treatment of juvenile periodontitis with …...meticulous scaling and root planing of all teeth with...

PEDIATRIC DENTISTRY/Copyright @1985 byThe American Academy of Pediatric Dentistry

Volume 7 Number 4

Treatment of juvenile periodontitis with microbiologicallymodulated 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 toas the Keyes Technique were directed at suppression ofthe periodontopathic microflora of 7 juvenile periodontitispatients who were treated and followed for at least 22months.

Following collection of baseline clinical andmicrobiological parameters, the patients receivedmeticulous scaling and root planing of all teeth withconcomitant irrigation to probing depth of saturatedinorganic salt solutions and 1% chloramine-T. Thepatients were recalled at approximately 2- to 3-monthintervals for maintenance care which was modulated byclinical parameters and phase-contrast microscopicfindings. Six patients received at least 2 courses ofsystemic tetracycline (1 gin/day for 14 days) during thestudy. Patient home treatments included daily applicationof a sodium bicarbonate/3% hydrogen peroxide paste, andinorganic salt irrigations.

Clinical reevaluations made an average of 29.6 monthsposttreatment showed statistically significant (p(.01)decreases in bleeding on probing in all patients.Significant decreases in probing depth, and gains inclinical attachment levels also were found in all patients,particularly in advanced sites initially 4-6 mm and >-7mm in probing depth. Among sites with initialattachment loss >-5 mm, 25.8% experienced a >-3 mmgain in clinical attachment level from baseline withtherapy. Significant decreases in motile organisms andcrevicular polymorphonuclear leukocytes present in thesubgingival plaque of the patients also occurred with theantimicrobial therapy employed.

These findings demonstrate that juvenile periodontitispatients can be treated successfully and maintained on along-term basis without periodontal surgery whenappropriate antimicrobial therapy is directed at thesubgingival periodontopathic microbiota.

A wide variety of therapeutic approaches have

been used to manage juvenile periodontitis (JP) pa-tients, even though the exact nature of its etiologyhas been understood poorly until recently. Almost allof these approaches have employed clinical peri-odontal parameters alone to guide therapy diagnost-ically, and determine its success or failure. 1-6 Mostalso have placed emphasis in treatment on mechan-ical control of bacteriologically undefined dentalplaque, and surgical correction of anatomic and mor-phologic defects associated with JP disease progres-sion (i.e., infrabony pockets, inflamed gingivaltissues). 1-6

Antimicrobial therapy targeted at specific disease-associated bacterial species in the subgingival plaquemicrobiota also has been suggested for treatment ofjp.7,s This rationale was applied initially to the treat-ment of adult periodontitis lesions, and has been re-ferred to widely as the Keyes Technique, 9 ormicrobiologically modulated periodontal therapy.1°-13 As a therapeutic strategy for the control of specific

plaque infections ~4,15 associated with human peri-odontal diseases, it incorporates microbiological eval-uations of the subgingival flora, such as with phase-contrast microscopy, into diagnostic decision-makingand patient management. 16-21 Additionally, chemicalantimicrobial agents are utilized in both office ther-apy and patient home treatment procedures as ad-juncts to mechanical plaque removal techniques, suchas root planing, flossing, and toothbrushing.~6-21

The concept of directing therapeutic measures atspecific microbial pathogens in JP has been supportedby recent cultural studies of subgingival plaque from

PEDIATRIC DENTISTRY: December 1985/Vol. 7 No. 4 259

JP subjects. These studies repeatedly have associatedelevated numbers of certain species of gram-negativerods with localized JP sites, especially Haemophilus(formerly Actinobacillus) actinomycetemcomitans (Ha). 23-25

Further, Ha has been shown to elaborate a numberof potential virulence factors (e.g., leukotoxin, colla-genase, immunoglobulin proteases, fibroblast growthinhibitors, and bone resorption factors), which maybe important in the pathogenesis of ]p.26

Some morphologic studies with phase-contrast,darkfield, and transmission electron microscopy alsohave revealed large numbers of spirochetes and mo-tile rods in localized JP subgingival plaque.7"8"21"27-31

Consistent with these findings, elevated serum titersof antibodies specific to antigenic determinants ofTreponema species also have been reported in individ-uals with localized jp.32,33 However, there is evi-dence that not all localized JP patients harbor highproportions of motile bacteria in their subgingival mi-croflora, 4"23’34"35 and the exact role of these organ-isms in JP is not well understood.

The purpose of the present investigation was todetermine whether the principles of microbiologicallymodulated perioclontal therapy (Keyes Tech-nique)7,s, lo-13, 16-20 could be applied successfully tothe long-term clinca[ management of JP.

Methods and Materials

This longitudinal therapeutic investigation wasconducted within the clinical research facilities of theNational Institute of Dental Research (NIDR), of theNational Institutes of Health (NIH) in Bethesda,Maryland. The patients studied were selected frompersons referred to the NIDR dental clinic for peri-odontal disease treatment. Seven untreated patientsyounger than 22 years of age with idiopathic JP, asdefined by Baer,36 were treated and followed for atleast 22 months posttreatment (Table 1). Five of theJP patients were classified as having localized cases(first molars, incisors, and additional teeth equaling<14 total teeth), and 2 patients had generalized cases(->14 total teeth involved), based on the number affected teeth. 37 The 5 females and 2 males in thestudy had a mean age of 18 years (range = 12-21 years),and 193 teeth on initial examination. The follow-upclinical observations on the patients ranged from 22to 39 months posttreatment, with a mean of 29.6months.

All patients were in good general health and pre-sented with radiographic evidence of >50% bone lossassociated with the permanent first molars and inci-sors (Fig 1), and clinical attachment loss of ->7 at these sites. Comprehensive medical and dentalhistories were obtained, with particular emphasis on

any renal disorders, hypertension, sodium intake re-strictions, or previous allergic reactions to tetracyclineantibiotics. All patients underwent complete physicaland hematological examinations (including CBC, SMA-12, and urinalysis) conducted by the NIH ClinicalCenter medical staff to exclude the presence of anycontributing systemic medical disorders. None of thesubjects had any systemic disorders reported to beassociated with periodontal manifestations in adoles-cents, such as diabetes mellitus, sarcoidosis, Down’ssyndrome, cyclic neutropenia, agranulocytosis, Pap-illon-Lef~vre syndrome, of Ch6diak-Higashi syn-drome. In vitro evaluations of neutrophil andmonocyte functions were unavailable at the start ofthese studies, and were not determined for the pa-tients followed. None of the patients had receivedany type of periodontal prophylaxis or systemic an-tibiotic therapy during the previous 6-month period.

Diagnostic Procedures

Clinical ExaminationsClinical parameters for all teeth were assessed in-

dependently by a single NIDR staff periodontist (au-thor WEW) who was unaware of the patient’s courseof therapy (single-blind evaluation). Periodontalprobing depths and clinical attachment levels weremeasured to the nearest mm at interproximal andbuccal surfaces of all teeth with a calibrated probe, asdescribed by Philstrom et al.38

The degree of gingival inflammation for each toothwas determined by scoring the amount of bleedingseen after gentle probing to the "bottom" of the gin-gival sulcus. A sulcular bleeding score was assignedas follows:.0 = no bleeding, 1 = spot bleeding pointonly, 2 = bleeding along the gingival margin.

Microbiological ExaminationsAt each patient appointment, the composition of

the subgingival plaque was monitored with phase-contrast microscopy at chairside to assess the effec-tiveness of the therapeutic measures. No cultural orimmunologic monitoring was conducted as part .ofthis study.

Enumeration of disease-associated morphotypes insubgingival plaque samples with phase-contrast mi-croscopy followed procedures previously de-scribed, 7"16-21 and included counts of spirochetes,brush formations, motile rods (large-, medium-, andsmall-sized), oral protozoa (i.e., Entamoeba gingivalis,Trichomonas tenax), .and accumulated crevicular poly-morphonuclear leukocytes.

Briefly, subgingival plaque was removed carefullyfrom periodontal sites with a sterile curette, placed

260 TREATMENT OF JUVENILE PERIODONTITIS: Rams et al.

FIG 1. Typical molar/incisor angular defects associated with untreated JP lesions.

into 0.02 ml of sterile water on a microscopic slide,coverslipped, and examined immediately at 400x and600x with a high quality, phase-contrast microscope.The highest scoring fields for each of the bacterial andcellular morphotypes then were recorded.

Based on previous research,17-18-21 patients withperiodontal pockets harboring ^ 125/highest scoringfields of either spirochetes, medium- or large-sizedmotile rods (spinning, 2 x 3-9+ |xm), or crevicularpolymorphonuclear leukocytes were considered in thisstudy to have elevated numbers of disease-associatedmorphotypes. Small, highly motile coccobacilli (0.1-0.2 u,m in diameter), which exhibited a circular "dart-ing" motion, were not considered to be disease-as-sociated in this study, since previous reports havefound this plaque morphotype predominantly inhealthy periodontal sites.17-18

Multiple (^ 2) periodontal sites in each patient weremonitored microbiologically as a supplement to clin-ical periodontal parameters. Advanced periodontalpockets and furcations in particular were monitoredclosely throughout the posttreatment observation pe-riods, since the possibility of a disease-associated floraremaining in subgingival sites after the completion oftreatment is known to increase significantly with re-sidual probing depth.39-40

As these sites came into microbiological control,samples from additional surfaces less severely in-volved in each quadrant were evaluated to confirmsuppression of the disease-associated morphotypes.However, microbiological data reported in the resultssection is limited to levels of disease-associated mor-photypes in periodontal sites presenting at recall ap-pointments with the worst clinical conditions (i.e.,gingival inflammation) in each patient, and/or sur-faces having the greatest residual probing depth orfurcation involvement. For some patients, additionalmicrobiological observations were collected for sev-

eral months after the last posttreatment clinical eval-uations were made.

Therapeutic Procedures

Professional Office TherapyAll teeth were subjected to meticulous subgingival

scaling and root planing until a smooth, hard rootsurface was detected clinically. Chemical antimicro-bial agents actively were delivered subgingivally andmaintained in periodontal pockets throughout theseprocedures. Between instrumentation of different rootsurfaces, instruments were disinfected routinely bypassage through antiseptic solutions, such as 1%chloramine-T (sodium para-toluene sulfonchloram-ide), or 3% hydrogen peroxide saturated with sodiumchloride.

All periodontal pockets were irrigated profession-ally to probing depth before, during, and after me-chanical instrumentation with chemical antimicrobialagents. Chloramine-T (1%) was used for this pur-pose, along with a saturated inorganic salt solutionconsisting of sodium bicarbonate (NaHCO3) or so-dium chloride (NaCl).

To facilitate rapid subgingival drug delivery toprobing depth, especially into advanced sites (^ 7mm) and furcations, oral irrigation devices weremodified with foot-activated on/off switches, andequipped with monojet irrigation tips having 23- or25-gauge blunt needle or cannula extensions 10 mmlong, as described elsewhere.41 The extended tip wasadvanced like a periodontal probe to probing depthand into furcations to maximize contact and exposureof subgingival plaque bacteria to the antiseptic agentsduring the mechanical debridement sessions.

Approximately 4-6 hr were required for initial me-chanical instrumentation and professionally applied


subgingival chemotherapy. No surgical flaps or os-seous recontouring procedures were employed. Allcarious lesions and defective restorations were re-stored or replaced as needed.

Patient Home Treatment ProceduresAll patients were instructed in sulcular toothbrush-

ing and flossing. As previously described,7"8 patientsalso were directed to apply daily a saturated inor-ganic salt solution (i..e., 2 tablespoons of NaHCO3 orNaC1 dissolved into 112 fl oz warm water) with an oralirrigation device (unmodified) at a moderate-to-highpressure setting. This was then to be followed byapplication of a sodium bicarbonate/3% hydrogenperoxide paste or slurry to the dentogingival surfacesvia toothbrushing, flossing, interdental brushes, andrubber cone stimulators (#600a). Instruction and re-inforcement was emphasized to encourage the pa-tients to deliver the antimicrobia! chemicals as deeplyas possible into the sulcus/pocket spaces during theself-applied treatments. All of the patients were ca-pable of completing this home treatment regimen inapproximately 10-15 min.

At each recall appointment, patients viewed phase-contrast microscopic projections showing the bacte-riologic composition of their subgingival plaque onequipment previously described. 7 This served as afeedback mechanism aiding in patient education, mo-tivation, and compliance with prescribed home treat-ment procedures. The microscopic analysis also aidedthe treating clinician in assessing the self-care abilityof patients to deliver antimicrobials into the targetedtreatment sites.

Modulation of TherapyThe antimicrobial effects of the professional and

home treatment procedures were monitored by (1)clinical examinations for evidence of changes in gin-gival inflammation and periodontal attachment level,and (2) phase-contrast microscopy to determinewhether a satisfactory elimination of the initial per-iodontopathic subgingival flora had been obtained.Levels of motile bacteria and accumulated crevicularpolymorphonuclear leukocytes in subgingival plaquesamples were used in this study as "indicator" mor-photypes to assess the presence of a disease-associ-ated subgingival flora, and to identify patients atincreased risk of destructive disease activity.

Patients suffering additional clinical deteriorationand/or identified as remaining with elevated numbersof disease-associated morphotypes in their subgin-gival flora after repeated use of the locally appliedchemomechanical procedures described above, were

#600 -- John O. Butler Co: Chicago, IL.

placed on a short-term course of systemic tetracyclineHCI therapy (1 grn/day for 14 days). As previouslystated, patients with periodontal sites harboring ~125/highest scoring fields of either spirochetes, me-dium- to large-sized motile rods (spinning, 2 x 3-9+

~m), or crevicular leukocytes were considered in thisstudy to have elevated numbers of disease-associatedmorphotypes. The effects of adjunctive antibiotictherapy on motile bacteria and crevicular leukocytelevels were checked, by examining new subgingivalplaque samples with phase-contrast microscopy at theend of the 14-day drug course.

Periodontal recall therapy was carried out a.t ap-proximately 2-3 month intervals, and included rein-forcement of patient home treatment procedures,mechanical instrumentation of all tooth surfaces, andsubgingival irrigations to probing depth of all siteswith chemical antimicrobial agents. Additional sys-temic tetracycline therapy as described above wasprescribed if further clinical deterioration appearedand/or persistent reinfection of the subgingival mi-croflora with high levels (~ 125/highest scoring fields)of motile bacteria or accumulated crevicular leuko-cytes were seen with phase-contrast microscopicmonitoring.

Data Analysis

Patient means for probing depth and attachmentlevel were calculated after categorizing the baselineand posttreatment data on the basis of the covariateof the original probing depth, as suggested by Pihls-trom et al., 38 into 3 categories of pockets initially 1-3ram, 4-6 mm, and those ~ 7 mmo A paired t-test wasutilized to determine statistically significant differ-ences with treatment in probing depth and attach-ment level from baseline measurements. A value ofp ~ 0.05 was required for statistical significance.

The number of sites having major changes in at-tachment level (~ 3 mm) between baseline and post-treatment examinations were tabulated to supplementinterpretation of mean values reported for attach-ment level alterations, as suggested by Haffajee et

TABLE 1. Patient Characteristics

Length ofPatient DiaBnosis ABe Race Sex Follow up (mo)1. JP LJP 12 B F 362. JG LJP 16 B F 313. TC LJP 19 B F 394. NS LJP 21 C F 225. JB LJP 21 B M 256. JM GJP 16 B F 257. JF GJP 21 C M 29

~ = 18 ~ = 29.6

LJP = localized case, GJP = generalized case.


al. 42 This enabled determination of the frequency ofsignificant clinical improvement or deterioration atindividual periodontal sites which, according to Lindheet al.,4a are unlikely to be explained by measurementerror.

Differences in the frequency distribution of sulcularbleeding scores and microbiological parameters be-tween baseline and posttreatment examinations wereanalyzed by the Wilcoxon rank sum test.44

Results

Clinical FindingsTooth Mortality: None of the 193 teeth treated in the

7 JP patients were lost during the course of the study.Gingival Inflammation: The degree of gingival in-

flammation, as measured by the amount of bleedingon probing, was reduced significantly at the post-treatment examinations from the pretreatment base-line measurements (p < 0.01, Table 2). Prior to thestart of periodontal therapy, 56.1% of all teeth hadsulcular bleeding scores of 2. At the posttreatmentevaluations, sulcular bleeding scores of 2 were foundon only 5.6% of all teeth, while 65.8% of all teeth hadno bleeding on probing present (Table 2). A similarreduction in gingival inflammation was seen on asubset of 124 teeth (64.2% of all teeth) having one more surfaces with ~ 5 mm of attachment loss. Sul-cular bleeding scores of 2 were found on only 4.8%of these severely affected teeth after treatment, com-pared to 66.9% before treatment.

Mean Probing Depth and Clinical Attachment LevelChanges -- (A) For Sites Initially 1-3 ram: Sites withinitial probing depths of 1-3 mm experienced a sta-tistically significant slight decrease in probing depth(0.10 ram) following treatment. No statistically sig-nificant changes in clinical periodontal attachment wereassociated with treatment of initially shallow surfaces(Table 3).

(B) For Sites Initially 4-6 mm: Periodontal pocketsinitially 4-6 mm in depth exhibited a statistically sig-nificant (p < 0.01) decrease from pretreatment base-line values in pocket depth of approximately 1 mm,and a mean gain in clinical periodontal attachmentlevel of 0.77 mm (Table 3).

(C) For Sites Initially ~ 7 mm: In advanced JP sites

"¢,~BtE 2. Gingival Inflammation: Bleeding After Probing

Frequency Distribution of Sulcular

Bleeding Scores (all teeth)

0 1 2

Baseline 32.0% 9.7 56.1Posttreatment 65.8 28.6 5.6"

* Significantly different from baseline, p < .01.

initially ~ 7 mm, marked decreases (mean = 2.85mm) were found with therapy in pocket depth (Table3). Most of the pocket depth reductions were due tolarge gains in clinical periodontal attachment levels.An average of 2.66 mm of clinical periodontal attach-ment level gain relative to the pretreatment m~asure-ments was recorded at advanced sites after treatment(Table 3). Both the mean probing depth and clinicalperiodontal attachment level changes seen with treat-ment were statistically significant from pretreatmentbaseline values (p < 0.01).

Prevalence of Major Changes in Clinical Attachment Level:A ~ 3 mm gain in clinical periodontal attachmentlevel from pretreatment values following therapy wasrecorded at 62 sites in 6 of the study patients. Theseindividual surfaces experiencing large beneficialchanges in clinical periodontal attachment level rep-resented 10.7% of all sites followed in the study pa-tients, and 25.8% of sites with initial clinical periodontalattachment loss of ~ 5 mm.

Sites having major loss of clinical periodontal at-tachment during the posttreatment observation pe-riods were rare. Seven sites in 3 patients, constituting1.2% of all sites treated, suffered a ~ 3 mm loss ofclinical periodontal attachment from the pretreatmentbaseline measurements. Of these 7 sites, 1 initiallyhad clinical periodontal attachment loss of 5 mm, and6 had initial loss of 2-3 mm.

Adverse Reactions and Side Effects: No adverse reac-tions or side effects to systemic tetracycline therapyoccurred in the patients followed. No adverse reac-tions or side effects (such as periodontal abscesses)were associated with daily applications of inorganicsalt solutions with an oral irrigation device at mod-erate-to-high pressure settings. Daily use of an H202/

NaHCO3 slurry as a topical antimicrobial treatmentagent did not lead to black hairy tongue conditions,or damage hard or soft tissues in any of the patientsafter completion of initial periodontal therapy.

Microbiological Findings

PretreatmentPrior to the start of any therapy, all subgingival

plaque samples examined from the study subjectscontained high levels (~ 125/highest scoring fields)of spirochetes, medium- to large-sized motile rods(spinning, 2 x 3-9+ ~m), and accumulated crevicularpolymorphonuclear leukocytes (Figs .2-4). Highlystructured brush formations with coordinated spiro-chetal movement, as previously described,17,18,21 were.observed in 58.3% of the pretreatment plaque sam-ples, and oral amoebae (E. gingivalis) were present in41.7%.


TABLE 3. Analysis of Mean Differences in Probing Depth and Clinical Attachment Level

Mean ClinicalInitial 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 -- no statistically significant difference frompretreatment.

LEVELS OF SPIROCHETES (JUVENILE PERIODONTITIS)

~NITIAL BEFORE 0-6 7-12 tI-1B 19-24 25-30 31-36 37-57 TOTALDX TETRA 0 57

CYCLINE MONTHS AFTER FIRST COURSE[1 4 Mo.} OF TETRACYCLINE

F=G 2. Changes with treatment in subgingival spirochetes.

LEVELS OF MOTILE RODS (JUVENILE PERIODONTITIS)

INITIAL BEFOREDX TETRA-

CYCLINE(1-4

SAMPLESEXAMINED 12 29SUBJECTS 7 7

06 712 1318 1924 25-30 313~ 3757 TOTAL057

MONTHS AFTER FIRST COURSEOF TETRACYCLINE

637 4t7 3~7 3~6 2~5 13 11 22~7

MOTILE RODS/ ̄ TNC I) 125IFIELD

F=G 3. Changes with treatment in subgingival motile rods.

Pretetracycline Therapy

With local periodontal treatment consisting of re-peated root planing, subgingival chemotherapy, and

patient home treatment procedures, a significant re-duction was achiew.~d during the first 4-month periodin the numbers of motile bacteria and crevicular leu-kocytes in sampled sites (p < 0.01), (Figs 2-4). ever, spirochetes, medium- to large-sized motile rods,and crevicular leukocytes still were found to be ele-vated (~> 125/highest scoring fields) in 44.8%, 51.7%,

LEVELS OF CREVICULAR LEUKOCYTES(JUVENILE PERIODONTITIS)

o ~INITIAL BEFORE

DX TETRA:CYCLINE

0-6 7-12 13-18 19.24 25-30 31 36 37-57 TOTAL0-57

MONTHS AFTER FIRST COURSE-OF TETRACYCLINE

SUBJECTS 7 7 7 7 6 4 2

CREVICULAR LEUKOCYTES/̄ TNC () 125)FIELD B 50 100+

F=G 4. Changes with treatment in crevicular polymorphonu-clear leukocytes.

and 72.4%, respectively, of the subgingival plaquesamples microscopically examined during this pe-riod. Brush formations also were detected in 24.1%of the samples. All of the study subjects had at leastone periodontal ~ite remaining with elevated num-bers of disease-associated morphotypes (spirochetes,motile rods, and/or crevicular leukocytes present at~ 125/highest scoring fields), following application oflocal periodontal treatments.

Based on the persistence of these disease-associ-ated morphotypes, all of the study patients then wereprescribed systemic tetracycline therapy (1 grn/dayfor 14 days).

Posttetracycline TherapyAt all time periods after completion of the first course

of systemic tetracycline therapy (0-6 months through37-57 months), the prevalence of spirochetes, motilerods, and crevicular leukocytes was reduced signifi-cantly (p < 0.01) relative to the baseline and prete-tracycline therapy periods (Figs 2-4). Additionally,brush formations were seen in only 6.3%, and E. gin-givalis in only 3.2% of the 222 plaque samples ex-amined after the administration of systemic tetracyclinetherapy.

Immediately after completion of the.first 14-day


systemic tetracycline course, all monitored sites (N 24 sites) had significantly reduced (4 10/highest scor-ing fields) or undetectable levels of spirochetes andmotile rods present in the subgingival microflora.Spirochetes, in particular, appeared quite suscepti-ble, with 91.7% of the plaque samples taken imme-diately after systemic tetracycline therapy having nospirochetes present. Subsequently, low or undetect-able levels of spirochetes were found in 79.3% of thesubgingival plaque samples examined during the 0to 6-month posttetracycline therapy period, and in78.8% of all samples taken up to 57 months posttreat-ment (Fig 2). A similar pattern was seen with motilerods, with 71.1% of all samples analyzed up to 57months posttreatment having only low or undetect-able levels of medium- to large-sized motile rodspresent (Fig 3).

Most monitored sites (70.8%) also had low levels(4 25/highest scoring fields) of crevicular leukocytesimmediately after completion of systemic tetracyclinetherapy. However, 6 periodontal sites, representing25.0% of the 24 sites monitored during systemic tet-racycline therapy, continued to have elevated num-bers (~ 125/highest scoring fields) of crevicularleukocytes immediately after the 14-day drug course.During the 57omonth posttreatment period, a highpercentage of monitored sites (85.1%) harbored onlylow or moderate levels of crevicular leukocytes (Fig4).

Additional adjunctive systemic tetracycline therapywas prescribed to 6 of the study patients within 12months of the first antibiotic course. Three patientsreceived additional systemic tetracycline therapy (1gm/day for 14 days) at approximately 12-month in-tervals. Three patients required only I additional sys-temic tetracycline course, which was given within 6months of the original course. In 9 of 11 instanceswhere additional systemic tetracycline therapy wasprescribed, elevated levels of both motile bacteria andcrevicular leukocytes were seen microscopically. In 6of these cases, organized brush formations also werepresent. In 2 cases, additional systemic tetracyclinetherapy was given where high levels of crevicularleukocytes (~ 125/highest scoring fields) alone werebeing detected consistently, even in the relative ab-sence of motile disease-associated morphotypes in theaccompanying subgingival flora.

Microscopic Findings Relative to MajorAttachment Level Changes

Of the 7 sites which experienced a ~ 3 mm loss ofclinical periodontal attachment from pretreatmentbaseline measurements, 4 of these sites were moni-tored microscopically throughout the posttreatmentobservation period. Only 1 of these sites (25%) re-colonized with high levels of spirochetes during the

posttreatment period, while only 2 of the sites (50%)were found reinfected with high levels of motile rods.However, in contrast to the findings with motile bac-teria, all 4 (100%) of the monitored sites with ~ 3 of clinical periodontal attachment loss consistently hadhigh levels (~ 125/highest scoring fields) of crevicularleukocytes throughout the posttreatment period. Inthis regard, none of the 10 microscopically monitoredsites experiencing a ~ 3 mm gain in clinical peri-odontal attachment from pretreatment values had el-evated crevicular leukocyte levels present at anyexamination during the posttreatment period.

Discussion

The early onset and rapidly progressive attachmentloss characteristic of JP has been related clearly tosubgingival colonization by suspected periodontalpathogens, and the presence of host cell-mediatedimmunodeficiencies, particularly in monocyte andneutrophil leukocyte functions. 4s Considerable re-search attention is being focused on elucidating theexact nature of these host immune defects, and pre-liminary studies seeking therapeutic measures to en-hance impaired leukocyte functions appearpromising.46,47 However, until these approaches aredeveloped more thoroughly, the clinical managementof JP needs to be directed primarily at elimination ofthe subgingival periodontopathic flora.

The results of the present investigation demon-strate that a combined local and systemically deliv-ered antimicrobial treatment approach can producelong-term apparent arrest of destructive disease ac-tivity in most JP lesions without periodontal surgery.Marked clinical improvements were seen posttreat-ment, with significantly reduced bleeding on prob-ing, decreased probing depths, and gains in clinicalperiodontal attachment being measured in all of thestudy subjects.

Pronounced clinical changes were especially evi-dent in JP sites having advanced periodontal break-down. In sites with initial probing depths of ~ 7 mm,large gains in clinical periodontal attachment (mean= 2.66 mm), and highly significant decreases inprobing depth from pretreatment baseline measure-ments (p < 0.01), were associated with the treatmentregimen studied (Table 3). Additionally, 25.8% of alltreated surfaces presenting with initial clinical peri-odontal attachment loss of ~ 5 mm experienced a ~3 mm gain in clinical periodontal attachment from thepretreatment evaluations. Only 1.2% of all sites treatedlost ~ 3 mm of clinical periodontal attachment frombaseline values, and no teeth were extracted duringthe course of the study, despite advanced clinical at-tachment loss initially present on severely affectedteeth.


Standardized probing forces with pressure-sensi-tive periodontal probes were not used in this studyfor assessment of clinical parameters. Smaller vari-ances in clinical measurements, though not statisti-cally significant, are found with standardized versusnonstandardized probing forces. 48 However, in thepresent study, reproducibility of clinical parameterswas maintained by having a single periodontist col-lect (on a single-blind basis) all of the probing depthand clinical periodontal attachment level measure-ments.

The findings reported here are consistent with otherclinical studies describing long-term successful treat-ment and maintenance of JP lesions. 1"2"4’5 However,the present investigation differs from these previousstudies in that (1) microbiologic criteria supple-mented clinical parameters for therapeutic decision-making, (2) local subgingival chemotherapy was ad-ministered both professionally and in home treat-ment procedures as adjuncts to mechanicaldebridement, and (3) no periodontal surgical proce-dures were employed.

Lindhe4,5 previously has called for studies of non-surgical treatment modalities for JP. The observationsreported in the present study unequivocally docu-ment that stabilization and long-term arrest of mostJP lesions can be attained without periodontal sur-gery. These findings represent the first long-termclinical results beyond 18 months for a nonsurgicaltherapeutic approach to JP. Similarly, Genco et al.49

treated 9 localized JP patients with a nonsurgicaltreatment regimen consisting of scaling and rootplaning in combination with systemic tetracyclinetherapy (1 grn/day for 14 days every 8 weeks). Overan 18-month period no further alveolar bone loss wasseen with standardized radiographs in any of the mo-lar/incisor infrabony defects monitored, and in one-third of the defects an increase was seen in the al-veolar bone levels after treatment.

The study design followed in this investgafion doesnot allow direct comparisons to be made between ournonsurgical treatment results and those reported us-ing periodontal surgery. However, it is clear from thedegree of clinical stabilization and long-term arrest ofclinical periodontal attachment loss in the patientsstudied, that surgical intervention may not be anobligatory component critical for the successful man-agement of most JP lesions. In fact, some of the pa-tients treated nonsurgically with these antimicrobialapproaches stabilized to such an extent that fixed or-thodontic repositioning of maloccluded teeth wascarried out without complication,s° Thus, further in-vestigative research is warranted on nonsurgicaltreatment modalities based on control of specific dis-ease-associated plaque organisms.

Supplementing mechanical plaque removal ap-

proaches (i.e., root planing, tooth brushing, flossing)with local subgingival applications of chemothera-peutic agents has been suggested previously,14,5~ butrarely utilized in the treatment or adult or JP patients.In carefully controlled clinical studies on adult peri-odontitis patients,s2"s3 subgingival applications of so-dium bicarbonate (NaI-ICO3) , sodium chloride (NaC1),and hydrogen peroxide were found to enhance sig-nificantly the microbiological and clinical effects ofperiodontal scaling and root planing. Significantlymore profound reductions in probing depths, gainsin clinical periodontal attachment levels, and in-creased alveolar bone density in sequential standard-ized radiographs of interproximal areas were seen after12 months, especially in advanced sites initially >~ 7mm in depth, after a combined chemomechanicaltherapeutic approach was employed.52

Rosling et al. s4 also have shown that in multirootedteeth with furcation involvements, where mechanicaldebridement is difficult and likely to be imperfect,irrigating the furcation areas with chemical antimi-crobial agents enhances conventional periodontaltherapy. Significantly greater reductions in motilebacteria, and gains in clinical periodontal attachmentwere found after 1 year in furcated sites that receivedadjunctive subgingival iodine irrigation during peri-odontal scaling and root planing.54

In JP patients, Adcock et al. 5s have reported thatsubgingival sodium hypochlorite and 5% citric acidapplications used in conjunction with subgingival cu-rettage significantly reduced spirochetes and cultiv-able gram-negative anaerobic rods for at least a 3-month posttreatment period in advanced localized JPlesions. However, repeated root planing alone, or inconjunction with topically applied 10% povidone-io-dine is ineffective in adequately reducing subgingivallevels of Ha in localized JP pockets.29,56

In the present investigation, inorganic salts, chlor-amine-T, and hydrogen peroxide were used as localchemotherapeutic agents on JP sites. These com-pounds were selected on the basis of their availabil-ity, lo’w toxicity, antibacterial properties, andrecognition as accepted dental therapeutic agents bythe American Dental Association.s7 In contrast, mostcommercially available toothpastes have almost noantibacterial effects against plaque organisms,ss

In vitro studies have found that hydrogen perox-ide, in addition to its antiseptic properties, can in-activate the inhibitory effects of bacterial endotoxinson gingival fibroblast growth.59 However, it is notpresently known if this occurs in vivo.

Saturated NaHCO3 and NaC1 solutions have beenshown to be rapidly bactericidal to oral spirochetesand motile rods, and can induce ultrastructural changescytotoxic to subgingival plaque microorganisms fromdiseased sites after brief in vitro exposure.6° In cul-


turing studies by Newbrun et al., 61 a large numberof suspected periodontopathic microbial species, in-cluding organisms closely associated with JP, werefound to be highly susceptible in vitro to the anti-microbial effects of NaHCO3, NaC1, and chloramine-T. The minimal bactericidal concentrations (MBCs) NaHCO3 and NaC1 against Ha and Capnocytophagawere ~ 2.5%. The MBCs of these salts were ~ 5.0%against Bacteroides gingivalis, which also has been im-plicated as a possible periodontopathogen in gener-alized JP patients.62

The therapeutic doses of these inorganic salts asapplied in office and home irrigations in this studywere approximately 14% for NaHCO3, and 18% forNaC1 (i.e., 2 tablespoons of the salt dissolved into 12fl oz warm water). The 1% chloramine-T concentra-tion used in this study for office irrigation of JP sitesis also rapidly bactericidal to oral spirochetes and mo-tile rods,6° and is effective against Ha and B. gingivalisat a minimal inhibitory concentration of ~ 0.3%.61

Thus, NaHCO3, NaC1, and chloramine-T were intro-duced repeatedly into JP lesions during this study attherapeutically significant levels known to be bacte-ricidal or inhibitory to suspected periodontopatho-gens associated with JP lesions.

Regardless of the in vitro capabilities of the afore-mentioned compounds, it must be stressed that ef-fective clinical use of chemical antimicrobial agents inperiodontal therapy requires adequate subgingivaldrug delivery into the targeted treatment sites. Thisconcept is essential to both professional- and patient-administered regimens. Inorganic salts and hydrogenperoxide do not alter significantly the subgingival mi-croflora or clinical parameters of advanced periodon-tal pockets if applied only supragingivally, such aswith tooth brushing.63 Similar findings have been re-ported with mouthrinsing of chlorhexidine 64 andstannous fluoride, 6s presumably because of insuffi-cient sulcular penetration.

In the present study, modified oral irrigation de-vices with extended tips 41 were employed to over-come these problems in subgingival delivery ofchemical antimicrobials into advanced periodontalsites. Additionally, patient home treatment regimensincluded daily applications of saturated inorganic saltsolutions via unmodified oral irrigation devices, inorder to extend subgingival bacterial control.

Oral irrigation devices (unmodified) have beenshown to penetrate solutions most commonly to 75%of the clinical probing depth of sites ~ 7 mm,66 andin some studies, to at least 6 mm below the free gin-gival margin.67 Eakle et al. 6s also have demonstratedthat both oral irrigation with water and 0.1% stan-nous fluoride can reduce significantly the proportionsof spirochetes in the subgingival flora of untreatedsites 4 mm or greater in probing depth. Significantly

greater improvements in clinical periodontal param-eters were seen in these sites with irrigation of theantimicrobial agent.69

Despite the intensive local subgingival chemother-apy and mechanical debridement, all patients in thepresent investigation required administration of sys-temic tetracycline therapy, which was given for a 2-week period (1 g/day). This suggests that sustainedsuppression of disease-associated microscopic mor-photypes with nonsurgical treatment modalities maybe difficult to attain in advanced JP sites without ad-junctive systemic antibiotic therapy. The need forsystemic tetracycline therapy most likely was due tothe invasion and colonization by periodontopathicbacteria of gingival connective tissues and epitheliumadjacent to infected pockets,7° although no histologicstudies of gingival tissue biopsies were conducted tosubstantiate this hypothesis.

Clinical studies have demonstrated that markedsuppression or elimination of subgingival Ha, whichmay invade subepithelial tissues, 7° can be achievedvia (1) 3 weeks of systemic tetracycline HC1 therapy(1 g/day)29, or by (2) surgical excision of inflamedgingival tissues using either soft tissue curettage orperiodontal flap surgery.7~ Genco et al. 49 also havereported that the ability of nonsurgical treatments toarrest progressive bone loss in localized JP sites isenhanced significantly with systemic tetracyclinetherapy.

In the present study, additional courses of systemictetracycline therapy were needed during mainte-nance therapy due to the reestablishment of a dis-ease-associated microflora in some sites. This mayhave been due to incomplete suppression and sub-sequent regrowth of suspected periodontal patho-gens, such as Ha, which can persist in someperiodontal sites after only 2 weeks of systemic tet-racycline therapy. 29 The presence of elevated num-bers of crevicular polymorphonuclear leukocytes in 6periodontal sites immediately after 2 weeks of sys-temic tetracycline therapy may have reflected the per-sistence of a periodontopathic subgingival microfloraincompletely eradicated by the systemic tetracyclineregimen used in this study. However, in all othersites monitored, significant and sustained decreasesin subgingival spirochetes, motile rods, and crevi-cular polymorphonuclear leukocytes were achievedfollowing systemic tetracycline therapy. Low or un-detectable levels of these disease-associated morpho-types were maintained for extended periods with localchemomechanical measures (Figs 2-4).

In regard to this, locally applied antimicrobials, suchas inorganic salts and chloramine-T, may be partic-ularly valuable during periodontal maintenance. Theeffects of these agents may act to prolong the im-mediate efficacy of other therapeutic measures (i.e.,


root planing, tetracycline, periodontal surgery) by fa-voring posttherapy colonization of treated sites bymicrobial species which are antagonistic to the re-growth of a pathogenic microbiota. Hillman andSocransky72 have demonstrated that Streptococcus san-guis, Streptococcus ~beris, and Actinomyces taken fromhealthy periodontal sites or from sites with periodon-tal disease other than JP are inhibitory to the growthof Ha strain Y4. Such species were not present in JPsites highly infected with the Ha strain Y4. Bonta etal. 7a also have reported that S. sanguis, S. mitis, andS. salivarius are inhibitory to the growth of Ha, andare twice as prevalent in healthy versus diseased sitesin JP patients. However, a mutually antagonistic re-lationship apparently exists between these microbialspecies, since sonic extracts of Ha also exert a bacter-istatic effect against S. sanguis and Actinomyces.74

Clinical research has shown that successful treat-ment of JP lesions is attained with suppression of Ha,and posttreatment colonization of the subgingivalecosystem by S. sanguis, anaerobic gram-positive cocci,and Actinomyces species.7s Interestingly, this type ofbacterial conversion to a predominantly gram-pos-itive flora may be responsible for the increased post-treatment calculus formation seen in some JP patientsby Harvey et al. 3s S. sanguis and Actinomyces havebeen found to be less susceptible to the antimicrobialeffects of NaHC03, NaC1, and chloramine-T than areHa and most other periodontal pathogens.61 Thus,subgingival delivery of these antimicrobials duringregular office maintenance appointments and by pa-tients may comprise a useful clinical method for al-tering the subgingival environment, and promotingposttreatment growth of nonpathogenic organisms,

¯ like S. sanguis, which may act to inhibit furthersubgingival colonization by some periodontopathicspecies. In fact, Socransky76 has suggested thatsubgingival development of a "protective" flora in-hibitory to periodontal pathogens after initial peri-odontal therapy may be essential for preventingposttreatment disease relapse. Further investigativeresearch on these points is needed.

In this study phase-contrast microscopic analysisof motile rods and spirochetes was unable to identifysome JP sites which remained, despite therapy, atincreased risk of further destructive disease activity.Four microscopically monitored sites experienced sig-nificant clinical deterioration from the pretreatmentbaseline examinations (~> 3 mm of clinical attachmentloss). Elevated levels of motile rods were found aftertreatment in 2 of these deteriorating sites, and ele-vated levels of spirochetes in only 1 of the sites. Sim-ilar observations on JP patients have been reportedby other investigators.4"29

However, the 4 deteriorating sites all consistentlyharbored elevated levels of crevicular leukocytes

throughout the posttreatment period. High levels ofcrevicular leukocytes are characteristic of untreatedJP sites, 2L77-79 even though these sites commonly arecolonized by Ha, which elaborates a leukotoxin andfactors which inhibit leukocyte chemotaxis.26 Severalstudies have found the numbers of crevicularleukocytes in untreated JP sites to be similar to thoselevels seen in untreated adult periodontitis sites.21,77-79

Additionally, healthy periodontal sites in JP patientscontain approximately tenfold fewer numbers ofcrevicular leukocytes than diseased sites.77

Thus, the presence of elevated crevicular leuko-cytes after completion of therapeutic measures mayreflect the persistence or regrowth of a periodonto-pathic microbiota. Chairside microscopic counts ofcrevicular leukocytes then may be particularly valu-able as a diagnostic marker in assessing the risk ofdestructive disease activity, and in determining"endpoints" for periodontal treatment procedures.However, further clinical and laboratory investiga-tions of these approaches are needed.

ConclusionsIn conclusion, the clinical and microbiological ob-

servations seen in this study suggest that:

1. JP patients can be treated successfully and main-tained on a long-term basis without periodontalsurgery if appropriate antimicrobial therapeuticinterventions (chemical, mechanical, or both) aretargeted against the subgingival periodontopathicmicroflora.

2. Systemic tetracycline therapy longer than 2 weeksappears necessary if a nonsurgical approach is fol-lowed in the treatment of JP. This is presumablyto eradicate adequately periodontal pathogens re-siding in gingival connective tissues and epithe-lium.3. Local subgingival application of chemical anti-microbials, such as inorganic salts and chloramine-T, as part of professional- and patient-appliedtherapy, may be valuable adjuncts in extendingthe antibacterial effects of mechanical debridementprocedures. This may reduce the need for surgicaltreatment modalities, and may help prevent thereestablishment of a periodontopathic microbiotain JP patients after its suppression by initial peri-odontal therapy and systemic antibiotics.

4. Microscopic monitoring of motile microorgan-isms alone in JP subgingival plaque does not iden-tify accurately treated sites remaining at increasedrisk of disease progression. Additional micro-scopic monitoring of crevicular leukocyte levels,and/or identification of other disease-associatedorganisms with cultural or immunological tech-niques appears necessary.


The authors acknowledge the generous support and assistance ofDr. Andrew Christopher, chairman of the Department of Com-munity Dentistry at Georgetown University, and the NIDR dentalclinic staff, especially Drs. Surya Howard, David E. Sarfatti, JohnFolio, and Michael W. Roberts, chief, NIDR Patient Care Section.

Dr. Rams was a dental staff fellow, Clinical Investigations andPatient Care Branch, National Institute of Dental Research, Na-tional Institutes of Health, Bethesda, Maryland. He is now a clin-ical assistant professor of microbiology, School of Medicine, andcommunity dentistry, School of Dentistry, Georgetown University,Washington, DC 20007, and a postgraduate resident in periodon-tics, Veterans Administration Medical Center, 408 First Ave., NewYork, NY 10010. Dr. Keyes was a senior investigator, Laboratoryof Microbiology and Immunology, National Institute of Dental Re-search, National Institutes of Health, and is now a professoriallecturer of community dentistry, School of Dentistry, GeorgetownUniversity, and chairman, board of trustees, International DentalHealth Foundation, Reston, Virginia. Dr. Wright is a senior staffperiodontist, Clinical Investigations and Patient Care Branch, Na-tional Institute of Dental Research, National Institutes of Health.Reprint requests should be sent to Dr. Rams.

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