PEDIATRICDENTISTRY/Copyright @1985 by TheAmerican Academy of Pediatric Dentistry Volume7 Number4

Treatment of juvenile periodontitis with microbiologically modulated periodontal therapy (Keyes Technique)

Thomas E. Rams, DDS, MHS Paul H. Keyes, DDS, MS William E. Wright, DDS, MS

Abstract Antimicrobial therapeutic strategies widely referred to A wide variety of therapeutic approaches have as the Keyes Technique were directed at suppression of been used to manage juvenile periodontitis (JP) pa- the periodontopathicmicroflora of 7 juvenile periodontitis patients whowere treated and followed for at least 22 tients, even though the exact nature of its etiology months. has been understood poorly until recently. Almost all Followingcollection of baseline clinical and of these approaches have employed clinical peri- microbiological parameters,the patients received odontal parameters alone to guide therapy diagnost- meticulous of all teeth with ically, and determine its success or failure. 1-6 Most concomitantirrigation to probing depth of saturated also have placed emphasis in treatment on mechan- inorganic salt solutions and 1%chloramine-T. The ical control of bacteriologically undefined dental patients were recalled at approximately 2- to 3-month plaque, and surgical correction of anatomic and mor- intervals for maintenancecare which was modulated by phologic defects associated with JP disease progres- clinical parametersand phase-contrast microscopic sion (i.e., infrabony pockets, inflamed gingival findings. Six patients received at least 2 courses of tissues). 1-6 systemic (1 gin/day for 14 days) during the Antimicrobial therapy targeted at specific disease- study. Patient hometreatments included daily application of a sodium bicarbonate/3% paste, and associated bacterial species in the subgingival plaque inorganic salt irrigations. microbiota also has been suggested for treatment of Clinical reevaluations madean average of 29.6 months jp.7,s This rationale was applied initially to the treat- posttreatment showedstatistically significant (p(.01) ment of adult periodontitis lesions, and has been re- 9 decreases in bleeding on probingin all patients. ferred to widely as the Keyes Technique, or Significant decreases in probing depth, and gains in microbiologically1°- modulated periodontal therapy. clinical attachmentlevels also were found in all patients, 13 As a therapeutic strategy for the control of specific particularly in advancedsites initially 4-6 mmand >-7 plaque infections ~4,15 associated with human peri- mmin probing depth. Amongsites with initial odontal diseases, it incorporates microbiological eval- attachment loss >-5 mm, 25.8% experienced a >-3 mm uations of the subgingival flora, such as with phase- gain in clinical attachmentlevel from baseline with contrast microscopy, into diagnostic decision-making therapy. Significant decreases in motile organismsand and patient management. 16-21 Additionally, chemical crevicular polymorphonuclearleukocytes present in the subgingival plaque of the patients also occurredwith the antimicrobial agents are utilized in both office ther- antimicrobial therapy employed. apy and patient home treatment procedures as ad- These findings demonstratethat juvenile periodontitis juncts to mechanical plaque removal techniques, such patients can be treated successfully and maintainedon a as~6- root21 planing, flossing, and toothbrushing. long-term basis without periodontal surgery when The concept of directing therapeutic measures at appropriate antimicrobial therapy is directed at the specific microbial pathogens in JP has been supported subgingival periodontopathic microbiota. by recent cultural studies of subgingival plaque from

PEDIATRICDENTISTRY: December 1985/Vol. 7 No. 4 259 JP subjects. These studies repeatedly have associated any renal disorders, hypertension, sodium intake re- elevated numbers of certain species of gram-negative strictions, or previous allergic reactions to tetracycline rods with localized JP sites, especially Haemophilus antibiotics. All patients underwent complete physical (formerly Actinobacillus) actinomycetemcomitans(Ha). 23-25 and hematological examinations (including CBC, SMA- Further, Ha has been shown to elaborate a number 12, and urinalysis) conducted by the NIH Clinical of potential virulence factors (e.g., leukotoxin, colla- Center medical staff to exclude the presence of any genase, immunoglobulin proteases, fibroblast growth contributing systemic medical disorders. None of the inhibitors, and bone resorption factors), which may subjects had any systemic disorders reported to be be important in the pathogenesis of ]p.26 associated with periodontal manifestations in adoles- Some morphologic studies with phase-contrast, cents, such as diabetes mellitus, sarcoidosis, Down’s darkfield, and transmission electron microscopy also syndrome, cyclic neutropenia, agranulocytosis, Pap- have revealed large numbers of spirochetes and mo- illon-Lef~vre syndrome, of Ch6diak-Higashi syn- tile rods in localized JP subgingival plaque.7"8"21"27-31 drome. In vitro evaluations of neutrophil and Consistent with these findings, elevated serum titers monocyte functions were unavailable at the start of of antibodies specific to antigenic determinants of these studies, and were not determined for the pa- Treponemaspecies also have been reported in individ- tients followed. None of the patients had received uals with localized jp.32,33 However, there is evi- any type of periodontal prophylaxis or systemic an- dence that not all localized JP patients harbor high tibiotic therapy during the previous 6-month period. proportions of motile bacteria in their subgingival mi- croflora, 4"23’34"35 and the exact role of these organ- Diagnostic Procedures isms in JP is not well understood. The purpose of the present investigation was to determine whether the principles of microbiologically Clinical Examinations modulated perioclontal therapy (Keyes Tech- Clinical parameters for all teeth were assessed in- nique)7,s, lo-13, 16-20 could be applied successfully to dependently by a single NIDRstaff periodontist (au- the long-term clinca[ managementof JP. thor WEW)who was unaware of the patient’s course of therapy (single-blind evaluation). Periodontal probing depths and clinical attachment levels were Methods and Materials measured to the nearest mm at interproximal and This longitudinal therapeutic investigation was buccal surfaces of all teeth with a calibrated probe, as conducted within the clinical research facilities of the described38 by Philstrom et al. National Institute of Dental Research (NIDR), of the The degree of gingival inflammation for each tooth National Institutes of Health (NIH) in Bethesda, was determined by scoring the amount of bleeding Maryland. The patients studied were selected from seen after gentle probing to the "bottom" of the gin- persons referred to the NIDRdental clinic for peri- gival sulcus. A sulcular bleeding score was assigned odontal disease treatment. Seven untreated patients as follows:.0 = no bleeding, 1 = spot bleeding point younger than 22 years of age with idiopathic JP, as only, 2 = bleeding along the . defined by Baer, 36 were treated and followed for at least 22 months posttreatment (Table 1). Five of the Microbiological Examinations JP patients were classified as having localized cases At each patient appointment, the composition of (first molars, incisors, and additional teeth equaling the subgingival plaque was monitored with phase- <14 total teeth), and 2 patients had generalized cases contrast microscopy at chairside to assess the effec- (->14 total teeth involved), based on the number tiveness of the therapeutic measures. No cultural or affected teeth. 37 The 5 females and 2 males in the immunologic monitoring was conducted as part .of study had a meanage of 18 years (range = 12-21 years), this study. and 193 teeth on initial examination. The follow-up Enumeration of disease-associated morphotypes in clinical observations on the patients ranged from 22 subgingival plaque samples with phase-contrast mi- to 39 months posttreatment, with a mean of 29.6 croscopy followed procedures previously de- months. scribed, 7"16-21 and included counts of spirochetes, All patients were in good general health and pre- brush formations, motile rods (large-, medium-, and sented with radiographic evidence of >50%bone loss small-sized), oral protozoa (i.e., Entamoebagingivalis, associated with the permanent first molars and inci- tenax), .and accumulated crevicular poly- sors (Fig 1), and of ->7 morphonuclear leukocytes. at these sites. Comprehensive medical and dental Briefly, subgingival plaque was removed carefully histories were obtained, with particular emphasis on from periodontal sites with a sterile curette, placed

260 TREATMENTOF JUVENILE PERIODONTITIS: Ramset al. FIG 1. Typical molar/incisor angular defects associated with untreated JP lesions.

into 0.02 ml of sterile water on a microscopic slide, eral months after the last posttreatment clinical eval- coverslipped, and examined immediately at 400x and uations were made. 600x with a high quality, phase-contrast microscope. The highest scoring fields for each of the bacterial and Therapeutic Procedures cellular morphotypes then were recorded. Based on previous research,17-18-21 patients with periodontal pockets harboring ^ 125/highest scoring Professional Office Therapy fields of either spirochetes, medium- or large-sized All teeth were subjected to meticulous subgingival motile rods (spinning, 2 x 3-9+ |xm), or crevicular scaling and root planing until a smooth, hard root polymorphonuclear leukocytes were considered in this surface was detected clinically. Chemical antimicro- study to have elevated numbers of disease-associated bial agents actively were delivered subgingivally and morphotypes. Small, highly motile coccobacilli (0.1- maintained in periodontal pockets throughout these 0.2 u,m in diameter), which exhibited a circular "dart- procedures. Between instrumentation of different root ing" motion, were not considered to be disease-as- surfaces, instruments were disinfected routinely by sociated in this study, since previous reports have passage through antiseptic solutions, such as 1% found this plaque morphotype predominantly in chloramine-T (sodium para-toluene sulfonchloram- healthy periodontal sites.17-18 ide), or 3% hydrogen peroxide saturated with sodium Multiple (^ 2) periodontal sites in each patient were chloride. monitored microbiologically as a supplement to clin- All periodontal pockets were irrigated profession- ical periodontal parameters. Advanced periodontal ally to probing depth before, during, and after me- pockets and furcations in particular were monitored chanical instrumentation with chemical antimicrobial closely throughout the posttreatment observation pe- agents. Chloramine-T (1%) was used for this pur- riods, since the possibility of a disease-associated flora pose, along with a saturated inorganic salt solution remaining in subgingival sites after the completion of consisting of sodium bicarbonate (NaHCO3) or so- treatment is known to increase significantly with re- dium chloride (NaCl). sidual probing depth.39-40 To facilitate rapid subgingival drug delivery to As these sites came into microbiological control, probing depth, especially into advanced sites (^ 7 samples from additional surfaces less severely in- mm) and furcations, oral irrigation devices were volved in each quadrant were evaluated to confirm modified with foot-activated on/off switches, and suppression of the disease-associated morphotypes. equipped with monojet irrigation tips having 23- or However, microbiological data reported in the results 25-gauge blunt needle or cannula extensions 10 mm section is limited to levels of disease-associated mor- long, as described elsewhere.41 The extended tip was photypes in periodontal sites presenting at recall ap- advanced like a to probing depth pointments with the worst clinical conditions (i.e., and into furcations to maximize contact and exposure gingival inflammation) in each patient, and/or sur- of subgingival plaque bacteria to the antiseptic agents faces having the greatest residual probing depth or during the mechanical sessions. furcation involvement. For some patients, additional Approximately 4-6 hr were required for initial me- microbiological observations were collected for sev- chanical instrumentation and professionally applied

PEDIATRIC DENTISTRY: December 1985/Vol. 7 No. 4 261 subgingival chemotherapy. No surgical flaps or os- placed on a short-term course of systemic tetracycline seous recontouring procedures were employed. All HCI therapy (1 grn/day for 14 days). As previously carious lesions and defective restorations were re- stated, patients with periodontal sites harboring ~ stored or replaced as needed. 125/highest scoring fields of either spirochetes, me- dium-+ to large-sized motile rods (spinning, 2 x 3-9 Patient HomeTreatment Procedures ~m), or crevicular leukocytes were considered in this All patients were instructed in sulcular - study to have elevated numbers of disease-associated ing and flossing. As previously described, 7"8 patients morphotypes. The effects of adjunctive antibiotic also were directed to apply daily a saturated inor- therapy on motile bacteria and crevicular leukocyte ganic salt solution (i..e., 2 tablespoons of NaHCO3or levels were checked, by examining new subgingival NaC1dissolved into 112 fl oz warmwater) with an oral plaque samples with phase-contrast microscopy at the irrigation device (unmodified) at a moderate-to-high end of the 14-day drug course. pressure setting. This was then to be followed by Periodontal recall therapy was carried out a.t ap- application of a sodium bicarbonate/3% hydrogen proximately 2-3 month intervals, and included rein- peroxide paste or slurry to the dentogingival surfaces forcement of patient home treatment procedures, via toothbrushing, flossing, interdental brushes, and mechanical instrumentation of all tooth surfaces, and rubber cone stimulators (#600a). Instruction and re- subgingival irrigations to probing depth of all sites inforcement was emphasized to encourage the pa- with chemical antimicrobial agents. Additional sys- tients to deliver the antimicrobia! chemicals as deeply temic tetracycline therapy as described above was as possible into the sulcus/pocket spaces during the prescribed if further clinical deterioration appeared self-applied treatments. All of the patients were ca- and/or persistent reinfection of the subgingival mi- pable of completing this home treatment regimen in croflora with high levels (~ 125/highest scoring fields) approximately 10-15 min. of motile bacteria or accumulated crevicular leuko- At each recall appointment, patients viewed phase- cytes were seen with phase-contrast microscopic contrast microscopic projections showing the bacte- monitoring. riologic composition of their subgingival plaque on equipment previously described. 7 This served as a Data Analysis feedback mechanism aiding in patient education, mo- Patient means for probing depth and attachment tivation, and compliance with prescribed home treat- level were calculated after categorizing the baseline ment procedures. The microscopic analysis also aided and posttreatment data on the basis of the covariate the treating clinician in assessing the self-care ability of the original probing depth, as suggested by Pihls- of patients to deliver antimicrobials into the targeted trom et al., 38 into 3 categories of pockets initially 1-3 treatment sites. ram, 4-6 mm, and those ~ 7 mmoA paired t-test was utilized to determine statistically significant differ- Modulation of Therapy ences with treatment in probing depth and attach- The antimicrobial effects of the professional and ment level from baseline measurements. A value of home treatment procedures were monitored by (1) p ~ 0.05 was required for statistical significance. clinical examinations for evidence of changes in gin- The number of sites having major changes in at- gival inflammation and periodontal attachment level, tachment level (~ 3 mm) between baseline and post- and (2) phase-contrast microscopy to determine treatment examinations were tabulated to supplement whether a satisfactory elimination of the initial per- interpretation of mean values reported for attach- iodontopathic subgingival flora had been obtained. ment level alterations, as suggested by Haffajee et Levels of motile bacteria and accumulated crevicular polymorphonuclear leukocytes in subgingival plaque TABLE1. Patient Characteristics samples were used in this study as "indicator" mor- photypes to assess the presence of a disease-associ- Length of Patient DiaBnosis ABe Race Sex Follow up (mo) ated subgingival flora, and to identify patients at 1. JP LJP 12 B F 36 increased risk of destructive disease activity. 2. JG LJP 16 B F 31 Patients suffering additional clinical deterioration 3. TC LJP 19 B F 39 and/or identified as remaining with elevated numbers 4. NS LJP 21 C F 22 of disease-associated morphotypes in their subgin- 5. JB LJP 21 B M 25 gival flora after repeated use of the locally applied 6. JM GJP 16 B F 25 7. JF GJP 21 C M 29 chemomechanical procedures described above, were ~ = 18 ~ = 29.6

#600 -- John O. Butler Co: Chicago, IL. LJP = localized case, GJP= generalized case.

262 TREATMENTOF JUVENILEPERIODONTITIS: Rams et al. al. 42 This enabled determination of the frequency of initially ~ 7 mm, marked decreases (mean = 2.85 significant clinical improvement or deterioration at mm) were found with therapy in pocket depth (Table individual periodontal sites which, according to Lindhe 3). Most of the pocket depth reductions were due to et al.,4a are unlikely to be explained by measurement large gains in clinical periodontal attachment levels. error. An average of 2.66 mmof clinical periodontal attach- Differences in the frequency distribution of sulcular ment level gain relative to the pretreatment m~asure- bleeding scores and microbiological parameters be- ments was recorded at advanced sites after treatment tween baseline and posttreatment examinations were (Table 3). Both the mean probing depth and clinical analyzed44 by the Wilcoxon rank sum test. periodontal attachment level changes seen with treat- ment were statistically significant from pretreatment Results baseline values (p < 0.01). Prevalenceof MajorChanges in Clinical AttachmentLevel: A ~ 3 mmgain in clinical periodontal attachment Clinical Findings level from pretreatment values following therapy was Tooth Mortality: Noneof the 193 teeth treated in the recorded at 62 sites in 6 of the study patients. These 7 JP patients were lost during the course of the study. individual surfaces experiencing large beneficial Gingival Inflammation: The degree of gingival in- changes in clinical periodontal attachment level rep- flammation, as measured by the amount of bleeding resented 10.7% of all sites followed in the study pa- on probing, was reduced significantly at the post- tients, and 25.8%of sites with initial clinical periodontal treatment examinations from the pretreatment base- attachment loss of ~ 5 mm. line measurements (p < 0.01, Table 2). Prior to the Sites having major loss of clinical periodontal at- start of periodontal therapy, 56.1% of all teeth had tachment during the posttreatment observation pe- sulcular bleeding scores of 2. At the posttreatment riods were rare. Seven sites in 3 patients, constituting evaluations, sulcular bleeding scores of 2 were found 1.2% of all sites treated, suffered a ~ 3 mmloss of on only 5.6% of all teeth, while 65.8% of all teeth had clinical periodontal attachment from the pretreatment no present (Table 2). A similar baseline measurements. Of these 7 sites, 1 initially reduction in gingival inflammation was seen on a had clinical periodontal attachment loss of 5 mm,and subset of 124 teeth (64.2% of all teeth) having one 6 had initial loss of 2-3 mm. more surfaces with ~ 5 mmof attachment loss. Sul- cular bleeding scores of 2 were found on only 4.8% Adverse Reactions and Side Effects: No adverse reac- tions or side effects to systemic tetracycline therapy of these severely affected teeth after treatment, com- occurred in the patients followed. No adverse reac- pared to 66.9% before treatment. tions or side effects (such as periodontal abscesses) Mean Probing Depth and Clinical Attachment Level were associated with daily applications of inorganic Changes -- (A) For Sites Initially 1-3 ram: Sites with salt solutions with an oral irrigation device at mod- initial probing depths of 1-3 mmexperienced a sta- erate-to-high pressure settings. Daily use of an H202/ tistically significant slight decrease in probing depth NaHCOslurry as a topical antimicrobial treatment (0.10 ram) following treatment. No statistically sig- 3 agent did not lead to black hairy tongue conditions, nificant changes in clinical periodontal attachment were associated with treatment of initially shallow surfaces or damagehard or soft tissues in any of the patients after completion of initial periodontal therapy. (Table 3). (B) For Sites Initially 4-6 mm: Periodontal pockets initially 4-6 mmin depth exhibited a statistically sig- Microbiological Findings nificant (p < 0.01) decrease from pretreatment base- line values in pocket depth of approximately 1 mm, and a mean gain in clinical periodontal attachment Pretreatment level of 0.77 mm(Table 3). Prior to the start of any therapy, all subgingival (C) For Sites Initially ~ 7 mm:In advanced JP sites plaque samples examined from the study subjects contained high levels (~ 125/highest scoring fields) "¢,~BtE 2. Gingival Inflammation: Bleeding After Probing of spirochetes, medium- to large-sized motile rods (spinning, 2 x 3-9+ ~m), and accumulated crevicular Frequency Distribution of Sulcular polymorphonuclear leukocytes (Figs .2-4). Highly Bleeding Scores (all teeth) structured brush formations with coordinated spiro- 0 1 2 chetal movement,as previously described, 17,18,21 were. Baseline 32.0% 9.7 56.1 Posttreatment 65.8 28.6 5.6" observed in 58.3% of the pretreatment plaque sam- ples, and oral amoebae(E. gingivalis) were present in * Significantly different from baseline, p < .01. 41.7%.

PEDIATRICDENTISTRY: December 1985/Vol. 7 No. 4 263 TABLE3. Analysis of MeanDifferences in Probing Depthand Clinical AttachmentLevel

MeanClinical Initial No. of Mean Probing Mean Probing Mean Probing Attachment Pocket Depth Sites Depth Pretreatment (mm) Depth Posttreatment (mm)* Depth Reduction Level Gain (mm) 1-3 mm 339 2.60 2.50 0.10 _ 0.03** -0.04 - 0.03 (NS) 4-6 mm 157 4.86 3.79 1.07--- 0.11"* 0.77 --- 0.10"* ~>7 mm 83 7.95 5.10 2.85 _ 0.33** 2.66 _+ 0.30**

* Mean= 29.6 too. ** Statistically significant difference from pretreatment,p < 0.01. NS-- nostatistically significant differencefrom pretreatment.

LEVELS OF SPIROCHETES(JUVENILE PERIODONTITIS) LEVELS OF CREVICULAR LEUKOCYTES (JUVENILE PERIODONTITIS)

~NITIALBEFORE 0-6 7-12 tI-1B 19-24 25-3031-36 37-57 TOTAL o ~ DX TETRA 057 INITIALBEFORE 0-6 7-12 13-18 19.24 25-30 31 36 37-57 TOTAL CYCLINE MONTHSAFTER FIRST COURSE DX TETRA: 0-57 [1 4 Mo.} OFTETRACYCLINE CYCLINE MONTHSAFTER FIRST COURSE- OFTETRACYCLINE

SUBJECTS7 7 7 7 6 4 2

CREVICULARLEUKOCYTES/ ¯ TNC() 125) FIELD B 50 100+

F=G2. Changeswith treatment in subgingival spirochetes. F=G4. Changeswith treatment in crevicular polymorphonu- clear leukocytes.

LEVELS OF MOTILE RODS(JUVENILE PERIODONTITIS) and 72.4%, respectively, of the subgingival plaque samples microscopically examined during this pe- riod. Brush formations also were detected in 24.1% of the samples. All of the study subjects had at least one periodontal ~ite remaining with elevated num- bers of disease-associated morphotypes (spirochetes, motile rods, and/or crevicular leukocytes present at INITIALBEFORE 06 712 1318 1924 25-30 313~ 3757 TOTAL ~ 125/highest scoring fields), following application of DX TETRA- 057 CYCLINE MONTHSAFTER FIRST COURSE (1-4 OFTETRACYCLINE local periodontal treatments. SAMPLESEXAMINED 12 29 Based on the persistence of these disease-associ- SUBJECTS 7 7 637 4t7 3~7 3~6 2~5 13 11 22~7 ated morphotypes, all of the study patients then were MOTILERODS/ ¯ TNCI) 125I FIELD prescribed systemic tetracycline therapy (1 grn/day for 14 days).

F=G3. Changeswith treatment in subgingival motile rods. Posttetracycline Therapy At all time periods after completion of the first course Pretetracycline Therapy of systemic tetracycline therapy (0-6 months through With local periodontal treatment consisting of re- 37-57 months), the prevalence of spirochetes, motile peated root planing, subgingival chemotherapy, and rods, and crevicular leukocytes was reduced signifi- patient home treatment procedures, a significant re- cantly (p < 0.01) relative to the baseline and prete- duction was achiew.~d during the first 4-month period tracycline therapy periods (Figs 2-4). Additionally, in the numbers of motile bacteria and crevicular leu- brush formations were seen in only 6.3%, and E. gin- kocytes in sampled sites (p < 0.01), (Figs 2-4). givalis in only 3.2% of the 222 plaque samples ex- ever, spirochetes, medium- to large-sized motile rods, amined after the administration of systemic tetracycline and crevicular leukocytes still were found to be ele- therapy. vated (~> 125/highest scoring fields) in 44.8%, 51.7%, Immediately after completion of the.first 14-day

264 TREATMENTOF JUVENILE PERIODONTITIS:Rams et al. systemic tetracycline course, all monitored sites (N posttreatment period, while only 2 of the sites (50%) 24 sites) had significantly reduced (4 10/highest scor- were found reinfected with high levels of motile rods. ing fields) or undetectable levels of spirochetes and However, in contrast to the findings with motile bac- motile rods present in the subgingival microflora. teria, all 4 (100%) of the monitored sites with ~ 3 Spirochetes, in particular, appeared quite suscepti- of clinical periodontal attachment loss consistently had ble, with 91.7% of the plaque samples taken imme- high levels (~ 125/highest scoring fields) of crevicular diately after systemic tetracycline therapy having no leukocytes throughout the posttreatment period. In spirochetes present. Subsequently, low or undetect- this regard, none of the 10 microscopically monitored able levels of spirochetes were found in 79.3% of the sites experiencing a ~ 3 mmgain in clinical peri- subgingival plaque samples examined during the 0 odontal attachment from pretreatment values had el- to 6-month posttetracycline therapy period, and in evated crevicular leukocyte levels present at any 78.8% of all samples taken up to 57 months posttreat- examination during the posttreatment period. ment (Fig 2). A similar pattern was seen with motile rods, with 71.1% of all samples analyzed up to 57 Discussion months posttreatment having only low or undetect- able levels of medium- to large-sized motile rods The early onset and rapidly progressive attachment present (Fig 3). loss characteristic of JP has been related clearly to Most monitored sites (70.8%) also had low levels subgingival colonization by suspected periodontal (4 25/highest scoring fields) of crevicular leukocytes pathogens, and the presence of host cell-mediated immediately after completion of systemic tetracycline immunodeficiencies, particularly in monocyte and therapy. However, 6 periodontal sites, representing neutrophil leukocyte functions. 4s Considerable re- 25.0% of the 24 sites monitored during systemic tet- search attention is being focused on elucidating the racycline therapy, continued to have elevated num- exact nature of these host immunedefects, and pre- bers (~ 125/highest scoring fields) of crevicular liminary studies seeking therapeutic measures to en- leukocytes immediately after the 14-day drug course. hance impaired leukocyte functions appear During the 57omonth posttreatment period, a high promising. 46,47 However, until these approaches are percentage of monitored sites (85.1%) harbored only developed more thoroughly, the clinical management low or moderate levels of crevicular leukocytes (Fig of JP needs to be directed primarily at elimination of 4). the subgingival periodontopathic flora. Additional adjunctive systemic tetracycline therapy The results of the present investigation demon- was prescribed to 6 of the study patients within 12 strate that a combined local and systemically deliv- months of the first antibiotic course. Three patients ered antimicrobial treatment approach can produce received additional systemic tetracycline therapy (1 long-term apparent arrest of destructive disease ac- gm/day for 14 days) at approximately 12-month in- tivity in most JP lesions without periodontal surgery. tervals. Three patients required only I additional sys- Marked clinical improvements were seen posttreat- temic tetracycline course, which was given within 6 ment, with significantly reduced bleeding on prob- months of the original course. In 9 of 11 instances ing, decreased probing depths, and gains in clinical where additional systemic tetracycline therapy was periodontal attachment being measured in all of the prescribed, elevated levels of both motile bacteria and study subjects. crevicular leukocytes were seen microscopically. In 6 Pronounced clinical changes were especially evi- of these cases, organized brush formations also were dent in JP sites having advanced periodontal break- present. In 2 cases, additional systemic tetracycline down. In sites with initial probing depths of ~ 7 mm, therapy was given where high levels of crevicular large gains in clinical periodontal attachment (mean leukocytes (~ 125/highest scoring fields) alone were = 2.66 mm), and highly significant decreases in being detected consistently, even in the relative ab- probing depth from pretreatment baseline measure- sence of motile disease-associated morphotypes in the ments (p < 0.01), were associated with the treatment accompanying subgingival flora. regimen studied (Table 3). Additionally, 25.8% of all treated surfaces presenting with initial clinical peri- Microscopic Findings Relative to Major odontal attachment loss of ~ 5 mmexperienced a ~ Attachment Level Changes 3 mmgain in clinical periodontal attachment from the Of the 7 sites which experienced a ~ 3 mmloss of pretreatment evaluations. Only 1.2% of all sites treated clinical periodontal attachment from pretreatment lost ~ 3 mmof clinical periodontal attachment from baseline measurements, 4 of these sites were moni- baseline values, and no teeth were extracted during tored microscopically throughout the posttreatment the course of the study, despite advanced clinical at- observation period. Only 1 of these sites (25%) re- tachment loss initially present on severely affected colonized with high levels of spirochetes during the teeth.

PEDIATRICDENTISTRY: December 1985/Vol. 7 No. 4 265 Standardized probing forces with pressure-sensi- proaches (i.e., root planing, tooth brushing, flossing) tive periodontal probes were not used in this study with local subgingival applications of chemothera- for assessment of clinical parameters. Smaller vari- peutic agents has been suggested previously, 14,5~ but ances in clinical measurements, though not statisti- rarely utilized in the treatment or adult or JP patients. cally significant, are found with standardized versus In carefully controlled clinical studies on adult peri- nonstandardized probing forces. 48 However, in the odontitis patients, s2"s3 subgingival applications of so- present study, reproducibility of clinical parameters dium bicarbonate (NaI-ICO3) , sodium chloride (NaC1), was maintained by having a single periodontist col- and hydrogen peroxide were found to enhance sig- lect (on a single-blind basis) all of the probing depth nificantly the microbiological and clinical effects of and clinical periodontal attachment level measure- periodontal scaling and root planing. Significantly ments. more profound reductions in probing depths, gains The findings reported here are consistent with other in clinical periodontal attachment levels, and in- clinical studies describing long-term successful treat- creased alveolar bone density in sequential standard- ment and maintenance of JP lesions. 1"2"4’5 However, ized radiographs of interproximal areas were seen after the present investigation differs from these previous 12 months, especially in advanced sites initially >~ 7 studies in that (1) microbiologic criteria supple- mm in depth, after a combined chemomechanical mented clinical parameters for therapeutic decision- therapeutic52 approach was employed. making, (2) local subgingival chemotherapy was ad- Rosling et al. s4 also have shownthat in multirooted ministered both professionally and in home treat- teeth with furcation involvements, where mechanical ment procedures as adjuncts to mechanical debridement is difficult and likely to be imperfect, debridement, and (3) no periodontal surgical proce- irrigating the furcation areas with chemical antimi- dures were employed. crobial agents enhances conventional periodontal Lindhe4,5 previously has called for studies of non- therapy. Significantly greater reductions in motile surgical treatment modalities for JP. The observations bacteria, and gains in clinical periodontal attachment reported in the present study unequivocally docu- were found after 1 year in furcated sites that received ment that stabilization and long-term arrest of most adjunctive subgingival iodine irrigation during peri- JP lesions can be attained without periodontal sur- odontal54 scaling and root planing. gery. These findings represent the first long-term In JP patients, Adcocket al. 5s have reported that clinical results beyond 18 months for a nonsurgical subgingival sodium hypochlorite and 5% citric acid therapeutic49 approach to JP. Similarly, Gencoet al. applications used in conjunction with subgingival cu- treated 9 localized JP patients with a nonsurgical rettage significantly reduced spirochetes and cultiv- treatment regimen consisting of scaling and root able gram-negative anaerobic rods for at least a 3- planing in combination with systemic tetracycline month posttreatment period in advanced localized JP therapy (1 grn/day for 14 days every 8 weeks). Over lesions. However, repeated root planing alone, or in an 18-month period no further alveolar bone loss was conjunction with topically applied 10%povidone-io- seen with standardized radiographs in any of the mo- dine is ineffective in adequately reducing subgingival lar/incisor infrabony defects monitored, and in one- levels of Ha in localized JP pockets.29,56 third of the defects an increase was seen in the al- In the present investigation, inorganic salts, chlor- veolar bone levels after treatment. amine-T, and hydrogen peroxide were used as local The study design followed in this investgafion does chemotherapeutic agents on JP sites. These com- not allow direct comparisons to be made between our pounds were selected on the basis of their availabil- nonsurgical treatment results and those reported us- ity, lo’w toxicity, antibacterial properties, and ing periodontal surgery. However,it is clear from the recognition as accepted dental therapeutic agents by degree of clinical stabilization and long-term arrest of the American Dental Association. s7 In contrast, most clinical periodontal attachment loss in the patients commercially available toothpastes have almost no studied, that surgical intervention may not be an antibacterialss effects against plaque organisms, obligatory componentcritical for the successful man- In vitro studies have found that hydrogen perox- agement of most JP lesions. In fact, some of the pa- ide, in addition to its antiseptic properties, can in- tients treated nonsurgically with these antimicrobial activate the inhibitory effects of bacterial endotoxins approaches stabilized to such an extent that fixed or- on gingival fibroblast growth. 59 However, it is not thodontic repositioning of maloccluded teeth was presently knownif this occurs in vivo. carried out without complication, s° Thus, further in- Saturated NaHCO3and NaC1 solutions have been vestigative research is warranted on nonsurgical shown to be rapidly bactericidal to oral spirochetes treatment modalities based on control of specific dis- and motile rods, and can induce ultrastructural changes ease-associated plaque organisms. cytotoxic to subgingival plaque microorganisms from Supplementing mechanical plaque removal ap- diseased sites after brief in vitro exposure.6° In cul-

266 TREATMENTOF JUVENILE PERIODONTITIS:Rams et al. turing studies by Newbrun et al., 61 a large number greater improvements in clinical periodontal param- of suspected periodontopathic microbial species, in- eters were seen in these sites with irrigation of the cluding organisms closely associated with JP, were antimicrobial69 agent. found to be highly susceptible in vitro to the anti- Despite the intensive local subgingival chemother- microbial effects of NaHCO3,NaC1, and chloramine- apy and mechanical debridement, all patients in the T. The minimal bactericidal concentrations (MBCs) present investigation required administration of sys- NaHCO3and NaC1 against Ha and temic tetracycline therapy, which was given for a 2- were ~ 2.5%. The MBCsof these salts were ~ 5.0% week period (1 g/day). This suggests that sustained against Bacteroides gingivalis, which also has been im- suppression of disease-associated microscopic mor- plicated as a possible periodontopathogen in gener- photypes with nonsurgical treatment modalities may alized62 JP patients. be difficult to attain in advanced JP sites without ad- The therapeutic doses of these inorganic salts as junctive systemic antibiotic therapy. The need for applied in office and homeirrigations in this study systemic tetracycline therapy most likely was due to were approximately 14% for NaHCO3, and 18% for the invasion and colonization by periodontopathic NaC1(i.e., 2 tablespoons of the salt dissolved into 12 bacteria of gingival connective tissues and epithelium fl oz warm water). The 1% chloramine-T concentra- adjacent to infected pockets, 7° although no histologic tion used in this study for office irrigation of JP sites studies of gingival tissue biopsies were conducted to is also rapidly bactericidal to oral spirochetes and mo- substantiate this hypothesis. tile rods,6° and is effective against Ha and B. gingivalis Clinical studies have demonstrated that marked at61 a minimal inhibitory concentration of ~ 0.3%. suppression or elimination of subgingival Ha, which Thus, NaHCO3,NaC1, and chloramine-T were intro- may invade subepithelial tissues, 7° can be achieved duced repeatedly into JP lesions during this study at via (1) 3 weeks of systemic tetracycline HC1therapy therapeutically significant levels knownto be bacte- (1 g/day) 29, or by (2) surgical excision of inflamed ricidal or inhibitory to suspected periodontopatho- gingival tissues using either soft tissue curettage or gens associated with JP lesions. periodontal flap surgery. 7~ Genco et al. 49 also have Regardless of the in vitro capabilities of the afore- reported that the ability of nonsurgical treatments to mentioned compounds, it must be stressed that ef- arrest progressive bone loss in localized JP sites is fective clinical use of chemical antimicrobial agents in enhanced significantly with systemic tetracycline periodontal therapy requires adequate subgingival therapy. drug delivery into the targeted treatment sites. This In the present study, additional courses of systemic concept is essential to both professional- and patient- tetracycline therapy were needed during mainte- administered regimens. Inorganic salts and hydrogen nance therapy due to the reestablishment of a dis- peroxide do not alter significantly the subgingival mi- ease-associated microflora in some sites. This may croflora or clinical parameters of advanced periodon- have been due to incomplete suppression and sub- tal pockets if applied only supragingivally, such as sequent regrowth of suspected periodontal patho- with tooth brushing. 63 Similar findings have been re- gens, such as Ha, which can persist in some ported with mouthrinsing of 64 and periodontal sites after only 2 weeks of systemic tet- stannous fluoride, 6s presumably because of insuffi- racycline therapy. 29 The presence of elevated num- cient sulcular penetration. bers of crevicular polymorphonuclear leukocytes in 6 In the present study, modified oral irrigation de- periodontal sites immediately after 2 weeks of sys- vices with extended tips 41 were employed to over- temic tetracycline therapy may have reflected the per- come these problems in subgingival delivery of sistence of a periodontopathic subgingival microflora chemical antimicrobials into advanced periodontal incompletely eradicated by the systemic tetracycline sites. Additionally, patient hometreatment regimens regimen used in this study. However, in all other included daily applications of saturated inorganic salt sites monitored, significant and sustained decreases solutions via unmodified oral irrigation devices, in in subgingival spirochetes, motile rods, and crevi- order to extend subgingival bacterial control. cular polymorphonuclear leukocytes were achieved Oral irrigation devices (unmodified) have been following systemic tetracycline therapy. Low or un- shown to penetrate solutions most commonly to 75% detectable levels of these disease-associated morpho- of the clinical probing depth of sites ~ 7 mm,66 and types were maintained for extended periods with local in some studies, to at least 6 mmbelow the free gin- chemomechanical measures (Figs 2-4). gival margin.67 Eakle et al. 6s also have demonstrated In regard to this, locally applied antimicrobials, such that both oral irrigation with water and 0.1% stan- as inorganic salts and chloramine-T, may be partic- nous fluoride can reduce significantly the proportions ularly valuable during periodontal maintenance. The of spirochetes in the subgingival flora of untreated effects of these agents may act to prolong the im- sites 4 mmor greater in probing depth. Significantly mediate efficacy of other therapeutic measures (i.e.,

PEDIATRICDENTISTRY: December 1985/Vol. 7 No. 4 267 root planing, tetracycline, periodontal surgery) by fa- throughout the posttreatment period. High levels of voring posttherapy colonization of treated sites by crevicular leukocytes are characteristic of untreated microbial species which are antagonistic to the re- JP sites, 2L77-79 even though these sites commonlyare growth of a pathogenic microbiota. Hillman and colonized by Ha, which elaborates a leukotoxin and Socransky72 have demonstrated that Streptococcus san- factors which inhibit leukocyte chemotaxis. 26 Several guis, Streptococcus ~beris, and Actinomyces taken from studies have found the numbers of crevicular healthy periodontal sites or from sites with periodon- leukocytes in untreated JP sites to be similar to those tal disease other than JP are inhibitory to the growth levels21,77-7 seen9 in untreated adult periodontitis sites. of Ha strain Y4. Such species were not present in JP Additionally, healthy periodontal sites in JP patients sites highly infected with the Ha strain Y4. Bonta et contain approximately tenfold fewer numbers of al. 7a also have reported that S. sanguis, S. mitis, and crevicular leukocytes than diseased sites.77 S. salivarius are inhibitory to the growth of Ha, and Thus, the presence of elevated crevicular leuko- are twice as prevalent in healthy versus diseased sites cytes after completion of therapeutic measures may in JP patients. However, a mutually antagonistic re- reflect the persistence or regrowth of a periodonto- lationship apparently exists between these microbial pathic microbiota. Chairside microscopic counts of species, since sonic extracts of Haalso exert a bacter- crevicular leukocytes then may be particularly valu- istatic effect against S. sanguis and Actinomyces.74 able as a diagnostic marker in assessing the risk of Clinical research has shown that successful treat- destructive disease activity, and in determining ment of JP lesions is attained with suppression of Ha, "endpoints" for periodontal treatment procedures. and posttreatment colonization of the subgingival However, further clinical and laboratory investiga- ecosystem by S. sanguis, anaerobic gram-positive cocci, tions of these approaches are needed. and Actinomyces species. 7s Interestingly, this type of bacterial conversion to a predominantly gram-pos- Conclusions itive flora may be responsible for the increased post- In conclusion, the clinical and microbiological ob- treatment formation seen in some JP patients servations seen in this study suggest that: by Harvey et al. 3s S. sanguis and Actinomyces have been found to be less susceptible to the antimicrobial 1. JP patients can be treated successfully and main- effects of NaHC03,NaC1, and chloramine-T than are tained on a long-term basis without periodontal Ha and most other periodontal pathogens. 61 Thus, surgery if appropriate antimicrobial therapeutic subgingival delivery of these antimicrobials during interventions (chemical, mechanical, or both) are regular office maintenance appointments and by pa- targeted against the subgingival periodontopathic tients may comprise a useful clinical method for al- microflora. tering the subgingival environment, and promoting 2. Systemic tetracycline therapy longer than 2 weeks posttreatment growth of nonpathogenic organisms, appears necessary if a nonsurgical approach is fol- ¯ like S. sanguis, which may act to inhibit further lowed in the treatment of JP. This is presumably subgingival colonization by some periodontopathic to eradicate adequately periodontal pathogens re- species. In fact, Socransky 76 has suggested that siding in gingival connective tissues and epithe- subgingival development of a "protective" flora in- lium. hibitory to periodontal pathogens after initial peri- 3. Local subgingival application of chemical anti- odontal therapy may be essential for preventing microbials, such as inorganic salts and chloramine- posttreatment disease relapse. Further investigative T, as part of professional- and patient-applied research on these points is needed. therapy, may be valuable adjuncts in extending In this study phase-contrast microscopic analysis the antibacterial effects of mechanical debridement of motile rods and spirochetes was unable to identify procedures. This may reduce the need for surgical some JP sites which remained, despite therapy, at treatment modalities, and may help prevent the increased risk of further destructive disease activity. reestablishment of a periodontopathic microbiota Four microscopically monitored sites experienced sig- in JP patients after its suppression by initial peri- nificant clinical deterioration from the pretreatment odontal therapy and systemic antibiotics. baseline examinations (~> 3 mmof clinical attachment 4. Microscopic monitoring of motile microorgan- loss). Elevated levels of motile rods were found after isms alone in JP subgingival plaque does not iden- treatment in 2 of these deteriorating sites, and ele- tify accurately treated sites remaining at increased vated levels of spirochetes in only 1 of the sites. Sim- risk of disease progression. Additional micro- ilar observations on JP patients have been reported scopic monitoring of crevicular leukocyte levels, by4"2 other9 investigators. and/or identification of other disease-associated However, the 4 deteriorating sites all consistently organisms with cultural or immunological tech- harbored elevated levels of crevicular leukocytes niques appears necessary.

268 TREATMENTOF JUVENILE PERIODONTITIS: Ramset al. The authors acknowledge the generous support and assistance of (’Keyes technique’) on advanced adult periodontitis. JADA Dr. Andrew Christopher, chairman of the Department of Com- 111:429-41, 1985. munity Dentistry at Georgetown University, and the NIDRdental 17. Keyes PH, Rogosa M, Rams TE, Sarfatti DE: Diagnosis of clinic staff, especially Drs. Surya Howard, David E. Sarfatti, John creviculoradicular infections: disease-associated bacterial pat- Folio, and Michael W. Roberts, chief, NIDRPatient Care Section. terns in periodontal lesions, in Host-Parasite Interactions in Periodontal Diseases, Genco RJ, Mergenhagen SE, eds. Washington, DC; American Society for Microbiology, 1981, Dr. Ramswas a dental staff fellow, Clinical Investigations and pp 395-403. Patient Care Branch, National Institute of Dental Research, Na- 18. Keyes PH, Rams TE: A rationale for the management of peri- tional Institutes of Health, Bethesda, Maryland. He is now a clin- odontal diseases: rapid identification of microbial ’therapeutic ical assistant professor of microbiology, School of Medicine, and targets’ with phase-contrast microscopy. JADA106:803-12, community dentistry, School of Dentistry, Georgetown University, 1983. Washington, DC 20007, and a postgraduate resident in periodon- 19. Keyes PH, RamsTE: Clinical applications of microbiologically tics, Veterans Administration Medical Center, 408 First Ave., New monitored and modulated periodontal therapy. NYState Dent York, NY10010. Dr. Keyes was a senior investigator, Laboratory J 49:478~1, 1983. of Microbiology and Immunology, National Institute of Dental Re- 20. RamsTE, Keyes PH: A rationale for the management of peri- search, National Institutes of Health, and is now a professorial odontal diseases: effects of tetracycline on subgingival bac- lecturer of community dentistry, School of Dentistry, Georgetown teria. JADA107:37-41, 1983. University, and chairman, board of trustees, International Dental 21. Rams TE, Keyes PH: Direct microscopic features of subgin- Health Foundation, Reston, Virginia. Dr. Wright is a senior staff gival plaque in localized and generalized juvenile periodontis. periodontist, Clinical Investigations and Patient Care Branch, Na- Pediatr Dent 6:23-27, 1984. tional Institute of Dental Research, National Institutes of Health. 22. Potts TV, Zambon JJ, Genco RJ: Reassignment of Actinoba- Reprint requests should be sent to Dr. Rams. cillus actinomycetemcomitans to the genus Haemophilus as Haemophilus actinomycetemcomitans comb nov. Int J Sys 1. Nahoum H, Tennenbaum B: Long-term study of periodon- Bact 35:337-41, 1985. tosis. J Periodontol 45:765-71, 1974. 23. NewmanMG, Socransky SS, Savitt ED, Propas DA, Crawford 2. WaerhaugJ: Plaque control in the treatment of juvenile peri- A: Studies of the microbiology of . J Periodontol odontitis. J Clin Periodontol 4:29-40, 1977. 47:373-79, 1976. 3. Ashrafi MH, Durr DP, Meister F: Early diagnosis and suc- 24. Slots J: The predominant cultivable organisms in juvenile cessful management of periodontosis. JADA105:50-55, 1982. periodontitis. Scand J Dent Res 84:1-10, 1976. 4. Lindhe J: Treatment of localized juvenile periodontitis, in Host- 25. Slots J, Reynolds HS, Genco RJ: Actinobacillus actinomycetem- Parasite Interactions in Periodontal Diseases, Genco RJ, Mer- comitans in human : a cross-sectional mi- genhagen SE, eds. Washington, DC: American Society for crobiological investigation. Infect Immun29:1013-20, 1980. Microbiology, 1982 pp 382-94. 26. Slots J, Genco RJ: Black-pigmented Bacteroides species, Cap- 5. Lindhe J, Liljenberg B: Treatment of localized juvenile peri- nocytophaga species, and Actinobacillus actinomyceterncomi~ans odontitis. Results after 5 years. J Clin Periodontol 11:399-410, in human periodontal disease: virulence factors in coloniza- 1984. tion, survival, and tissue destruction. J Dent Res 63:412-21, 6. Mattout P, Roche M: Juvenile periodontitis: healing following 1984. autogenous iliac marrow graft, long-term evaluation. J Clin 27. Westergaard J, Frandsen A, Slots J: Ultrastructure of the Periodontol 11:274-79, 1984. subgingival microflora in juvenile periodontitis. Scand J Dent 7. Keyes PH, Wright WE, Howard SA: The use of phase-con- Res 86:421-29, 1978. trast microscopy and chemotherapy in the diagnosis and 28. Tempro PJ, Reynolds HS, Slots J: Microbial morphotypes in treatment of periodontal lesions -- an initial report (I). Quin- periodontal health and disease. IADRProgram and Abstracts, tessence Int 9:51-56, 1978. no 77, 1983. 8. Keyes PH, Wright WE, Howard SA: The use of phase-con- 29. Slots J, Rosling BG: Suppression of the periodontopathic mi- trast microscopy and chemotherapy in the diagnosis and croflora in localized juvenile periodontitis by systemic tetra- treatment of periodontal lesions -- an initial report (II). Quin- cycline. J Clin Periodontol 10:465-86, 1983. tessence Int 9:69-76, 1978. 30. Savitt ED, Socransky SS: Distribution of certain subgingival 9. Scheffler RM, Rovin S: Preventing and treating periodontal microbial species in selected periodontal conditions. J Perio- disease with the Keyes technique: a preliminary assessment. dont Res 19:111-23, 1984. Prev Med 11:677-95, 1982. 31. M~iller H-P, Flores-de-Jacoby L: The composition of the 10. Keyes PH: Microbiologically modulated periodontal thera- subgingival microflora of young adults suffering from juve- peutics: an introduction. Quintessence Int 13:1325-32, 1982. nile periodontitis. J Clin Periodontol 12:113-23, 1985. 11. Keyes PH: A treatment rationale for the managementof peri- 32. Walker J, Tall DB, Suzuki JB, NaumanRK: Antibody to Tre- odontal diseases. J Alabama Dent Assoc 68:18-25, 1984. ponema denticola in juvenile periodontitis. IADRProgram and 12. Rams TE: Microbiologically monitored and modulated peri- Abstracts, no 355, 1983. odontal therapy. Keyes therapy, pro and con. J Okla Dent 33. Tew JG, Ranney RR, Scott A, Smibert RM: Serum antibody Assoc 74:23-25, 1983. against treponemes in adolescents and young adults with 13. Keyes PH: Microbiologically monitored and modulated peri- periodontitis. IADRProgram and Abstracts, no 176, 1984. odontal therapy. Gen Dent 33:105-13, 1985. 34. Liljenberg B, Lindhe J: Juvenile periodontitis: some micro- 14. Loesche WJ: Chemotherapy of infections. Oral biological, histopathological, and clinical characteristics. J Clin Sci Rev 9:65-107, 1976. Periodontol 7:48~1, 1980. 15. Loesche WJ: Clinical and microbiological aspects of chemo- 35. Harvey RF, Jones WB, Chan ECS, deVries J, Wilika H: Per- therapeutic agents used according to the specific plaque hy- iodontosis. Part IIh Barbados study. Can Dent Assoc J 47:449- pothesis. J Dent Res 58:2404-12, 1979. 58, 1981. 16. Rams TE, Keyes PH, Wright WE, Howard SA: Long-term 36. Baer PN: The case for periodontosis as a clinical entity. J Per- effects of microbiologically modulated periodontal therapy iodontol 42:516-20, 1971.

PEDIATRICDENTISTRY: December 1985/Vol. 7 No. 4 269 37. HormandJ, Frandsen A: Juvenile periodontitis: localization mercially available toothpastes in vitro. Br Dent J 156:175-78, of bone loss in relation to age, sex, and teeth. J Clin Perio- 1984. dontol 6:407-16, 1979. 59. DeRenzis FA: Endotoxin-inactivating potency of hydrogen 38. Pihlstrom BL, Ortiz-Campos C, McHugh RB: A randomized peroxide: effect on cell growth. J Dent Res 60:933-35, 1981. four-year study of periodontal therapy. J Periodontol 52:227- 60. Rams TE, Keys PH, Jenson AB: Morphological effects of in- 42, 1981. organic salts, chloramine-T, and citric acid on subgingival 39. Slots J, Rosling BG, Emrich LJ, Christersson LA, Genco RJ: plaque bacteria. Quintessence Int 15:835M4, 1984. Relationship between certain subgingival bacteria and gain or 61. Newbrun E, Hoover CI, Ryder MI: Bactericidal action of bi- loss of periodontal .attachment after periodontal therapy. IADR carbonate ion on selected periodontal pathogenic microor- Program and Abst:~acts, no 122, 1983. ganisms. J Periodontol 55:65~67, 1984. 40. Magnusson I, Lindhe J, Yoneyama T, Liljenberg B: Recolono 62. Mouton C, Hammond PG, Slots J, Genco RJ: Serrum anti- ization of a subgingival microbiota following scaling in deep bodies to oral Bacteroides asscharolyticus (Bacteroides gingivalis): pockets. J Clin Periodontol 11:193-207, 1984. relationship to age and periodontal disease. Infect Immun 41. Rams TE, Keyes PH: Modifying oral irrigation devices for 31:182-92, 1981. subgingival periodontal chemotherapy. Gen Dent 32:302-5, 63. Cerra MB, Killoy WJ: The effect of sodium bicarbonate and 1984. hydrogen peroxide on the microbial flora of periodontal pock- 42. Haffajee AD, Socransky SS, Lindhe J: Comparison of statis- ets. J Periodontol 53:599-603, 1982. tical methodsof analysis of data from clinical periodontal trials. 64. F16tra L, Gjermo P, R611a G, Waerhaug J: A 4-month study J Clin Periodontol 10:247-56, 1983. on the effect of chlorhexidine on 50 soldiers. 43. Lindhe J, Haffajee AD, Socransky SS: Progression of peri- Scand J Dent Res 80:10-17, 1972. odontal disease in adult subjects in the absence of periodontal 65. Tinanoff N, Hock J, Camosci D, Hellden L: Effect of stannous therapy. J Clin Periodontol 10:433-42, 1983. fluoride mouthrinse on dental plaque formation. J Clin Per- 44. RimmAA, Hartz AJ, Kalbleisch JH, Anderson AJ, Hoffmann iodontol 7:232-41, 1980. RG: Basic Biostatistics in Medicine and Epidemiology. New 66. Eakle WS, Ford CM: Depth of penetration of periodontal York; Appleton-Century-Crofts, 1980 pp 275-76. pockets with oral irrigation. IADRProgram and Abstracts, no 45. NewmanMG: Localized juvenile periodontitis (periodonto- 1550, 1984. sis). Pediatr Dent 3:121-26, 1981. 67. West B: An evaluation of an oral irrigation device’s ability to 46. Debski BF, Ranney RR, Carchman RA: Modulation of neu- reduce the microbial count of subgingival plaque at 6 mmin trophil dysfunctions associated with juvenile periodontitis. depth. Thesis, University of Missouri at Kansas City School IADR Program and Abstracts, no 509, 1982. of Dentistry, 1983. 47. Nakamura M, Mashimo PA, Genco RJ: Effects of bestatin and Eakle W, Buchanan S, Leggott P, Quinn R, Boyd R, Chambers forphenicine on polymorphonuclear leukocyte (PMN) func- 68. tions in periodontal disease. IADRProgram and Abstracts, D: Daily oral irrigation with 0.1% SnF~ to control subgingival no 1091, 1983. bacteria. IADRProgram and Abstracts, no 356, 1983. 48. Van der Velden U, deVries JH: The influence of probing force 69. Boyd RL, Leggott P, Eakle S, Quinn RS, Buchanan S, Cham- on the reproducibility of pocket depth measurements. J Clin bers D: Effect of daily irrigation with 0.1% SnF2 in control of Periodontol 7:414-120, 1980. periodontal disease. IADR Program and Abstracts, no 1090, 49. Genco RJ, Cianciola LJ, Rosling B: Treatment of localized ju- 1983. venile periodontitis. IADRProgram and Abstracts, no 872, 70. Saglie FR, Carranza FA, Newman MG, Cheng L, Lewin KL: 1981. Identification of tissue-invading bacteria in human periodon- 50. Folio J, Rams TE, Keyes PH: Orthodontic therapy in patients tal disease. J Periodont Res 17:452-55, 1982. with juvenile periodontitis: clinical and microbiologic effects. 71. Christersson L, Slots J, Rosling B, Genco RJ: Suppression of AmJ Orthod 87:421-31, 1985. Actinobacillus actinomycetemcomitansin localized juvenile peri- 51. Keyes PH, Shern RJ: Chemical adjuvants for control and pre- odontitis. IADRProgram and Abstracts, no 256, 1983. vention of dental plaque disease. J AmSoc Prey Dent 1:18- 72. Hillman JD, Socransky SS: Bacterial interference of Actinoba- 34, 1971. cillus. IADRProgram and Abstracts, no 1174, 1981. 52. Rosling BG, Slots ], Webber RL, Christersson LA, Genco RJ: 73. Bonta Y, ZambomJJ, Christersson LA, Genco RJ: Distribution Microbiological and clinical effects of topical subgingival an- of bacterial inhibitors to Actinobacillus actinomycetemcomitansin timicrobial treatment on human periodontal disease. J Clin localized juvenile periodontitis patients. IADRProgram and Periodontol 10:487--514, 1983. Abstracts, no 1014, 1985. 53. Rosling BG, Christersson LA, Slots J, Genco RJ: Predictability 74. HammondBF, Stevens RH, Bonner P, Lillard SE: Toxicity of of topical and subgingival antimicrobial therapy in the man- Actinobacillus actinomycetemcomitansextracts for crevicular bac- agement of advanced adult periodontitis. IADRProgram and teria. IADRProgram and Abstracts, no 830, 1984. Abstracts, no I672, 1985. 75. Haffajee AD, Socransky SS, Ebersole JL, Smith DJ: Clinical, 54. Rosling BG, Slots J, Christersson LA, Genco RJ: Clinical and microbiological, and immunological features associated with microbiological effects of surgical and nonsurgical treatment the treatment of active periodontosis lesions. J Clin Perio- of multi-rooted teeth in adult periodontitis. IADRProgram dontol 11:600-618, 1984. and Abstracts, no 311, 1984. 76. Socransky SS: Microbiology of plaque. Compend Cont Educ 55. Adcock JE, Berry WC, Kalkwarf KL: Effect of sodium hypo- Dent Suppl 5:53-56, 1984. chlorite solution on the subgingival microflora of juvenile 77. Murray PA, Patters MR: Gingival crevice neutrophil function periodontitis lesions, Pediatr Dent 5:190-94, 1983. in periodontal lesions. J Periodont Res 15:463-69, 1980. 56. Robertson PB, Kornman KS: Longitudinal clinical and micro- 78. Barnett ML, Baker RL: Ultrastructure of crevicular washings biological evaluation of therapy for juvenile periodontitis. IADR from advanced periodontal lesions in youths. IADR Program Program and Abstracts, no 316, 1984. and Abstracts, no 1260, 1982. 57. ADACouncil on Dental Therapeutics: Accepted Dental Ther- 79. SandholmL: Cells and cellular interactions in gingival crevice apeutics, 37th ed. Chicago; American Dental Association, 1977. washings from patients with juvenile periodontitis. Scand J 58. Moran J, Addy M: The antibacterial properties of some corn- Dent Res 92:436-42, 1984.

270 TREATMENTOFJUVENILE PERIODONTITIS: Rams et al.