divided into
two main categories: health-impairing behaviors (poor
oral hygiene, increased tobacco, and alcohol consumption,
and poor nutritional intake) and pathophysiological fac-
tors that lead to higher glucocorticoid and catecholamine
levels which indirectly affect hormonal, inflammatory, and
immunological profiles, increasing susceptibility to peri-
odontal disease.20‒22
To date, only a few studies reported the influence of
psychosocial factors on periodontal healing after peri-
odontal treatment.12‒14,23 Patients with impaired response
to periodontal treatment presented greater stress,12,24,25 a
higher psychosocial strain and a more passive-dependent
personality.23 However, due to the high heterogeneity of
study design, studied population, type of administered
questionnaires, evaluated biomarkers, and contradictory
results, the demonstration of their real impact still remains
to be elucidated.26‒28
To fill this gap of knowledge and to be able to better char-
acterize the “at-risk” patients, the aim of this study was to
evaluate the influence of psychological stress and coping
behaviors on SRP outcomes at 6 months in a French pop-
ulation suffering from severe chronic periodontitis (stage
3/4 generalized periodontitis).
2 MATERIALS AND METHODS
2.1 Study protocol
This study was conducted in accordance with the Dec-
laration of Helsinki and approved by Ethical Committee
(Comité de protection des personnes: 3/30; Clinical trials:
NCT02568163). All participants were informed about the
protocol and aim of the study and gave written consent
before their participation in the study.
2.2 Inclusion criteria
Patients attending periodontal consultation at the Depart-
ment of periodontology, University Hospital of Strasbourg,
France, and fulfilling the following criteria were invited
to participate in this prospective study: aged >18 years,
>15 teeth (third molars were excluded), diagnosis of gen-
eralized severe chronic periodontitis29 (stage 3/4 gener-
alized periodontitis)30 with at least 5% of the sites with
PD >5 mm and radiographic bone loss. Patients with sys-
temic diseases (diabetes, auto-immune diseases, chronic
inflammatory diseases) and/or treated with medications
that could affect periodontium such as antibiotics, anti-
inflammatory drugs, or psychotropic drugs in the last 6
months were excluded. Patients treated with specialized
periodontal treatment in the last 6 months, as well as preg-
nant women and patients wearing orthodontic appliances
were also excluded.
PETIT et al.
2.3 Psychological measurements
Psychological status was evaluated using self-administered
questionnaires at baseline. First, a binary question
(yes/no) was asked to the patient (“Do you feel stressed
on a regular basis?”). Then, French version of Depression,
Anxiety and Stress Scale (DASS-42)31 was given to the
patients. Coping strategies were evaluated by the Toulouse
coping scale questionnaire (TCS) validated for French
population.32 This test is composed of 54 multiple-choice
questions with five alternatives each and is based on six
coping strategies: focalization, social support, withdrawal,
conversion, control, and denial. This test was developed
from a critical analysis of those used by Lazarus and
Folkman33 and was adapted to French population. Addi-
tionally, this test helps to determine positive/negative
coping scores. Positive coping score describes the active
strategies developed by the individual in a stressful
situation and includes seeking help or social support
(cooperation, information, affective support) while nega-
tive coping score describes withdrawal and denial of the
situation.32 Questionnaire scores were masked to both the
patients and investigators in charge of the periodontal
examination and SRP. Scores were calculated by an
investigator not involved in patient treatment or follow-up
and, in case of high score, patient was referred to a mental
health professional.
2.4 Blood sampling
At baseline, before SRP, and at 6 months, peripheral blood
sample from each patient were collected in EDTA and cen-
trifuged for 10 minutes at 10,000 g and stored at -80◦ C
until analysis. To avoid bias associated with diurnal cycle
and glucose levels, blood samples were collected for each
patient in the morning and patients were advised to keep
an empty stomach overnight before the blood sampling.
For chromogranin-A, plasma samples were analyzed using
an automated immunoassay kit Kryptor Compact plus
(Thermo Fisher, Illkirch-Graffenstaden, France) and for
plasmatic cortisol, measurements were performed using
an automated immunoassay kit on Cobas e 601 (Roche
Diagnostics, Meylan, France).
2.5 Non-surgical periodontal treatment
and follow-up
At baseline, periodontal indexes (PI,34 BOP, PD, CAL)
were recorded before the treatment using a PCPUNC 15
periodontal probe (Hu-Friedy, Chicago, IL, USA) at six
3
sites/tooth. Non-surgical periodontal treatment (SRP) con-
sisted in OHI regarding brushing technique and the use of
interproximal hygiene devices. Then, supragingival scaling
at all sites and root planing at sites exhibiting PD >3 mm
were performed by trained periodontists (CP, VA-R) using
ultrasonic devices (Suprasson Newtron, Satelec, France)
and manual curets (Deppeler, Switzerland) under local
anesthesia, in two sessions within 2 weeks. Following each
session, patients were instructed to rinse with chlorhex-
idine (0.12%) mouthwash (Eludril, Pierre Fabre, France)
2 times/day for 15 days. The removal of retentive factors
such as overhanging fillings/crowns or caries was per-
formed when needed. According to the study protocol,
neither antibiotics were used nor periodontal surgery was
performed during the entire 6 months follow-up. At 3
months, PI, BOP, PD, CAL were measured. Additionally,
OHI were reinforced and sites with PD >3 mm were re-
instrumented. At 6 months, full periodontal examination
was performed. All periodontal examination, as well as
SRP, were performed by the same operator masked to psy-
chological assessment results. Patients that did not attend
recall, or had used antibiotics or anti-inflammatory drugs,
were excluded from the study.
2.6 Statistical analysis
The assessment of examiner reliability showed that >90%
of the repeated measurements were within ± 1 mm of
the original, indicating good intra-examiner reliability and
agreement (kappa-score >0.9). Quantitative variables were
described by using position and variability statistics, such
as mean, variance, minimum, and maximum. Qualita-
tive variables were described by using effectives and pro-
portions for each of their modality. Gaussian quantita-
tive variables were modeled by mixed linear regression
and binary outcomes by mixed logistic regressions, respec-
tively. For each of these models, an interaction with time
was added to the linear predictor for presenting the corre-
lation between all three variables: the covariable, the vari-
able of interest, and time. All interactions were tested by
the Wald procedure in generalized linear models. All sta-
tistical tests were two-tailed. A P value <0.05 was con-
sidered statistically significant and missing data were not
considered. All analyses were performed using R software
under its version 3.0 (R Core Team (2014). R: A language
and environment for statistical computing. Vienna, Aus-
tria). The number of subjects required was calculated using
the Pearson correlation coefficient between PD and DASS-
stress. For an alpha risk of 5% and a power of 80%, the
number of subjects required was 47 to obtain a correla-
tion coefficient of 0.4. By adding 15% in case of possible
4 PETIT et al.

FIGURE 1 Flowchart of the study

drop out, the minimal number of subjects required was 54 TA B L E 1 Characteristics of the population at baseline, 3 and 6
patients. months
Baseline 3 months 6 months
Age (mean; SD) 51.3 (9.7) 51.5 (10.1) 51.2 (10.1)
3 RESULTS Sex (mean; %)
Female 40 (56) 32 (55) 30 (56)
3.1 Patient demographic and Male 31 (44) 26 (45) 24 (44)
socioeconomic characteristics Social status (mean;
%)
At baseline, 71 patients fulfilling inclusion criteria were
Employed 51 (72) 41 (71) 39 (72)
included in this study. Thirteen patients were excluded
Unemployed 5 (7) 4 (7) 4 (8)
during the first 3 months of the follow-up and four between
Retired 15 (21) 13 (22) 11 (20)
3 and 6 months due to their lack of compliance with
Alcohol
the study’s protocol (Fig. 1). After 6 months, 54 patients
consumption
attended the final reevaluation. Sample population age
(mean; %)
ranged from 29 to 74 years, with a mean age of 51.3
Never 19 (27) 15 (26) 14 (26)
years. Most of the patients were employed (72%) and mar-
Occasionally 39 (55) 31 (53) 29 (54)
ried (71%). Regarding periodontal risk factors, 41% of the
Daily (≥1 day) 13 (18) 12 (21) 11 (20)
patients were smokers with 19 of them consuming >10
cigarettes/day. All demographic and socioeconomic data Smoking (mean; %)
are summarized in Table 1. Non-smoker 22 (31) 19 (33) 19 (35)
Ex-smoker 20 (28) 17 (29) 14 (26)
Smoker 29 (41) 22 (38) 21 (39)
3.2 Evaluation of psychological status Marital status
(mean; %)
At baseline, 52% of the patients declared being Single 13 (18) 10 (17) 10 (19)
stressed. Psychological status of patients was evalu- Married 50 (71) 42 (73) 38 (70)
ated at baseline using DASS questionnaire and TCS. Divorced 8 (11) 6 (10) 6 (11)
Mean score of 10.1 (8.3) for DASS-stress, 5.7 (5.8) for
PETIT et al. 5

TA B L E 2 Psychological status assessed by DASS-42 and TCS at T A B L E 3 Plasmatic cortisol and chromogranin-A dosage at
baseline baseline and 6 months
Baseline Baseline 6 months
DASS-42 (mean; SD) Cortisol (μg/L) (mean; SD) 363.3 (189.3) 375.1 (159.3)
DASS-depression 5.7 (5.8) Chromogranin-A (μg/L) 59.2 (38.3) 67.1 (51.2)
DASS-anxiety 6.3 (6) (mean; SD))
DASS-stress 10.1 (8.3)
TSC (mean; SD) 3.4 Non-surgical periodontal treatment
Action 53.1 (8.1) outcomes
Information 56.1 (8.9)
Emotion 46.8 (8) At 3 and 6 months, SRP was effective to reduce mean PI,
Negative 67.4 (11.7) BOP, and mean PD as well as the total number of dis-
Positive 88.9 (15.8) eased sites (PD >3 mm) and the number of deep sites
Do you feel stressed? (n; %)
(PD >5 mm) (P <0.05) (Table 4). An average PD reduction
of 0.73 ± 0.11 mm was measured at 6 months. Same trend of
Yes 37 (52)
results was observed when considering CAL, BOP, and PI
No 34 (48)
(P <0.05) emphasizing the positive effects of the treatment.
A binary Yes/No question was also asked to the patients (“Do you feel stressed
on a regular basis?”). DASS, Depression Anxiety Stress Scale; TCS, Toulouse
coping scale. 3.5 Multivariate analysis of covariance
between periodontal treatment outcomes
and psychological scores
DASS-depression and 6.3 (6) for DASS-anxiety was
recorded. Score was considered within the normal range As expected, the presence of well-described risk factors
(<14) for 81% of the patients considering DASS-stress, 81% such as smoking (> 10 cig/days) influenced negatively
for DASS-depression (<10) and 69.1% for DASS-anxiety the baseline parameters such as BOP, mean PD, number
(< 8) (Table 2). Therefore, according to DASS-stress of sites with PD >3 mm (OR = 5.43, P <0.001), num-
scale, 2.4% patients were considered suffering from mild ber of sites with CAL >3 mm (OR = 6.08, P <0.05)
stress, 11.8% from moderate stress, and 4.8% from severe while age was also identified as a negative factor for PI
to extremely severe stress. Regarding DASS-depression (P <0.05), mean CAL ( <0.05) and number of sites with
scale, 7.1% patients were considered suffering from mild CAL >3 mm (OR = 1.06, P <0.05) (Table 5). To deter-
depression, 7.1% from moderate depression and 4.8% mine the association between psychological status and
from severe to extremely severe depression. Furthermore, SRP outcomes, multivariable analysis was conducted using
according to DASS-anxiety questionnaire, 9.5% patients variance component models. Significant associations were
were considered suffering from mild anxiety, 9.5% from demonstrated between SRP outcomes at 6 months and psy-
moderate anxiety, and 11.9% from severe to extremely chological scores. Indeed, DASS-stress score was associ-
severe anxiety. Interestingly, no correlation was found ated to worsened SRP outcomes regarding the evolution of
between the Yes/No question related to stress and the BOP (OR = 1.02, P <0.05) and mean PD (P <0.05) between
DASS-stress score (P >0.05). baseline and 6 months. Moreover, DASS-depression was
also associated with impaired SRP response. In fact, it neg-
atively influenced the reduction of PD >5 mm (OR = 1.06,
3.3 Evaluation of cortisol and P <0.05), PD >7 mm (OR = 1.17, P <0.01), CAL >5 mm
chromogranin-A levels (OR = 1.03, P <0.05) and CAL >7 mm (OR = 1.07, P <0.05)
between baseline and 6 months. Interestingly, high DASS-
At baseline, before SRP and at 6 months, cortisol and anxiety score was associated with reduced PI.
chromogranin-A levels were evaluated from peripheral When coping strategies were evaluated, patients exhibit-
blood samples. Mean concentrations of cortisol and ing high score of negative coping were more prone to hav-
chromogranin-A were 363.3 μg/L (189.3) and 59.2 μg/L ing reduced SRP outcomes (BOP: OR = 1.07, P <0.001;
(38.3), respectively. No correlations were found between ΔPD >3 mm: OR = 1.02, P <0.05; ΔPD >5 mm: OR = 1.04,
cortisol and chromogranin-A levels, and psychological sta- P <0.001; ΔPD >7 mm: OR = 1.07, P <0.05).
tus measured by DASS-42. No significant changes were A specific focus has been made on the interpretation
found between levels at baseline and that at 6 months for scores related to DASS. In this regard, a dichotomy has
both cortisol and chromogranin-A (P >0.05) (Table 3). been made between patients with normal/mild (score: 0 to
6 PETIT et al.

TA B L E 4 Periodontal treatment outcomes at 3 and 6 months

Baseline (T0) 3 months (T3) 6 months (T6)
Periodontal parameters (n = 71) (n = 58) (n = 54) T0-T3 T0-T6
a a
PI (mean; SD) 1.3 (0.51) 0.75 (0.51) 0.61 (0.40) −0.55 (0.0) −0.69 (0.11)
a a
BOP (mean; SD) 0.63 (0.21) 0.36 (0.19) 0.28 (0.18) −0.27 (0.02) −0.35 (0.03)
a a
Mean PD (mean; SD) 3.82 (0.68) 3.23 (0.59) 3.09 (0.57) −0.59 (0.09) −0.73 (0.11)
a a
No. of sites with PD >3 mm (mean; SD) 67.2 (25.8) 41.9 (25.8) 37.7 (23.9) −24.28 (18.5) −27.4 (17.7)
a a
%PD >3 mm (mean; SD) 47 (18) 30 (18) 26 (17) −17 (0) −21 (1)
a a
No. of sites with PD >5 mm (mean; SD) 23.9 (18.5) 12.4 (14.1) 10.6 (12.3) −11.38 (11.7) −12.22 (12)
a a
%PD >5 mm (mean; SD) 17 (13) 9 (1) 7 (9) −8 (3) −10 (4)
a a
No. of sites with PD >7 mm (mean; SD) 4.3 (5.1) 1.9 (3.3) 1.7 (2.7) −2.3 (4.3) −2.4 (3.9)
a a
%PD >7 mm (mean; SD) 3 (4) 1 (2) 1 (2) −2 (2) −2 (2)
a a
Mean CAL (mean; SD) 5.07 (1.15) 4.47 (1.13) 4.44 (1.13) −0.60 (0.02) −0.63 (0.02)
a a
No. of sites with CAL >3 mm (mean; SD) 99.8 (27.1) 82.3 (31.1) 83.7 (29.1) −15.3 (16.8) −12.2 (19.6)
a a
%CAL >3 mm (mean; SD) 70 (20) 58 (23) 59 (22) −12 (3) −11 (2)
a a
No. of sites with CAL >5 mm (mean; SD) 52.5 (27.7) 36.8 (27) 36.8 (27) −14 (14.3) −12.5 (15.2)
a a
%CAL >5 mm (mean; SD) 37 (21) 26 (20) 26 (20) −11 (1) −11 (1)
No. of sites with CAL >7 mm (mean; SD) 20.1 (17) 14.1 (16.2) 13.8 (16.5) −5.3 (7.8) −4.7 (9.11)
%CAL >7 mm (mean; SD) 15 (14) 10 (12) 10 (12) −5 (2) −5 (2)
PI, plaque index; BOP, bleeding on probing; PD, probing depth; CAL, clinical attachment loss.
PI, BOP, mean PD, number of sites with PD >3 mm, PD >5 mm, PD >7 mm, mean CAL, number of sites with CAL >3 mm, CAL >5 mm and CAL >7 mm were
measured at baseline (T0), 3 months (T3), and 6 months (T6).
a
Represents statistical significance (P <0.05) between T0 and T3 and T0 and T6.

TA B L E 5 Multivariate analysis of covariance between periodontal treatment outcomes and psychological scores
Variable Influencing factor Estimate (SD) OR (CI) P
ΔPI DASS-depression 0.01 (0.01) 0.013
DASS-anxiety −0.02 (0.01) <0.001
DASS-stress 0.01 (0.00) <0.001
Negative coping −0.01 (0.00) <0.001
Positive coping −0.01 (0.00) <0.001
ΔBOP DASS-depression 1.04 (1.01–1.07) 0.018
DASS-anxiety 0.96 (0.94–0.98) <0.001
DASS-stress 1.02 (1.00–1.04) 0.04
Negative coping 1.07 (1.06–1.09) <0.001
Positive coping 0.97 (0.96–0.99) <0.001
ΔPD (mean) DASS-depression 0.01 (0.01) 0.46
DASS-anxiety −0.01 (0.01) 0.06
DASS-stress 0.01 (0.005) 0.03
Negative coping −0.012 (0.01) 0.01
Positive coping −0.011 (0.01) <0.001
ΔPD >3 mm DASS-depression 1.02 (0.99–1.05) 0.17
DASS-anxiety 0.97 (0.95–0.99) 0.007
DASS-stress 1.01 (0.99–1.03) 0.31
Negative coping 1.02 (1.01–1.04) 0.01
Positive coping 1.02 (0.99–1.02) 0.12
ΔPD >5 mm DASS-depression 1.06 (1.01–1.11) 0.01
(Continues)
PETIT et al. 7

TA B L E 5 (Continued)
Variable Influencing factor Estimate (SD) OR (CI) P
DASS-anxiety 0.98 (0.96–1.02) 0.42
DASS-stress 1.00 (0.97–1.03) 0.96
Negative coping 1.04 (1.02–1.07) <0.001
Positive coping 0.99 (0.97–1.00) 0.72
ΔPD >7 mm DASS-depression 1.17 (1.04–1.31) 0.008
DASS-anxiety 0.99 (0.93–1.06) 0.86
DASS-stress 0.94 (0.87–1.01) 0.09
Negative coping 1.06 (0.99–1.12) 0.08
Positive coping 1.05 (0.98–1.12) 0.19
ΔCAL (mean) DASS-depression 0.015 (0.012) 0.22
DASS-anxiety −0.03 (0.008) 0.001
DASS-stress 0.01 (0.008) 0.02
Negative coping −0.02 (0.007) <0.001
Positive coping −0.02 (0.005) <0.001
ΔCAL >3 mm DASS-depression 1.00 (0.98–1.03) 0.77
DASS-anxiety 0.95 (0.93–0.97) <0.001
DASS-stress 1.02 (1.00–1.04) 0.04
Negative coping 1.01 (0.99–1.02) 0.46
Positive coping 0.99 (0.98–1.00) 0.07
ΔCAL >5 mm DASS-depression 1.03 (0.99–1.06) 0.05
DASS-anxiety 0.99 (0.97–1.00) 0.31
DASS-stress 1.00 (0.98–1.02) 0.69
Negative coping 1.04 (1.03–1.06) <0.001
Positive coping 0.97 (0.96–0.99) <0.001
ΔCAL >7 mm DASS-depression 1.07 (1.01–1.12) 0.01
DASS-anxiety 0.97 (0.95–0.99) 0.04
DASS-stress 1.00 (0.97–1.03) 0.98
Negative coping 1.05 (1.02–1.07) <0.001
Positive coping 0.98 (0.95–1.01) 0.13
PI, plaque index; BOP, bleeding on probing; PD, probing depth; CAL, clinical attachment loss; DASS, Depression Anxiety Stress Scale.
Associations between periodontal parameters and psychological scores were analyzed by linear and logistic mixed regression models considering psychological
parameters at baseline and the evolution of periodontal parameters between baseline and 6 months. All potential influencing variables were considered (age,
smoking, sex) in the mathematical model. Significant associations are in bold (P < 0.05). ΔPI, ΔBOP, ΔPD, ΔCAL represent the difference for mean PI BOP, PD,
and CAL between baseline and 6 months, respectively; ΔPD >3 mm, ΔPD >5 mm, ΔPD >7 mm represent the difference for number of sites with PD >3 mm, >5 mm,
>7 mm between baseline and 6 months. ΔCAL >3 mm, ΔCAL >5 mm, ΔCAL >7 mm represent the difference for number of sites with PD >3 mm, >5 mm, >7 mm
between baseline and 6 months

18) versus moderate/severe (score >18) stress, normal/mild
(score: 0 to 13) versusmoderate/severe (score > 13) depres-
sion and normal/mild (score: 0 to 9) versus moder-
ate/severe (score > 9) anxiety. The multivariate analysis
showed that the decrease of PI between baseline and 6
months was reduced in moderate/severe DASS-depression
patients in comparison with patients with normal/mild
scores (P <0.0001) while lower PI was measured at 6
months for patients with moderate/high DASS-anxiety
score (P <0.0001). Interestingly, the reduction of BOP was
lower in patients with moderate/severe DASS-depression
than in patients with normal/mild scores (P = 0.01). Nev-
ertheless, the reduction of PD >3 mm, mean CAL, and
CAL >3 mm were decreased in patients with moder-
ate/high scores of DASS-anxiety and DASS-stress in com-
parison with patients with normal/mild scores (P <0.05).
4 DISCUSSION
This study demonstrated the negative impact of psycho-
logical factors such as stress and depression on SRP out-
comes in severe generalized chronic periodontitis (stage
3/4 generalized periodontitis) highlighting the need of
psychological evaluation and management as part of the
8 PETIT et al.
overall patient care. It also validated the potential use of
DASS-42 self-administered questionnaire as an interesting
tool to determine psychological status of patients under-
going periodontal treatment and to identify those at risk of
reduced SRP outcomes.
Management of patients affected by severe chronic peri-
odontitis is challenging as it is well-described that SRP
response is reduced at deep sites.35‒37 In this study, SRP was
effective to improve significantly periodontal parameters
such as PI, BOP, PD, and CAL.8,38 Obviously, it decreased
significantly the mean PD, mean CAL, and the number of
diseased sites. However, at 6 months, around 40% of the
deep sites (PD >5 mm) were still detected illustrating the
limit of this therapeutic procedure39 and, consequently, the
need of additional therapy such as surgical approaches,
antibiotics39,40 or others adjunctive treatments like photo-
dynamic therapy.35
This study also highlights the need to better identify
patients at risk to adapt treatment protocols. Herein, the
negative effect of smoking on periodontal conditions was
confirmed as suggested previously.6,41 A specific empha-
sis was made on the psychological status. The detrimen-
tal role of psychosocial factors in periodontal disease onset
and treatment has been evaluated for decades with some
contradictory results due to the differences in terms of
the population included, type of tools used to evaluate
psychosocial parameters, definitions of diseases and type
of treatment provided.12,13 Stress is a complex multifacto-
rial process influenced by environmental parameters such
as professional activity, marital status, and socioeconomic
status.42 In this study, a negative influence of stress on
SRP outcomes was observed. This result is in accordance
with previous studies13,23 where stress was also demon-
strated as a risk factor for impaired treatment response.
However, the nature of the influence should be determined
in future studies as stress can have a direct effect on peri-
odontal tissues and immune response and also on indi-
rect parameters through changes in lifestyle that include
smoking or oral hygiene habits.43 Earlier, a role has been
suggested for several salivary stress biomarkers such as
catecholamine metabolites including metanephrine and
cortisol that may increase growth and virulence of peri-
odontal pathogens such as Porphyromonas gingivalis.19,44
In this study, we did not find any correlation between plas-
matic cortisol and chromogranin-A with psychological sta-
tus or SRP outcomes.
To assess the depression, anxiety, and stress levels,
DASS-42 questionnaire was used. It should be noticed that
the tools used in previous studies were not similar. In the
study of Vettore et al.,13 the Stress Symptoms Inventory
(SSI) was used while cortisol levels and Perceived Stress
Scale (PSS) were used by Bakri et al.12 DASS-42 question-
naire is a self-reported questionnaire yielding concomi-
tantly three factors (depression, anxiety, stress) reflecting
the last 7 days. This questionnaire is widely used to charac-
terize psychological trait and is reliable as it correlates with
other well described questionnaires such as Beck Anxiety
Inventory or Beck Depression Inventory.45 Such question-
naire displays several advantages including its availability
in several languages and an easy interpretation that follows
an established scale.
In this study, stress coping strategies were also identified
as influencing factors of SRP outcomes. Herein, patients
display negative coping strategies including withdrawal,
denial, or alexithymia, a personality construct character-
ized by the subclinical inability to identify and describe
experienced emotions.46 This result is consistent with the
study of Wimmer et al. where patients with passive coping
strategies not only exhibit poor SRP outcomes14 but also
poor treatment response in the context of other inflam-
matory diseases such as inflammatory bowel disease and
rheumatoid arthritis.47
Few studies investigated the effect of stress management
on inflammatory or chronic diseases management such as
cancer and demonstrated its positive effects on treatment
outcomes.48 In the context of periodontitis, it was sug-
gested that yoga, as a stress management strategy, would be
helpful to improve periodontal treatment.49 Such observa-
tion should be linked to the influence of inadequate coping
strategies such as defensive or suppressive coping strate-
gies on periodontal treatment outcomes.14 Therefore, psy-
chological management should be considered for at-risk
patients, especially in case of reduced treatment outcomes
or disease recurrence. As a drastic modification of coping
behavior will be highly challenging for the periodontist,
specific information should be given targeting stress asso-
ciated adverse behaviors such as smoking or drug usage.14
Several limitations might explain the mitigated
results observed in this study. Owing to the strict inclu-
sion/exclusion criteria, only patients with severe forms
of periodontitis were evaluated. This may explain the
limited SRP outcomes observed in this cohort of patients
as all of them presented deep (>5 mm) lesions at baseline.
Therefore, the local parameters may have blunted the
influence of systemic or environmental factors. This
study was also designed as a longitudinal prospective
study where psychological status was evaluated through
DASS-42 questionnaire. However, due to the masking
of DASS-42 scores, only a limited number of included
patients were categorized with severe stress, depression,
or anxiety. Specific studies should be designed focusing
on such an identified population to have a more precise
comprehension of the influence of psychological status
and diseases on both periodontal conditions and treatment
outcomes. To overcome such limitation, a dichotomy has
been made between patients with normal/mild versus
PETIT et al.
moderate/severe DASS-stress, depression, and anxiety,
confirming the analysis. Moreover, the use of short ver-
sion of DASS questionnaire such as DASS-21 or DASS-12
should be considered to allow its use in dental practice,
however, the determination of precise score threshold
for each questionnaire should be performed to identify
precisely the at-risk patients. Nevertheless, the use of
specific biomarkers could be a reliable tool if the selected
biomarker relates to the chronic psychological status.
Psychological status, such as stress level and depres-
sion, and negative coping strategies of patients under peri-
odontal treatment should be considered as a risk factor
for reduced periodontal treatment outcomes. The assess-
ment of stress level and depression may be valuable in
the establishment of periodontal treatment prognosis and
in the holistic management of periodontitis. However,
interventional trials assessing the impact of psychological
interventions/therapies need to be conducted.
AC K N OW L E D G M E N T S
This study was funded by University Hospital of Stras-
bourg through grant AAPJC 2013 HUS N◦ 5502. The
authors report no conflicts of interest related to this study.
AUTHOR CONTRIBUTIONS
All authors have made substantial contributions to con-
ception and design of the study. Catherine Petit, Victor
Anadon-Rosinach, Laurence Rettig, Catherine Schmidt-
Mutter, Nicolas Tuzin, Jean-Luc Davideau, Olivier Huck
contributed to data collection and data analysis. Cather-
ine Petit, Nicolas Tuzin, Olivier Huck contributed to data
interpretation and drafting and critical revision of the
manuscript.
REFERENCES
1. Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal dis-
eases. Nat Rev Dis Primer. 2017;3:17038.
2. Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray
CJL, Marcenes W. Global burden of severe periodontitis in
1990-2010: a systematic review and meta-regression. J Dent Res.
2014;93:1045-1053.
3. Martinez-Canut P. Predictors of tooth loss due to periodon-
tal disease in patients following long-term periodontal mainte-
nance. J Clin Periodontol. 2015;42:1115-1125.
4. Ng SKS, Leung WK. Oral health-related quality of life and peri-
odontal status. Community Dent Oral Epidemiol. 2006;34:114-
122.
5. Heitz-Mayfield LJA, Trombelli L, Heitz F, Needleman I, Moles
D. A systematic review of the effect of surgical debridement
vs non-surgical debridement for the treatment of chronic peri-
odontitis. J Clin Periodontol. 2002;29:92-102.
9
6. Jiao J, Shi D, Cao Z-Q, et al. Effectiveness of non-surgical peri-
odontal therapy in a large Chinese population with chronic peri-
odontitis. J Clin Periodontol. 2017;44:42-50.
7. Leininger M, Tenenbaum H, Davideau J-L. Modified peri-
odontal risk assessment score: long-term predictive value of
treatment outcomes. A retrospective study. J Clin Periodontol.
2010;37:427-435.
8. Petit C, Schmeltz S, Burgy A, Tenenbaum H, Huck O, Davideau
J-L. Risk factors associated with long-term outcomes after active
and supporting periodontal treatments: impact of various com-
pliance definitions on tooth loss. Clin Oral Investig. 2019;62:218-
219.
9. Bouaziz W, Davideau J-L, Tenenbaum H, Huck O. Adiposity
measurements and non-surgical periodontal therapy outcomes.
J Periodontol. 2015;86:1030-1037.
10. Tomasi C, Leyland AH, Wennström JL. Factors influencing the
outcome of non-surgical periodontal treatment: a multilevel
approach. J Clin Periodontol. 2007;34:682-690.
11. Van der Weijden GA, Dekkers GJ, Slot DE. Success of non-
surgical periodontal therapy in adult periodontitis patients-A
retrospective analysis. Int J Dent Hyg. 2019;17:309-317.
12. Bakri I, Douglas CWI, Rawlinson A. The effects of stress on
periodontal treatment: a longitudinal investigation using clin-
ical and biological markers. J Clin Periodontol. 2013;40(10):955-
961.
13. Vettore M, Quintanilha RS, Monteiro da Silva AM, Lamarca
GA, Leão ATT. The influence of stress and anxiety on the
response of non-surgical periodontal treatment. J Clin Periodon-
tol. 2005;32(12):1226-1235.
14. Wimmer G, Köhldorfer G, Mischak I, Lorenzoni M, Kallus KW.
Coping with stress: its influence on periodontal therapy. J Peri-
odontol. 2005;76:90-98.
15. Koolhaas JM, Bartolomucci A, Buwalda B, et al. Stress revisited:
a critical evaluation of the stress concept. Neurosci Biobehav Rev.
2011;35:1291-1301.
16. Sahle BW, Chen W, Melaku YA, Akombi BJ, Rawal LB, Ren-
zaho AMN. Association of psychosocial factors with risk of
chronic diseases: a nationwide longitudinal study. Am J Prev
Med. 2020;58:e39-50.
17. Akcali A, Huck O, Tenenbaum H, Davideau J-L, Buduneli N.
Periodontal diseases and stress: a brief review. J Oral Rehabil.
2012;40:60-68.
18. Ardila CM, Guzmán IC. Association of Porphyromonas gin-
givalis with high levels of stress-induced hormone cortisol in
chronic periodontitis patients. J Investig Clin Dent. 2016;7:361-
367.
19. Akcalı A, Huck O, Buduneli N, Davideau J-L, Köse T,
Tenenbaum H. Exposure of Porphyromonas gingivalis to
cortisol increases bacterial growth. Arch Oral Biol. 2014;59:
30-34.
20. Boyapati L, Wang H-L. The role of stress in periodontal disease
and wound healing. Periodontol 2000. 2007;44:195-210.
21. Genco RJ, Ho AW, Grossi SG, Dunford RG, Tedesco LA. Rela-
tionship of stress, distress and inadequate coping behaviors to
periodontal disease. J Periodontol. 1999;70:711-723.
22. Rosania AE, Low KG, McCormick CM, Rosania DA. Stress,
depression, cortisol, and periodontal disease. J Periodontol.
2009;80:260-266.
10
23. Axtelius B, Söderfeldt B, Nilsson A, Edwardsson S, Attström R.
Therapy-resistant periodontitis. Psychosocial characteristics. J
Clin Periodontol. 1998;25:482-491.
24. Laforgia A, Corsalini M, Stefanachi G, Pettini F, Di Venere D.
Assessment of psychopatologic traits in a group of patients with
adult chronic periodontitis: study on 108 cases and analysis of
compliance during and after periodontal treatment. Int J Med
Sci. 2015;12:832-839.
25. Linden GJ, Mullally BH, Freeman R. Stress and the progression
of periodontal disease. J Clin Periodontol. 1996;23:675-680.
26. Araújo MM, Martins CC, Costa LCM, et al. Association between
depression and periodontitis: a systematic review and meta-
analysis. J Clin Periodontol. 2016;43:216-228.
27. Kinane DF, Mark Bartold P. Clinical relevance of the host
responses of periodontitis. Periodontol 2000. 2007;43:278-293.
28. Peruzzo DC, Benatti BB, Ambrosano GMB, et al. A systematic
review of stress and psychological factors as possible risk factors
for periodontal disease. J Periodontol. 2007;78:1491-1504.
29. Armitage GC. Development of a classification system for peri-
odontal diseases and conditions. Ann Periodontol Am Acad Peri-
odontol. 1999;4:1-6.
30. Caton JG, Armitage G, Berglundh T, et al. A new classification
scheme for periodontal and peri-implant diseases and condi-
tions – Introduction and key changes from the 1999 classifica-
tion. J Periodontol. 2018;89:S1-S8.
31. Lovibond SH, Lovibond PF. Manual for the Depression Anxi-
ety Stress Scales. Sydney, N.S.W: Psychology Foundation of Aus-
tralia; 1996.
32. Tap P, Esparbès S, Sordes-der F. Stratégies de coping et person-
nalisation. Bulg J Psychol. 1995;2:59-80. [in French].
33. Lazarus RS, Folkman S. Stress, Appraisal, and Coping. New
York: Springer; 1984.
34. Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence
and severity. Acta Odontol Scand. 1963;21:533-551.
35. Harmouche L, Courval A, Mathieu A, et al. Impact of tooth-
related factors on photodynamic therapy effectiveness during
active periodontal therapy: a 6-months split-mouth randomized
clinical trial. Photodiagnosis Photodyn Ther. 2019;27:167-172.
36. Heitz-Mayfield LJA, Lang NP. Surgical and nonsurgical peri-
odontal therapy. Learned and unlearned concepts. Periodontol
2000. 2013;62:218-231.
37. Kolakovic M, Held U, Schmidlin PR, Sahrmann P. An estimate
of pocket closure and avoided needs of surgery after scaling and
root planing with systemic antibiotics: a systematic review. BMC
Oral Health. 2014;14:159.
38. Kanmaz B, Lappin DF, Nile CJ, Buduneli N. Effects of smok-
ing on non-surgical periodontal therapy in patients with
PETIT et al.
periodontitis stage III or IV, and grade C. J Periodontol.
2019;91(4):442-453.
39. Cosgarea R, Juncar R, Heumann C, et al. Non-surgical periodon-
tal treatment in conjunction with 3 or 7 days systemic admin-
istration of amoxicillin and metronidazole in severe chronic
periodontitis patients. A placebo-controlled randomized clinical
study. J Clin Periodontol. 2016;43:767-777.
40. Pretzl B, Sälzer S, Ehmke B, et al. Administration of systemic
antibiotics during non-surgical periodontal therapy-a consensus
report. Clin Oral Investig. 2018;93:1045-1013.
41. Trombelli L, Rizzi A, Simonelli A, Scapoli C, Carrieri A, Farina
R. Age-related treatment response following non-surgical peri-
odontal therapy. J Clin Periodontol. 2010;37:346-352.
42. Marcenes WS, Sheiham A. The relationship between work stress
and oral health status. Soc Sci Med. 1992;35:1511-1520.
43. Bansal J, Bansal A, Shahi M, Kedige S, Narula R. Periodontal
emotional stress syndrome: review of basic concepts, mecha-
nism and management. OJMP. 2014;3:250-261.
44. Mesa F, Magán-Fernández A, Muñoz R, et al. Catecholamine
metabolites in urine, as chronic stress biomarkers, are associ-
ated with higher risk of chronic periodontitis in adults. J Peri-
odontol. 2014;85:1755-1762.
45. Brown TA, Chorpita BF, Korotitsch W, Barlow DH. Psychome-
tric properties of the depression anxiety stress scales (DASS) in
clinical samples. Behav Res Ther. 1997;35:79-89.
46. Sifneos PE. The prevalence of “alexithymic” characteristics
in psychosomatic patients. Psychother Psychosom. 1973;22:
255-262.
47. Santiago T, Geenen R, Jacobs JWG, Da Silva JAP. Psychologi-
cal factors associated with response to treatment in rheumatoid
arthritis. Curr Pharm Des. 2015;21:257-269.
48. Antoni MH, Dhabhar FS. The impact of psychosocial stress and
stress management on immune responses in patients with can-
cer. Cancer. 2019;125:1417-1431.
49. Sudhanshu A, Sharma U, Vadiraja HS, Rana RK, Singhal R.
Impact of yoga on periodontal disease and stress management.
Int J Yoga. 2017;10:121-127.
How to cite this article: Petit C,
Anadon-Rosinach V, Rettig L, et al. Influence of
psychological stress on non-surgical periodontal
treatment outcomes in severe chronic periodontitis
patients. J Periodontol. 2020;1–10.
https://doi.org/10.1002/JPER.20-0105