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  1. 1. Clinical ResearchResponse of Pulp Sensibility Test Is Strongly Influencedby Periodontal Attachment Loss and Gingival RecessionCristiane Rutsatz, DDS,* Simone Glesse Baumhardt, MSc,* Carlos Alberto Feldens, PhD,†Cassiano Kuchenbecker R€sing, PhD,‡ Renata Grazziotin-Soares, MSc,† oand Fernando Branco Barletta, PhD†AbstractIntroduction: To assess, in vivo, the influence of Key Wordsperiodontal attachment loss and gingival recession on Dental pulp test, gingival recession, periodontal attachment lossresponses to pulp sensibility tests (PSTs) with coldstimuli in mandibular incisors in adult patients.Methods: This cross-sectional study included 45patients 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 criticalincisor was randomly selected for analysis. One cali- literature review (4) and on the microbiological evaluation of isolated clinical casesbrated dentist performed all periodontal assessments. (5). Conversely, the effects of pulp disease on the periodontium are well documentedPeriodontal 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 compromisedby application of the PST on the buccal surface of the teeth remains an important challenge in dental practice. It is possible that teeth withtooth by an independent operator. Each patient was varying degrees of periodontal involvement may respond differently to pulp sensibilityasked to indicate a score for pain intensity on a numeric tests (PSTs) when compared with periodontally healthy teeth. Moreover, the inherentvisual 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 inloss and gingival recession) and reported pain. Simple teeth with varying degrees of periodontal attachment loss is scarce, and studies designedand 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 andMultivariate analysis showed that periodontal attach- to quantify this correlation and propose a function to describe the variation in responsesment 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 predictorsmm in periodontal attachment loss resulted in a decrease and the outcome (r = 0).of approximately 0.5 score on the pain scale. Gingivalrecession 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 Designscores for every 1-mm increase in gingival recession. The All adults seeking treatment at the School of Dentistry of Universidade de Santacorrelations 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 4gingival recession strongly influenced reported pain in mandibular incisors without carious lesions were selected for inclusion. Theresponse 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 spontaneousgradually 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, eCanoas, RS, Brazil 92425-900. E-mail address: regrazziotin@gmail.com0099-2399/$ - see front matter Copyright ª 2012 American Association of Endodontists.doi:10.1016/j.joen.2012.01.011580 Rutsatz et al. JOE — Volume 38, Number 5, May 2012
  2. 2. Clinical Researchpredictors (periodontal attachment loss and gingival recession) and the level and at the subject (tooth) level were assessed using intraclassoutcome (response to PST) as quantitative variables. These variables re- correlation coefficient (ICC) (13).sulted in a minimum sample size of 29 subjects (9), which wasincreased by 50% for multivariate analysis purposes and to avoid Statistical Analysisa 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). Periodontalresponding 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 Pearson1 number was drawn, and the corresponding tooth was selected for correlation coefficient was used to assess and quantify the correlationperiodontal 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 theat 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 werement, teeth were isolated with cotton rolls, and measurements were included in the analysis. Multivariate analysis started with potentialmade 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 wasbuccal, distobuccal, mesiolingual, middle lingual, and distolingual (10, retained in the models as a possible confounder regardless of statistical11). 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, varianceattachment 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 recessionlated as the sum of probing depth plus gingival recession. Gingival (model 2).recession was defined as the distance between the CEJ and the freegingival margin (FGM). Gingival recession was scored as zero when Resultsthe 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) andPST 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% wereloss. 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 periodontalsurface of the selected tooth using a cotton pellet tightly wrapped attachment loss, gingival recession, and pain results obtained inaround the tip of a tweezer (12). Patients were asked to rate their the sample. Periodontal attachment loss and gingival recession resultspain 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 1.8pain 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 rangedA 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 attachmentapplications 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) responsesexamination environment and standardized equipment. Written instruc- to the PST (P = .180) or between subjects 45 years and $45 yearstions 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 correlationodontal assessments was trained and calibrated before the beginning of between periodontal attachment loss and reported pain; this predictorthe 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 correlationloss and gingival recession reproducibility measurements at the site with pain intensity, explaining 42% of its variance. Table 3 shows theTABLE 1. Results Obtained in the Sample for the Predictor Variables (periodontal attachment loss and gingival recession) and the Outcome of Interest (painresponse 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 1.5JOE — Volume 38, Number 5, May 2012 Factors Associated with Responses to Pulp Sensibility Test 581
  3. 3. Clinical ResearchTABLE 2. Correlation between Periodontal Attachment Loss and Gingival secondary dentin formation may yield false-negative results when theRecession 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 cavityresults 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 haveuted significantly to the prediction of reported pain on PST (P .001). influenced the relationship between predictor variables and theEvery increase of 1 mm in periodontal attachment loss resulted in outcome of interest. In addition, our methodology considered thea decrease of approximately 0.5 score on the pain scale. Model 2 subject as the unit of analysis to avoid limitations previously describedalso 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 thepain 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 suchassess this interaction were the main motivations for the present study. measures, it is possible to mention the use of a numeric visual analogOur results strongly suggest that periodontal disease gradually and scale for the classification of pain intensity and the selection of patientsinversely affects pain intensity (ie, the more severe the periodontal among individuals seeking regular treatment (ie, without acute pulpcondition, 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 eliminatehigher results for periodontal involvement (periodontal attachment differences related to individual pain sensation. Some individuals mayloss and gingival recession) responded with lower pain intensity scores have referred higher or lower degrees of pain in any of their teethon the PST. This effect was constant (ie, pain response to the PST regardless of the periodontal condition. In this context, the design ofdecreased gradually with increases in periodontal attachment loss a new study using teeth as controls in each individual could complementand gingival recession values). The plausibility of the relationship our findings. However, from a different perspective, if there really wasamong 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 biasamong 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 onlytial role of pulp recession as a protection mechanism. Periodontal lower incisors were analyzed. The inclusion of posterior and/or upperattachment loss and gingival recession result in an increased exposure teeth would possibly modify the results. Conversely, based on theof cementum and dentin. The exposure of dentinal tubules and the strength of association observed, it is plausible that the correlationcontinuous 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 [cavitydentinal tubules to be open to allow fluid flow. Changes in temperature test]) measure pulp nerve responses only, not pulp blood flow. Thesetend to influence dentinal fluid flow and, subsequently, the mechanical tests measure the presence of neural response in the pulp but do notstimulation of pulp nerves (15–19). Enamel and dentin are thermal provide information on vascular health (21). Our findings suggestinsulators (20) known to interfere with the passage of cold tempera- that teeth with lower pain levels in response to the PST have a decreasedtures; therefore, teeth with closed dentinal tubules and substantial pulp neural response. This hypothesis has been confirmed byTABLE 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
  4. 4. Clinical ResearchVaitkeviciene et al (27) in a morphometric study using light microscopy 5. Zehnder M. Endodontic infection caused by localized aggressive periodontitis:with nerve fibers from the human dental pulp. Those authors concluded a case report and bacteriologic evaluation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:440–5.that the decreased sensitivity of periodontally diseased teeth might be 6. Ehnevid H, Jansson LE, Lindskog SF, Bloml€f LB. Periodontal healing in relation to orelated to the degeneration of myelinated nerve fibers in the pulp. radiographic attachment and endodontic infection. J Periodontol 1993;64: Also, in the presence of pulp disease, nerve tissues are the last to 1199–204.degenerate, a fact that was first shown in the 1970s by Torneck, using 7. Jansson LE, Ehnevid H, Lindskog SF, Bloml€f LB. Radiographic attachment in oelectron microscopy (28). In other words, pulp nerve fibers may main- periodontitis-prone teeth with endodontic infection. J Periodontol 1993;64: 947–53.tain their structural identity even in the presence of advanced pulpitis or 8. Jansson L, Ehnevid H, Lindskog S, Bloml€f L. The influence of endodontic infection oconsiderable destruction of other pulp tissue components. In this way, on progression of marginal bone loss in periodontitis. J Clin Periodontol 1995;22:in our sample, an advanced process of vascular degeneration was also 729–34.probably present. Blood supply and vascular status can only be 9. Hulley SB, Cummings SR, Browner WS, Grady DG, Newman TB. Designing Clinical Research, 3rd ed. Philadelphia: Lippincott Williams Wilkins; 2007.measured using pulp vitality tests (21), such as the laser Doppler 10. Susin C, Haas AN, Oppermann RV, Haugejorden O, Albandar JM. Gingival recession:flow meter (25, 29) and pulse oximetry (30). The assessment of epidemiology and risk indicators in a representative urban Brazilian population.vascular health was beyond the scope of the present study. J Periodontol 2004;75:1377–86. The present findings add to the existing body of knowledge by 11. Haas AN, R€sing CK, Oppermann RV, Albandar JM, Susin C. Association among ocontributing to an improved understanding and interpretation of diag- menopause, hormone replacement therapy, and periodontal attachment loss in southern Brazilian women. J Periodontol 2009;80:1380–7.nostic tests used in endodontically and periodontally compromised 12. Alomari FA, Al-Habahbeh R, Alsakarna BK. Responses of pulp sensibility tests duringteeth, with possible influences on treatment planning. Moreover, the orthodontic treatment and retention. Int Endod J 2011;44:635–43.relationship between periodontal and endodontic conditions affecting 13. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psy-tissues reinforces the importance of a global, integrated vision of health chol Bull 1979;86:420–8. 14. Staquet MJ, Durand SH, Colomb E, et al. Different roles of odontoblasts and fibro-care among dental practitioners (31). blasts in immunity. J Dent Res 2008;87:256–61. In sum, dentists should be aware of the fact that, in the presence of 15. N€rhi MV. The characteristics of intradental sensory units and their responses to ahigh levels of periodontal attachment loss, pulp tissues may be altered, stimulation. J Dent Res 1985;64:564–71.a finding that has already been shown in the literature through bacteri- 16. N€rhi MV, Hirvonen T. The response of dog intradental nerves to hypertonic solu- aological evaluation (5), pointing to the need for combined treatments. tions of CaCl2 and NaCl, and other stimuli, applied to exposed dentine. Arch Oral Biol 1987;32:781–6.Retrospective studies have already shown the influence of endodontic 17. Byers MR, N€rhi MV, Mecifi KB. Acute and chronic reactions of dental sensory nerve ainfection on the progression of marginal bone loss in periodontitis as fibers to cavities and desiccation in rat molars. Anat Rec 1988;221:872–83.well as on the healing process after scaling and root planing (6–8). 18. Chidchuangchai W, Vongsavan N, Matthews B. Sensory transduction mechanismsTherefore, it is essential to recognize that pulp inflammation and responsible for pain caused by cold stimulation of dentine in man. Arch Oral Biol 2007;52:154–60.necrosis may reflect negatively on the periodontium in terms of both 19. Lin M, Liu S, Niu L, Xu F, Lu TJ. Analysis of thermal-induced dentinal fluid flow andthe pathophysiological process and treatment response. its implications in dental thermal pain. Arch Oral Biol 2011;56:846–54. The present findings allow us to conclude that periodontal attach- 20. Brown WS, Dewey WA, Jacobs HR. Thermal properties of teeth. J Dent Res 1970;49:ment loss and gingival recession strongly influence patient response to 752–5.PST. This effect is constant, with gradual decreases in pain response, as 21. Jafarzadeh H, Abbott PV. Review of pulp sensibility tests, part I: general information and thermal tests. Int Endod J 2010;43:738–62.a result of changes caused by increases in periodontal attachment loss 22. Oi T, Saka H, Ide Y. Three-dimensional observation of pulp cavities in the maxillaryand gingival recession. first premolar tooth using micro-CT. Int Endod J 2004;37:46–51. 23. Hujoel PP, DeRouen TA. Determination and selection of the optimum number of sites and patients for clinical studies. J Dent Res 1992;71:1516–21. 24. Altman DG, Bland JM. Statistics notes. Units of analysis. BMJ 1997;314:1874. Acknowledgments 25. Chen E, Abbott PV. Evaluation of accuracy, reliability, and repeatability of five dental The authors deny any conflicts of interest related to this study. pulp tests. J Endod 2011;37:1619–23. 26. Rothman KJ, Greenland S. Modern Epidemiology, 2nd ed. Philadelphia: Lippincott Williams Wilkins; 1998. 27. Vaitkeviciene I, Vaitkevicius R, Paipaliene P, Zekonis G. Morphometric analysis of References pulpal myelinated nerve fibers in human teeth with chronic periodontitis and 1. Reit C, Petersson K. Diagnosis of pulpal and periapical disease. In: Bergenholtz G, root sensitivity. Medicina (Kaunas) 2006;42:914–22. Hørsted-Bindslev P, Reit C, eds. Textbook of Endodontology, 2nd ed. Oxford: Wiley 28. Torneck CD. Changes in the fine structure of the human dental pulp subsequent to Blackwell; 2010:235–54. carious exposure. J Oral Pathol 1977;6:82–95. 2. Olgart L, Bergenholtz G. The dentin-pulp complex: structures, functions and 29. Kijsamanmith K, Timpawat S, Vongsavan N, Matthews B. A comparison between red responses to adverse influences. In: Bergenholtz G, Hørsted-Bindslev P, Reit C, and infrared light for recording pulpal blood flow from human anterior teeth with eds. Textbook of Endodontology, 2nd ed. Oxford: Wiley Blackwell; 2010:11–32. a laser Doppler flow meter. Arch Oral Biol 2011;56:614–8. 3. Trabert KC, Kang MK. Diagnosis and management of endodontic-periodontal 30. Karayilmaz H, Kirziolu Z. Comparison of the reliability of laser Doppler flowmetry, g lesions. In: Newman MG, Takei H, Klokkevold PR, et al., eds. Carranza’s Clinical pulse oximetry and electric pulp tester in assessing the pulp vitality of human teeth. Periodontology, 11th ed. Philadelphia: Elsevier; 2012:507–10. J Oral Rehabil 2011;38:340–7. 4. Harrington GW, Steiner DR, Ammons WF. The periodontal-endodontic controversy. 31. Shanley DB. Convergence towards higher standards in international dental educa- Periodontol 2000 2002;30:123–30. tion. N Y State Dent J 2004;70:35–9.JOE — Volume 38, Number 5, May 2012 Factors Associated with Responses to Pulp Sensibility Test 583