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Home , Bleeding on probing, Dental plaque, Gingival recession, Periodontology, Tooth mobility

J Periodont Res 2014; 49: 696–702 © 2013 John Wiley & Sons A/S. All rights reserved Published by John Wiley & Sons Ltd

JOURNAL OF PERIODONTAL RESEARCH doi:10.1111/jre.12151

M. Galvan 1, S. Gonzalez1, Periodontal effects of 0.25% C. L. Cohen1, F. A. Alonaizan2, C. T-L. Chen1, S. K. Rich1, J. Slots1 sodium hypochlorite twice- 1 Graduate Clinic, Ostrow School of of USC, Los Angeles, CA, USA and 2Graduate Endodontic Clinic, Ostrow weekly oral rinse. A pilot School of Dentistry of USC, Los Angeles, CA, study USA

Galvan M, Gonzalez S, Cohen CL, Alonaizan FA, Chen CT-L, Rich SK, Slots J. Periodontal effects of 0.25% sodium hypochlorite twice-weekly oral rinse. A pilot study. J Periodont Res 2014; 49: 696–702. © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Background and Objective: The study aimed to evaluate the effect of 0.25% sodium hypochlorite twice-weekly oral rinse on plaque and in patients with minimally treated periodontitis.

Material and Methods: The study included 30 patients with periodontitis, it lasted 3 mo, and it was performed as a randomized, controlled, single-blinded, clinical trial in parallel groups. Fifteen patients rinsed for 30 s with 15 mL of a fresh solution of 0.25% sodium hypochlorite (test) and 15 patients rinsed with 15 mL of water (control). Cloroxâ regular bleach was the source of the sodium hypochlorite. At baseline and at 2 wk, the study patients received professional subgingival irriga- tion for 5 min with either 0.25% sodium hypochlorite or water, but no subgingival or supragingival scaling. The presence or absence of supragingival plaque on facial and lingual surfaces was determined by visual inspection; each was dried with air and mouth mirror rotation was used to provide light reflection to identify plaque on smooth surfaces and at the tooth line angles. Gingival bleeding within 30 s after probing to full pocket depth was assessed in six sites of each tooth. Adverse events were evaluated by questionnaire and visual examination. Results: All 30 patients in the study completed the baseline and the 2 wk parts of the study and a subset of 12 participants completed the 3 mo part of the study. The sodium hypochlorite rinse group and the water rinse group, respec- tively, showed increases from baseline to 3 mo of 94% and 29% (3.2-fold differ- ence) in plaque-free facial surfaces, of 195% and 30% (6.5-fold difference) in plaque-free lingual surfaces, and of 421% and 29% (14.5-fold difference) in number of teeth with no . The differences in clinical improvement between the sodium hypochlorite rinse group and the water rinse Jørgen Slots, DDS, DMD, PhD, MS, MBA, group were statistically significant. No adverse events were identified in any of Professor of Periodontology and Microbiology, Ostrow School of Dentistry of USC, the study patients, except for minor complaints about the taste of bleach. Los Angeles, CA 90089-0641, USA Tel: 213-740-1091 Conclusion: A twice-weekly oral rinse with 0.25% sodium hypochlorite pro- e-mail: [email protected] duced marked decreases in level and bleeding on probing and Key words: dental plaque; gingival bleeding; may constitute a promising new approach to the management of periodontal household bleach; mouth rinse; . Long-term controlled studies on the effectiveness of sodium hypochlo- treatment; sodium hypochlorite rite oral rinse are needed and encouraged. Accepted for publication October 19, 2013 Sodium hypochlorite oral rinse 697

Periodontal diseases have a global dis- human drinking water supply, and 0.25% sodium hypochlorite twice- tribution and include a broad spec- serves as a bleaching agent and a food weekly for 3 mo. trum of illnesses ranging from mild additive in industry. Sodium hypo- gingivitis to severe periodontitis. Vir- chlorite at 0.5% (Dakin’s solution) Material and methods tually all types of periodontal disease was used with great success to control are infectious disorders that result infections of combat wounded soldiers Study participants from the interplay between pathogenic during World War I, before antibiotics agents (, viruses, yeasts) and (4), and was recently found effective in A total of 17 males and 13 females, host immune responses. The major the treatment of wounded soldiers with a mean age of 41 years, who elements of causative periodontal ther- with potentially deadly angioinvasive were patients at the graduate peri- apy are mechanical pocket debride- fungal infections (5). The intermittent odontology clinic at the Ostrow ment, periodontal pocket irrigation use of dilute sodium hypochlorite in School of Dentistry of USC, were with potent antiseptics, treatment of “bleach baths” has shown efficacy as enrolled in the study. Patients had an advanced disease with systemic adjunctive therapy for atopic dermati- average of 27 teeth. Each patient antibiotics, and attention to proper tis (6,7). exhibited at least four separate teeth self-care (1). Sodium hypochlorite in concentra- with a pocket depth of ≥ 6 mm. None The worldwide increase of antibi- tions of 1.0–6.0% has been employed of the participants required emergency otic-resistant bacteria and the high in root canal disinfection for a cen- dental care or revealed systemic con- costs of new, effective antibiotics have tury, and remains the favored anti- ditions that would affect their peri- created interest in using inexpensive septic irrigant in (8). odontal status or contraindicate antiseptics to combat surface infec- However, use of sodium hypochlorite participation in the study. Excluded tions, such as those of the periodon- for treating other types of oral infec- from the study were patients who tium. Antiseptics are broad-spectrum tion has been surprisingly rare. Only were diabetic, pregnant, immunocom- microbicidal agents that are applied two periodontal studies have been promised, unable to comply with the topically onto living tissue to prevent published on the clinical efficacy of research protocol, smoked > 10 ciga- or treat clinical infections by bacteria dilute sodium hypochlorite. Lobene rettes daily, or had received periodon- and viruses. The halogen group of et al. (9) studied dental hygiene stu- tal therapy or systemic antibiotics antiseptics (fluorine, chlorine, bro- dents with a generally healthy peri- during the 6 mo before entering the mine, iodine) possesses the highest odontium; De Nardo et al. (10) study. The study was approved by the electronegativity (i.e. ability to attract studied prisoners who had undergone University of Southern California electrons to itself) of all elements professional periodontal therapy. The Health Sciences Campus Institutional (chlorine’s electronegativity = 3.16), study individuals, in the framework Review Board (no. HS-10-00509). All and strongly oxidizes (i.e. loss of elec- of the experimental gingivitis model, patients understood and signed trons) low electronegative atoms that received sodium hypochlorite rinse or informed consent and HIPAA docu- bond to halogens. water rinse and abstained from other ments before enrolling in the study. Sodium hypochlorite is the most types of . The sodium commonly used chlorine-releasing hypochlorite group showed 47% (9) Study design and clinical agent. It is ionized in water to Na+ and 48% (10) reduction in dental À measurements and the hypochlorite ion, OCl , which plaque and a significant improvement establishes an equilibrium with hypo- in gingival inflammation compared to The patients were divided into two chlorous acid, HOCl, the active moi- the water rinse group. The American groups and the study was performed ety (2). Sodium hypochlorite destroys Dental Association Council on Den- as a randomized (using a random by oxidation of pro- tal Therapeutics has designated 0.1% number table), controlled, single- teins, nucleotides and lipids, and is sodium hypochlorite a “mild antisep- blinded, clinical trial in parallel particularly effective against biofilm tic mouth rinse” and suggested its groups according to established crite- infections (3). The attack of multiple use for direct application to mucous ria (12). The test group of 15 patients components of infectious agents membranes (11). The present study received sodium hypochlorite rinse, practically eliminates the risk of resis- was undertaken to confirm and and control group of 15 patients tance development. Sodium hypochlo- expand the usefulness of sodium received water rinse. The clinical rite occurs naturally in activated hypochlorite rinse in was performed by a human and , therapy. The clinical improvement single-blinded examiner, who was cali- and plays an important antimicrobial was assessed in patients with peri- brated to accomplish more than 90% role in the innate immunity system (3). odontitis, who received initial subgin- reproducibility in repeated measure- It does not evoke allergic reactions, is gival irrigation with 0.25% sodium ments of the clinical variables studied. not a mutagen, carcinogen or terato- hypochlorite (half-strength Dakin’s All study patients received a gen, and has a century-long safety solution) or water but no subgingival comprehensive clinical examination record. It is used as a disinfectant or supragingival scaling, and who at baseline (visit 1), at day 14 (visit in , animal facilities and in were instructed to rinse orally with 2) and at month 3 (visit 3). The 698 Galvan et al. following clinical variables were species, Campylobacter group were provided with Clorox assessed in each participant, according rectus, Parvimonas micra, Eubacterium bleach (6%) and instructed to mix to the standard protocol for patients species, beta-hemolytic streptococci, 5 mL (one teaspoonful) of Clorox with periodontitis: medical question- staphylococci, gram-negative enteric bleach with 120 mL (one-half glass) naire and general oral examination, rods and Candida species. of tap water to yield a sodium hypo- full-mouth dental radiographs, num- chlorite concentration of 0.25%. A ber of teeth, presence of dental fresh bleach solution should be made Patient treatment and instruction plaque, gingival bleeding on probing, up at each time of rinsing. Following periodontal pocket depth (in mm), Cloroxâ regular bleach (The Clorox rinsing with the diluted bleach solu- (in mm), furcation Company, Oakland, CA, USA) tion, the test group participants were involvement and . diluted with tap water served as the to expectorate and refrain from rins- The main clinical variables of the source of 0.25% sodium hypochlo- ing with water for at least 10 min. study were assessed as follows. The rite. According to the manufacturer, The procedure for mixing the bleach presence or absence of supragingival Clorox regular bleach contains (in with water and the rinsing method plaque on the facial and lingual sur- order of declining concentration) were provided in writing, and faces of each tooth was determined by water, 6% sodium hypochlorite, explained and practiced under the visual inspection with no use of dis- sodium chloride (stabilize formula), supervision of the investigator. The closing solution. The tooth surface sodium carbonate (alkalinity builder), control group (the participants was dried with air for enhanced visibil- sodium hydroxide (< 1%; pH adjus- believed that the supplied water con- ity, and indirect vision and light reflec- ter), and a small amount of sodium tained an active ingredient) was tion with mouth mirror rotation were polyacrylate (assist cleaning). It has a instructed in the same manner, but used to assess presence of plaque on pH of about 11 and forms no dioxins used water rinse only. In an effort to smooth surfaces and at the tooth line nor causes buildup of by-products ensure compliance, all study partici- angles. A value of “0” was assigned to over time. The retail cost of 1 US pants were provided with a rinse log surfaces with absence of plaque and a gallon (3.8 L) of Clorox regular to record the exact date and time of value of “1” was assigned to surfaces bleach is 2.0–2.5 US$. Diluted bleach rinsing, and they were requested to with any presence of plaque. Bleeding loses activity over time and may be bring the rinse log with them to the on probing was assessed within 30 s discarded after 1–2d. final visit. They were also telephoned after probing to the full pocket depth, At visit 1 and at visit 2, the study regularly to remind them to rinse and and was recorded on the facial, lin- participants received oral hygiene to inquire about any problems with gual, mesiofacial, distofacial, mesiolin- instruction followed by professional the rinsing protocol. In addition, par- gual and distolingual surfaces of each subgingival irrigation with either ticipants received an end-of-study tooth. A value of “0” was assigned to 0.25% sodium hypochlorite (test) or written questionnaire to gain evalua- teeth showing absence of gingival water (control). No subgingival or tive feedback about their satisfaction bleeding in all six study sites, and a supragingival scaling was carried out. or concerns with the study. value of “1” was assigned to teeth The subgingival irrigation was per- At the conclusion of the study, each revealing gingival bleeding in any of formed using a 3 mL Monojectâ study participant received standard the six tooth sites. Probing depths Endodontic Syringe with a 23-gauge therapy for periodontitis, including were measured in millimeters using a cannula (metal with a blunt end and further explanation about the cause of Marquis CP-12 probe (Hu-Friedy side ports) (Covidien, Mansfield, MA, the disease, instruction in oral hygiene, Mfg. Co., Chicago, IL, USA) with a USA). The syringe tip was placed at , supragingival probing force of approximately the bottom of the pockets of each polishing, and recall schedule to 0.75 N. Pocket depth and gingival tooth, and sodium hypochlorite or prevent disease recurrence. recession were measured on the facial, water rinse was repeatedly applied in lingual, mesiofacial, distofacial, mesio- a circular manner around all teeth of Statistics lingual and distolingual surfaces of the dentition for a total of 5 min. each tooth. Participants were also given a manual Individual patients served as the unit A pooled microbiological sample Oral-Bâ and dental floss for statistical analysis. The mean from two deep periodontitis lesions of samples and instructed to brush twice value of each study variable was each study patient was obtained at all a day, using the modified Bass tech- obtained for each patient at each visit three study visits before the clinical nique, and to floss once a day. and used in the statistical analysis. examination and was analyzed by The instructions for oral rinsing at For each of the dependent variables, established anaerobic culture methods home were as follows. Participants a Wilcoxon signed-rank test was used (13). The microorganisms studied were asked to rinse their mouth every to test for difference within each study included Aggregatibacter actinomyce- Wednesday and Sunday for 30 s with group. The Wilcoxon–Mann–Whitney temcomitans, Prophyromonas gingiva- either 15 mL of a fresh solution of test was used to compare improve- lis, , 0.25% sodium hypochlorite or 15 mL ment between study groups by calcu- intermedia, Dialister pneumosintes, of water. Participants in the test lating the score difference between Sodium hypochlorite oral rinse 699 visits. The Friedman test was used to whitening of their teeth; all of these hypochlorite group demonstrated clini- assess differences in the dependent participants were in the test group. cal changes beyond that shown by the variables within each study group No study participants reported stain control group for every study variable, over time. Spearman’s correlation test or discoloration of their teeth or den- including a 3.2-fold increase in plaque- determined the correlation coefficient tal restorations. None of the partici- free facial surfaces (p = 0.04), a between the difference in absence of pants experienced or tingling 6.5-fold increase in plaque-free lingual plaque from visit 1 to visit 3 and the sensation of the buccal mucosa or the surfaces (p = 0.04), and a 14.5-fold difference in absence of bleeding on tongue. increase in bleeding on probing-free probing from visit 1 to visit 3. The Table 1 shows that the initial ther- teeth (p = 0.01) (Table 3). significance level was set at a = 0.05. apy in the sodium hypochlorite group The study found a statistically sig- The statistical analysis was performed resulted in a statistically significant nificant correlation (Spearman’s corre- using the STATA statistical software increase in facial tooth surfaces free lation coefficient of 0.62; p = 0.03) release 12 (StataCorp, College of dental plaque. No significant between the difference in absence of Station, TX, USA). change was found in any of the clini- plaque and the difference in absence of cal study variables in the control bleeding on probing from visit 1 to group. Table 2 reveals that the clini- visit 3. No statistically significant Results cal improvement continued in the changes were found in periodontal Of the 30 study participants, 18 sodium hypochlorite group until the pocket depth, gingival recession, furca- adhered to the rinsing regimen for end of the study, with significant tion involvement or tooth mobility, 2 wk and then exited the study. Con- increases in plaque-free facial and lin- within or between the test and control cerns expressed were unwillingness to gual tooth surfaces and in number of groups, from visit 1 to visit 2 or visit 3. delay periodontal treatment for the teeth associated with absence of The microbiological study of the additional 10 wk required for visit 3, bleeding on probing. Again, no signif- sodium hypochlorite group revealed and difficulty with transportation due icant clinical improvement was identi- statistically significant decreases in the to residing in locations distant from fied in the control group during the subgingival proportion of fusobacteria the . Of the 12 partici- 3 mo study period. at visit 2 and in gram-negative enteric pants completing the 3 mo study, Table 3 depicts the level of clinical rods at visit 3. The control group seven were in the test group and five improvement within and between the demonstrated no significant decrease in the control group. The participants test and control group of those individ- in any of the microorganisms studied. who left the study prematurely were uals who completed the study. From None of the test microorganisms clinically similar to those who com- baseline to third visit, the sodium showed overgrowth to indicate super- pleted the study. hypochlorite group showed statistically infection. Evaluation of the questionnaire of significant multifold increases in compliance revealed that 25 of the 30 plaque-free tooth surfaces, and as Discussion (83%) participants fully understood much as a 4.2-fold increase in bleeding the instructions for mixing the rinsing on probing-free teeth. The control There exists an urgent need to develop solution and complied with the twice- group exhibited only non-significant effective and affordable self-care weekly rinsing guidelines. Of the five Hawthorne-like effect improvements techniques for the prevention and participants who did not completely of 0.3-fold (Table 3). The sodium treatment of periodontal disease. As follow the rinsing protocol, three for- got to rinse at least once (one was test and two were control group partici- Table 1. Clinical variables after initial subgingival irrigation and oral rinse with 0.25% pants) and two missed some rinses sodium hypochlorite or water due to a perception of a “bad taste.” Thirteen participants complained of a Sodium hypochlorite (test) group Water (control) group bad taste after using the solution, which lasted from 5 min to 1 h, but Baseline Week 2 Baseline Week 2 was not by itself severe enough for Items (visit 1) (visit 2) p-values* (visit 1) (visit 2) p-values* them to request discontinuance from Total number of 394 (15) 394 (15) – 404 (15) 404 (15) – the study; all of the individuals claim- teeth (patients) ing bad taste were in the test group. Plaque-free facial 33%a 52% 0.009 40%a 47% 0.19 Two of the participants swallowed surfaces (25%) (26%) (25%) (23%) part of the bleach solution, but expe- Plaque-free 19% 29% 0.09 21% 23% 0.84 rienced no adverse effects. Twelve of lingual surfaces (21%) (18%) 24%) (23%) the 30 participants noticed less gingi- Bleeding on 32% 37% 0.22 42% 46% 0.09 val inflammation and bleeding; 10 probing-free teeth (29%) (29%) (30%) (31%) were test group and two were control *The Wilcoxon signed-ranked test for comparison between visit 1 and visit 2. group participants. Eleven perceived aPercentage of total surfaces/teeth (standard deviation among patients). 700 Galvan et al.

Table 2. Clinical variables after 3 mo rinse with 0.25% sodium hypochlorite or water for individuals completing the study

Sodium hypochlorite (test) group Water (control) group

Baseline Week 2 Month 3 Baseline Week 2 Month 3 Items (visit 1) (visit 2) (visit 3) p-values* (visit 1) (visit 2) (visit 3) p-values*

Total number of 205 (7) 205 (7) 205 (7) – 138 (5) 138 (5) 138 (5) – teeth (patients) Plaque-free facial 38%a 62% 74% 0.02 34%a 49% 44% 0.63 surfaces (29%) (20%) (17%) (30%) (26%) (30%) Plaque-free lingual 18% 37% 53% 0.07 30% 38% 39% 0.95 surfaces (23%) (20%) (13%) (33%) (27%) (23%) Bleeding on 12% 18% 62% 0.002 31% 34% 40% 0.84 probing-free teeth (18%) (25%) (29%) (32%) (33%) (45%)

*Friedman’s non-parametric repeated measures analysis over the three study visits. aPercentage of total surfaces/teeth (standard deviation among patients).

Table 3. Comparison in clinical improvement between 0.25% sodium hypochlorite rinse and water rinse for individuals completing the study

p-values* Fold improvement between Fold improvement Additional fold improvement visit 1 and visit 3 for the between visit 1 and in the sodium hypochlorite Between Between sodium hypochlorite rinse visit 3 for the water rinse group vs. the water visit 1 and visit 1 and Items group rinse group rinse group visit 2 visit 3

Plaque-free facial surfaces 0.94 0.29 3.2 0.17 0.042 Plaque-free lingual surfaces 1.95 0.30 6.5 0.17 0.042 Bleeding on probing-free 4.21 0.29 14.5 0.72 0.012 teeth

*The Wilcoxon–Mann–Whitney test to compare the clinical improvement between the sodium hypochlorite rinse group and the water rinse group. pointed out elsewhere, the current highly diluted sodium hypochlorite sodium hypochlorite rinse group and methods for removing dental plaque solution (0.05%), used twice-daily as the water rinse group, respectively, are cumbersome, provide limited bene- an oral rinse in an experimental gingi- showed increases of 94% and 29% fits and perform poorly for many indi- vitis design study, was able to reduce (3.2-fold difference) in plaque-free viduals (1). Toothbrushing reduces the dental plaque index scores by 48%, facial surfaces, of 195% and 30% average plaque scores only by about gingival inflammation index score by (6.5-fold difference) in plaque-free half and plaque is left behind on 85% 52%, and bleeding on probing sites lingual surfaces, and of 421% and of interdental surfaces; interdental by 39% compared with water rinse 29% (14.5-fold difference) in number brushes, toothpicks and dental floss (10). However, as the twice-daily use of teeth with no bleeding on probing. fail to eliminate all interdental plaque of a freshly made sodium hypochlo- The sodium hypochlorite rinse group, and are only used by 5–10% of the rite solution may be impractical for but not the water rinse group, demon- population; most are most individuals, we sought to exam- strated continued clinical improve- expensive and do not significantly ine if a five times more concentrated ments up to the 3 mo endpoint of the enhance plaque removal by tooth- sodium hypochlorite oral rinse solu- study, suggesting that the difference brushing alone; and commercial tion (0.25%), used only twice in a between the sodium hypochlorite test are expensive and, with week, would provide similar clinical group and the water control group the exception of , essen- improvements. The present findings would widen even further with a longer tially only serve a cosmetic purpose are consistent with those of previous study period. The biochemical basis (1). High prices and low performance studies (9,10). The sodium hypochlo- for the remarkable decrease in dental of current self-care devices and thera- rite oral rinse group showed marked plaque after only a twice-weekly pies are some of the biggest issues in improvements from baseline to 3 mo sodium hypochlorite rinse is unknown, periodontal healthcare. in plaque-free facial surfaces but substantivity to the tooth surface is Sodium hypochlorite represents (p = 0.02), plaque-free lingual surfaces an intriguing possibility. potentially an efficacious, safe, inex- (p = 0.07) and bleeding on probing- Oral rinses penetrate only 0.1– pensive and readily available comple- free teeth (p = 0.002). The clinical 0.2 mm into periodontal pockets ment or alternative to current changes in the control group were (14,15), but this study found marked periodontal self-care techniques. A statistically non-significant. The clinical improvements in periodontitis Sodium hypochlorite oral rinse 701 lesions as well. The most likely expla- can interfere, at least for 24 h, with 5. Lewandowski L, Purcell R, Fleming M, nation relates to the sustained absence the ability of dental plaque to pro- Gordon WT. The use of dilute Dakin’s of supragingival plaque, which is duce an acidic environment (9) and solution for the treatment of angioinva- sive fungal infection in the combat known to affect the subgingival ecol- that dilute sodium hypochlorite can wounded: a case series. Mil Med 2013; ogy and reduce periodontopathogen penetrate 0.1 mm into exposed den- 178:e503–507. counts in pockets up to 5 mm in depth tinal tubules and potentially kill 6. Huang JT, Rademaker A, Paller AS. (16–18). Another possibility is that the invading cariogenic bacteria (22). Dilute bleach baths for Staphylococcus initial subgingival bleach irrigation In conclusion, the increasing costs aureus colonization in atopic dermatitis suppressed periodontal herpesviruses, of periodontal healthcare combined to decrease disease severity. Arch Derma- 147 – which are highly susceptible to sodium with a growing number of under- tol 2011; :246 247. 7. Ryan C, Shaw RE, Cockerell CJ, Hand hypochlorite. As herpesvirus infections served populations worldwide under- S, Ghali FE. Novel sodium hypochlorite support periodontopathic bacteria scores the need for finding alternative cleanser shows clinical response and (19), a reduced herpesvirus level may ways of managing periodontal excellent acceptability in the treatment of decrease subgingival bacterial counts disease. Patients ought to be able to atopic dermatitis. Pediatr Dermatol and clinical signs of disease. 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Lang et al. (21) showed effectiveness, safety, affordability, sodium hypochlorite oral rinse on supra- that periodontal sites demonstrating accessibility and convenience. How- gingival biofilm and gingival inflamma- bleeding on probing at four consecu- ever, in spite of the encouraging find- tion. Int Dent J 2012;62:208–212. tive maintenance visits had a 30% ings on the sodium hypochlorite oral 11. American Dental Association. Accepted risk of losing attachment, whereas rinse, controlled studies are still Dental Therapeutics. Chicago, IL: ADA, sites exhibiting bleeding on probing in needed to determine its periodontal 1984:326. one of four recall visits had only a benefits with long-term use. In addi- 12. Altman DG, Schulz KF, Moher D et al., CONSORT GROUP (Consolidated 3% risk of further breakdown. In tion, although the concept of antimi- Standards of Reporting Trials). 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