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MONITORING OF SUBGINGIVAL BACTEROIDES GINGIVALIS AND ACTINOBACILL US ACTINOMYCE TEMCOMITANS IN THE MANAGEMENT OF ADVANCED PERIODONTITIS L.A. CHRISTERSSON 1 *, B.G. ROSLING 2 , R.G. DUNFORD 1 , U.M.E. WIKESJO 1 , JJ. ZAMBON 1 , AND RJ. GENCO 1 Departments of Oral Biology and Periodontology, Periodontal Disease Clinical Research Center2, School of Dental Medicine, State University of New York at Buffalo, Buffalo, New York 14214, U.S.A.; and The Department of Periodontology, Public Dental Services2, Helsingborg, Sweden Adv Dent Res 2(2):382-388, November, 1988 ABSTRACT n a series of clinical trials involving 79 adult periodontitis patients, we evaluated the clinical and microbiological effects of H O , NaHCO , and a commercially available povidine solution, as adjuncts to I mechanical periodontal debridement. Each trial included a placebo as a control. The healing response was 2 2 3 monitored clinically by measurement of changes in probing attachment levels after treatment. The current report includes data from single-rooted teeth only. In general, healing in severely advanced periodontal lesions (initial pocket depth > 7 mm) was enhanced by the use of the listed topical antimicrobial agents administered subgingivally during mechanical debridement. Correlations were sought between changes in probing attachment levels 12 months after treatment, and the presence of subgingival B. gingivalis and A. actinomycetemcomitans in the periodontal lesions. For a total of 428 lesions included in this report, B. gingivalis was detected in 53.1% of lesions showing probing attachment loss (>1.5 mm), but in only 4.7% of lesions showing gain (> 1.5 mm). Either B. gingivalis or A. actinomycetemcomitans was detected in 70.1% of the lesions showing loss and in only 4.8% of those showing gain. These studies indicate the benefits of the adjunctive antimicrobial therapy described, and the usefulness of specific microbiological monitoring as an aid to clinical measurements in the evaluation of success or failure of treatment of chronic adult periodontitis. PERIODONTITIS: AN INFECTIOUS DISEASE Studies performed several decades ago have clearly defined the relationship between dental plaque and the diseases gingivitis and periodontitis. More recent studies have specifically indicated Gram-negative organisms as the principal micro-organisms involved in their pathogenesis (Newman and Socransky, 1977; Socransky, 1977; Slots, 1979; van Palenstein Helderman, 1981). For example, Bacteroides gingivalis has been implicated as a key organism in severe forms of adult Presented at the Sunstar Portside Symposium, November 14-15, 1986, Kobe, Japan *To whom correspondence should be addressed 382 periodontitis (Tanner et al, 1979; Slots, 1982; Slots and Genco, 1984), and is also reported to be predominant in isolated cases of juvenile periodontitis (Wilson et al., 1985). Actinobacillus actinomycetemcomitans is generally recognized as the main infectious agent in localized juvenile periodontitis (Slots et al., 1980; Zambon et al., 1983; Mandell, 1984; Zambon, 1985) and is also found in adult periodontitis patients (Slots and Genco, 1984). Eikenella corrodens and Capnocyto- phaga sp. are also prominent members of the subgingival flora in pockets of juvenile periodontitis patients (Newman and Socransky, 1977; Mandell, 1984). Other organisms often found in subgingival plaque samples from periodontal lesions include Eubacterium, Haemophilus, Wolinella, Fusobacterium, and Selenomonas; Vol. 2 No. 2 MONITORING OF B. gingivalis AND A. actinomycetemcomitans however, their role in periodontal disease is as yet not clear. The concept that periodontal diseases may be caused by specific micro-organisms — i.e., organisms not regularly found in the healthy gingival sulci and/or oral cavity —suggests the possibilities of using these criteria in the monitoring of periodontal treatment (Genco et al, 1986, 1988). Furthermore, recent studies have reported on the development of methodologies which will provide the technology for rapid assays useful for this purpose (Bonta et al, 1985; Zambon et al., 1985). 383 process over an extensive period of time related to the initial severity of the disease (Badersten, 1984). Regardless of the therapy employed, the outcome in gain of attachment level is reported to be related to the degree of plaque control and the trauma from the technique involved. Furthermore, long-term evaluations of periodontal therapy have suggested that an appropriate maintenance regime, controlling for reinfection, is more important than the regime used to eliminate the initial periodontal infection (Lindhe and Nyman, 1984). MANAGEMENT OF PERIODONTAL DISEASES AS INFECTIOUS DISEASES ADJUNCTIVE ANTIMICROBIAL AGENTS IN THE MANAGEMENT OF THE PERIODONTAL INFECTION Presently, the emphasis in periodontics is directed toward three major goals: (1) treatment of the disease, i.e., elimination of the infection per se; (2) reconstruction of tooth support, i.e., regeneration of lost periodontal tissues; and (3) maintenance of periodontal health. Since periodontal diseases are primarily infections, an anti-infectious approach is the main choice of therapy. Different ways to treat periodontitis have been known for decades. Since complete knowledge of the cause of disease is not available, clinical treatment modalities have often been directed toward technical solutions, such as pocket elimination and reshaping of the diseased alveolar processes by osseous surgical procedures. Today, it is reasonable to consider replacing these technical procedures with therapeutic modalities which are directed to reduction, or elimination, of the infectious agents causing the disease. The importance of plaque control measures and mechanical debridement in various forms of surgical and non-surgical periodontal therapy has been very well-documented in clinical trials over the years (Ramfjord et al, 1973,1975; Zamet, 1975; Lindhe and Nyman, 1975,1984; Nyman et al, 1975,1977; Rosling et al, 1976a, b; Waite, 1976; Knowles et al, 1979,1980; Axelsson and Lindhe, 1981a, b; Badersten et al, 1981, 1984a, b; Hill et al, 1981; Pihlstrom et al, 1981, 1983; Lindhe et al, 1982; Isidor et al, 1984). Results from these studies clearly indicate that the progressive destruction of periodontal support can be arrested, regardless of the specific techniques used for subgingival instrumentation. Also, these studies show that it is possible to eliminate gingival inflammation and progressive periodontitis by combining periodontal therapy with a carefully exercised and supervised maintenance program. Numerous studies have shown the potential of scaling and root planing procedures alone to resolve even advanced periodontitis (Zamet, 1975; Waite, 1976; Hill et al, 1981; Lindhe et al, 1982, 1984; Garrett, 1983; Rosling et al, 1983a, b; Badersten et al, 1984a; Isidor et al, 1984). However, the healing following non-surgical therapy is suggested to be a gradual Since access to most of the infecting organisms in periodontal disease can be accomplished through the orifice of the periodontal pocket, application of antimicrobial agents locally into the periodontal pocket represents a logical alternative for management of the periodontal infection. Also, the use of antimicrobial agents administered systemically or topically to enhance the result of mechanical subgingival debridement is clinically attractive. However, the potential risk for uncontrolled adverse reactions and bacterial drug resistance to antibiotics has to be considered (Genco, 1981; Baker et al, 1985). In order for the risks involved to be minimized, antimicrobial agents with low toxicity and a broad antimicrobial spectrum have been tested and found to enhance the effects of mechanical subgingival debridement (Rosling et al, 1983a, b, 1985, 1986; Christersson et al, 1985a). In the present report, we describe four clinical treatment studies designed to evaluate the effects of adjunctive topical antimicrobials on the changes in clinical attachment level after periodontal therapy. The patient groups included a total of 79 patients, 45 males and 34 females, with an average age of 43 years (Table 1). All patients were systemically healthy and exhibited moderate to severe adult periodontitis. Periodontal examinations were performed at baseline, 6, and 12 months postoperatively, by means of probing pocket depth and probing attachment level (Rosling et al, 1983a). The clinical protocols were similar for all four studies and were designed to evaluate the effects of topical antimicrobial agents as adjuncts to scaling and root planing procedures. Briefly, all patients received three visits of oral hygiene instructions accompanied by supragingival debridement and professional tooth cleaning. Then, subgingival debridements were performed under local anesthesia, with the additional delivery of a test compound or a placebo. The test antimicrobial compounds were: (Study I) a povidine solution (Jodopax®, Ferrosan, Malmo, Sweden) with a final concentration of 0.05% active iodine; (Study 384 Adv Dent Res November 1988 CHRISTERSSON et al. TABLE 1 NUMBER, AGE, AND GENDER OF ADULT PERIODONTITIS PATIENTS INCLUDED IN FOUR CLINICAL TREATMENT STUDIES Study3 Gender Ratio Number of Subjects Mean Age Age Range (males/females) 19 18 18 24 44 41 44 44 28-61 32-61 29-65 33-56 12/7 II III IV Total 79 43 28-65 45/34 I a 8/10 11/7 14/10 Study I: Non-surgical treatment 4- topical iodine application. Study II: Non-surgical treatment + topical baking soda application. Study III: Non-surgical treatment + topical hydrogen peroxide application. Study IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application. II) a baking soda "tooth powder" (NaHCO 3 , Church & Dwight, Princeton, NJ); (Study III) a 3% hydrogen peroxide solution (Swan® 3% H 2 O 2 , Cumberland, Smyrna, TN); and (Study IV) a combination of baking soda (ACO, Sundbyberg, Sweden) and hydrogen peroxide (ACO, Sundbyberg, Sweden). The test compounds and respective placebos were, for all groups, professionally administered at the time of subgingival debridement. The iodine, hydrogen peroxide, and saline (placebo) solutions were administered by connection of a pressurized tank to the cooling system of the ultrasonic unit. The baking soda, the baking soda + hydrogen peroxide mixture, and their corresponding placebos (calcium-diphosphate powder and calcium-diphosphate + saline) were administered as a "slurry" and applied directly into the gingival pockets at the time of subgingival debridement. These compounds were also professionally applied at each postoperative visit. In addition, the patients used their respective compound at home as a substitute for regular toothpaste. In this report, we will describe the overall results of changes in probing attachment level and the correlation of these changes with subgingival B. gingivalis and A. actinomycetemcomitans to evaluate the usefulness of microbiological tests in monitoring success or failure of therapy. Teeth included in this presentation were all non-surgically treated, with subgingival debridement achieved by ultrasonic debridement alone (Odontoson®, Goof A/S, Ftyrsholm, Denmark) in Studies I and III, and debridement with hand instrument alone in Studies II and IV. Periodontal healing was ensured by biweekly professional tooth cleaning for the first three months postoperatively (Rosling et al., 1983a). The baseline values for the percent of pockets 5 mm or greater on single-rooted teeth ranged from 27r.7% to 49.6%. The average percent of these deeper pockets was lowered to between 2.3% and 17.4% at the 12-month examination (Table 2). Reduction in the proportions of deeper pockets was approximately the same in test as in placebo groups, indicating the ability of the non-surgical regimes to manage moderate to severe periodontal disease. The clinical measurements also indicated a gain in the overall average probing attachment level for all groups (data not shown). The proportions of periodontal lesions, which were initially 7 mm or greater in pocket depth, that gained probing attachment level were generally greater for the test groups than for the placebo groups. In the test groups, the proportions of deep sites gaining probing attachment levels of 2 mm or more ranged between 53% and 81%. The corresponding values for the placebo groups were 39% and 55% (Table 3). Conversely, the placebo groups showed higher proportions of sites losing probing attachment level compared with the test groups (Table 3). These results further substantiate previous reports indicating that adjunctive antimicrobial therapy can result in an additional gain in probing attachment level in deep pockets, compared with that achievable with mechanical scaling and root planing alone. BACTERIAL MONITORING AS A SPECIFIC PARAMETER IN PERIODONTAL THERAPY Studies have clearly indicated a strong relationship between elimination of A. actinomycetemcomitans and healing of periodontal defects in localized juvenile periodontitis patients (Slots and Rosling, 1983; Christersson et al., 1985b, 1986; Kornman and Robertson, 1985; Mandell et al., 1986), and hence, therapy can be directed toward elimination of A. actinomycetemcomitans. Studies on the effects of systemic antimicrobial therapy alone further substantiate this concept (Christersson et al., 1985c, 1986; Christersson, 1986). Monitoring black-pigmented Bacteroides in adults has revealed a relationship between recurrent or continuing periodontitis and detectable levels of B. gingivalis at examinations 12 months after therapy (Rosling et al., 1983b, 1986; Slots et al., 1985). The initially promising results from clinical studies utilizing bacterial monitoring, and the development of rapid microbiological techniques (Bonta et al., 1985; Zambon et al., 1985), may represent the advent of a new era in clinical periodontology. For this presentation, we analyzed the results of specific microbiologic monitoring of periodontal healing in the four studies. B. gingivalis and A. actinomycetemcom- itans were assessed as specific indicators of success or failure in treatment of individual deep lesions. The presence or absence of B. gingivalis was analyzed for a total of 428 subgingival plaque samples obtained 12 Vol. 2 No. 2 MONITORING OF B. gingivalis AND A. actinomycetemcomitans 385 TABLE 2 PERCENT OF MEASUREMENT SITES WITH A PROBING POCKET DEPTH > 5 mm AT BASELINE, 6-MONTH, AND 12-MONTH EXAMINATIONS Study3 Group Sites Baseline (%) 6 Months (%) 12 Months (%) I test placebo test placebo test placebo test placebo 510 480 516 526 962 935 546 504 42.2 36.7 27.7 48.7 34.8 28.1 48.0 49.6 2.7 5.8 5.2 5.3 5.3 2.3 11.0 17.3 7.2 5.6 6.4 6.1 14.3 16.7 17.4 13.3 II III IV a Study Study Study Study I: Non-surgical treatment + topical iodine application. II: Non-surgical treatment + topical baking soda application. III: Non-surgical treatment + topical hydrogen peroxide application. IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application. TABLE 3 DISTRIBUTION (%) OF MEASUREMENT SITES RELATED TO CHANGES IN PROBING ATTACHMENT LEVEL AT THE 12-MONTH EXAMINATION FOR SITES WITH INITIAL PROBING POCKET DEPTH > 7mm Studva Test Groups Changes in Probing Attachment Level (% sites) >-2 mm -1,0, + l m m 6 20 19 43 42 80 81 54 53 0 15 5 3 45 46 44 46 55 39 51 50 2 31 67 6 45 49 I II III IV 0 0 Average(%) a Study Study Study Study > +2 mm Placebo Groups Changes in Probing Attachment Level (% sites) >-2 mm -1,0, 4-lmm >+2mm r\ D I: Non-surgical treatment -f topical iodine application. II: Non-surgical treatment + topical baking soda application. III: Non-surgical treatment + topical hydrogen peroxide application. IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application. months after periodontal therapy for patients in Studies I, II, III, and IV. The presence or absence of A. actinomycetemcomitans was analyzed for a total of 265 samples from patients in Studies I, III, and IV. All subgingival plaque samples were obtained with the paper-point technique (Rosling et al, 1983a). Presence of B. gingivalis and A. actinomycetemcomitans was assessed by the indirect immunofluorescence method (Bonta et al, 1985; Zambon et al, 1985). Overall, B. gingivalis was found in 15.2% of the lesions, and A. actinomycetemcomitans in 11.7%, 12 months post-treatment (Table 4). Of the 428 lesions monitored for B. gingivalis, 172 (40.2%) gained probing attachment level (> 1.5 mm) and 32 (7.5%) lost attachment (> 1.5 mm) between baseline and the 12month examination. Of the 172 lesions which gained attachment, eight (4.7%) were positive for B. gingivalis. In contrast, 17 (53.1%) out of the 32 lesions that lost probing attachment level (> 1.5 mm) were pos- itive for B. gingivalis. Forty (17.9%) of 224 periodontal lesions which showed only small or no changes in probing attachment level ( - 1 , ±0, + 1 mm) were also positive for this micro-organism (Table 5). The relationship between presence of A. actinomycetemcomitans and changes in probing attachment level is presented in Table 6. It can be seen that three (2.9%) of the 104 lesions that showed gain in probing attachment level (> 1.5 mm) harbored A. actinomycetemcomitans and, conversely, that seven (29.1%) of the 24 lesions which lost attachment harbored the organism. In conclusion, a high proportion of lesions losing probing attachment level was found to harbor B. gingivalis and/or A. actinomycetemcomitans. The change in probing attachment levels and the results of the microbiological monitoring were strongly correlated (p < 0.001). To illustrate the usefulness of a bacteriological "test", the Fig. depicts the data from three of the four studies 386 Adv Dent Res November 1988 CHR1STERSS0N et al. TABLE 4 NUMBER OF SUBGINGIVAL PLAQUE SAMPLES POSITIVE FOR B. gingivalis AND A. actinomycetemcomitans AT THE 12MONTH EXAMINATION IN FOUR CLINICAL TREATMENT STUDIES Study 3 Number of Samples Number of Samples Positive for Number of Samples Positive for A. actinomycetemcomitansb B. gingivalisb (10.9)c (12.3) (14.0) (24.2) I II III IV 73 163 93 99 8 20 13 24 Total 428 65 (15.2) 8 (10.9) N.A.d 18 (19.4) 5 (5.1) 31 (11.7)c a Study I: Non-surgical treatment + topical iodine application. Study II: Non-surgical treatment 4- topical baking soda application. Study III: Non-surgical treatment + topical hydrogen peroxide application. Study IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application. b Determined by indirect immunofluorescence microscopy (Bonta et al, 1985; Zambon et ah, 1985). c Values within brackets describe percent of samples. d Not Available. e Value within brackets describe percent of samples positive out of 265 samples available. TABLE 5 RELATIONSHIP BETWEEN PRESENCE OF SUBGINGIVAL B. gingivalis AND CHANGE IN PROBING ATTACHMENT LEVEL AT THE 12-MONTH EXAMINATION Number of Positive/Total Number Tested Subgingival Plaque Samplesb by Change, Gain ( + ) , or Loss ( - ) in Probing Attachment Level - 1.0 to Study3 ^ - 1.5 mm + 1.0 mm ^ + 1.5 mm I 4/8 4/28 0/37 II 1/8 6/68 13/87 III 0/2 11/62 2/29 IV 12/14 12/47 0/38 17/32 40/224 8/172 a Study I: Non-surgical treatment + topical iodine application. Study II: Non-surgical treatment + topical baking soda application. Study III: Non-surgical treatment + topical hydrogen peroxide application. Study IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application. b Determined by indirect immunofluorescence microscopy (Zambon et ah, 1985). (265 monitored sites). The "test 7 ' using only B. gingivalis identified 66.7% of the lesions labeled "losers", those periodontal lesions showing loss of 1.5 mm or more as determined by probing attachment measurements. Only 1.9% of the "gamers", those lesions showing an increase of 1.5 mm or more in probing attachment level, showed presence of B. gingivalis (Fig.). The g r o u p of l e s i o n s c o n s i d e r e d " u n changed", based upon measured change in average TABLE 6 RELATIONSHIP BETWEEN PRESENCE OF SUBGINGIVAL A. actinomycetemcomitans AND CHANGE IN PROBING ATTACHMENT LEVEL AT THE 12-MONTH EXAMINATION Number of Positive/Total Number Tested Subgingival Plaque Samples13 by Change, Gain ( + ), or Loss ( - ) in Probing Attachment Level - 1.0 to Study 3 I III IV ^ - 1.5 mm 4/8 0/2 3/14 4- 1.0 mm 4/28 15/62 Z/47 ^ + 1.5 mm 0/37 3/29 0/38 7/24 21/137 3/104 a Study I: Non-surgical treatment 4- topical iodine application. Study III: Non-surgical treatment + topical hydrogen peroxide application. Study IV: Non-surgical treatment 4- topical baking soda and hydrogen peroxide application. b Determined by indirect immunofluorescence microscopy (Bonta et al., 1985). level of > - 1.5 mm to > + 1 . 5 mm over 12 months, exhibited evidence of the presence of B. gingivalis in 19.7% of the lesions. The clinical and microbiological evaluations were in "agreement" for 86% of the lesions. The 14% of "disagreement" should not necessarily be classified as "false" results; they may be interpreted as an indication of the need for further therapy. The "test" which includes the presence of either B. gingivalis or A. actinomycetemcomitans gave similar re- sults, however, with a slightly higher proportion (70.1%) of the "losers" identified as microbiologically positive. The use of additional marker organisms may Vol. 2 No. 2 A. e. gingivalis "losers" D MONITORING OF B. gingivalis AND A. actinomycetemcomitans 387 REFERENCES "unchanged" B. gingivalisandlor ' A. actinomycetemcomitans "unchanged" Fig. —Results of the bacteriological "tests", applied to data obtained 12 months after treatment, for 265 monitored periodontal lesions. The percent values indicate the proportion of lesions, within each category, positive for respective organisms and/or combinations of organisms. "Losers" indicates lesions with an average loss of >1.5 mm of probing attachment level, "unchanged" indicates lesions with an average change of - 1 , 0, or +1 mm of probing attachment level at the adjacent two interproximal measurement sites, and "gainers" indicates lesions with an average gain of >1.5 mm of probing attachment level at the adjacent two interproximal measurement sites. increase the detection of sites undergoing, or being at risk for, loss. Interestingly, the use of two suspected periodontopathogens did not markedly increase the proportion of "gainers" positive (4.8%) for the test (Fig.) —further evidence of the usefulness of bacteriological monitoring as a parameter in the management of periodontal disease. Since periodontal disease is an infectious disease, successful treatment regimes must be anti-infectious in nature. Success in control and prevention will be based on our understanding of the cause of the disease, as indicated by the results from our investigations. Furthermore, monitoring of the subgingival microflora is likely to become useful in the management of periodontitis. Restorative procedures, whether indicated by functional or esthetic needs, do not control the disease per se. Hence, they have to be recognized as separate entities unrelated to efforts directed at controlling the infection. ACKNOWLEDGMENTS This study was supported in part by USPHS Research Grant DE04898 from the National Institute of Dental Research, National Institutes of Health, Bethesda, MD 20892. The authors would also like to express their sincere thanks to Mr. Homer Reynolds for technical assistance, and to Ms. Phyllis Hill for preparing the manuscript. AXELSSON, P. and LINDHE, J. (1981a): Effect of Controlled Oral Hygiene Procedures on Caries and Periodontal Disease in Adults (Results After 6 Years), / Clin Periodontol 8: 239-248. AXELSSON, P. and LINDHE, J. (1981b): The Significance of Maintenance Care in the Treatment of Periodontal Disease, / Clin Periodontol 8: 281-294. BADERSTEN, A. (1984): Nonsurgical Periodontal Therapy. Doctoral Dissertation, University of Lund, Sweden. BADERSTEN, A.; NILVEUS, R.; and EGELBERG, J. (1981): Effect of Nonsurgical Periodontal Therapy, I. Moderately Advanced Periodontitis, / Clin Periodontol 8: 57-72. BADERSTEN, A.; NILVEUS, R.; and EGELBERG,). 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