Pulp testing

Clinical Research

Response of Pulp Sensibility Test Is Strongly Influenced
by Periodontal Attachment Loss and Gingival Recession
Cristiane Rutsatz, DDS,* Simone Glesse Baumhardt, MSc,* Carlos Alberto Feldens, PhD,†
Cassiano Kuchenbecker R€sing, PhD,‡ Renata Grazziotin-Soares, MSc,†
o
and Fernando Branco Barletta, PhD†

Abstract
Introduction: To assess, in vivo, the influence of Key Words
periodontal attachment loss and gingival recession on Dental pulp test, gingival recession, periodontal attachment loss
responses to pulp sensibility tests (PSTs) with cold
stimuli in mandibular incisors in adult patients.
Methods: This cross-sectional study included 45
patients aged 30 to 60 years treated at a university
O ver recent years, several possible relationships between periodontal disease and
dental pulp tissues have been investigated (1–3). For example, periodontal
disease has been suggested to be a direct cause of pulpal degeneration (3). However,
dental health service. In each patient, 1 mandibular this hypothesis lacks consistent evidence once it is based on the findings of a critical
incisor was randomly selected for analysis. One cali- literature review (4) and on the microbiological evaluation of isolated clinical cases
brated dentist performed all periodontal assessments. (5). Conversely, the effects of pulp disease on the periodontium are well documented
Periodontal attachment loss and gingival recession (3, 6–8).
were measured at 6 sites of the selected tooth followed In this context, assessing pulp status in patients with periodontally compromised
by application of the PST on the buccal surface of the teeth remains an important challenge in dental practice. It is possible that teeth with
tooth by an independent operator. Each patient was varying degrees of periodontal involvement may respond differently to pulp sensibility
asked to indicate a score for pain intensity on a numeric tests (PSTs) when compared with periodontally healthy teeth. Moreover, the inherent
visual analog scale. The Pearson correlation coefficient limitations of the different methods available for assessing pulp sensibility may be maxi-
was used to investigate and quantify the correlation mized by an additional factor, namely the presence of periodontal attachment loss.
between predictor variables (periodontal attachment Nevertheless, literature devoted to the assessment of responses to pulp stimulation in
loss and gingival recession) and reported pain. Simple teeth with varying degrees of periodontal attachment loss is scarce, and studies designed
and multiple linear regression analyses were performed to investigate this association using multivariate analysis are currently lacking.
to determine the impact of periodontal attachment loss Therefore, the aims of this study were to investigate the correlation between peri-
and gingival recession on PST pain scores. Results: odontal attachment loss/gingival recession and responses to PST with cold stimuli and
Multivariate analysis showed that periodontal attach- to quantify this correlation and propose a function to describe the variation in responses
ment loss contributed significantly to the prediction of to PST as a result of different degrees of periodontal attachment loss and gingival reces-
pain in response to the PST (P < .001). Increases of 1 sion. The null hypothesis was that there would be no correlation between the predictors
mm in periodontal attachment loss resulted in a decrease and the outcome (r = 0).
of approximately 0.5 score on the pain scale. Gingival
recession also contributed as a predictor of the outcome Materials and Methods
(P < .001) with a decrease of approximately 0.7 in pain Patient Selection and Study Design
scores for every 1-mm increase in gingival recession. The
All adults seeking treatment at the School of Dentistry of Universidade de Santa
correlations were in the opposite direction than ex-
Cruz do Sul, Southern Brazil, between August 2010 and October 2010, were consid-
pected. Conclusions: Periodontal attachment loss and
ered eligible for the present cross-sectional study. Adult patients presenting with 4
gingival recession strongly influenced reported pain in
mandibular incisors without carious lesions were selected for inclusion. The
response to PST with cold stimuli. The effect of both
following exclusion criteria were considered: the presence of systemic diseases;
variables was constant (ie, responses to PST decreased
treatment with anti-inflammatory agents; and lower incisors with spontaneous
gradually with increases in periodontal attachment
pain, restorations, crowns or veneers, trauma history, previous root canal treatment,
loss and gingival recession). (J Endod 2012;38:580–583)
or tooth wear.
Sample size was calculated considering a 95% confidence level, 80% power, and
the ability of the study to detect at least a moderate correlation (r = 0.5) between the

From the *School of Dentistry, Universidade de Santa Cruz do Sul (UNISC), Santa Cruz do Sul, Brazil; †School of Dentistry, Universidade Luterana do Brasil (ULBRA),
Canoas, Brazil; ‡School of Dentistry, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brazil.
Address requests for reprints to Dr Renata Grazziotin-Soares, Faculdade de Odontologia, Universidade Luterana do Brasil, Av. Farroupilha 8001, Prdio 59, 3 andar,
e
Canoas, RS, Brazil 92425-900. E-mail address: regrazziotin@gmail.com
0099-2399/$ - see front matter
Copyright ª 2012 American Association of Endodontists.
doi:10.1016/j.joen.2012.01.011

580 Rutsatz et al. JOE — Volume 38, Number 5, May 2012

Clinical Research
predictors (periodontal attachment loss and gingival recession) and the level and at the subject (tooth) level were assessed using intraclass
outcome (response to PST) as quantitative variables. These variables re- correlation coefficient (ICC) (13).
sulted in a minimum sample size of 29 subjects (9), which was
increased by 50% for multivariate analysis purposes and to avoid Statistical Analysis
a potential loss of information. The final sample comprised 45 subjects. Statistical analysis was performed using the Statistical Package for
Tooth randomization was performed as follows: 4 numbers, cor- the Social Sciences version 16.0 (SPSS Inc, Chicago, IL). Periodontal
responding to each 1 of the lower incisors, were placed in an opaque, attachment loss and gingival recession results were analyzed consid-
sealed envelope. For each patient who agreed to participate in the study, ering the mean of the 6 sites measured for each tooth. The Pearson
1 number was drawn, and the corresponding tooth was selected for correlation coefficient was used to assess and quantify the correlation
periodontal examination and PST application. between periodontal attachment loss and gingival recession variables
The study was approved by the local ethics committee. All subjects and pain reported on the PST.
signed an informed consent form before their inclusion in the study. Simple and multiple linear regression analyses were performed to
determine the impact of periodontal attachment loss and gingival reces-
Periodontal Examinations sion on PST pain scores. First, the B coefficients and 95% confidence
Periodontal examinations were performed by a calibrated dentist interval (CI) of each variable were estimated separately. Because the
at the main university dental clinic. All teeth in the lower incisor region effects of periodontal attachment loss and gingival recession on re-
were subjected to clinical examination. During the periodontal assess- ported pain may be influenced by age and sex, these variables were
ment, teeth were isolated with cotton rolls, and measurements were included in the analysis. Multivariate analysis started with potential
made as follows: periodontal attachment loss and gingival recession predictors and confounders for reported pain, and backward elimina-
were measured in millimeters at 6 sites per tooth: mesiobuccal, middle tion was used whenever Wald P values were higher than .05. Age was
buccal, distobuccal, mesiolingual, middle lingual, and distolingual (10, retained in the models as a possible confounder regardless of statistical
11). A manual periodontal probe, color coded at 1, 2, 3, 5, 7, 8, 9, and significance. Because periodontal attachment loss and gingival reces-
10 mm (PCP10-SE; Hu-Friedy, Chicago, IL), was used. Periodontal sion showed a high level of collinearity (Pearson r = 0.943, variance
attachment loss was defined as the distance between the cementoena- inflation factor = 9.01), 2 separate models were constructed, 1 for peri-
mel junction (CEJ) and the bottom of the pocket/sulcus and was calcu- odontal attachment loss (model 1) and another for gingival recession
lated as the sum of probing depth plus gingival recession. Gingival (model 2).
recession was defined as the distance between the CEJ and the free
gingival margin (FGM). Gingival recession was scored as zero when Results
the FGM was located at the CEJ and was assigned a negative value All reproducibility measurements showed almost perfect agree-
when the FGM was located coronal to the CEJ. ment. At the subject level, ICC values for mean periodontal attachment
loss and mean gingival recession were 0.93 (95% CI, 0.90–0.96) and
PST 0.99 (95% CI, 0.98–1.00), respectively. At the site level, ICC values for
periodontal attachment loss and gingival recession were 0.97 (95% CI,
A PST was also conducted under isolation with cotton rolls by an
0.93–1.00) and 0.99 (95% CI, 0.95–1.00), respectively.
examiner who was not aware of the final measurements of attachment
The study population comprised 45 adults, of whom 40% were
loss. A refrigerant spray (Endo-Frost-50 C; Coltene/Whaledent, Altst€t-
a
men (18/45). Patient age varied from 32 to 55 years (mean = 45, stan-
ten, Switzerland) was applied to the middle/incisal third of the buccal
dard deviation [SD] = 6.5, median = 44). Table 1 shows periodontal
surface of the selected tooth using a cotton pellet tightly wrapped
attachment loss, gingival recession, and pain results obtained in
around the tip of a tweezer (12). Patients were asked to rate their
the sample. Periodontal attachment loss and gingival recession results
pain on a 0 to 10 numeric visual analog scale, with 0 representing no
showed a wide variation among subjects, with a mean Æ SD of 3.2 Æ 1.8
pain and 10 indicating the worst pain the patient has ever experienced.
mm and 2.3 Æ 1.4 mm, respectively. Pain response to the PST ranged
A 0 score was defined as the absence of response after two 15-second
from 0 to 8, with a mean Æ SD of 4.9 Æ 1.5. Periodontal attachment
applications of the refrigerant spray at a 2-minute interval.
loss, gingival recession, and pain response to the PST showed
an approximately normal distribution (Kolmogorov-Smirnov test,
Quality Control P .05). There were no statistically significant differences between
A quality control protocol was followed to ensure a standardized male (mean Æ SD = 4.50 Æ 1.6) and female (5.11 Æ 1.4) responses
examination environment and standardized equipment. Written instruc- to the PST (P = .180) or between subjects 45 years and $45 years
tions describing in detail all the clinical procedures involved in the study (5.26 Æ 1.3 and 4.45 Æ 1.5, respectively) (P = .068).
were provided to the examiners. Also, the examiner in charge of peri- Table 2 shows a statistically significant negative correlation
odontal assessments was trained and calibrated before the beginning of between periodontal attachment loss and reported pain; this predictor
the study. A total of 20 subjects were examined twice, at a 2-week variable was found to explain 31.5% of the variance of the outcome.
interval, to allow reproducibility assessment. Periodontal attachment Gingival recession also presented a significant negative correlation
loss and gingival recession reproducibility measurements at the site with pain intensity, explaining 42% of its variance. Table 3 shows the

TABLE 1. Results Obtained in the Sample for the Predictor Variables (periodontal attachment loss and gingival recession) and the Outcome of Interest (pain
response to the PST)
Minimum Median (P25 to P75) Maximum Mean SD
Periodontal attachment loss (mm) 1.25 2.75 (1.87 to 3.87) 10.0 3.2 1.8
Gingival recession (mm) 1.00 1.75 (1.37 to 2.87) 7.5 2.3 1.4
Pain/pulp sensibility test 0 5.0 (4.0 to 6.0) 8.0 4.9 1.5

JOE — Volume 38, Number 5, May 2012 Factors Associated with Responses to Pulp Sensibility Test 581

Clinical Research
TABLE 2. Correlation between Periodontal Attachment Loss and Gingival secondary dentin formation may yield false-negative results when the
Recession and Referred Pain in Response to the PST PST is used with cold stimuli (21).
Pearson In the present study, dentin mineralization and pulp recession may
have created limitations for the adequate performance of the PST. In
Variable R Adjusted R2 P value order to decrease the possibility of measurement bias, teeth were
Periodontal attachment loss À0.575 0.315 .001 isolated with cotton rolls and air dried. Moreover, the decision to
Gingival recession À0.657 0.419 .001 include only adult patients, between 30 and 60 years of age, aimed to
restrict variations in pain response caused by age-related mineraliza-
tion. The literature has confirmed age-related decreases in pulp cavity
results of the 2 linear regression models. Sex was excluded from the 2 size and shape using micro–computed tomography images (22). Inter-
final models. Model 1 showed that periodontal attachment loss contrib- estingly, in our multivariate analysis, patient age did not seem to have
uted significantly to the prediction of reported pain on PST (P .001). influenced the relationship between predictor variables and the
Every increase of 1 mm in periodontal attachment loss resulted in outcome of interest. In addition, our methodology considered the
a decrease of approximately 0.5 score on the pain scale. Model 2 subject as the unit of analysis to avoid limitations previously described
also showed a significant contribution of gingival recession toward for the use of the tooth as such unit (23, 24).
pain intensity (P .001), with a decrease of approximately 0.7 in Another difficulty in the interpretation of our results refers to the
pain scores for every 1-mm increase in gingival recession. subjectivity of the PST (ie, the possibility of obtaining different responses
to stimuli depending on the patient assessed). Indeed, some authors
have considered interindividual sensibility differences to reinforce the
Discussion validity of their results (25). Fear, anxiety, and pain may all influence
The complexity of diagnosing pulp abnormalities in patients with reported pain (1). Some measures were taken to minimize this limita-
periodontal disease (3) and the absence of clinical studies designed to tion and to reduce possible errors in data interpretation. Among such
assess this interaction were the main motivations for the present study. measures, it is possible to mention the use of a numeric visual analog
Our results strongly suggest that periodontal disease gradually and scale for the classification of pain intensity and the selection of patients
inversely affects pain intensity (ie, the more severe the periodontal among individuals seeking regular treatment (ie, without acute pulp
condition, the lower the intensity of pain in response to PST with inflammation or other conditions that could influence pain response).
cold stimuli). In our sample, contrary to our expectations, teeth with However, we are aware that such measures do not completely eliminate
higher results for periodontal involvement (periodontal attachment differences related to individual pain sensation. Some individuals may
loss and gingival recession) responded with lower pain intensity scores have referred higher or lower degrees of pain in any of their teeth
on the PST. This effect was constant (ie, pain response to the PST regardless of the periodontal condition. In this context, the design of
decreased gradually with increases in periodontal attachment loss a new study using teeth as controls in each individual could complement
and gingival recession values). The plausibility of the relationship our findings. However, from a different perspective, if there really was
among the studied variables, the strength of the association, and the an error in pain assessment in our study, it would have been a nondif-
dose-response effect observed suggest a strong relationship of causality ferential misclassification. Considering that this type of error would bias
among the variables assessed. the study results toward the null hypothesis (26), we believe that the
One possible explanation for the lower pain scores obtained in the methodology used did not influence the reported correlations.
presence of more severe indicators of periodontal disease is the poten- An additional potential limitation of our study was the fact that only
tial role of pulp recession as a protection mechanism. Periodontal lower incisors were analyzed. The inclusion of posterior and/or upper
attachment loss and gingival recession result in an increased exposure teeth would possibly modify the results. Conversely, based on the
of cementum and dentin. The exposure of dentinal tubules and the strength of association observed, it is plausible that the correlation
continuous process of aggregation of subgingival biofilm could cause between the variables assessed will also be present in other teeth.
pulp degeneration (3, 5) where pulp mesenchymal cells are Finally, the presence of information bias during periodontal measure-
activated, leading to the formation of reactionary dentin (14). This ments is unlikely, considering that the examiner was previously cali-
phenomenon has been documented as a protective response of the brated and that an almost perfect agreement was obtained.
pulp against external stimuli (2). The so-called pulp sensibility tests (ie, thermal [heat and cold]
According to the hydrodynamic theory, thermal tests require stimulation, electrical stimulation, or direct dentin stimulation [cavity
dentinal tubules to be open to allow fluid flow. Changes in temperature test]) measure pulp nerve responses only, not pulp blood flow. These
tend to influence dentinal fluid flow and, subsequently, the mechanical tests measure the presence of neural response in the pulp but do not
stimulation of pulp nerves (15–19). Enamel and dentin are thermal provide information on vascular health (21). Our findings suggest
insulators (20) known to interfere with the passage of cold tempera- that teeth with lower pain levels in response to the PST have a decreased
tures; therefore, teeth with closed dentinal tubules and substantial pulp neural response. This hypothesis has been confirmed by

TABLE 3. Simple and Multivariate Linear Regression Analysis for Referred Pain on the PST
Simple linear regression Multivariate linear regression*

Model Variable B 95% CI P value B 95% CI P value
1 Constant 6.39 (5.63 to 7.16) .001 7.83 (5.63 to 7.16) .001
Periodontal attachment loss À0.48 (À0.69 to À0.27) .001 À0.47 (À0.68 to À0.26) .001
2 Constant 6.45 (5.80 to 7.10) .001 8.04 (5.21 to 10.44) .001
Gingival recession À0.68 (À0.92 to À0.44) .001 À0.67 (À0.90 to À0.43) .001
*Adjusted for age.

582 Rutsatz et al. JOE — Volume 38, Number 5, May 2012

Clinical Research
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a
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