J Periodont Res 2014 © 2014 John Wiley & Sons A/S. All rights reserved Published by John Wiley & Sons Ltd

JOURNAL OF PERIODONTAL RESEARCH doi:10.1111/jre.12219

S. Gonzalez1, C. L. Cohen1, Gingival bleeding on M. Galvan 1, F. A. Alonaizan2, S. K. Rich1, J. Slots1 1Graduate Clinic, Ostrow School of Dentistry of USC, Los Angeles, CA, probing: relationship to 2 USA and Graduate Endodontic Clinic, Ostrow School of Dentistry of USC, Los Angeles, CA, change in periodontal pocket USA depth and effect of sodium hypochlorite oral rinse

Gonzalez S., Cohen C. L., Galvan M., Alonaizan F. A., Rich S. K., Slots J. Gingival bleeding on probing: relationship to change in periodontal pocket depth and effect of sodium hypochlorite oral rinse. J Periodont Res 2014; doi: 10.1111/ jre.12219. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Background and Objective: This study evaluated the potential of gingival bleed- ing on probing to serve as a predictor of future periodontal breakdown. It also assessed the ability of 0.25% sodium hypochlorite twice-a-week oral rinse to convert periodontal pockets showing bleeding on probing to nonbleeding sites.

Material and Methods: The study was performed as a randomized, single- blinded, clinical trial in parallel groups. Seven periodontitis patients rinsed twice-weekly for 3 mo with 15 mL of a fresh solution of 0.25% sodium hypochlorite, and five periodontitis patients rinsed with water. The 12 study patients received no subgingival or supragingival scaling. Cloroxâ Regular- Bleach was the source of sodium hypochlorite. At baseline and 3-mo visits, gingival bleeding was assessed within 30 s after probing to full pocket depth using an approximate force of 0.75 N. Results: A total of 470 (38%) of 1230 periodontal pockets in the bleach-rinse group revealed bleeding on probing at the initial visit but not at the 3-mo visit; only 71 (9%) of 828 pockets in the control group became bleeding-negative during the study (p < 0.001). Bleeding on probing in 4- to 7-mm-deep pockets decreased by 53% in the bleach-rinse group but increased by 6% in the water-rinse group (p < 0.001). Ninety-seven pockets showed depth increases of ≥ 2 mm after 3 mo: 60 (62%) of those pockets exhibited bleeding on probing at both the initial and the 3-mo visits; 24 (25%) bled at only one of the two visits; < Jørgen Slots, DDS, DMD, PhD, MS, MBA, and 13 (13%) never demonstrated gingival bleeding (p 0.001). Department of Periodontology and Microbiology, Ostrow School of Dentistry of Conclusions: Persistent gingival bleeding on probing was associated with an USC, Los Angeles, CA 90089-0641, USA increased risk for periodontal breakdown, and the absence of gingival bleeding Tel: +1 213 740 1091 seemed to be a useful, although not perfect, indicator of disease stability. Twice- e-mail: [email protected] weekly oral rinsing with dilute bleach (0.25% sodium hypochlorite) produced a Key words: ; gingival bleeding on significant reduction in bleeding on probing, even in deep unscaled pockets. probing; household bleach; mouthrinse; periodontal treatment; sodium hypochlorite Sodium hypochlorite constitutes a valuable antiseptic in periodontal self-care. Accepted for publication June 21, 2014 2 Gonzalez et al.

Periodontitis remains a diagnostic and Other types of diagnostic tests to or supragingival scaling before or dur- therapeutic challenge. Dental profes- predict periodontal breakdown have ing the study in order to stress-test sionals lack accurate biomarkers to also been evaluated. A high score of 4 the boundary of effectiveness of predict ongoing or future progression in the Community Periodontal Index sodium hypochlorite oral rinse. of , and practitio- of Treatment Needs screening system ners often resort to surgery to prevent yielded a low positive-predictive value Material and methods an anticipated scenario of continued for progressive periodontitis, but low attachment loss. Successful treatment sextant scores of 0–2 provided a pre- The details of the material and meth- of aggressive/active periodontitis usu- sumptive identification of nonprogres- ods are outlined elsewhere and are ally requires surgical intervention sive sites (10). The absence of a only briefly summarized below (24). and/or adjunctive systemic antibiotic radiographic lamina dura in angular The study included 12 periodontitis therapy (1). On the other hand, as periodontal defects (11) and in peri- patients, who completed a controlled many as 85% of patients with chronic implantitis lesions (12) was an indica- clinical trial with sodium hypochlorite periodontitis may remain disease-sta- tor of progressive disease, although oral rinse. The study patients had a ble for 5–6 years after only a one-time with low positive predictability, but mean age of 41 years and an average scaling (2) or no treatment at all (3), periodontal sites with a radiographi- of 28.6 teeth. Each patient exhibited and may derive relatively little benefit cally intact crestal lamina dura exhib- at least four separate teeth with a from surgical treatment. The avail- ited literally no risk of disease pocket depth of ≥ 6 mm. The patients ability of a reliable test to assess risk progression for at least 2 years (13). were medically healthy and required for periodontal disease activity would The lack of periodontal disease pro- no emergency dental care. Excluded help to optimize treatment of individ- gression at Ramfjord’s six index teeth from the study were individuals who ual patients and specific periodontal was suggestive of a low risk of pro- were unable to comply with the sites. gressive disease in the entire dentition research protocol, smoked > 10 ciga- Gingival bleeding on probing com- (14). A clinically based periodontal rettes daily or had received periodon- prises one of the more promising risk calculator failed, largely because of tal therapy or systemic antibiotics diagnostic predictability tests in peri- false-positive high-risk scores, to reli- during the 6 mo before entering the odontics. Claffey et al. (4) found loss ably predict progression of periodontal study. The University of Southern of probing attachment in 41% of disease during a 3-year post-treatment California Health Sciences Campus periodontal sites that bled on probing period (15). Periodontopathic bacteria Institutional Review Board approved at 75% of recall visits during a 3.5- in subgingival plaque (7,16–18) or the study (# HS-10-00509). All patients year observation period. Lang et al. saliva (19), or gingival crevice fluid understood and signed informed con- (5) reported that periodontal sites biomarkers (20,21), may also serve as sent and HIPAA documents before which bled on probing at four consec- indicators of periodontal disease sta- enrolling in the study. utive maintenance visits showed a tus. The modest to moderate positive- All study patients received a com- 30% risk of losing attachment, predictive value of diagnostic tests for prehensive clinical examination and whereas sites with bleeding on prob- progressive periodontal disease are conventional instruction ing at one out of four consecutive the result of a low incidence of dis- at baseline, but no subgingival or recall visits had only a 3% risk of ease-active periodontitis and a rela- supragingival scaling. Standard peri- breakdown, and periodontitis patients tively high number of false-positive odontal therapy was performed at the who demonstrated gingival bleeding assessments (22). Diagnostic tests may conclusion of the study. By random in fewer than 10% of sites in the den- be improved by combining several assignment, seven study participants tition were at low risk for progressive independent variables from different rinsed with sodium hypochlorite (test disease. A meta-analysis showed that aspects of the periodontal disease pro- group) and five rinsed with water persistent bleeding on probing after cess (7,23), but such an approach (control group). The source of sodium treatment was associated with pro- remains to be defined and validated in hypochlorite was Cloroxâ Regular- gression of periodontitis with an odds periodontics. Bleach (The Clorox Company, ratio of 2.8 (6). Charalampakis et al. As persistent bleeding on probing Oakland, CA, USA), which contains (7) found that bleeding on probing provides one of the most robust pre- 6% sodium hypochlorite and is yielded a better prediction of progres- dictors of periodontal breakdown, registered as a bacteriocide, virucide sive periodontal disease if combined and because little information exists and fungicide agent with the United with quantified bacterial markers. on the potential of periodontal self- States Environmental Protection Also, repeated mucosal bleeding on care to resolve gingival bleeding, this Agency (CAS number 5813-100). probing around implants may serve study examined the ability of 0.25% Participants in the sodium hypochlorite as a risk indicator of peri-implantitis sodium hypochlorite oral rinse, used rinse group were provided with Clorox (8), and the absence of mucosal twice-weekly for 3 mo, to convert gin- Regular-Bleach and instructed to bleeding may be an indicator of low gival bleeding sites to nonbleeding mix 5 mL (one teaspoonful) of bleach risk for implant failure as a result of sites in periodontitis patients. The with 120 mL (one half-glass) of tap infection (9). study subjects received no subgingival water to yield a sodium hypochlorite Gingival bleeding on probing 3 concentration of 0.25%. A fresh bleach solution was to be made up at each time of rinsing. The study patients were requested to rinse their mouth for 30 s every Wednesday and Sunday for 3 mo, with either 15 mL of a fresh solution of 0.25% sodium hypochlorite or 15 mL of water, and were given a rinse log to record the exact date and time of rinsing. A calibrated blinded examiner ol)

determined pocket depth and gingival h) at baseline and at 3 mo, in control bleeding within 30 s after probing to full pocket depth using a Marquis CP-12 probe (Hu-Friedy Mfg. Co., Chicago, IL, USA) and a probing force of approximately 0.75 N (76 gram-force). Mid-facial, mid-lingual, mesiofacial, distofacial, mesiolingual and distolingual surfaces were exam- ined, and a total of 1230 pockets in the bleach-rinse group and 828 pockets in the water-rinse group were studied. The statistical analysis was per- formed using the SPSS-19.0 software program (SPSS Inc., Chicago, IL, USA). The individual pockets were treated as independent statistical units, based on the nonspecific and wide-ranging antimicrobial action of sodium hypochlorite and the observa- tions that pockets with a large range of depths responded positively to the bleach treatment and that residual bleeding on probing sites showed no tendency to cluster in particular patients or around specific teeth. Based on the percentage of periodontal pock- ets with bleeding on probing and pocket depth changes, the chi-square test was used to identify significant differences between the bleach-rinse and the water-rinse groups. The Spear- man’s rank correlation coefficient test assessed the relationship between the frequency of bleeding on probing and increased pocket depth. A p-value of ≤ 0.05 was considered statistically significant.

Results The post-study interview and the patient rinse log revealed that the Bleeding on probing (BOP) in relation to periodontal pocket depth in patients receiving 0.25% sodium hypochlorite rinse (test) or water rinse (contr study participants fully understood the instructions for mixing the bleach Values are given asand no. test of groups. bleeding pockets/no. of total pockets at the specific pocket depth (percentage of bleeding pockets at the specific pocket dept rinse solution and complied with the Table 1. 4 Gonzalez et al.

Table 2. Periodontal pocket depth changes in relation to changes in bleeding on probing

aPercentage of total pockets in the particular Table row. ‘Visit 1’ denotes baseline and ‘Visit 2’ denotes termination of the study at 3 mo. Test patients rinsed with 0.25% sodium hypochlorite and control patients rinsed with water. twice-weekly rinsing guidelines. No water-rinse groups in decrease of per- rinse and control groups, during the adverse events were identified in any centage of ≥ 8 mm pockets and bleed- 3-mo study. of the participants, except for minor ing sites was statistically significant complaints about the taste of bleach. (p < 0.001). Discussion Table 1 details bleeding on probing Table 2 describes how changes in in relation to periodontal pocket bleeding on probing affected periodon- This study sought to assess the profi- depth. Both the bleach-rinse group tal pocket depth. A total of 470 (38%) ciency of bleeding on probing to pre- with 1230 pockets and the water-rinse periodontal pockets in the bleach-rinse dict progression of periodontal disease group with 828 pockets showed posi- group revealed bleeding on probing at and the capability of sodium hypochlo- tive correlations at baseline between the initial visit but not at the 3-mo rite oral rinse to resolve bleeding on frequency of gingival bleeding and visit; only 71 (9%) pockets in the con- probing in periodontal pockets of dif- increased pocket depth (p < 0.001). trol group became bleeding-negative ferent depths. Bleeding on probing is a No periodontal site of 1 mm depth during the study (p < 0.001). Con- potentially attractive risk indicator for bled on probing at any study time versely, 197 (16%) periodontal pockets periodontal breakdown because it is a point. At baseline, bleeding on prob- in the bleach-rinse group, but as many relatively simple, quick, all-or-none ing occurred in 37% of 2- to 3-mm- as 387 (47%) pockets in the control visual testing method that is not greatly deep pockets and in 88% of pockets group, showed persistent bleeding dependent on special skills or excep- with a depth of ≥ 6 mm. At 3 mo, throughout the study (p < 0.001). tional tactile sensitivity on the part of a bleeding on probing in pockets of 4– Ninety-seven pockets (5% of the total clinical observer. Also, probing of the 7 mm depth showed a 53% decrease pockets in the study) increased in prob- periodontal pocket depth is already a in the bleach-rinse group but a 6% ing depth by ≥ 2 mm: 60 (62%) of standard assessment technique in dental increase in the water-rinse group those pockets exhibited bleeding on practice, requiring no extra training for (p < 0.001). At baseline, 27 pockets in probing at both the initial and the 3-mo experienced operators. However, to the bleach-rinse group had a probing visits; 24 (25%) bled at only one of the avoid underestimating gingival bleeding, depth of ≥ 8 mm and all bled on two visits; and 13 (13%) never demon- we probed to the base of periodontal probing. At the 3-mo visit, the strated gingival bleeding (p < 0.001). A pockets and not just around the gingival bleach-rinse group revealed the pres- total of 25 pockets in the bleach-rinse margin (25) and used a probing force of ence of only three pockets of ≥ 8 mm, group (2% of test pockets) developed approximately 0.75 N instead of the con- and none showed bleeding. In com- bleeding on probing during the study; ventional 0.50 N (26). Lang et al. (27) parison, 127 pockets in the control none of those pockets showed a depth showed that an increase in probing force group had probing depths of ≥ 8mm reduction of ≥ 2mm,andfour(0.3%) from 0.50 to 0.75 N doubled the percent- at baseline and 108 (85%) bled on pockets experienced a depth increase age of periodontal pockets that bled on probing. At 3 mo, 114 control pock- of ≥ 2 mm. No statistically significant probing. ets of ≥ 8 mm depth were present and changes were found in gingival reces- Bleeding on probing occurred in 91 (80%) bled on probing. The differ- sion, furcation involvement or tooth 55% of untreated periodontal pockets ence between the bleach-rinse and the mobility, within or between the bleach- in our study compared with 71% (28), Gingival bleeding on probing 5

63% (29) and 57% (30) pockets in pre- 3 mo following nonsurgical or surgical Bleach occur naturally in the human vious studies. We found that therapy. However, our study revealed body (24), dilute bleach oral rinse untreated, 3-mm-deep pockets exhib- that 3 mo of twice-weekly rinsing with does not give rise to allergic reactions ited a frequency of bleeding on prob- sodium hypochlorite/dilute bleach gave or other types of disease. ing of 43%, whereas Farina et al. (31) rise to a 49% decrease in gingival In summary, bleeding on probing reported a frequency of bleeding on bleeding in pockets ≥ 5 mm deep. The tended to persist in periodontal sites probing of 18%. Bleeding on probing finding that bleeding on probing was with progressive disease, as measured scores are elevated with deep pockets resolved in sites with deep probing by an increase in probing pocket depth and heavy plaque accumulation, and depths, exposed to sodium hypochlo- of ≥ 2 mm, and to remain absent or are reduced by cigarette smoking, rite oral rinsing, which has not been discontinue in disease-stable or healing which may explain some of the differ- reported previously, lends substantial sites. Continued absence or cessation ences in the findings across studies credence to the use of sodium hypo- of bleeding on probing appeared to be (28,31,32). Rather than merely deter- chlorite in periodontal maintenance a useful, but not perfect, indicator of mine an overall correlation between care. Further studies are needed to stable periodontal conditions. Twice- bleeding on probing and progression determine if periodontitis patients may weekly oral rinsing with sodium hypo- of periodontal disease, we aimed to experience even less disease progression chlorite/dilute bleach, coupled with quantify, in more detail, the relation- if rinsing with dilute bleach is com- conventional oral hygiene, controlled ship between bleeding on probing and bined with . bleeding on probing more efficiently periodontal disease activity. Of the 97 The marked decrease in gingival than conventional oral hygiene alone, pockets (5% of the total pockets in the bleeding occurred despite oral rinse and provided a resolution of bleeding study) that showed increased probing only penetrates 0.1–0.2 mm into the on probing even in pockets of consid- depth of ≥ 2 mm, disease progression subgingival area (34). The improved erable depth. The reduction in bleeding was detected 2.5-fold more frequently gingival health after rinsing with on probing in this study, beyond those in pockets that bled on probing at sodium hypochlorite was most proba- noted in previous oral rinse studies, both the initial and the 3-mo visits (60 bly a result of the very low level of was probably the result of substantial pockets) than in pockets that bled on supragingival plaque, causing a antimicrobial, anti-inflammatory and probing at only one of the two visits decrease in the subgingival counts of tooth-substantive properties of sodium (24 pockets). Disease progression pathogenic bacteria (35–37). Lobene hypochlorite. Dilute bleach used as occurred in only 13 (1.5%) of the 854 et al. (38) and De Nardo et al. (39) an oral rinse offers convenience for pockets that never demonstrated found anti-plaque and anti- patients and deserves serious consider- bleeding on probing. The increased effects of sodium hypochlorite oral ation in periodontal healthcare. rate of periodontal breakdown in rinse similar to those reported here. An periodontal sites having repeat bleed- attractive feature of the present rinsing ing on probing and the low occur- protocol is the minimal extra time Acknowledgement rence of false-negative readings show (30 s, twice weekly) that is imposed on The study was funded in part by a the benefits of maintaining the patients’ usual oral hygiene effort. grant from The Clorox Company, in a nonbleeding state. Sodium hypochlorite is a powerful Oakland, California, USA. Bleeding on probing can decrease bactericidal and antiviral agent (40), substantially after mechanical depura- which can even neutralize hard-to- tion but, as also shown in the control destroy pathogenic prions (41). 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