Вы находитесь на странице: 1из 10

J Clin Periodontol 2005; 32: 1226–1235 doi: 10.1111/j.1600-051X.2005.00852.

x Copyright r Blackwell Munksgaard 2005

M. Vettore1,2, R. S. Quintanilha1,
The influence of stress and A. M. Monteiro da Silva3,
G. A. Lamarca4 and A. T. T. Leão1

anxiety on the response of non-


1
Department of Dental Clinic/Periodontology,
Federal University of Rio de Janeiro, Rio de
Janeiro, Brazil; 2Department of Epidemiology

surgical periodontal treatment


and Quantitative Methods in Health, National
School of Public Health, Oswaldo Cruz
Foundation, Rio de Janeiro, Brazil; 3Institute
of Human and Social Sciences, Rural Federal
University of Rio de Janeiro, Rio de Janeiro,
Vettore M, Quintanilha RS, Monteiro da Silva AM, Lamarca GA, Leão ATT. The Brazil; 4Section of Periodontology, Brazilian
influence of stress and anxiety on the response of non-surgical periodontal treatment. Dental Association-Regional Petropolis,
J Clin Periodontol 2005; 32: 1226–1235. doi: 10.1111/j.1600-051X.2005.00852.x. Petropolis, Brazil
r Blackwell Munksgaard, 2005.

Abstract
Aim: The aim of this study was to evaluate the influence of stress and anxiety on the
response to non-surgical periodontal treatment (NPT) in patients with chronic
periodontitis.
Method: Sixty-six patients (mean age 46.1  8 years) were assigned to three groups:
control group, probing pocket depth (PPD) 44 mm, n 5 20; T1, at least four sites with
PPD X4 and 46 mm, n 5 26; and T2, at least four sites with PPD 46 mm, n 5 20.
Stress, state anxiety (SA) and trait anxiety (TA) and plaque index (PI), gingival index,
PPD and clinical attachment level (CAL) were recorded at baseline and 3 months after
NPT.
Results: TA scores were different among groups at baseline and after NPT. TA was
related to periodontitis at baseline and after NPT. PI was associated with the SA at
baseline. The reduction of frequency of CAL 46 mm was correlated with TA after
Key words: anxiety; chronic periodontits;
adjusting for confounders. Stressed subjects did not show reduction of frequency of
periodontal treatment; psychosocial factors;
PPD 46 mm (T1), CAL 4–6 mm and CAL 46 mm (T2). stress
Conclusions: The data suggest an influence of trait of anxiety and stress on the
response to NPT. Accepted for publication 18 August 2005

Periodontal diseases are characterized tobacco use, oral cleanliness) and syste- or quality of life confirm its benefits
by a bacterial challenge that can lead mic disorders (e.g. uncontrolled diabetes (Hujoel et al. 2000). Recognized risk
to periodontal attachment loss, bone loss mellitus patients) play an important role factors for periodontal disease onset
and, ultimately, possible tooth loss. Epi- in the pathogenesis of periodontitis and progression have also been asso-
demiological studies related to periodon- (Shlossman et al. 1990, Barbour et al. ciated with poor response to conven-
tal diseases search for both determinants 1997). tional periodontal treatment (Hempton
of its occurrence and progression, as The most common form of perio- & Leone 1997).
well as for preventive strategies and dontal therapy in subjects with chronic Recently, researchers have tested the
effective treatments. Several observa- periodontitis includes instruction for hypothesis that psychosocial factors can
tional studies were conducted, and re- dental biofilm self-control, scaling and contribute to periodontitis. Several psy-
cognized risk factors are well known for root planing. Periodontal healing based chological disorders have been shown to
periodontal tissues breakdown (Grossi on surrogate endpoints such as probing be associated with chronic and aggres-
et al. 1994, Page & Beck 1997). pocket depth (PPD) reduction, probing sive periodontitis, as well as with pro-
Specific subgingival microorganisms clinical attachment level (CAL) main- gression of periodontal disease (Monteiro
clustered in microbial complexes are tenance and suppression of gingival in- da Silva et al. 1996, Genco et al. 1999,
considered determinant agents for perio- flammation is usually obtained when Vettore et al. 2003).
dontal disease onset and progression, as non-surgical periodontal treatment (NPT) Current research has focused on opti-
well as for refractory/recurrent perio- is conducted (Badersten et al. 1981, mal ways of delivering non-surgical
dontitis (Offenbacher 1996, Colombo 1984, Nordland et al. 1987). Similarly, periodontal therapy but relatively little
et al. 1998, Socransky et al. 1998). In the effects of NPT on major disease is known about patient factors that affect
addition, behavioural risk factors (e.g. endpoints such as tooth loss, edentulism the variability in outcome of this impor-
1226
The influence of stress and anxiety on the response to NPT 1227

tant treatment modality (Kinane 2005, four sites with PPD X4.0 and 46.0 mm Clinical measurements
Koshy et al. 2005, Wennstrom et al. and Test group 2 (T2) had at least four
2005). To date, few studies reported sites with PPD 46 mm. After all questionnaires were completed,
the influence of psychosocial factors on After signing an informed consent patients underwent a clinical examina-
periodontal healing after periodontal consisting of the study aims, procedure tion. Two calibrated examiners assessed
treatment (Axtelius et al. 1998, Wimmer and the voluntary character of their PI, Gingival Index (GI) (Löe 1967),
et al. 2004). Patients responding less participation, medical history and socio- PPD and CAL. These were recorded at
well to periodontal treatment had more economic data were collected. Socio- six sites per tooth (mesiobuccal, buccal,
psychosocial strain and a more passive- economic data included the following: distobuccal, distolingual, lingual and
dependent personality (Axtelius et al. age, gender, employment status, marital mesiolingual) at all teeth excluding third
1998). Inadequate coping behaviours in- status, schooling, familial income, molars. PPD and CAL measures were
cluding passive coping strategies were smoking history, number of cigarettes taken as the average of two previous
more pronounced in cases of poor smoked per day and alcoholic drink measures. Such measurements were
response to NPT (Wimmer et al. 2004). consumption. Subsequently, three self- recorded to the nearest millimetre using
In a previous study, patients with high reported questionnaires were used to a North Carolina periodontal probe (Hu-
levels of trait anxiety (TA) had a higher evaluate stress and anxiety. All pati- Friedy, Chicago, IL, USA).
frequency of moderate CAL (4–6 mm) ents were examined for periodontal
and moderate PPD (4–6 mm) (Vettore et clinical parameters by two previously Periodontal therapy
al. 2003). The aim of the present study calibrated examiners. Those presenting
was to assess the possible influence of periodontal disease were submitted to Periodontal therapy consisted initially of
stress and anxiety on the response to NPT. Periodontal clinical measurements instruction in self-care of plaque control
NPT in patients with different levels of and stress and anxiety assessment were for all participants. Patients with PPD
chronic periodontitis. also registered 3 months after NPT less than 4.0 mm were submitted to
for all subjects. supragingival scaling, coronal polishing
and topical fluoride gel when necessary.
Patients with periodontal disease also
Material and Methods received scaling and root planing in all
Psychosocial measurements sites with PPD 43 mm. Scaling and
In this case–control, longitudinal, dou-
ble-blind study, stress and anxiety in Psychological measures to assess stress root planing were conducted using
patients with different levels of chronic and anxiety included three psychometric Gracey curettes no 1–2, 7–8, 11–12,
periodontitis before and after NPT were instruments. The Stress Symptoms In- 13–14 (Hu-Friedy). The removal of
assessed. After approval of the Federal ventory (SSI) (Lipp & Guevara 1994) retentive factors for dental plaque accu-
University of Rio de Janeiro (UFRJ) aims to detect whether a patient presents mulation including overhanging restora-
Ethics Committee, individuals attending a clinical stress syndrome. Patients were tions and carious cavities was performed
the Clinical Dentistry Department of the asked to indicate whether a number of according to need. NPT was completed
Dental School of the UFRJ were invited physical and psychological stress symp- in at most four appointments of 1 h
to take part in this study. The inclusion toms had occurred recently (involving sessions. Local and systemic antibiotics
criteria consisted of participants being the last day, week and month). The SSI were not administered to any patient. In
over 35 years of age and presenting at is based on Selye’s concepts of the addition, surgical procedures for perio-
least 50% of dental surfaces with plaque General Adaptation Syndrome (Selye dontal disease treatment were not per-
index (PI) X2 (Silness & Löe 1964). 1963). There are 53 items divided into formed.
The exclusion criteria included patients three sections. Each of them corres- Periodontal clinical examination and
presenting acute necrotizing ulcerative ponds to one of Selye’s stress stages: treatment procedures were performed by
gingivitis, acute necrotizing ulcera- alarm reaction, stage of resistance and two clinicians, in such a way that one of
tive periodontitis, systemic conditions stage of exhaustion. If somebody is cli- them treated half of the patients who had
associated with periodontal disease, pre- nically stressed, it is also possible to been previously examined by the other
gnancy and those who received perio- identify the stress phase. one and vice versa. The clinicians were
dontal therapy during the last 6 months. Anxiety was assessed with the Spiel- blinded to patients’ stress and anxiety
In addition, patients taking drugs that berger State-Trait Anxiety Inventory status during the whole period of the
could affect the progression or treatment (STAI) adapted to the Brazilian popula- study. The scaling and root planing
of periodontal diseases were excluded. tion by Biaggio et al. (1977). This inven- procedures were appraised by a third
A pilot study including 15 patients tory consists of two self-report scales. periodontist in each session.
with at least four sites with PPD Each of them has 20 items followed by a After the completion of the NPT, all
44.0 mm was conducted to calibrate four-point scale. These self-report scales patients had supportive monthly perio-
the examiners, and to test the under- measure two different dimensions of dontal therapy, which consisted of oral
standing and the layout of the stress and anxiety: state anxiety (SA) and TA. hygiene instructions, coronal polish-
anxiety questionnaires. The TA scale requires that subjects des- ing and supragingival scaling when
In the main study, patients considered cribe the way they generally feel. The necessary.
suitable were assigned to one of the SA scale asks respondents to indicate
following three groups in accordance how they feel at a specific moment in Follow-up assessment
with their PPD levels: the control group time. The range of possible score varies
(C) had less than four sites with PPD from a minimum score of 20 to a max- Three months after the last session of
44.0 mm, Test group 1 (T1) had at least imum score of 80 on both scales. periodontal therapy, all subjects were
1228 Vettore et al.

invited for re-assessment on stress, anxi- two strategies. The frequency of PPD Of the 85 originally selected partici-
ety and periodontal clinical parameters. and CAL categories of o4 mm (shal- pants, a total of 66 were considered for
A similar protocol was used to obtain low), 4–6 mm (moderate) and 46 mm the final analysis. Sixteen patients were
measures at baseline and at the 3-month (deep) were compared between baseline excluded, seven used antibiotics during
follow-up appointment, given that socio- and after NPT for stressed and non- the course of the study and 12 failed to
economic data were not collected at stressed patients in each group by the return for the follow-up appointment.
follow-up assessment. The periodontal Wilcoxon signed-rank test.
examinations at baseline and 3 months The differences of PPD and CAL
after NPT were performed by the same frequency X4, 4–6, 46 mm between Socioeconomic data
examiner. Those patients who had taken initial and 3 months after NPT were The demographic and socioeconomic
antibiotics or reported systemic condi- computed to assess the reduction of characteristics of all subjects are sum-
tions that could affect periodontal dis- periodontal disease clinical parameters. marized in Table 1. There were no sig-
ease during the course of the study were Univariate analysis of covariance was nificantly statistical differences among
excluded. carried out on the reduction of PPD and three groups. Statistical analysis compar-
CAL frequencies (dependent variables) ing marital status, number of cigarettes/
Statistical methods
with all psychosocial measures (inde- day between smokers and alcoholic
pendent variables) adjusting for dental drink consumption among groups could
Data were analysed using SPSS 10.0 plaque and number of cigarettes (cov- not be performed because of the small
(Statistical Package for Social Sciences ariates). number of subjects in some cells.
for Windows, SPSS Inc., Chicago, IL, Although not significant, a smaller
USA). The significance level estab- percentage of smokers were found in the
Results
lished for all analysis was 5% (p40.05). control group. In addition, the number
Socioeconomic data were computed A clinical calibration for periodontal
parameters was performed in the pilot of cigarettes smoked/day was greater in
for each participant from data provided patients with periodontitis.
in the baseline questionnaire. The three study for the two examiners involved
groups were compared with respect to Kappa measure and Intra-class Correla-
age by a Kruskal–Wallis test and for the tion Coefficient of agreement findings for Clinical parameters
remaining socioeconomic data, w2 tests CAL and PPD intra- and inter-examiner
were performed. were over 0.71. The results have been The clinical parameters data at baseline
Clinical parameters were registered described previously (Vettore et al. 2003). and 3 months after NPT for the three
and averaged for each patient in the
three groups. Differences among clini-
Table 1. Demographic and socioeconomic characteristics of participants in the three groups
cal parameters were examined in sites
subset according to PPD and CAL cate- Demographic and socioeconomic Control Test group 1 Test group 2 p
gories of o4 mm (shallow), 4–6 mm characteristics of subjects (N 5 20) (N 5 26) (N 5 20)
(moderate) and 46 mm (deep). Signifi-
Age (mean  SD)n 45.9  8.3 46.4  8.9 46.1  7.8 0.96
cance of differences among the three Gender (%)w 0.14
groups before and after periodontal ther- Male 45 73.1 55
apy was verified by Kruskal–Wallis Female 55 26.9 45
tests. Comparisons within each group Employment status (%)z –
between baseline and after periodontal Unemployed 5 15 15
therapy were made using the Wilcoxon Employed 85 73 75
signed-rank test. Retired 10 12 10
The significance of differences in the Marital status (%)w 0.36
Unmarried/divorced/widowed 75 57.7 55
frequency of participants with clinical Married/mate 25 42.3 45
stress among the three groups was Schooling (%)w 0.93
examined using the w2 test. Kruskal– 48 years 55 50 50
Wallis tests were used to compare the 48 years 45 50 50
three groups in terms of SA and TA. The Household income in minimum salaries (%)w 0.93
stress and anxiety comparisons among o3 25 30.7 20
groups were conducted at baseline and 3 3–6 35 30.8 35
months after NPT. Possible associations 46 40 38.5 45
Smokers (%)w 30 42 55 0.28
between psychosocial factors and perio- No of cigarettes/day between smokers (%)z –
dontal parameters were examined by 1–10 83 36 55
non-parametric Spearman’s linear cor- 11–20 17 55 27
relation coefficients at baseline and 3 420 0 9 18
months after NPT. Internal consisten- Alcoholic drink consumption (%)z –
cies for the SSI and for the two scales of Less than two glasses per week 80 70 76.9
the STAI were evaluated by the Cron- One glass almost every day 15 25 19.2
Two or more glasses per day 5 5 3.8
bach’s a coefficient at baseline and 3
months after NPT. n
Kruskal–Wallis test.
w 2
The influence of psychosocial factors w test.
z
on periodontal status was assessed using Statistical test could not be performed.
The influence of stress and anxiety on the response to NPT 1229

groups are presented in Tables 2–4. All and BOP dropped significantly in all months after NPT, the coefficients were
periodontal measures were significantly groups. 0.85, 0.87 and 0.84, respectively.
different among the three groups at both
baseline and 3 months after NPT analy-
sis, with the exception of PI. The ana- Psychosocial variables findings
Analysis among groups of participants
lysis of CAL and PPD periodontal sites with different levels of periodontal
The SSI and STAI understanding and
categories of o4, 4–6 and 46 mm
layout were tested and adjusted when disease and psychosocial factors
showed a gradual increase of deeper
necessary in a pilot study (Vettore et al.
PPD and CAL frequencies, when the Figure 1 shows the prevalence of sub-
2003).
three groups were compared. Frequen- jects with clinical stress at baseline and
cies of deeper PPD and CAL were 3 months after NPT for the three groups.
higher in groups with more periodontal Internal consistency of the SSI and Group T1 showed the highest frequency
disease. Bleeding on probing (BOP) was of patients with clinical stress at both
STAI
also related to poorer periodontal con- assessment times. The frequency of
dition (po0.01). The number of psychosocial items in the stressed patients 3 months after NPT
A significant reduction in the fre- subscales that comprise the SSI, State- increased in control and T1 groups
quencies of moderate (4–6 mm) and Anxiety Inventory (SAI) and Trait-An- from 19.1–29.4% to 47.0–58.9%, res-
deep (46 mm) PPD and CAL cate- xiety Inventory (TAI) were 53, 20 and pectively. Among stressed patients, par-
gories was observed 3 months after 20, respectively. Results for the internal ticipants in the alarm stage at baseline
NPT for group T2 (po0.01). Similarly, consistency of the items within each were detected in the control group
moderate (4–6 mm) and deep (46 mm) scale were computed at baseline and 3 (2.4%) and 3 months after NPT in group
PPD categories had reduced 3 months months after NPT. Baseline Cronbach’s T1 (5.9%). No participant was in the
after NPT for group T1. The percent- coefficients for SSI, SAI and TAI were stage of exhaustion. No significant dif-
age of sites with visible dental plaque 0.77, 0.86 and 0.76, respectively. Three ferences for clinical stress among groups

Table 2. Mean percentages ( SD) of clinical attachment level in the three groups at baseline and after therapy and according to the stress status
Clinical attachment level Control group Test group 1 Test group 2 pnn

baselinew after NPT baselinew after NPT baselinew after NPT

o 4 mm
All subjects 90.6  9.6 90.0  12.5 69.0  16.6 75.0  16.7 31.9  20.2 46.5  25.0 o0.01

Non-stressed 88.7  11.2 89.4  14.2 73.9  17.4 79.9  11.2 32.3  20.8 48.1  26.9 o0.01

Stressed 95.2  3.5 92.1  8.4 63.5  14.4 69.9  20.8 30.9  20.7 42.4  21.5 o0.01

4–6 mm
All subjects 9.0  0.9 9.0  10.8 27.4  15.2 22.0  14.2 47.3  15.2 39.0  19.0 o0.01

Non-stressed 10.8  10.2 9.7  11.9 23.2  17.7 18.4  10.7 45.6  16.7 35.7  18.6 o0.01

Stressed 4.5  3.0 7.7  8.4 32.3  12.2 26.2  17.0 52.5  19.6 49.2  19.1 o0.01

46 mm

All subjects 0.5  1.0 0.7  2.0 3.5  5.2 2.7  4.5 20.7  15.4 14.2  16.7 o0.01

Non-stressed 0.5  1.2 1.0  2.5 2.9  3.5 1.7  2.4 22.1  17.5 16.2  18.8 o0.01

Stressed 0.3  0.7 0.2  0.4 4.2  6.8 3.9  6.1 16.6  5.9 8.4  6.6 o0.01
Control group, all subjects, N 5 20; non-stressed, N 5 14; stressed, N 5 6.
Test group 1: all subjects, N 5 26; non-stressed, N 5 14; stressed, N 5 12.
Test group 2: all subjects, N 5 20; non-stressed, N 5 15; stressed, N 5 5.
nn
p refers to the Kruskal–Wallis test for comparison among groups at baseline and after non-surgical therapy.
n
po0.01 refers to Wilcoxon’s test for comparison within groups at baseline and after non-surgical therapy.
w
There were no significant differences between stressed and non-stressed patients on the baseline data for all periodontal clinical parameters.
1230 Vettore et al.

Table 3. Mean percentages ( SD) of periodontal pocket depth in the three groups at baseline and after therapy and according to the stress status

Periodontal pocket depth Control group Test group 1 Test group 2 pnn

baselinew after NPT baselinew after NPT baselinew after NPT

o4 mm
All subjects 97.0  5.2 96.6  6.7 77.7  12.7 87.0  13.7 43.7  20.2 65.2  19.0 o 0.01

Non-stressed 96.5  6.2 97.4  6.2 81.6  11.9 89.8  10.3 44.2  20.3 66.1  19.8 o 0.01

Stressed 98.1  1.9 94.9  8.1 73.3  12.6 83.7  16.9 42.5  22.4 62.7  17.6 o 0.01

4–6 mm
All subjects 3.0  6.5 3.2  6.7 20.6  11.7 12.4  12.8 42.0  17.6 27.6  13.2 o 0.01

Non-stressed 3.5  6.2 2.6  6.3 17.3  11.6 9.8  9.9 40.4  16.3 25.6  12.4 o 0.01

Stressed 1.9  1.9 4.8  8.3 24.6  11.2 15.4  15.6 46.2  22.8 33.8  15.1 o 0.01

46 mm
All subjects 0.0  0.0 0.1  0.3 1.6  2.7 0.6  1.3 14.4  10.2 7.0  9.7 o 0.01

Non-stressed 0.0  0.0 0.1  0.2 1.1  1.9 0.4  1.2 15.5  11.6 8.3  10.9 o 0.01

Stressed 0.0  0.0 0.3  0.4 2.1  3.4 0.9  1.6 11.2  3.4 3.5  4.1 o 0.01

Control group, all subjects, N 5 20; non-stressed, N 5 14; stressed, N 5 6.


Test group 1: all subjects, N 5 26; non-stressed, N 5 14; stressed, N 5 12.
Test group 2: all subjects, N 5 20; non-stressed, N 5 15; stressed, N 5 5.
n
po0.01 refers to Wilcoxon’s test for comparison within groups at baseline and after non-surgical therapy.
NS, not significant at the level of p 5 0.05.
w
There were no significant differences between stressed and non-stressed patients on the baseline data for all periodontal clinical parameters.
nn
p refers to the Kruskal–Wallis test for comparison among groups at baseline and after non-surgical therapy.

were found at baseline and 3 months period of time, only baseline scores for assessment times (N 5 8), and without
after NPT. TA were analysed. Significant associa- diagnoses of clinical stress (N 5 29) are
The average mean scores for TA tions were observed between PPD and shown in Tables 2–4. Baseline PPD and
among the three groups were statisti- CAL frequencies X4.0 and 4–6 mm and CAL frequencies o4.0 and X4.0 mm
cally different at baseline and 3 months high scores of TA in baseline and 3 were similar between participants with-
after NPT (po0.05). The mean baseline months after NPT (po0.05). Frequen- out stress and those with stress, as well
scores for TA for the three groups, cies of deeper PPD at baseline and as visible dental plaque and BOP.
control, T1 and T2, were 38.4, 40.5 frequencies of deeper CAL 3 months Decreases in PPD and CAL frequencies
and 45.3, respectively. After NPT, the after NPT were also found to be sig- X4.0 mm were significant in both groups
mean scores were 38.3, 41.7 and 47.2. nificantly associated with high scores of of participants: those with or without
No significant differences among the anxiety trait (po0.05). High scores of stress (po0.05). Significant reductions
three groups were found for mean scores SA at baseline were significantly asso- of visible dental plaque and BOP were
of SA before and after NPT. ciated with visible dental plaque also observed in both groups.
(po0.05).
Correlation analysis between Univariate analysis of covariance
psychosocial factors and periodontal Periodontal clinical parameters changed between reduction of PPD and CAL
clinical measures from baseline to 3 months after NPT in frequencies, socioeconomic data and
stressed and non-stressed subjects psychosocial factors
Table 5 presents the non-parametric
Spearman linear correlations between The comparisons of periodontal para- Univariate analysis of covariance was
TA and periodontal clinical measures. meters between baseline and 3 months performed on the reduction of PPD and
Since TA seems stable over a short after NPT of patients with stress in both CAL frequencies 44, 4–6 and 46 mm
The influence of stress and anxiety on the response to NPT 1231

Table 4. Mean percentages (  SD) of plaque index and gingival index in the three groups at baseline and after therapy and according to the stress
status

Clinical Parameters Control group Test group 1 Test group 2 pnn

baseline after NPT baseline after NPT baseline after NPT

PIX2

All subjects 56.5  19.4 11.4  16.5 51.0  21.0 20.3  20.9 59.3  17.1 20.0  20.3 NS

Non-stressed 58.3  19.8 12.2  19.2 47.5  22.1 21.0  22.2 59.8  17.4 15.9  16.1 o0.01

Stressed 52.7  19.7 9.8  9.1 55.5  19.2 19.6  20.3 58.1  18.3 32.4  28.5 o0.01

Gingival index BOP


All subjects 6.4  22.6 11.0  20.0 39.3  29.0 23.0  27.0 67.5  23.5 43.3  24.4 o0.01

Non-stressed 15.3  24.1 9.5  19.3 29.0  22.2 14.0  15.3 67.1  21.5 41.6  23.0 o0.01

Stressed 19.2  20.7 14.8  23.5 51.4  32.3 34.1  34.1 69.9  31.8 48.7  32.4 o0.01

Control group, all subjects, N 5 20, non-stressed, N 5 14; stressed, N 5 6.


Test group 1: all subjects, N 5 26, non-stressed, N 5 14; stressed, N 5 12.
Test group 2: all subjects, N 5 20, non-stressed, N 5 15; stressed, N 5 5.
nn
p refers to the Kruskal–Wallis test for comparison among groups at baseline and after non-surgical therapy.
n
po0.01 refers to Wilcoxon’s test for comparison within groups at baseline and after non-surgical therapy.
NS, not significant at the level of p 5 0.05.
PI, plaque index; BOP, bleeding on probing.

100 PPD frequencies 44.0 mm (p 5 0.026).


The association between reduction of
Alarm Stage Stage of Resistance Stage of Exhaustion deeper CAL frequencies (46 mm) and
scores of TA remained statistically sig-
Frequencies of stressed subjects

80
nificant after adjusting for dental plaque
and number of cigarettes (p 5 0.011).

60
Discussion
The findings in the present study
40 demonstrated an influence of stress and
TA on periodontal healing after non-
53
surgical periodontal therapy. Signifi-
47 cantly higher TA scores were observed
20 for subjects with chronic periodontitis at
16.7 29.4 29.4
baseline and 3 months after NPT. These
11.8 results support the hypothesis that psy-
2.4 5.9
0 chosocial factors can contribute to perio-
B NPT B NPT B NPT dontal disease aetiology and also affect
Control Test group 1 Test group 2 periodontal status after periodontal
treatment.
Fig. 1. Frequency subjects with stress in the groups at baseline (B) and 3 months after non-
surgical therapy (NPT). Control group, less than four sites with probing pocket depth (PPD)
The search for behavioural and psy-
44 mm; Group 1, at least four sites with PPD X4 and 46 mm; Group 2, at least four sites chosocial risk indicators for periodontal
with PPD X6 mm. There were no significantly statistical differences among the three groups. disease remains an important field in
(Baseline: p 5 0.18; 3 months after NPT: p 5 0.69; w2 test.) periodontology. Early evidence in this
was obtained in studies that showed that
with all psychosocial measures (Table frequencies (46 mm) (p 5 0.011), acute necrotizing ulcerative gingivitis
6). Scores of TA were statistically asso- reduction of deeper PPD frequencies incidence was strongly predicted by
ciated with the reduction of deeper CAL (46 mm) (p 5 0.030) and reduction of endocrine imbalances caused by stress
1232 Vettore et al.

Table 5. Correlation matrix (Spearman coefficient) between the total score of trait anxiety and Solis et al. 2004). The methodological
periodontal clinical parameters at baseline and 3 months after non-surgical periodontal therapy approaches used in those studies are
(NPT) quite different, which may be responsi-
Clinical parameters Trait anxiety ble for the conflicting results between
some studies. Such differences involve
baseline 3 months after NPT the type of psychosocial variable ana-
lysed, the questionnaire used for its
Periodontal pocket depth (%)
assessment, the type of periodontal dis-
X4 mm 0.305 (p 5 0.013)n 0.275 (p 5 0.026)n
4–6 mm 0.306 (p 5 0.012)n 0.276 (p 5 0.025)n ease investigated, the parameters used
46 mm 0.300 (p 5 0.015)n 0.239 (p 5 0.053) for periodontal status evaluation and ade-
Clinical attachment loss (%) quate control for potential confounders.
X4 mm 0.304 (p 5 0.013)n 0.288 (p 5 0.019)n The scientific evidence of the rela-
4–6 mm 0.289 (p 5 0.018)n 0.294 (p 5 0.017)n tionship between anxiety and perio-
46 mm 0.224 (p 5 0.070) 0.269 (p 5 0.029)n dontal disease has been demonstrated
n
po0.05. in a previous paper when the frequency
of moderate CAL and moderate PPD
were found to be significantly associated
Table 6. Univariate analysis of variance on the reduction of clinical attachment level frequencies with higher trait-anxiety scores after ad-
46 mm justing for socioeconomic data and ciga-
Source Mean of squares df F p-value rette consumption (Vettore et al. 2003).
In the present investigation, there was a
Anxiety 154.534 1 7.664 0.011 significant difference of TA scores
Dental plaque 28.096 1 1.393 0.249 among groups with different levels of
Number of cigarettes 0.341 1 0.017 0.898 chronic periodontitis. There is a dose–
Error 483.902 24 response effect between the averaged
mean TA scores and chronic perio-
dontitis (Fig. 2).
80
Other studies did not find differences
for anxiety when groups with different
levels of periodontal disease were com-
pared (Monteiro da Silva et al. 1996,
70 Moss et al. 1996, Genco et al. 1999,
Mean of State-Trait Anxiety Inventory

Solis et al. 2004). Possible explanations


(Variability of Scale 20 to 80 points)

Trait Anxiety State Anxiety


for the different findings include meth-
60 odological issues. The psychometric
instrument used to assess anxiety in
Genco and co-worker’s study was the
47.2 Hopkins-Symptom Checklist 90-revise
50
45.3
(SCL-90-R), which involves nine symp-
41.7 41.8 tom dimensions of psychological and
38.3 40.5 40.3
38.437.6 36.5 37.6 37.6 somatic symptom patterns (Genco et
40
al. 1999). Of the 53 items in this scale,
only six are used to evaluate the anxiety.
In common with Genco and co-workers’
30
study, Moss and colleagues used a simi-
lar questionnaire to assess anxiety. They
used an abbreviated version of the SCL-
20 90-R that provides an assessment of
BN PT B NPT BN PT
psychological symptoms in nine areas
Control Test group 1 Test group 2 including anxiety (Moss et al. 1996).
Fig. 2. Mean scores of State-Trait Anxiety Inventory at baseline (B) and 3 months after non- However, despite using the same psy-
surgical therapy (NPT). Control group, less than four sites with probing pocket depth (PPD) chometric instrument used in the present
44 mm; Group 1, at least four sites with PPD X4 and 46 mm; Group 2, at least four sites investigation to assess TA, early studies
with PPD X6 mm. There were significantly statistical difference among groups for trait- did not detect differences of anxiety
anxiety. (Trait-Anxiety: B: p 5 0.02; NPT: p 5 0.05; State-Anxiety: B: p 5 0.23; NPT: mean scores between groups with and
p 5 0.53; Kruskal–Wallis.) without periodontal disease (Monteiro
da Silva et al. 1996, Solis et al. 2004).
In an overall overview of the levels of
situations (Shannon et al. 1969, Maupin tions between psychosocial factors and TA in such studies, the anxiety scores in
& Bell 1975, Cogen et al. 1983, Cohen- periodontal illness (Marcenes & Shei- all studies were similar and cannot be
Cole et al, 1983, Stevens et al. 1984). In ham 1992, Monteiro da Silva et al. 1996, responsible for the differences in the
the last two decades, several investiga- Moss et al. 1996, Croucher et al. 1997, findings between the present study and
tions have been carried out on associa- Genco et al. 1999, Vettore et al. 2003, others.
The influence of stress and anxiety on the response to NPT 1233

Nonetheless, the clinical criteria of Environmental variables related to formed by controlling this confounding
diagnostic used to periodontal disease stress include work-related mental de- variable. In addition, The General Lin-
were quite different. In contrast with the mand, marital quality and socioeconomic ear Model test was conducted to control
present study, chronic periodontitis was status, which in turn were associated for other possible confounding vari-
considered when subjects were over 35 with periodontal status (Marcenes & ables, such as number of cigarettes.
years of age and presented horizontal Sheiham 1992). Marital status (widow/ Few studies tried to demonstrate a
bone loss (Monteiro da Silva et al. widower) and external locus of control possible influence of psychosocial fac-
1996). Conventional periodontal clinical significantly increased the risk of severe tors on periodontal status after anti-
parameters to assess periodontal disease periodontal disease (Hugoson et al. 2001). infectious periodontal therapy (Axtelius
including PPD, clinical attachment loss Current theories on the evolution of et al. 1998, Wimmer et al. 2005). Pas-
and BOP were not used for periodontitis psychological mechanisms as a part of sive coping strategies were more pro-
diagnostic. In another study, the cases the stress process focus on appraisal and nounced in cases of poor response to a
were patients with ‘‘established perio- contextual cues (Lazarus & Folkman non-surgical periodontal treatment. In
dontitis’’, according to Machtei et al. 1984). The elicitation of stress responses addition, active coping strategies were
(1992) (Solis et al. 2004). The severity vary; while some divergent responses are associated with a favourable course of
and distribution of periodontal disease based on biological predispositions, periodontal treatment (Wimmer et al.
in patients at Solis and co-worker’s many others are explained in terms of 2005). Another investigation compared
study might have been different from differences between stressors, contexts in psychological variables between patients
the present investigation. The non- which they occur and perceived abilities responding well to periodontal treatment
differential misclassification bias on to cope with them. Styles of coping with against those classified as responding
periodontal disease assessment might stress as well as psychological supports less well to periodontal treatment. On
have occurred in these studies, and and assets will affect the stressor res- one hand, the group responding well to
could also have affected the association ponses and the ultimate consequences of periodontal treatment displayed a more
between anxiety and periodontal dis- exposure to them (Kanner et al. 1981). resilient personality and possibly a less
ease. In this context, Genco et al. (1999) stressful psychosocial situation in the
The frequency of subjects with clin- detected a greater risk of severe attach- past. On the other, the group with pati-
ical stress was similar among groups at ment loss in subjects with high emotion- ents responding less well to periodon-
baseline and 3 months after non-surgical focused coping and more financial tal treatment had more psychological
periodontal therapy. This finding is in strain. In addition, inadequate stress be- strains and a more passive-dependent
accordance with previous studies on the haviour strategies (defensive coping) personality (Axtelius et al. 1998).
association between stress and chronic were strongly associated with the risk The present study supports the hypoth-
periodontitis (Monteiro da Silva et al. for severe periodontal disease (Wimmer esis that psychosocial factors must be
1996, Moss et al. 1996). Conversely, in et al. 2002). considered an important variable in the
other investigations groups that had The efficacy of the periodontal ther- response to periodontal therapy. The
higher scores for stress showed more apy observed in the present study is in reduction of severe CAL frequencies
severe periodontal disease (Marcenes agreement with data observed in long- was significantly predicted by TA scores.
& Sheiham 1992, Croucher et al. 1997, itudinal studies (Badersten et al. 1981, This is the first study that shows the link
Genco et al. 1999, Hugoson et al. 2002, 1984, Nordland et al. 1987, Claffey between anxiety and periodontal healing.
Wimmer et al. 2002). et al. 1988). Improvements in periodontal Socioeconomic characteristics were not
The differences in the above-men- clinical parameters after scaling and significantly different among the three
tioned results may be explained by the root planing followed by instruction in groups, although a tendency on the varia-
stress model used in the studies. Stress is oral hygiene included reduction of the bility was observed. The three groups’
a complex process by which an organ- percentage of sites with deep and mod- sample size may have influenced these
ism responds to certain environmental erate PPD and CAL. Large amounts of results. More than half of the subjects
or psychological events, called stressors, dental plaque comprised the inclusion involved were employed and married and
that pose a challenge or danger to the criterion for participants, and it was reported low alcohol consumption. The
organism (Gatchel et al. 1989). The SSI the only clinical parameter similar for main variables were statistically con-
(Lipp & Guevara 1994) used in the pre- the three groups at baseline. As dental trolled through general linear model dur-
sent study is based on the General plaque accumulation was high in all ing the analysis of the relationship of
Adaptation Syndrome proposed by Selye patients, it was possible to establish PPD and CAL measurement reduction
(1956). General Adaptation Syndrome reliable associations between dental bio- after NPT and TA scores. The present
consists of three stages of response: film and psychosocial factors. Plaque study showed significantly positive cor-
alarm reaction, stage of resistance and levels were associated with anxiety sta- relations between TA and frequencies of
exhaustion. The alarm stage starts when tus before periodontal treatment. This clinical parameters for periodontal dis-
the organism becomes aware of a stres- suggests that those who were more ease. Moreover, TA remained associated
sor or the presence of a noxious stimu- anxious may have not cleaned teeth so with periodontal healing after controlling
lus. This reaction is considered universal well. This can be associated with health for confounders. The periodontal healing
for all human beings. The stage of re- self-care and internal locus of control was associated with the only psychoso-
sistance and exhaustion involves coping (Monteiro da Silva et al. 1995). The cial factor that represents a characteristic
mechanisms and adaptive reserves’ con- decrease in plaque levels 3 months after of personality and, therefore, has more
sumption, and personality and environ- NPT was significant for all groups. The temporal stability.
mental variables can affect the stress analysis of the influence of stress and Stress did influence the periodontal
process (Bartlett 1998). anxiety on periodontal healing was per- healing after non-surgical periodontal
1234 Vettore et al.

treatment. The findings in the present characteristics. Journal of Clinical Perio- of stress, distress, and inadequate coping
investigation are in accordance with dontology 25, 482–491. behaviors to periodontal disease. Journal of
previous studies, despite the lack of Badersten, A., Nilveus, R. & Egelberg, J. (1981) Periodontology 70, 711–723.
standardization in the model to assess Effect of nonsurgical periodontal therapy I. Grossi, S. G., Zambon, J. J., Ho, A. W., Koch,
Moderately advanced periodontitis. Journal G., Dunford, R. G., Machtei, E. E., Norderyd,
stress among studies. To analyse the
of Clinical Periodontology 8, 57–72. O. M. & Genco, R. J. (1994) Assessment of
influence of stress on the response of Badersten, A., Nilveus, R. & Egelberg, J. (1984) risk for periodontal disease. I. Risk indicators
non-surgical periodontal therapy, sub- Effect of nonsurgical periodontal therapy II for attachment loss. Journal of Perio-
jects who completed the periodontal Severely advanced periodontitis. Journal of dontology 65, 260–267.
treatment were grouped into ‘‘non-stres- Clinical Periodontology 11, 63–76. Gupta, O. P. (1966) Psychosomatic factors in
sed patients’’ and ‘‘stressed patients’’ Barbour, S. E., Nakashima, K., Zhang, J. B., periodontal disease. Dental Clinics of North
groups. The reduction of PPD and CAL Tangada, S., Hahn, C. H., Schenckein, H. A. America 7, 11–19.
frequencies 4–6 and 46 mm was not & Tew, J. G. (1997) Tobacco and smoking: Hempton, T. J. & Leone, C. (1997) The effects
observed in stressed subjects in different environmental factors that modify the host of smoking on periodontal disease and perio-
response (immune system) and have an dontal therapies. Journal of Massachusetts
groups with periodontal disease. On the
impact on periodontal health. Critical Dental Society 46, 33–35, 38–40.
other hand, non-stressed patient groups Reviews on Oral Biology and Medicine 8, Hugoson, A., Ljungquist, B. & Breivik, T.
showed significant decreases in all PPD 437–460. (2001) The relationship of some negative
and CAL frequencies 4–6 and 46 mm. Bartlett, D. (1998) Stress: Perspectives and events and psychological factors to perio-
This lack of reduction in clinical para- Process, pp. 62–83. Open University Press, dontal disease in an adult Swedish population
meters observed in the stressed group Buckingham. 50 to 80 years of age. Journal of Clinical
may either be owing to an influence of Biaggio, A. M. B., Natalı́cio, L. & Spielberger, Periodontology 29, 247–253.
stress in periodontal healing or else the C. D. (1977) Desenvolvimento da forma Hugoson, A., Ljungquist, B. & Breivik, T.
sample size of this group. experimental em português do Inventário de (2002) The relationship of some negative
Ansiedade Traço-Estado (IDATE). Arquivos events and psychological factors to perio-
Stress and TA prediction for poor
Brasileiros De Psicologia Aplicada 29, dontal disease in an adult Swedish population
response to periodontal therapy may be 31–44.
explained by a similar model used to 50 to 80 years of age. Journal of Clinical
Claffey, N., Loos, B., Gantes, B., Martin, M., Periodontology 29, 247–253.
link the social environmental and psycho- Heins, P. & Egelberg, J. (1988) The relative Hujoel, P. P., Leroux, B. G., Selipsky, H. &
logical features that may trigger physio- effects of therapy and periodontal disease on
White, B. A. (2000) Non-surgical periodontal
logical processes leading to disease loss of probing attachment after root debride-
therapy and tooth loss. A cohort study. Jour-
susceptibility. Immune system modifi- ment. Journal of Clinical Periodontology 15,
nal of Periodontology 71, 736–742.
cations (Rogers et al. 1979), crevicular 163–169.
Kanner, A. D., Coyne, J. C., Schaefer, C. &
interleukin-1 alterations (Deinzer et al. Cogen, R. B., Stevens, A. W., Cohen-Cole, S.
Lazarus, R. S. (1981) Comparison of two
A., Kirk, K. & Freeman, A. (1983) Leukocyte
1999), changes in gingival circulation modes of stress measurement daily hassles
function in the etiology of acute necrotizing
(Manhold et al. 1971), alteration in ulcerative gingivitis. Journal of Perio-
and uplifts versus major life events. Journal
salivary flow and components (Gupta of Behavioral Medicine 41, 1–39.
dontology 54, 402–407.
1966) and/or endocrine changes (Davis Kinane, D. F. (2005) Single-visit, full-mouth
Cohen-Cole, S. A., Cogen, R. B., Stevens Jr., A.
& Jenkins 1962) are possible mediating ultrasonic debridement: a paradigm shift in
W., Kirk, K., Gaitan, E., Bird, J., Cooksey, R.
periodontal therapy. Journal of Clinical
mechanisms involved in that process. & Freeman, A. (1983) Psychiatric, psychoso-
cial, and endocrine correlates of acute necro- Periodontology 32, 732–733.
Knowledge concerning the possible Koshy, G., Kawashima, Y., Kiji, M., Nitta, H.,
influence of psychosocial factors on perio- tizing ulcerative gingivitis (trench mouth): a
preliminary report. Psychology and Medicine Umeda, M., Nagasawa, T. & Ishikawa, I.
dontal healing is scarce. More studies are (2005) Effects of single-visit full-mouth
1, 215–225.
needed to clarify the real effect of stress Colombo, A. P., Haffajee, A. D., Dewhirst, F. ultrasonic debridement versus quadrant-wise
and anxiety on periodontal therapy res- E., Paster, B. J., Smith, C. M., Cugini, M. A. ultrasonic debridement. Journal of Clinical
ponse. In the future, new possible influ- & Socransky, S. S. (1998) Clinical and Periodontology 32, 734–743.
ence of psychological interventions on microbiological features of refractory perio- Lazarus, R. S. & Folkman, S. (1984) Stress,
periodontal disease control therapies dontitis subjects. Journal of Clinical Perio- Appraisal and Coping. New York: Springer.
should be considered since behavioural dontology 25, 169–180. Lipp, M. E. N. & Guevara, A. J. H. (1994)
Croucher, R., Marcenes, W. S., Torres, M. C. Validação empı́rica do Inventário de Sinto-
and social components are already asso-
M. B., Hughes, E. & Sheiham, A. (1997) The mas de Stress (ISS). Estudos de Psicologia
ciated with periodontal disease. 11, 43–49.
relationship between life-events and perio-
dontitis. A case–control study. Journal of Löe, H. (1967) The gingival index, the plaque
Clinical Periodontology 24, 39–43. index and the retention index system. Journal
Acknowledgements Davis, C. H. & Jenkins, C. D. (1962) Mental of Periodontology 38, 610–616.
stress and oral diseases. Journal of Dental Machtei, E. E., Christersson, L. A., Grossi, S.
The authors are grateful to Dr. Eduardo
Research 41, 1045–1049. G., Dunford, R., Zambon, J. J. & Genco, R. J.
Feres, Professor of Periodontology at (1992) Clinical criteria for the definition of
Deinzer, R., Föster, P., Fuck, L., Herforth, A.,
Federal University of Rio de Janeiro, Stiller-Winkler, R. & Idel, H. (1999) Increase ‘‘established periodontitis’’. Journal of
and to Dr. Ronnir Raggio for their of crevicular interleukin 1 under academic Periodontology 63, 206–214.
assistance with statistical analyses. stress at experimental gingivitis sites and at Manhold, J. H., Doyle, J. L. & Weisinger, E. H.
sites of perfect oral hygiene. Journal of (1971) Effects of social stress on oral and
Clinical Periodontology 26, 1–8. other bodily tissues. II. Results offering sub-
References Gatchel, R. J., Baum, A. & Krantz, D. S. (1989) stance to a hypothesis for the mechanism of
An Introduction to Health Psychology, 2nd formation of periodontal pathology. Journal
Axtelius, B., Söderfeldt, B., Nilsson, A., edition. New York: McGraw-Hill. of Periodontology 42, 109–111.
Edwardsson, S. & Attström, R. (1998) Ther- Genco, R. J., Ho, A. W., Grossi, S. G., Dunford, Marcenes, W. S. & Sheiham, A. (1992) The
apy-resistant periodontitis. Psychosocial R. G. & Tedesco, L. A. (1999) Relationship relationship between work stress and oral
The influence of stress and anxiety on the response to NPT 1235

health status. Social Science and Medicine cal review. Psychosomatic Medicine 41, Vettore, M. V., Leão, A. T., Monteiro da Silva,
35, 1511–1520. 147–164. A. M., Quintanilha, R. S. & Lamarca, G. A.
Maupin, C. C. & Bell, W. B. (1975) The Shlossman, M., Knowler, W. C., Pettitt, D. J. & (2003) The relationship of stress and anxiety
relationship of 17-hydroxy-corticosteroid to Genco, R. J. (1990) Type 2 diabetes mellitus with chronic periodontitis. Journal of Clin-
acute necrotizing ulcerative gingivitis. Jour- and periodontal disease. Journal of the Amer- ical Periodontology 30, 394–402.
nal of Periodontology 46, 721–722. ican Dental Association 121, 532–536. Wennström, J. L., Tomasi, C., Bertelle, A. &
Monteiro da Silva, A. M., Newman, H. N. & Selye, H. (1956) The Stress of Life. New York: Dellasega, E. (2005) Full-mouth ultra-
Oakley, D. A. (1995) Psychosocial factors in McGraw Hill. sonic debridement versus quadrant scaling
inflammatory periodontal – A review. Jour- Selye, H. (1963) A syndrome produced by and root planing as an initial approach
nal of Clinical Periodontology 22, 516–526. diverse nocous agentes. Nature 138, 32. in the treatment of chronic periodontitis.
Monteiro da Silva, A. M., Oakley, D. A., New- Shannon, I. L., Kilgore, W. G. & O’Leary, T. J. Journal of Clinical Periodontology 32,
man, H. N., Nohl, F. S. & Lloyd, H. M. (1969) Stress as a predisposing factor in 851–859.
(1996) Psychosocial factors and adult onset necrotizing ulcerative gingivitis. Journal of Wimmer, G., Janda, M., Wieselmann-Penkner,
rapidly progressive periodontitis. Journal of Periodontology 40, 240–242. K., Jakse, N., Polansky, R. & Pertl, C. (2002)
Clinical Periodontology 26, 789–794. Silness, J. & Löe, H. (1964) Periodontal disease Coping with stress: its influence on perio-
Moss, M. E., Beck, J. D., Kaplan, B. H., in pregnancy. II. Correlation between oral dontal disease. Journal of Periodontology 73,
Offenbacher, S., Weintraub, J. A., Koch, G. 1343–1351.
hygiene and periodontal condition. Acta
G., Genco, R. J., Machtei, E. E. & Tedesco, Wimmer, G., Köhldorfer, G., Mischak, I., Lor-
Odontologica Scandinavia 22, 121–135.
L. A. (1996) Exploratory case-control enzoni, M. & Kallus, W. (2005) Coping with
Socransky, S. S., Haffajee, A. D., Cugini, M. A.,
analysis of psychosocial factors and adult stress: its influence on periodontal therapy.
Smith, C. & Kent Jr., R. L. (1998) Microbial
periodontitis. Journal of Periodontology 67, Journal of Periodontology 76, 90–98.
complexes in subgingival plaque. Journal of
1060–1069.
Clinical Periodontology 25, 134–144.
Nordland, P., Garret, S., Kiger, R., Vanoote-
Solis, A. C., Lotufo, R. F., Pannuti, C. M.,
ghem, R., Hutchens, L. H. & Egelberg, J.
(1987) The effect of plaque control and root Brunheiro, E. C., Marques, A. H. & Lotufo-
Address:
debridement in molar teeth. Journal of Clin- Neto, F. (2004) Association of periodontal Mario Vianna Vettore
ical Periodontology 14, 231–236. disease to anxiety and depression symptoms, Universidade Federal do Rio de Janeiro
Offenbacher, S. (1996) Periodontal diseases: and psychosocial stress factors. Journal of (UFRJ)
pathogenesis. Annals of Periodontology 1, Clinical Periodontology 31, 633–638. Faculdade de Odontologia
821–878. Stevens, A. W. Jr., Cogen, R. B., Cohen-Cole, Departamento de Clinica Odontologica/
Page, R. & Beck, J. (1997) Risk assessment for S. & Freeman, A. (1984) Demographic and Periodontia
periodontal diseases. International Dental clinical data associated with acute necrotizing Avenida Brigade´iro Trompovsky S/N
Journal 47, 61–87. ulcerative gingivitis in a dental school popu- Cidade Universitaria
Rogers, M. P., Dubey, D. & Reich, P. (1979) lation (ANUG-demographic and clinical Galeao-Rio de Janeiro - RJ
The influence of the psyche and brain on data). Journal of Clinical Periodontology CEP 21949-900 Brazil
immunity and disease susceptibility. A criti- 11, 487–493. Email: mario@ensp.fiocruz.br

Вам также может понравиться