Bleeding on Probing As It Relates to Smoking Status in Patients Enrolled in Supportive Periodontal Therapy for at Least 5&#X

J Clin Periodontol 2015; 42: 150–159 doi: 10.1111/jcpe.12344

Christoph A. Ramseier1, Bleeding on Probing as it relates Damiano Mirra1, Christian Schutz€ 1, Anton Sculean1, Niklaus P. Lang1, Clemens Walter2 and to smoking status in patients Giovanni E. Salvi1 1Department of Periodontology, School of Dental Medicine, University of Bern, Bern, enrolled in supportive Switzerland; and 2Department of Periodontology Endodontology and Cariology, School of Dental Medicine, University of periodontal therapy for at least Basel, Basel, Switzerland 5 years

Ramseier CA, Mirra D, Schutz€ C, Sculean A, Lang NP, Walter C, Salvi GE. Bleeding on Probing as it relates to smoking status in patients enrolled in supportive periodontal therapy for at least 5 years. J Clin Periodontol 2015; 42: 150–159. doi: 10.1111/jcpe.12344.

Abstract Aim: To relate the mean percentage of bleeding on probing (BOP) to smoking status in patients enrolled in supportive periodontal therapy (SPT). Materials and Methods: Retrospective data on BOP from 80741 SPT visits were related to smoking status among categories of both periodontal disease severity and progression (instability) in patients undergoing dental hygiene treatment at the Medi School of Dental Hygiene (MSDH), Bern, Switzerland 1985–2011. Results: A total of 445 patients were identified with 27.2% (n = 121) being smokers, 27.6% (n = 123) former smokers and 45.2% (n = 201) non-smokers. Mean BOP statistically significantly increased with disease severity (p = 0.0001) and periodontal instability (p = 0.0115) irrespective of the smoking status. Periodon- tally stable smokers (n = 30) categorized with advanced periodontal disease demonstrated a mean BOP of 16.2% compared to unstable smokers (n = 15) with a mean BOP of 22.4% (p = 0.0291). Assessments of BOP in relation to the percentage of sites with periodontal probing depths (PPD) ≥4 mm at patient-level yielded a statistically significantly decreased proportion of BOP in smokers compared to non-smokers and former smokers (p = 0.0137). Conclusions: Irrespective of the smoking status, increased mean BOP in SPT Key words: bleeding on probing; cigarette patients relates to disease severity and periodontal instability while smokers dem- smoking; supportive periodontal therapy onstrate lower mean BOP concomitantly with an increased prevalence of residual PPDs. Accepted for publication 25 November 2014

Conflict of interest and source of Bleeding on probing (BOP) has been 1971, Lang et al. 1986, 1990). In funding statement used in clinical practice as a brief, patients with a mean percent- diagnostic tool for many years to age of BOP ≤20% have been The authors declare that there are no evaluate both gingival inflammation acknowledged as periodontally sta- conflicts of interest in this study. and periodontal stability in patients ble while a mean BOP of ≥30% This study was supported by the Swiss attending supportive periodontal represented a greater risk for peri- National Program to Stop Smoking, € Switzerland. therapy (SPT) (Muhlemann & Son odontal disease progression and

150 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Bleeding on probing and smoking status 151 subsequent tooth loss (Joss et al. aim of this study was to evaluate the determined at the end of active peri- 1994, Matuliene et al. 2008). mean patient-level BOP as it relates odontal therapy and at each SPT Periodontal diseases are highly to the smoking status in a sample of visit based on the patient’s periodon- prevalent among smokers (Tomar & patients enrolled in SPT provided by tal parameters such as the percent- Asma 2000, Gatke et al. 2012). The dental hygiene students at the Medi age of BOP and the severity of impact of smoking on periodontal School of Dental Hygiene (MSDH), periodontal disease. Subsequent SPT diseases and their suspected patho- Bern, Switzerland. intervals were determined according genesis has continuously been to the BOP at each visit. With summarized within comprehensive patients demonstrating a BOP of less Materials and Methods literature reviews (Rivera-Hidalgo than 20%, the previously determined 2003, Palmer et al. 2005, Warn- SPT interval was increased by akulasuriya et al. 2010, Chambrone Study sample 1–2 months while not exceeding a et al. 2014). Due to the impaired This study was designed in continua- maximum of 12 months. In contrast, outcomes following active periodon- tion of the previously reported retro- with patients demonstrating a BOP tal treatment and lower attendance spective longitudinal cohort study of more than 20%, the previously compliance with SPT, the mainte- based on demographic and clinical determined SPT interval was nance of periodontal stability in cig- data collected from patient records decreased by 1–2 months down to a arette smokers remains to be a at the Medi School of Dental minimum of 3 months, respectively. difficult task (Matuliene et al. 2010, Hygiene (MSDH), Bern, Switzerland Meyer-Baumer€ et al. 2012, Ramseier over the years 1985–2011 (Ramseier Clinical records et al. 2014). et al. 2014). All patients treated at Periodontal tissues are well vas- the MSDH aged 20 years or older, Demographic data and medical his- cularised (Egelberg 1966). Upon bac- returning at least 5 years for SPT, tory information as recorded at the terial challenge of the dental biofilm, with known tobacco use status, and initial examination were gathered the clinical signs of tissue inflamma- complete information from clinical from the patient records such as the tion such as the changes in gingival records were considered for the general health status, the use of colour, the gingival swelling or the analysis. However, patients reporting medications, and tobacco use increase of gingival crevicular fluid to be diagnosed with Diabetes (Type recorded as smoker (i.e. current smo- flow are mainly caused by alterations I and II) or taking medication ker), former smoker (i.e. self- of the periodontal vascular system potentially affecting gingival bleed- reported ex-smoker), or non-smoker (Nair et al. 2003, Scott & ing were excluded from the study. (i.e. never smoker). Further informa- Singer 2004, Apatzidou et al. 2005, Due to the retrospective nature of tion was collected such as the dura- Mokeem et al. 2014). In cigarette this study no ethical approval from tion of active periodontal therapy, smokers, however, current evidence the Swiss Ethics Committee of the the initial interval for SPT as deter- suggests that as a consequence of Canton of Bern, Switzerland was mined following active periodontal tobacco use periodontal inflamma- mandatory. Further permission to treatment, and the duration of SPT tory responses to the bacterial chal- conduct this study was granted by provided at the MSDH. Retrospec- lenges are generally modified the Medi School of Dental Hygiene tive clinical data gathered from the (Meekin et al. 2000, Rezavandi et al. (MSDH), City of Bern, Switzerland. patient records at each SPT visit 2002, Mavropoulos et al. 2003, Shi- included the percentage of BOP, the mazaki et al. 2006, Farina et al. number of teeth and the number of 2013). The impact of smoking Patient care at the MSDH sites with periodontal probing depths includes various alterations on vas- As previously reported, upon their (PPD) of 4, 5 and ≥6 mm at six sites cular tissue metabolism, immune entry at the MSDH, all patients were per tooth respectively. According to response, vasoconstriction, angiogen- fully examined according to the stan- the standard of care at the MSDH, esis or oxygenation profiles even dard of care and diagnosed for oral sites with PPD 0–3 mm were not though a distinct smoking associated diseases (Ramseier et al. 2014). Peri- recorded. pathohistological correlate seems to odontally healthy patients were pro- be lacking (Preber & Bergstrom€ vided with adequate prophylaxis 1985, Bergstrom€ & Bostrom€ 2001, while periodontally diseased patients Severity of periodontal disease Nair et al. 2003, Scott & Singer were treated with non-surgical peri- For the purpose of this study and in 2004, Apatzidou et al. 2005, Souza odontal therapy by the dental hygiene order to relate patient-level mean et al. 2012, Liu et al. 2014). students. Each periodontal patient BOP to smoking status among sever- With potential significance to the was re-evaluated and treated with ity of periodontal disease, all clinical monitoring of smokers dur- periodontal surgery when indicated. patients were categorized according ing SPT, consequently, patient-level Following prophylaxis or active to their baseline PPD either with I) BOP may be lower leading to chal- periodontal therapy, all patients were “no or mild periodontal disease”, II) lenges regarding diagnosis and enrolled into the MSDH’s suppor- “moderate periodontal disease” and assessment of periodontal disease tive periodontal therapy (SPT) pro- III) “advanced periodontal disease”. progression and possibly to false gram according to the MSDH’s Patients within category I) presented negative interpretation (Preber & standards. with PPD of ≤4 mm (no site exceed- Bergstrom€ 1986, Dietrich et al. 2004, Throughout the study period, ing PPD of 4 mm) while patients Liu et al. 2014). Therefore, the main the appropriate SPT intervals were within category III) presented with © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 152 Ramseier et al.

PPD of ≥4 mm and at least 10 sites levels (non-smokers, former smokers distributed and were representative of PPD ≥6 mm. Consequently, and smokers) was tested using of the Swiss population in this period patients not fitting into the catego- approximate F-tests. (BAG 2013a,b). The mean age of the ries I) or III) were selected into cate- In order to analyse dependences entire patient sample was 42.6 gory II) demonstrating PPD of of categorical and categorized (11.5) years with a range of 20 to ≥4 mm and a maximum of 9 sites numerical variables with the binary- 81 years while 55.1% (n = 245) were with PPD of ≥6 mm. coded variable for periodontal stabil- females (Table 1). Of 445 patients, ity and instability, Fisher’s exact tests 27.2% (n = 121) were registered as were performed. When periodontal smokers, 27.6% (n = 123) former Periodontal stability/instability stability was tested against the smok- smokers, and 45.2% (n = 201) non- Acknowledging possible differences ing status, a Chi-square-test was smokers, respectively. The mean of mean patient-level BOP among applied. The association of smoking duration of active periodontal patients demonstrating periodontal status and periodontal stability was treatment from the entire sample was stability versus instability and further further analysed by computing odds 5.8 (SD 6.5) months while the relating their mean BOP with smok- ratios and confidence intervals using subsequent mean duration of SPT ing status, a further subgroup of Wald’s approximation. was 11.9 years ranging from 5 patients with higher risk for peri- The Kruskal–Wallis test was used to 25.7 years. The overall mean %- odontal disease progression (“peri- to assess the relationship between compliance was 66.9% with no statis- odontal instability”) was identified binary-coded BOP and mean per- tical significant difference among from this sample. Based on the out- centage of sites with PPD of ≥4 mm. non-smokers, former smokers and comes of a retrospective study by Due to the purely exploratory smokers in this sample (p = 0.061). Matuliene et al. (2008) demonstrat- nature of this data analysis, no Bon- ing an increased risk for periodontal ferroni correction for multiple testing disease progression in SPT patients was applied. Each hypothesis was Baseline clinical data presenting with residual sites with tested at the significance level of 0.05. Baseline clinical data from the initial PPD of ≥6 mm, periodontally unsta- examination are summarized in ble patients in this study were Table 2. The overall mean number Results selected when presenting with an of teeth in all patients was 26.7 increasing number of periodontal From 883 patients previously (SD 3.7) while the mean number sites with PPD of ≥6 mm over a per- reported by Ramseier et al. (2014) a of teeth in non-smokers, former iod of 5 years following their first total of 445 clinical records were smokers and smoker was 27.1 SPT visit (Matuliene et al. 2008). In selected for the analysis (Fig. 1) (SD 3.6), 26.2 (SD 4.3), and order to corroborate this selection, (Ramseier et al. 2014). Collecting ret- 26.5 (SD 3.1), respectively, with- periodontal stability versus instability rospective data on 80741 SPT visits out statistical significant difference was correlated with tooth loss over from this sample resulted in an obser- among non-smokers and former 5 years. vation period of 25.7 years ranging smokers (p = 0.1079) or smokers from 1985 to 2011. Gender, age and (p = 0.1043). smokers’ distribution were normally Statistical analysis The statistical analysis was performed using R (R-3.1.0 for Windows; Free Software Foundation, Boston, MA, USA, Statistics Department of the University of Auckland, USA). Descriptive statistics were performed for all patients as well as within the subgroups of smokers, former smokers and non-smokers and patients categorized with no or mild -, moderate - and advanced periodontal disease. Mean differences between patient-level percentages of BOP and smoking status were studied using classic one-way ANOVA. The null hypotheses of no mean difference between smokers and non-smokers or former smokers were tested by approximate t-tests or the Mann Whitney test if standard deviations among the subgroups were assumed Fig. 1. Patient selection diagram: Of 883 patients previously presented by Ramseier to be different. The null hypothesis et al. (2014), a group of 445 patients 20 years and older was identified returning at of equal means across all smoking least 5 years for SPT (at least 2 visits) (Ramseier et al. 2014). © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Bleeding on probing and smoking status 153

Table 1. Baseline demographic data from the initial examination and unadjusted qualitative analysis of 445 patients (non-smokers, former smokers and smokers) attending SPT for at least 5 years All patients Non-smokers Former smokers Smokers p-Values between (A) (B) (C) A&B&C n = 445 (100%) n = 201 (45.2%) n = 123 (27.6%) n = 121 (27.2%) (unadjusted)

Mean (SD) Min–Max Mean (SD) Mean (SD) Mean SD p-Values

Age at initial examination 42.6 (11.5) 20–81 44.5 (13.5) 44.4 (11.2) 39.0 (9.8) 0.0001 (years) Gender (female) 245 (55.1%) N.A. 135 (67.2%) 47 (38.2%) 63 (52.1%) <0.0001† Duration of active periodontal 5.8 ( 6.5) 0.03–96.5 5.4 (3.6) 4.9 (4.1) 7.2 (11.7) 0.0237 treatment (months) Number of SPT visits 19.7 (12.2) 2–70 19.4 (10.8) 19.2 (11.5) 20.5 (14.2) 0.6646 Mean SPT interval (months) 5.5 (2.3) 3–12 5.8 (2.3) 5.7 (2.3) 5.2 (2.4) 0.0484 Duration of SPT (years) 11.9 (5.5) 5.0–25.7 12.4 (5.6) 12.0 (5.5) 11.5 (5.5) 0.3333 %-Compliance 66.9% (21.7) 10.5–122.6% 70.1% (21.1) 66.1% (21.3) 64.6% (22.8) 0.0610

†Pearson’s Chi Square of independence among non-smokers, former smokers and smokers = 21.04 (p < 0.0001). SD, standard deviation; SPT, supportive periodontal therapy; %-Compliance (attended visits as a percentage of expected visits).

Table 2. Baseline clinical data from the initial examination and unadjusted qualitative analysis of 445 patients attending SPT for 5 or more years categorized either with I) no or mild -, II) moderate - or III) advanced periodontal disease All patients I) No or Mild II) Moderate III) Advanced p-Values Periodontal Periodontal Periodontal between Disease Disease PPD ≥4mm Disease PPD ≥4mm A&B&C PPD ≤4mm <10 sites with ≥10 sites with (unadjusted) (A) PPD ≥6mm PPD ≥6mm (B) (C) n = 445 (100%) n = 51 (11.5%) n = 242 (54.4%) n = 152 (34.2%) Value (SD) Value (SD) Value (SD) Value (SD) p-Values

Number of non-smokers 23 (45.1%) 117 (48.3%) 61 (40.1%) Number of former smokers 12 (23.5%) 65 (26.9%) 46 (30.3%) 0.5082† Number of smokers 16 (31.4%) 60 (24.8%) 45 (29.6%) Mean number of teeth All patients 26.7 (3.7) 28.3 (2.7) 27.2 (3.4) 25.8 (4.0) 0.0010 Non-smokers 27.1 (3.6) 28.9 (2.6) 27.3 (3.7) 26.5 (3.5) 0.1281 Former smokers 26.2 (4.3) (n.s.) 26.2 (3.6) (n.s.) 27.3 (2.8) (n.s.) 25.1 (5.2) (n.s.) 0.0736 Smokers 26.5 (3.1) (n.s.) 28.4 (1.8) (n.s.) 27.1 (3.3) (n.s.) 25.8 (2.9) (n.s.) 0.0199 Mean % of sites of PPD 4 mm All patients 16.2 (10.3) 5.9 (4.7) 14.5 (9.6) 22.4 (8.9) <0.0001 Non-smokers 15.7 (9.7) 5.1 (3.4) 14.4 (8.8) 22.2 (8.3) <0.0001 Former smokers 16.7 (10.8) (n.s.) 5.4 (3.9) (n.s.) 13.9 (9.4) (n.s.) 23.6 (9.7) (n.s.) <0.0001 Smokers 16.5 (10.9) (n.s.) 7.5 (6.5) (n.s.) 15.1 (11.4) (n.s.) 21.5 (8.8) (n.s.) <0.0001 Mean % of sites of PPD 5 mm All patients 7.5 (7.5) 0 4.4 (4.0) 15.0 (7.1) <0.0001 Non-smokers 6.7 (6.5) 0 4.1 (3.6) 14.1 (5.3) <0.0001 Former smokers 7.8 (7.1) (n.s.) 0 4.7 (4.0) (n.s.) 14.1 (6.4) (n.s.) <0.0001 Smokers 8.7 (9.3) 0 4.7 (4.7) 17.1 (9.3) (p = 0.0407) <0.0001 (p = 0.0234) (n.s., p = 0.345) Mean % of sites of PPD ≥6mm All patients 6.5 (10.0) 0 1.2 (1.6) 17.2 (10.7) <0.0001 Non-smokers 5.3 (8.6) 0 1.0 (1.4) 15.6 (9.4) <0.0001 Former smokers 7.1 (10.9) (n.s.) 0 1.2 (1.4) (n.s.) 17.3 (12.2) (n.s.) <0.0001 Smokers 7.9 (11.0) 0 1.5 (2.0) 19.3 (10.7) <0.0001 (p = 0.0203) (n.s., p = 0.0831) (n.s., p = 0.0627)

†Pearson’s Chi Square of independence among patients categorized with no/mild, moderate or advanced periodontal disease = 3.304 (p = 0.5082). Approximate t-tests within the respective subgroups among non-smokers and former smokers or smokers revealed signiﬁcant differences (p-Value) or no signiﬁcant differences (n.s.). PPD, periodontal probing depth; SD, standard deviation; SPT, supportive periodontal therapy; I-III) patients categorized with I) No or Mild Periodontal Disease: PPD ≤4 mm, II) Moderate Periodontal Disease: PPD ≥4 mm and <10 sites with PPD ≥6 mm, III) Advanced Peri- odontal Disease: PPD ≥4 mm and ≥10 sites with PPD ≥6 mm.

100% (a) T1: Inial exam signiﬁcantly less BOP compared with T2: Following acve periodontal treatment non-smokers (p = 0.038) in the cate- 80% T3: First SPT visit gory of moderate periodontal dis- T4: 5-year SPT visit * ease, no statistically signiﬁcant 4 mm * ≥ 60% *

ons of sites ons of difference of mean BOP was found * 40% among smoking status within the

with PPD *

Propor * remaining disease categories.

20% Mean BOP and periodontal stability/ 0% T1 T2 T3 T4 T1 T2 T3 T4 T1 T2 T3 T4 instability

Non-smokers Former-smokers Smokers To further relate patient-level mean n = 201 n = 123 n = 121 BOP to smoking status and “peri- 100% (b) 7.1 10.8 7.8 12.2 9.1 odontal stability”, a subgroup of 12.7 17.2 13.9 15.9 19.2 22.5 23.9 = 20.1 18.7 patients (n 92) was selected with a 80% 19.5 20.8

6 mm 20.5 21.6 ≥ 24.2 22.9 higher risk for periodontal disease 24.0 25.4 24.6 26.3 progression (“periodontal instabil- 60% % ≥6 mm ity”) demonstrating an increasing

ons of sites ons of % 5 mm

≥ 40% number of sites with PPD of 6mm 72.1 74.2 69.7 66.7 66.2 70.2 % 4 mm 62.0 61.2

Propor 56.7 57.4 over 5 years following their first SPT 52.9 49.8 20% visit. Periodontally unstable patients with PPD 4 mm, 5 mm and mm 5 mm, 4 with PPD demonstrated statistically signifi- 0% T1 T2 T3 T4 T1 T2 T3 T4 T1 T2 T3 T4 cantly higher rates of tooth loss (p = 0.0018), BOP (p = 0.0115) and Fig. 2. (a) Proportions of sites with initial periodontal probing pocket depths (PPD) lower %-compliance (p = 0.0258) ≥ and residual PPD of 4 mm in 445 patients according to smoking status. T1: initial compared with periodontally stable examination, T2: following active periodontal treatment, T3: first supportive periodon- patients (n = 383). The association tal therapy (SPT) visit, T4: 5-year SPT visit. (b) Proportions of sites with 4, 5 and ≥6 mm at T1, T2, T3 and T4. *statistically significant different reduction of PPD of smoking status with periodontal ≥4mm(p < 0.005). instability was close to statistical significance (p = 0.0548). However, computed odds ratios (OR) using Proportions of periodontal sites examination (T1), the re-evaluation Wald’s approximation revealed an with PPD of 4, 5, and ≥6mm following active periodontal treat- OR of 1.51 (95% confidence interval were calculated at patient-level. ment (T2), the first supportive peri- (CI) 0.86–2.7) for smokers and 1.93 Overall, patients presented with odontal therapy visit (T3) and the (95% CI 1.12–3.4) for former smok- 16.2% (SD 4.3) PPD of 4 mm, fist 5-year SPT visit (T4) (Fig. 2). In ers to be periodontally unstable. 7.5% (SD 4.3) PPD of 5 mm and all non-smokers, former smokers Mean BOP over 5 years SPT of 6.5% (SD 4.3) PPD of ≥6mm and smokers a significant reduction periodontally stable and unstable respectively. Within the correspond- of percentage of PPD ≥4 mm was patients initially categorized with ing subgroups of non-smokers, for- achieved between T1 and T2 as well advanced periodontal disease are mer smokers and smokers, the latter as T2 and T3 (p < 0.05), respec- presented in Figure 3. Non-smokers, demonstrated increased proportions tively. former smokers and smokers catego- of periodontal sites with PPD of rized as periodontally stable and 5mm (p = 0.0234) and ≥6mm unstable demonstrated a mean BOP = Mean BOP and severity of periodontal of 19.4%, 18.4%, 16.2% and 22.6%, (p 0.0203) when compared with disease non-smokers. 23.3%, 22.4% respectively. Between- The mean percentage of sites with Mean BOP related to periodontal group analysis of the smoking status PPD 4, 5, and ≥6 mm among disease disease category and smoking status within each category of periodon- categories I), II) and III) and the are presented in Table 3. Overall, tally stable and unstable patients corresponding smoking status are mean BOP statistically significantly using one-way ANOVA, however, did presented in Table 2. Smokers within differed (p=0.0001) between the not reach statistical significance. the category of advanced periodontal disease categories I) and II) as well Overall, periodontally unstable disease presented with a statistically as I) and III) respectively. With all patients presented with a mean BOP significantly higher mean % of PPD the SPT visits up to 27.5 years and of >20% while periodontally stable of 5 mm when compared with non- the subset of SPT visits over the first patients (n = 101) demonstrated a smokers from the same disease cate- 5 years and the subsequent 5– mean BOP of <20% (p = 0.0115). gory (p = 0.0407). 25.7 years following the first SPT In particular, periodontally stable visit, respectively, no statistically sig- smokers (n = 30) demonstrated a nificant difference of mean BOP was mean BOP of 16.2% yielding a sta- Periodontal probing depths (PPD) found between non-smokers, former tistically significant difference The proportion of sites with both smokers and smokers. Furthermore, (p = 0.0291) compared to periodon- initial and subsequent residual PPD with the exception of former tally unstable smokers (n = 15) with of ≥4 mm were assessed at the initial smokers demonstrating statistically a mean BOP of 22.4%. In contrast,

Table 3. Mean percentage of bleeding on probing (BOP) and unadjusted qualitative analysis of 445 patients categorized with either (I) no or mild -, (II) moderate -, or (III) advanced periodontal disease attending a total of 80741 SPT visits up to 25.7 years BOP All patients I) no or Mild II) Moderate III) Advanced p-Values Periodontal Periodontal Periodontal between Disease Disease PPD ≥5mm Disease PPD ≥5mm A&B&C PPD ≤4mm <10 sites with ≥10 sites with (unadjusted) (A) PPD ≥6mm PPD ≥6mm (B) (C) n = 445 (100%) n = 51 (11.5%) n = 242 (54.4%) n = 152 (34.2%) Mean (SD) Mean (SD) Mean (SD) Mean (SD) p-Values

At all SPT visits up to 27.5 years All patients 17.9 (14.8) 13.5 (12.3) 18.7 (14.9) 18.0 (15.0) 0.0001 Male 18.2 (15.5) 13.0 (12.3) 19.3 (15.6) 18.2 (15.7) 0.0001 Female 17.7 (14.3) 13.9 (12.4) 18.2 (14.4) 18.3 (9.5) 0.0001 Non-smokers 18.6 (14.8) 14.4 (12.1) 19.5 (15.0) 18.5 (14.8) 0.0001 Former smokers 17.4 (14.8) (n.s.) 15.3 (11.7) (n.s.) 17.2 (14.0) (n.s.) 17.8 (15.7) (n.s.) 0.0001 Smokers 17.3 (14.9) (n.s.) 11.4 (12.6) (n.s.) 18.6 (15.7) (n.s.) 17.5 (14.5) (n.s.) 0.0001 At ﬁrst SPT visit All patients 20.2 (15.7) 13.4 (12.1) 21.1 (15.6) 21.2 (16.4) 0.0001 Non-smokers 21.4 (16.9) 9.6 (7.9) 23.8 (16.3) 21.4 (18.9) 0.0001 Former smokers 19.6 (14.4) (n.s.) 17.5 (14.5) (†, n.s.) 18.5 (14.1)* 21.7 (14.9) (n.s.) 0.0001 Smokers 19.0 (14.8) (n.s.) 15.7 (14.3) (†, n.s.) 18.8 (15.2) (n.s.) 20.4 (14.4) (n.s.) 0.0001 Mean over 5 years All patients 19.3 (10.6) 12.6 (8.2) 20.5 (10.6) 19.7 (10.6) 0.0001 Non-smokers 20.2 (11.4) 10.9 (7.2) 21.9 (11.4) 20.4 (11.0) 0.0001 Former smokers 18.7 (9.6) (n.s.) 16.0 (6.8) (n.s.) 18.2 (8.4) (n.s.) 20.2 (11.5) (n.s.) 0.0001 Smokers 18.6 (10.3) (n.s.) 12.6 (10.1) (n.s.) 20.4 (10.8) (n.s.) 18.2 (9.1) (n.s.) 0.0001 Mean over 5–25.7 years All patients 19.2 (14.1) 13.0 (7.8) 20.1 (15.1) 19.7 (13.7) 0.0001 Non-smokers 19.0 (13.8) 13.2 (7.9) 20.8 (15.3) 17.5 (11.7) 0.0001 Former smokers 18.5 (19.2) (n.s.) 15.8 (8.6) (n.s.) 17.4 (10.7) (n.s.) 20.8 (16.1) (n.s.) 0.0001 Smokers 20.1 (15.8) (n.s.) 10.5 (6.7) (n.s.) 21.8 (18.2) (n.s.) 21.4 (13.5) (n.s.) 0.0001

BOP, percentage of bleeding on probing; SD, standard deviation; SPT: supportive periodontal therapy, I-III) patients categorized with I) No or Mild Periodontal Disease: PPD ≤4 mm, II) Moderate Periodontal Disease: PPD ≥4 mm and <10 sites with PPD ≥6 mm, III) Advanced Periodontal Disease: PPD ≥4 mm and ≥10 sites with PPD ≥6 mm. One-way ANOVA between A & B & C and approximate t-tests between A & B or A & C revealed significant differences (p = 0001). Approximate t-tests within the respective subgroups of non-smokers and former smokers or smokers revealed significant differences (*p < 0.05) or no significant differences (n.s.). (†, n.s.) Mann Whitney test with no significant difference. the mean BOP from periodontally BOP than PPD% (negative differ- Discussion stable non-smokers (p = 0.2900) or ences). Kruskal–Wallis test among former smokers (p = 0.1610) in this smoking status revealed a statisti- The findings of this study indicated subgroup were not statistically sig- cally significantly decreased propor- that the mean percentage of BOP in nificantly different. tion of BOP compared to PPD% in patients enrolled in supportive peri- In addition to the mean BOP, the smokers (p = 0.0137). odontal therapy (SPT) was statisti- mean % of sites with PPD of cally significantly increased with ≥4 mm (PPD%) is presented in initial disease severity and periodon- Computing BOP-stability threshold Fig. 3. Comparing PPD% between tal instability irrespective of the non-smokers and smokers revealed In order to estimate thresholds for smoking status. Over an average per- statistically significant differences periodontal stability in non-smokers, iod of 11.9 years, periodontally among patients categorized as both former smokers and smokers using unstable patients demonstrated a periodontally stable (p = 0.0118) and mean BOP and the increase or mean BOP >20% while periodon- unstable (p = 0.0107). Mean differ- decrease of % of sites with ≥6 mm, tally stable patients presented with a ences between BOP and PPD% were simple linear regression models were mean BOP <20% reaching statistical calculated with every patient in computed as presented in Fig. 4. significance. In particular, periodon- order to assess the PPD% in relation Even though the R2 from each regres- tally stable non-smokers and smok- to BOP. Both periodontally stable sion analysis lacks statistical signifi- ers initially categorized with and unstable non-smokers and for- cance in all the subgroups, BOP- advanced periodontal disease dem- mer smokers presented with higher intercepts of 20.3% from all patients onstrated a mean BOP of 19.4% mean values of BOP than PPD% (n = 445), 23.2% from non-smokers and 16.2% respectively. Moreover, (positive differences) while periodon- (n = 201), 23.4% from former smok- when comparing BOP with the mean tally stable and unstable smokers ers (n = 123) and 16.7% from smok- % of sites with PPD ≥4 mm (PPD demonstrated lower mean values of ers (n = 121) were identified. %) within the respective disease © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 156 Ramseier et al.

categories and in particular with smokers, lower mean patient-level BOP was found concomitantly with an increased prevalence of PPD% reaching statistical significance. Con- sequently, the use of BOP alone for monitoring periodontal stability may lead to false negative assumptions in smokers with increased prevalence of residual periodontal pockets during SPT. BOP has been used for many years as an indicator of the host’s periodontal inflammatory response to the dental biofilm. While individ- ≥ ual BOP-positive sites have been Fig. 3. Mean BOP, mean % of periodontal probing depths (PPD) 4 mm and calucat- associated with only a low positive ed difference per smoking status over 5 years SPT in n = 101 periodontally stable and n = 51 periodontally unstable patients initially categorized with advanced periodontal predictive value for periodontal dis- disease. Error indicators specify the standard deviation (SD), calculated negative dif- ease progression (Lang et al. 1986), ferences in both periodontally stable and unstable smokers represent a higher mean % the absence of BOP has been related of PPD ≥4 mm compared to a lower mean BOP. *statistically significant difference at with a high positive predictive value p < 0.05. for periodontal stability (Lang et al. 1990). Claffey & Egelberg (1995) reported that patient-level percentage of BOP could provide more defini- (a) All paents (n = 445) tive information on the overall peri- 10 odontal prognosis (Claffey & 9 8 Intercept: 20.3 Egelberg 1995). For monitoring peri- 7 odontal stability in patients enrolled 6 5 in SPT, both Claffey et al. (1990) 4 and Badersten et al. (1985, 1990) 3 2 reported that SPT patients with a 1 mean BOP of 20–30% yielded a 0 0 20 40 60 80 100 –1 higher risk for periodontal disease –2 progression compared with patients –3 y = 0.0472x – 0.9605 R² = 0.0314 –4 with lower BOP (Badersten et al. –5 1985, 1990, Claffey et al. 1990). A –6 –7 further study by Joss et al. (1994) –8 concluded that a mean patient-level Decreasing (–) and increasing (+) % of sites with ≥6mm PPD –9 ≤ –10 BOP 20% as a threshold predicted Mean BOP (%) periodontal stability in 39 patients maintained over 4.5 years (Joss et al. (b) Non-smokers (n = 201) Former smokers (n = 123) Smokers (n = 121) 10 10 10 1994). Regrettably, however, these 9 9 9 studies (Muhlemann€ & Son 1971, 8 Intercept: 23.2 8 Intercept: 23.4 8 Intercept: 16.7 7 7 7 Badersten et al. 1985, 1990, Lang 6 6 6 et al. 1986, 1990, Claffey et al. 1990, 5 5 5 4 4 4 Joss et al. 1994) on both site-level 3 3 3 and patient-level assessment of BOP 2 2 2 1 1 1 and periodontal stability failed to 0 0 0 020406080100 020406080100 020406080100 adjust for smoking status. The pres- –1 –1 –1 –2 –2 –2 ent study leads to the assumption –3 y = 0.0311x – 0.7219 –3 y = 0.0422x – 0.9894 –3 y = 0.0752x – 1.2572 that in smokers, a lower BOP- –4 R² = 0.024 –4 R² = 0.0217 –4 R² = 0.0528 –5 –5 –5 threshold may need to be associated –6 –6 –6 with periodontal stability. A mean –7 –7 –7 –8 –8 –8 BOP of 16.2% was found in peri- Decreasing (–) and increasing (+) % of sites with ≥6 mm PPD –9 Decreasing (–) and increasing (+) % of sites with ≥6 mm PPD –9 Decreasing (–) and increasing (+) % of sites with ≥6 mm PPD –9 odontally stable patients from this –10 –10 –10 Mean BOP (%) Mean BOP (%) Mean BOP (%) sample initially categorized with advanced periodontal disease. Fur- Fig. 4. Linear regressions of decreasing () and increasing (+) % of sites with peri- ≥ thermore, assessing all the smokers odontal probing depths (PPD) 6 mm and mean % of sites with bleeding on prob- = ing (BOP) in (a) all (n = 445) patients and (b) non-smokers, former smokers and (n 121) on their decreasing or smokers attending SPT for 5–25.7 years. Intercepts indicate suspected thresholds for increasing % of sites ≥6 mm, a cor- periodontal stability at their respective mean BOP overall (a) and per smoking responding BOP-threshold of 16.7% status (b). was found. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Bleeding on probing and smoking status 157

For the purpose of their study, consumption and time since cessa- due to impaired outcomes following Joss et al. (1994) identified periodon- tion was not recorded with our sam- active periodontal treatment and tally unstable patients with site-level ple. The patients’ smoking status as lower compliance with SPT, the periodontal clinical attachment loss recorded at their first visit was not maintenance of periodontal stability (CAL) of ≥2 mm measured by one updated throughout the study. Fur- in cigarette smokers remains chal- calibrated examiner over the course thermore, the numbers of cigarettes lenging. Therefore, with this study, a of the study (Joss et al. 1994). As smoked per day possibly creating a potential issue has been raised. Bet- the database from our study does different host-response on an indi- ter understanding of the relationship not include clinical attachment level vidual level, was not recorded. As of BOP and smoking status may be (CAL) measurements, the same presented by Ramseier et al. (2013), helpful when planning periodontal analysis was not reproducible. Matu- comprehensive tobacco use history therapy and successive SPT visits liene et al. (2008) associated residual taking at the MSDH was imple- with smokers and former smokers. PPD ≥6 mm with more disease pro- mented only in 2002 (Ramseier et al. Particularly in smokers, the selection gression and subsequent tooth loss 2013). Therefore, further information of appropriate SPT intervals seems (Matuliene et al. 2008). We therefore on pack years for both former and to be paramount for the mainte- selected a subgroup of periodontally current smokers to relate BOP with nance of periodontal stability. More- unstable patients with increasing smoking status was not available for over, as periodontal conditions of numbers of sites with PPD ≥6mm this analysis. However, when former smokers in this sample between the first SPT visit and the acknowledging the clinical data from improved compared with smokers, first subsequent SPT visit 5 years non-smokers, former smokers and the importance of smoking cessation later in order to compare these find- smokers in this study, their self- during SPT needs to be re-empha- ings with those of periodontally sta- reported information on smoking sized (Ramseier 2005, Ramseier ble patients without increasing status may still be accurate thus per- et al. 2010, Chambrone et al. 2013, numbers of sites with PPD ≥6 mm. mitting a reliable estimate of the Walter & Friedmann 2013). In the present study, periodontally effects of cigarette smoking on the In conclusion, the results of the unstable patients yielded statistically mean BOP at patient-level (Walter present study indicate that a lower significantly higher rates of tooth et al. 2012). BOP-threshold may be associated loss, BOP and lower compliance Compared with previous retro- with periodontal stability in smok- with SPT. Acknowledging these dif- spective clinical trials on periodontal ers. While a mean BOP ≤20% in ferences among the selection of peri- disease progression comparing peri- non-smokers or former smokers may odontally unstable and stable odontally stable and unstable still reflect periodontal stability, in patients may further provide valid patients, clinical attachment levels smokers with lowered BOP, more estimates of the effects of cigarette and radiographic data had been frequent SPT visits may need to be smoking on the mean BOP at included (Bragger€ et al. 1992, Joss scheduled according to the preva- patient-level. et al. 1994, Matuliene et al. 2008). lence of residual PPDs. A more recent study by Farina In the present study, however, clini- et al. (2011) reported that there were cal attachment levels were not col- Acknowledgements no differences of BOP with both lected nor has any information been smoking status and daily cigarette taken from intra-oral radiographs This study was supported by the consumption in a cohort of peri- used at the MSDH in patients Swiss National Program to Stop odontally diseased patients (Farina enrolled in SPT. Nevertheless, with Smoking, Switzerland. The authors et al. 2011). However, statistically the exception of the radiographic thank Dr. Herbert Hofstetter, Dr. significant differences were found at imaging, the clinical data included in Petra Hofmanner€ and the adminis- site-level where periodontal sites with our analysis reflect the information trative staff of the Medi School of increased PPD yielded a higher clinicians collect at every SPT visit. Dental Hygiene, Bern, Switzerland. probability for BOP than shallow Periodontal probing in all SPT Salome Kobrehel and Petra Staub sites. These findings are in agreement visits have been conducted by dental are acknowledged for their assistance with the present study and a later hygiene students at the MSDH with with the data extraction from the investigation by the aforementioned variable clinical experience poten- patients’ records. Furthermore, Gab- authors (Farina et al. 2013). tially leading to inaccurate measure- riel Fischer is acknowledged for his A few limitations of this study, ments in particular with PPD support with the statistical analysis. however, should be discussed. In the ≥6 mm. As a standard of care at the current analysis, the patients’ smok- MSDH, however, all measurements ing status was categorized according by the dental hygiene students were References to their self-reported data from the re-measured by experienced clinical Apatzidou, D. A., Riggio, M. P. & Kinane, D. F. general medical history either instructors. Consequently, PPD (2005) Impact of smoking on the clinical, recorded as smoker (i.e. current smo- recordings were modified if the first microbiological and immunological parameters ker), former smoker (i.e. self- measurements by the dental hygiene of adult patients with periodontitis. Journal of Clinical Periodontology 32, 973–983. reported ex-smoker) or non-smoker student differed from the one from Badersten, A., Nilveus, R. & Egelberg, J. (1985) (i.e. never smoker). Unfortunately, the instructor. Effect of nonsurgical periodontal therapy. VII. however, a more comprehensive Although periodontal therapy Bleeding, suppuration and probing depth in tobacco use history including rele- may be beneficial for all patients sites with probing attachment loss. Journal of Clinical Periodontology 12, 432–440. vant information on both daily irrespective of the smoking status, © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 158 Ramseier et al.

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Figure S1. Mean number of teeth T1: initial examination, T2: follow- odontally unstable patients initially including standard deviations in 445 ing active periodontal treatment, T3: categorized with moderate and patients according to smoking sta- ﬁrst supportive periodontal therapy advanced periodontal disease (cate- tus. (SPT) visit, T4: 5-year SPT visit. gory II and III). Figure S2. (A) Proportions of sites Figure S3. Mean BOP, mean % of with initial periodontal probing periodontal probing depths (PPD) pocket depths (PPD) and residual ≥4mm and calucated difference per PPD of 4mm, 5mm, or ≥6mm in 353 smoking status over 5 years SPT in Address: periodontally stable patients accord- all patients (353 periodontally stable Christoph A. Ramseier ing to smoking status. (B) Propor- and 92 periodontally unstable). Department of Periodontology School of Dental Medicine tions of sites with initial periodontal Figure S4. Mean BOP, mean % of University of Bern probing pocket depths (PPD) and periodontal probing depths (PPD) Freiburgstrasse 7, 3012 residual PPD of 4mm, 5mm, or ≥4mm and calucated difference per Bern, Switzerland ≥6mm in 92 periodontally unstable smoking status over 5 years SPT in E-mail: [email protected] patients according to smoking status. 306 periodontally stable and 88 peri-

Clinical Relevance disease severity and disease progres- stability may lead to false negative Scientific rationale for the study: sion (instability) irrespective of the assumptions in smokers presenting This study was designed to relate smoking status. In smokers, how- with increased prevalence of residual the mean percentage of bleeding on ever, lower mean patient-level BOP periodontal pockets during SPT. probing (BOP) to the smoking sta- was found concomitantly with an tus in patients enrolled in support- increased prevalence of sites with ≥ ive periodontal therapy (SPT). periodontal probing depths 4 mm. Principal findings: Mean BOP sig- Practical implications:Theuseof nificantly increased with initial BOP alone for monitoring periodontal