The International Journal of Periodontics & Restorative Dentistry

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Full-Mouth Disinfection as a Nonsurgical Treatment Approach for Drug-Induced Gingival Overgrowth: A Series of 11 Cases

Bettina Dannewitz, Priv Doz, Dr Med Dent1 Severe forms of gingival overgrowth Jörg Kristian Krieger, Dr Med Dent2 (GO) develop predominantly through Isabel Simon, Dr Med Dent2 use of systemic medication. Drugs 3 Jens Dreyhaupt, Dr Rer Nat, Dipl-Math associated with GO can be broadly 4 Hans Jörg Staehle, Prof Dr Med, Dr Med Dent divided into three categories: anti- Peter Eickholz, Prof Dr Med Dent5 convulsants, calcium channel blockers, and immunosuppressants.1,2 The The treatment of drug-induced gingival overgrowth is compounded by the high prevalence of drug-induced GO varies recurrence rate resulting from chronic use of the medication and the persistence among medications, and a variety of of other risk factors. In this case series, the treatment outcome of a nonsurgical risk factors have been identified and periodontal therapy, according to the concept of full-mouth disinfection in 11 reviewed recently, including age and patients with drug-induced gingival overgrowth, is described. All clinical parame- sex of the patient, drug variables, con- ters improved significantly after therapy. Only 6% of teeth received further surgical treatment. The clinical situation remained stable during the recall. The present comitant medication, genetic factors, case series suggests that full-mouth disinfection might be a beneficial treatment and the inflammatory status of the peri- 2,3 concept for drug-induced gingival overgrowth, reducing the need for further sur- odontal tissues. The nature of the gical intervention. (Int J Periodontics Restorative Dent 2010;30:63–71.) relationship between plaque and the expression of GO is unclear, and con- troversy exists as to whether plaque 1Associate Professor, Department of Conservative Dentistry, Clinic for Oral, Dental, and Maxillofacial Diseases, University Hospital Heidelberg, Heidelberg, Germany; Postdoctoral accumulation is the cause or conse- Research Fellow, Department of Periodontology, Center for Dental, Oral and Maxillofacial quence of the gingival changes. Medicine, University Hospital Frankfurt, Frankfurt, Germany. Severe GO is often disfiguring and can 2Postdoctoral Research Fellow, Department of Conservative Dentistry, Clinic for Oral, Dental, interfere with both speech and masti- and Maxillofacial Diseases, University Hospital Heidelberg, Heidelberg, Germany. 3Postdoctoral Research Fellow, Institute of Medical Biometry and Informatics, University of cation. Moreover, the massive plaque Heidelberg, Heidelberg, Germany. accumulation in the gingival pockets 4 Professor, Department of Conservative Dentistry, Clinic for Oral, Dental and Maxillofacial may be a consistent source for tran- Diseases, University Hospital Heidelberg, Heidelberg, Germany. 5Professor, Department of Periodontology, Center for Dental, Oral and Maxillofacial sient bacteremia, which increases the Medicine, University Hospital Frankfurt, Frankfurt, Germany. risk of systemic infections in immuno- compromised patients, leading to pro- Correspondence to: Dr Bettina Dannewitz, Department of Conservative Dentistry, Clinic for found complications.4 Oral, Dental, and Maxillofacial Diseases, University Hospital Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany; fax: +49-6221-56-5074; email: bettina_dannewitz@ The treatment of GO is com- med.uni-heidelberg.de. pounded by the high recurrence rate

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resulting from chronic use of the med- 74 years (mean, 53 ± 17 years) with ening over the tangent). The second ication and persistence of other risk drug-induced GO were consecutively component measured the extent of factors. Although surgery remains the scheduled for this study. GO resulted encroachment of the gingival tissues main option for treatment of drug- from therapy with calcium channel on the labial aspect of the adjacent induced GO, alternative strategies blockers (n = 4), cyclosporine (CsA; n tooth crown and ranged from 0 (no have been investigated to either pre- = 1), or a combination of CsA and cal- clinical evidence of overgrowth) to 3 vent this unwanted effect or reduce cium channel blockers (n = 6). All (overgrowth covering three-fourths of the incidence of its recurrence.5 A vari- patients were nonsmokers. the tooth crown). Since encroachment ety of conservative approaches have at the lingual aspect could not be been proposed, including nonsurgical examined properly on the pho- periodontal treatment, antiseptic Clinical examinations tographs, scoring was limited to the mouthwashes, systemic use of antibi- labial aspect. The papillae distal to the otics, and change of medication.5 The Before therapy (baseline), at reevalua- dental arch and sites adjacent to eden- primary aim of nonsurgical therapy is tion, and at the last recall visit, the fol- tulous spaces were not measured. The to reduce the inflammatory compo- lowing clinical parameters were maximum score possible using this nent in the gingival tissue by sup- assessed: number of teeth, probing method was 5. The degree of GO was pressing or minimizing the amount of pocket depth (PPD), bleeding on prob- expressed as a mean score and as a periodontal pathogens.6 To achieve ing (BOP), plaque control record percentage in relation to the total num- this, an anti-infective regime combin- (PCR),8 and gingival bleeding index ber of gingival units per patient. ing nonsurgical mechanical therapy (GBI).9 Because of the overgrowth, it Radiographic bone loss at the begin- and a chemotherapeutic approach was impossible to measure the clinical ning of periodontal therapy was mea- called “one-stage full-mouth disinfec- attachment level reliably at most sites sured at every tooth possible using a tion” was introduced by Quirynen and at baseline. Therefore, it was not con- Schei ruler to assess the percentage of coworkers.7 This strategy attempts to sidered for further analysis. bone loss in 20% increments.11 eradicate, or at least suppress, all peri- The degree of GO was graded odontal pathogens in a short time span numerically using a modification of a (24 hours), not only from the peri- scoring system described by Seymour Therapy odontal pockets but also from all their et al.10 Since plaster models were not intraoral habitats (ie, mucous mem- available for all patients, photographs Periodontal therapy consisted of an branes, tongue, saliva). of the clinical situation were taken rou- active phase including oral hygiene The aim of this retrospective case tinely in a standardized manner and instructions, professional cleaning of series was to evaluate whether a non- magnified for monitoring the treatment all teeth, subgingival scaling and root surgical approach according to the full- phase. Moreover, the scoring system planing, and if necessary, further surgi- mouth disinfection (FMD) concept is was expanded to allow recording of all cal intervention. In patients taking CsA, effective in preventing further surgical visible interdental sites, not only the periodontal therapy was performed excision of drug-induced GO. anterior sextant. A GO score was under antibiotic prophylaxis because assigned to each interdental unit (gin- of the patient’s increased susceptibil- gival unit) and was the sum of two com- ity to infections.4 Subgingival debride- Case reports ponents. The first component mea- ment was performed according to the sured the degree of gingival thickening FMD concept, which consisted of scal- Patients by means of a 3-point scale (0 = nor- ing and root planing of all pockets mal width, 1 = thickening up to a tan- (≥ 4 mm) in two visits within 24 hours, Eleven patients (four men, seven gent drawn between the labial surfaces using sonic scalers and hand instru- women) between the ages of 23 and of the two neighboring teeth, 2 = thick- mentation under local anesthesia.7

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Furthermore, the tongue was brushed site, discriminating between approxi- of 41.97% showing increased GO with 1% chlorhexidine gel (Chlor- mal and buccal/oral sites at posterior scores. The overall GO score at the hexamed, GlaxoSmithKline) for 1 and anterior teeth in the maxilla and reevaluation and the last recall visit was minute, the mouth was rinsed with a mandible. Data were analyzed descrip- reduced to 5.0% and 0.55%, respec- 0.12% chlorhexidine solution (Paroex, tively. Further, linear mixed-effects tively. Ninety-one gingival units of the John O. Butler) for 2 minutes, and all regression models were used to com- 105 examined in the anterior segment pockets were irrigated subgingivally pare the differences between mean (86.7%) and 90 of the 136 assessed in with the 1% chlorhexidine gel. For the PPD, PPD categories, and GO score the posterior (66.2%) showed GO at following 2 weeks, patients brushed values obtained at baseline, reevalua- baseline, with average scores of 2.45 their teeth with 1% chlorhexidine gel tion, and the last recall visit. Differences and 2.09, respectively. At the reevalu- and rinsed with 0.12% chlorhexidine in GBI and PCR between baseline, ation 16 of the 105 units examined in solution twice daily. After those 2 reevaluation, and the last recall were the anterior segment (15.2%) and 18 of weeks, all teeth were polished and analyzed with the one-sample t test. the 133 units analyzed in the posterior patients obtained further oral hygiene The individual patient was included as (13.5%) showed GO, with average instructions and motivation. a random effect in all mixed effects scores of 0.25 and 0.32, respectively. The FMD clinical situation was regression models since each patient At the last recall visit, 3 of the 93 units reevaluated 2 to 4 months later, and if gave more than one tooth. Statistical assessed in the anterior segment necessary, further surgical therapy was significance was set at P < .05. (3.2%) and 1 of the 121 units examined planned. Indication for surgical gin- in the posterior (0.8%) showed GO, givectomy was given in cases of per- with average scores of 0.04 and 0.02, sistently increasing PPD or GO that Results respectively. interfered with effective oral hygiene or The changes in PPD throughout impaired the patient’s esthetics. At baseline, 11 patients had a total of therapy regarding the different PPD After active periodontal therapy, 282 teeth, with a mean of 25.6 teeth categories are presented in Fig 2. The all patients were included in a regular per patient (range, 19 to 31 teeth). number of sites with PPD ≤ 4 mm supportive periodontal treatment pro- During active periodontal therapy, 6 increased significantly after FMD (from gram at intervals of 3 to 6 months (cal- teeth were extracted (3 teeth each in 57.58% to 95.62%). Concomitantly, the culated using an individual periodon- 2 patients). After reevaluation, an exter- number of sites with PPD of 5 to 6 mm tal risk assessment).12 All patients nal gingivectomy was performed in 1 and ≥ 7 mm decreased significantly completed the reevaluation, but one patient, which was limited to the area (from 27.72% to 3.92% and 14.7% to patient was lost to follow-up. The of the buccal aspect of the maxillary 0.47%, respectively). The improved remaining 10 patients were followed anterior teeth. Another 2 patients clinical situation remained stable dur- for a mean of 28 months (range, 11 to received internal gingivectomies car- ing maintenance and showed further 71 months). ried out locally at the posterior teeth. slight improvements. Altogether, further surgical interven- The site-based analysis at baseline tions were indicated for 17 teeth after showed a marked difference between Statistical analysis FMD according the previously men- PPD at approximal and buccal/oral tioned criteria. sites in the maxilla as well as the Statistical analysis was performed using The severity of GO, as measured mandible, with the approximal site in a commercially available software pro- by the modified Seymour index,10 for the maxilla revealing the highest PPD gram (SAS version 9.1, SAS Institute). the anterior and posterior segment in (Figs 3a and 3b). After therapy, the PPD was analyzed as follows: ≤ 4 mm, the maxilla and mandible is presented mean PPD was < 4 mm in all seg- 5 to 6 mm, and ≥ 7 mm. Moreover, in Fig 1. A total of 241 gingival units ments. mean PPD was evaluated based on were assessed at baseline, with a mean

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Fig 1 Mean GO score at baseline, at reevaluation, and at the last recall visit spec- * Baseline (n = 241) ified for anterior (incisors and canines) and 5 *** *** Reevaluation (n = 238) posterior teeth (premolars and molars) in Last recall (n = 214) *** *** the maxilla and mandible (maximum score 4 *** = 5).*P < .01; ***P < .001. * 3 * 2.80 2.76 2 2.16

Mean GO score 1.39 1 0.04 0.09 0.07 0.60 0.04 0.44 0.00 0.00 0 Posterior Anterior Posterior Anterior Maxilla Mandible

Fig 2 Distribution of PPDs ≥ 7 mm, 5 to 6 ≤ *** mm, and 4 mm at baseline, reevaluation, *** and the last recall visit. ***P < .001. 0.47 0.38 100 3.92 3.32 14.70 ≤ 4 mm 5–6 mm 80 ≥ 7 mm 27.72 60 % 40 57.58 95.62 96.30 20

0 Baseline Reevaluation Last recall (n = 1,618) (n = 1,644) (n = 1,458)

Regarding gingival inflammation, inflammation before therapy, BOP periodontal therapy resulted in a sta- could not be measured reliably at this tistically significant reduction in the GBI time. BOP decreased to 32.8% at (from 62.6% to 11.0%), which further reevaluation and 32.9% at the last visit. improved until the last recall visit (8.6%, Radiographic bone loss could be Fig 4). The individual PCR improved as assessed in 280 of 282 teeth at the well from baseline (57.6%) to the beginning of therapy. Three hundred reevaluation (41.5%) to the last recall fifty-three sites (63%) displayed bone visit (37.4%, Fig 4). However, the loss of ≤ 20%, 172 sites (30.7%) of ≤ change in PCR between baseline and 40%, 30 sites (5.4%) of ≤ 60%, 1 site the last recall was statistically not sig- (0.2%) of ≤ 80%, and 4 sites (0.7%) of nificant. On average, 70.8% of sites > 80%. Most patients (63%) showed showed BOP at baseline. However, only limited periodontal destruction considering the pronounced gingival (< 20% bone loss in 63%).

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Figs 3a and 3b Mean PPD in (top) the maxilla and (bottom) the mandible at base- Baseline (n = 11) line, reevaluation, and the last recall visit * Reevaluation (n = 11) specified for anterior and posterior teeth as 8 * * well as the buccal/oral and approximal sites. Last recall (n = 10) *** *P < .01; **P < .05; ***P < .001. 6 **

4 ** ** 5.25 Mean PPD (mm) 2 5.11 3.73 3.04 3.04 2.36 2.39 2.86 2.94 3.63 2.30 2.37 0 Approximal Buccal/oral Approximal Buccal/oral Posterior Anterior

Baseline (n = 11) 8 * Reevaluation (n = 11) Last recall (n = 10) * ** * ** 6 ** **

Mean PPD (mm) 2 4.30 3.73 4.81 2.86 2.94 2.35 2.36 2.38 2.43 3.11 1.77 1.89 0 Approximal Buccal/oral Approximal Buccal/oral Posterior Anterior

Fig 4 Mean and median GBI and PCR at baseline, reevaluation, and the last recall *** visit. **P < .05; ***P < .001. *** ** 62.6 100 Mean PCR (%) Mean GBI (%) 57.6 80 57.0 41.5 60 37.4 68.0 % 36.0 40 35.5

11.0 20 8.6

8.0 8.0 0 Baseline Reevaluation Last recall

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Discussion Most notably, immunosuppressed patients benefit from the 24-hour Different treatment strategies have approach since scaling and root plan- been discussed for drug-associated ing must be carried out under antibi- GO, including nonsurgical approaches, otic coverage, which can be limited to application of antiseptic mouthwashes, a short time period. The effect of the systemic antibiotics, change of med- additional systemic administration of ication, and surgical intervention.5,13–15 antibiotics on the treatment outcome The authors of two current reviews described in this case series is hard to addressing treatment options for GO, estimate, but cannot be ruled out. the authors concluded that surgery However, in most cases antibiotic pro- remains the main option, and that phylaxis was not given over a long scalpel gingivectomy is still the treat- period of time but rather was limited to ment of choice.5,16 As an alternative, the day of treatment. laser gingivectomy offers some advan- The one-stage FMD study was tages, including reduced hemorrhage repeated but without the use of during excision and minimal postop- chlorhexidine (one-stage full-mouth erative discomfort.16,17 Moreover, laser scaling). Both treatment strategies excision results in a reduced rate of resulted in nearly the same clinical and recurrence compared to scalpel gin- microbiologic improvements, with a givectomy.16 However, there is evi- slightly more pronounced and clearly dence that nonsurgical periodontal faster improvement for the one-stage therapy may resolve or at least reduce FMD involving the antiseptic.25 the severity of overgrowth and the Adjunctive chemical plaque need for surgical intervention.18–20 For removal has been used in the man- this purpose, the authors investigated agement of GO. Animal studies have the effect of the FMD concept as a shown that regular application of a nonsurgical approach in patients with chlorhexidine solution in rats med- drug-induced gingival enlargement. icated with CsA resulted in significantly A series of clinical and microbio- less overgrowth than in control ani- logic studies conducted by Quirynen mals.13 In humans, chlorhexidine has and coworkers revealed superior results only been evaluated in the therapy of for FMD compared to conventional phenytoin-induced GO, and it was quadrant-wise therapy.7,21 However, found that regular use of this recent studies comparing the FMD mouthrinse helps to reduce the recur- concept with quadrant scaling and root rence rate after surgery.26 Besides the planing at 1- or 2-week intervals failed aforementioned rationales for the use to demonstrate differences in the clin- of chlorhexidine, administration after ical, microbiologic, or immunologic out- scaling and root planing helped to comes.22,23 Therefore, the authors con- compensate for deficiencies in indi- cluded that the clinician should select vidual mechanical plaque control until the treatment modality based on prac- GO was reduced. tical considerations related to patient Applying the FMD regime in preference and clinical workflow.24 patients with drug-induced GO

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Figs 5a and 5b A 57-year-old female patient displaying GO induced by the systemic use of calcium channel blockers (left) before therapy and (right) 3 months after FMD.

resulted in a statistically significant The patients in this study were fol- reduction of the GO and concomi- lowed for a mean of 28 months. The tantly the PPDs (Figs 5a and 5b). GO most beneficial effects occurred within was graded according to a scoring 4 to 6 months posttreatment and were model described by Seymour et al.10 followed by a period of stability. The However, this method had to be mod- individual plaque control improved ified because plaster models were not throughout therapy but was still not available for all patients. Instead, pic- optimal in most patients at the re- tures of the clinical situation were used evaluation and the last recall visit. for the classification of GO. The scores However, no recurrence of GO could achieved with this modified method be observed; this may be attributable had to be evaluated critically because to regular professional tooth cleaning this method has not yet been vali- and maintenance scaling. dated. GO was assessed only at the This conservative approach com- labial aspect and in some cases, scor- bining chlorhexidine use and nonsur- ing of the distal teeth in the dental gical periodontal therapy reduced the arch was not possible. need for surgical intervention. External The results after nonsurgical ther- gingivectomy was necessary in only apy of drug-induced GO described in one case, and the decision for surgical the literature are conflicting. Some treatment was made considering the authors concluded that a nonsurgical individual esthetic concerns of the approach including supra- and sub- patient. Another two patients received gingival tooth cleaning was adequate localized internal gingivectomies, in treating drug-induced GO.6,18 In which were indicated as a result of per- contrast, other investigators demon- sistently increasing PPDs in the molar strated that oral hygiene programs or region. nonsurgical periodontal therapy, while of some benefit to the patient, failed to completely prevent or resolve GO.27,28

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Conclusion References

Within its limitations, the present 1. Dongari-Bagtzoglou A. Drug-associated gingival enlargement. J Periodontol case series suggests that FMD is a 2004;75:1424–1431. beneficial treatment concept for 2. Seymour RA. Effects of medications on drug-induced GO, combining the the periodontal tissues in health and dis- administration of chlorhexidine and ease. Periodontol 2000 2006;40:120–139. nonsurgical scaling and root planing 3. Seymour RA, Ellis JS, Thomason JM. Risk and thereby reducing the need for factors for drug-induced gingival over- further surgical intervention. However, growth. J Clin Periodontol 2000;27: 217–223. further controlled clinical trials need to 4. Guggenheimer J, Mayher D, Eghtesad B. be carried out to evaluate the effects A survey of dental care protocols among of FMD in a homogenous study pop- US organ transplant centers. Clin Trans- ulation. plant 2005;19:15–18. 5. Mavrogiannis M, Ellis JS, Thomason JM, Seymour RA. The management of drug- induced gingival overgrowth. J Clin Acknowledgments Periodontol 2006;33:434–439. 6. Somacarrera ML, Lucas M, Scully C, Barrios This work was supported by grants from the C. Effectiveness of periodontal treatments German Research Organisation/DFG to Dr on cyclosporine-induced gingival over- Bettina Dannewitz (DA 593/1-1), by the post- growth in transplant patients. Br Dent J doc program of the Medical Faculty of the 1997;183:89–94. University of Heidelberg, and by the Neue Arbeitsgruppe Parodontologie e.V. (NAgP). 7. Quirynen M, Bollen CML, Vandekerckhove BNA, Dekeyser C, Papaioannou W, Eyssen H. Full- vs. partial-mouth disinfection in the treatment of periodontal infections: Short- term clinical and microbiological observations. J Dent Res 1995;74:1459–1467. 8. O’Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972; 43:38. 9. Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J 1975;25:229–235. 10. Seymour RA, Smith DG, Turnbull DN. The effects of phenytoin and sodium valproate on the periodontal health of adult epilep- tic patients. J Clin Periodontol 1985;12: 413–419. 11. Schei O, Waerhaug J, Lovdal A, Amo A. Alveolar bone loss as related to oral hygiene and age. J Periodontol 1959;30: 7–16. 12. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev Dent 2003;1:7–16.

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13. Pilatti GL, Sampaio JE. The influence of 24. Kinane DF. Single-visit, full-mouth ultra- chlorhexidine on the severity of cyclo- sonic debridement: A paradigm shift in sporin A-induced gingival overgrowth. periodontal therapy? J Clin Periodontol J Periodontol 1997;68:900–904 [erratum 2005;32:732–733. 1998;69:102]. 25. Quirynen M, Mongardini C, de Soete M, et 14. Thompson EC, Gillespie JB. Hyperplasia of al. The role of chlorhexidine in the one- the gums following Dilantin therapy, with stage full-mouth disinfection treatment of gingivectomy for correction. J Am Dent patients with advanced adult periodonti- Assoc 1942;28:1613–1615. tis. Long-term clinical and microbiological 15. Wong W, Hodge MG, Lewis A, Sharpstone observations. J Clin Periodontol 2000;27: P, Kingswood JC. Resolution of cyclo- 578–589. sporin-induced gingival hypertrophy with 26. O’Neil TC, Figures KH. The effect of metronidazole. Lancet 1994;343:986. chlorhexidine and mechanical methods of 16. Mavrogiannis M, Ellis JS, Seymour RA, plaque control on the recurrence of gingi- Thomason JM. The efficacy of three dif- val hyperplasia in young patients taking ferent surgical techniques in the manage- phenytoin. Br Dent J 1982;152:130–133. ment of drug-induced gingival overgrowth. 27. Seymour RA, Smith DG. The effect of a J Clin Periodontol 2006;33:677–682. plaque control programme on the inci- 17. Bornstein MM, Suter VG, Stauffer E, Buser dence and severity of cyclosporin-induced gingival changes. J Clin Periodontol D. The CO2 laser in stomatology. Part 2 [in French and German]. Schweiz Monatsschr 1991;18:107–110. Zahnmed 2003;113:766–785. 28. Kantarci A, Cebeci I, Tuncer O, Carin M, 18. Aimetti M, Romano F, Debernardi C. Firatli E. Clinical effects of peridontal ther- Effectiveness of periodontal therapy on apy on the severity of cyclosporin A- the severity of cyclosporin A-induced gin- induced gingival hyperplasia. J Peri- gival overgrowth. J Clin Periodontol 2005; odontol 1999;70:587–593. 32:846–850. 19. Ciantar M. Nifedipine-induced gingival overgrowth: Remission following non-surgical therapy. Dent Update 1996;23: 374–377. 20. Hancock RH, Swan RH. Nifedipine- induced gingival overgrowth. Report of a case treated by controlling plaque. J Clin Periodontol 1992;19:12–14. 21. Quirynen M, De Soete M, Dierickx K, van Steenberghe D. The intra-oral transloca- tion of peridontopathogens jeopardises the outcome of periodontal therapy. A review of the literature. J Clin Periodontol 2001;28:499–507. 22. Apatzidou DA, Kinane DF. Quadrant root planing versus same-day full-mouth root planing. I. Clinical findings. J Clin Peri- odontol 2004;31:132–140. 23. Apatzidou DA, Riggio MP, Kinane DF. Quadrant root planing versus same-day full-mouth root planing. II. Microbiological findings. J Clin Periodontol 2004;31: 141–148.

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