subgingival microbial samples from patients with refractory

$: Subgingival Microbial Samples From Patients With Refractory$
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Clinical Implications of Recent Orthodontic- Periodontic Research Findings Bj6rn U. Zachrisson

During the past 15 years, advances in basic science related to periodontal biology, and clinical trials on prevention and treatment of periodontal disease, have dramatically changed many treatment concepts in periodontics. The most pertinent information for orthodontic practice from these studies is summarized. Also, recent advances in orthodontics, particularly regarding bonding of attachments to artificial tooth surfaces and improved long-term stabilization of orthodontic treatment results in adults by means of bonded lingual retainers have significant implications. This article outlines how recent research information from both dental specialties may be used by orthodontists to improve treatment planning, clinical management, and retention of their adult and elderly patients in whom different malocclusions are complicated by moderate to advanced periodontal destruction. (Semin Orthod 1996;2:4-12.) Copyright© 1996 by W.B. Saunders Company

T he changing concepts in periodontics can be illustrated by referr ing to the "10 Out-

dated Dogmas" presented by Ramt]ord a in 1984 (Table 1). Mthough excellent long-term follow-up studies (up to 10 years or more) both in Scandinavia and the United States have proven them to be partially or totally wrong (for up- dated interpretation, see1), they are still ac- cepted and used as guidelines in the clinical practice by many dentists.

Nature and Def in i t ion o f Per iodont i t i s

Prior to 1980, periodontists thought that nearly all adults had some periodontal disease; that the disease could not be stopped; that the deeper the pockets were, the poorer was the prognosis; and that periodontal breakdown was generalized and that it progressed linearly. Today, few adults are diagnosed as having severe periodontitis (see below). For most patients with advanced disease, the progress of at tachment loss can be stopped, and the at tachment levels can be maintained

From the Department of Orthodontics, University of Oslo, Norway.

Address correspondence to Bj6rn ~L Zachrisson, DDS, PhD, Stortingsgaten I0, 0161 Oslo, Norway.

Copyright © 1996 by W..B. Saunders Company 1073-8746/96/0201-000255. 00/0

unchanged for 10 or more years with regular recall care. 1-4 Recurrent periodontal disease in well-maintained patients is now regarded as a site-specific disorder, which evidently develops and progresses in a few, apparently unpredict- able sites (areas around the roots of teeth). 5,6 The adult form of destructive periodontitis is characterized by short periods of exacerbations, separated by relatively long periods of remis- sion. 6 The rest periods may last a few days or several years. 6

P l a q u e

There is still consensus among researchers that a cause and effect relationship exists between bacterial plaque and destructive periodontal disease. However, not all organisms in plaque are equally pathogenic, and plaque may vary consid- erably in composition between individuals and for different teeth in the same individual, as well as related to supragingival and subgingival loca- tion, and how long the plaque has been present. 1,7 In addition, the effect of bacterial plaque is influenced by host responses f rom the patient. At least 15 different microorganisms including P gingivalis, A actinomycetemcomitans (Aa) and P intermedius are associated with adult periodontitis, 8 and Aa has been significantly associated with juvenile periodontitis in most s tudies/

4 Seminars in Orthodontics, Vol 2, No 1 (March), 1996: pp 4-12

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Clinical Implications of Ortho-Perio Research

Table 1. Ramfjord's 10 Outdated Dogmas

Dogma 1: Periodontal crevices that can be probed clinically beyond 3 mm are progressive lesions previously untreated or treated.

Dogma 2: A surgical sculpturing of gingiva and bone resembling horizontal atrophy to the level of the deepest defect is needed to stop further loss of support.

Dogma 3: Complete plaque control by the patient is needed to stop the progress of periodontitis.

Dogma 4: Furcation involvement signifies such poor prognosis for the tooth and the adjacent teeth that extraction is preferable unless the furcation involvement can be eliminated by odontoplasty, hemisections, or ampu- tations.

Dogma 5: The deeper the pockets, the poorer the prognosis.

Dogma 6: The progress of advanced periodontal disease cannot be stopped by current treatment modalities.

Dogma 7: Healing after scaling and root planing is enhanced by soft tissue curettage.

Dogma 8: Teeth with less than 1 mm of attached gingiva will continue to lose attachment if not treated surgi- cally.

Dogma 9: Gingival blanching as a result of lip pull indi- cates need for mucogingival surgery.

Dogma 10: Teeth with increased mobility after periodontal therapy that includes occlusal adjustment should be splinted.

Surgical Versus Nonsurg~cal Treatment

T h e d e c i d i n g fac tor in a t t e m p t i n g to es tabl ish hea l thy p e r i o d o n t a l cond i t i ons in a d v a n c e d per i - odont i t i s pa t i en t s is accessabi l i ty to the e x p o s e d r o o t surface r a the r than the ac tual p o c k e t dep th . 1 Recen t inves t igat ions 9-13 ind ica te tha t surgical a n d nonsu rg i ca l a p p r o a c h e s are equa l ly effective r e g a r d i n g m a n a g e m e n t o f p l aque , b l e e d i n g on p rob ing , a t t a c h m e n t level changes , a n d p a t t e r n s o f bac te r ia l r eco lon iza t ion ; a l t h o u g h the re is

g r ea t e r p o c k e t r e d u c t i o n fo l lowing surgical p ro- c edu re s than fo l lowing scal ing a n d r o o t p l a n i n g in the t r e a t m e n t o f pocke t s d e e p e r than 6 mm. 12,14 However , i t is pa r t i cu la r ly no t ewor thy

tha t d e e p e r res idua l pocke t s ( and the e x t e n t o f a n a e r o b i c cond i t i ons thus p rov ided ) d o n o t al low for a m o r e r a p i d r e c o l o n i z a t i o n o f sus-

p e c t e d p e r i o d o n t o p a t h o g e n s than d o shal low pockets . 12 T h e r e f o r e , p o c k e t d e p t h measu re -

ments , a lone , is n o t a g o o d i n d i c a t o r o f success o r fa i lure fo l lowing p e r i o d o n t a l treatment.~5

Goal of Periodontal Treatment

Because of the p o o r c o r r e l a t i o n be tween p o c k e t d e p t h a n d the p r e s e n c e o r absence o f active disease, p o c k e t e l i m i n a t i o n is n o l o n g e r the goal o f p e r i o d o n t a l therapy.U6 T r e a t m e n t success will c e n t e r on conve r t i ng the active site to an inact ive state. Because a passive site may n o t p rogress and , i f i t does , its p rogress will be ep isodic , n o t l inear, the p r e s e n c e o f 4 m m a n d some 5 m m pocke t s may be wi thin n o r m a l , 15,a6 a n d c o u l d be

c o n t r o l l e d at r egu l a r recal l visits. F igure 1 i l lustrates the d i f f e rence in cl inical

a p p e a r a n c e o f two o r t h o d o n t i c pa t i en t s with s imi lar deg ree s o f p e r i o d o n t a l des t ruc t ion . The first p a t i e n t was t r ea t ed a c c o r d i n g to the o ld concep t s (Table 2), whereas the s e c o n d p a t i e n t was t r e a t ed a c c o r d i n g to the new concep t s (Table 2). T h e d i f f e r ence in den t a l es thet ics a n d qual i ty o f life for the pa t ien t s is obvious a n d self- exp lana to ry .

Figure 1. Comparison of clinical appearance of two patients with similarly advanced periodonti t is (arrows in C and F) after periodontal and or thodont ic therapy. The patient in A and C was treated periodontally according to the old concept with generalized gingivectomies aiming at pocket elimination, whereas the pat ient in D-F was treated nonsurgically with the goal to create passive sites. The difference in dental esthetics is striking.

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Table 2. Simplified Description of Old and New Concepts Regarding Periodontitis

Old New

Tmgetgroup Everyone 10% to 15% of population Nature Generalized Site-specific Treatment Surgical (pocket Nonsurgical (passive sites)

elimination)

See Figure 1 for difference in posttreatment appearance.

Implications Because subgingival scaling and root planing is a more effective t reatment in patients with moder- ately and severely advanced periodontitis than was previously thought, surgery is less frequently indicated than it was in the past. The indications for surgery should include other criteria, such as suppuration from one or more sites and bleeding on probing despite good hygiene, in addition to an increased pocket depth. In several important recent clinical studies on the effects of nonsurgical t reatment of deep pockets, 9-1~ the following conclusions were drawn:

1. Deep periodontal pockets may be successfully treated by plaque control and one episode of subgingival instrumentation.

2. Recurrence of disease caused by subgingival recolonization of microorganisms may not occur in adults with high standards of supragingival plaque control.

3. The full effect of subgingival scaling is not obtained until after approximately 4 to 6 months after the start of periodontal therapy.

One interesting implication for clinical orthodontics of these results is that before fixed appliance t reatment is started in adult patients with periodontitis, it seems advantageous to allow a time period of 4 to 6 months (depending on the severity of disease) following the periodontal treatment. This observation period will en- sure that the tooth movement will take place in healthy tissues, and it will also provide a check-up period of the patient's oral hygiene effectiveness and motivation.

Those special categories of patients, who may not respond adequately to conventional mechani- cal/surgical treatment, such as early onset periodontitis, rapidly progressing periodontis (RPP), periodontitis associated with systemic diseases, and refractory periodontitis 17 will not be ad- dressed in this article.

High-risk Markers

Epidemiological studies in developing and indus- trialized countries have demonstrated a world- wide prevalence of severe destructive periodontitis of only 7% to 15% of the adult population with teeth. 18,19 As ment ioned previously, the vast majority of patients show low to moderate disease progression, whereas a small percentage (5% to 10%) may show many sites with extensive progression of destruct ion? s-2° From an orthodontic perspective, it is important to be able to diagnose those patients belonging to the high- risk group. However, at present the ability to predict dangerous sites for future periodontal destruction is low. Unfortunately, few useful guidelines are available to clinicians to indicate which patients (or sites) are at a greater risk of additional periodontal breakdown. 21 The sensitiv- ity and specificity of clinical parameters such as age, visible plaque, pocket depth, previous attachment loss, and bleeding on probing are only slightly better than chance. It is of interest to orthodontists, however, that Claffey and Egel- berg 22 recently found that patients with multiple residual probing depths greater than or equal to 6 mm and bleeding on probing at a 3 month re-evaluation after periodontal treatment, may run a greater risk of developing sites with additional at tachment loss.

New Techniques

An extensive search for chair-side or laboratory markers to predict high-risk sites to supplement clinical probing and routine radiography have included tests for causative factors (bacteria culture, DNA probes, enzyme-linked immunosor- bent assay [ELISA], and benzoyl-DL-arginine- naphtylthylamide [BANA] ), tests for susceptible hosts (polymorphonuclear leukocyte [PMN] che- motaxis), markers of inflammation, tissue dam- age, and cell death (collagenases, elastase, prosta- glandins, aspartate aminotransferase [AST] ). For a review see Jeffcoat. s However, most such tests are yet in the clinical trial stage, but may become useful in practice in the near future when diag- nosing a patient with periodontitis. As discussed in the article by Magnusson and Lindhe 2~ recent improvements in the repeatability and accuracy of probing and new radiographic techniques may also allow better determinat ion of the pres- ence or absence of disease progression by compar-

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ing sequential probing or radiographic examina- tions taken during a shorter t ime than was previously thought possible.

Conclusion

On the basis of previous studies, the following guidelines can be r e c o m m e n d e d for t rea tment planning of adult and elderly patients with advanced periodontit is who are to undergo orthodontic therapy:

1. The periodontal t rea tment should include oral hygiene instruction and supra~ngival and subgingival sca l ing/root planing. A re- evaluation will indicate if additional treat- men t (flap surgery) is needed in sites which still bleed on probing in patients with excellent oral hygiene.

2. An observation per iod of 4 to 6 months before appliances are bonded will secure full benefi t of the subgingival instrumentat ion, allow the initial tooth movements to take place in healthy tissues, and provide a reliable check of the patient 's hygiene efficiency and motivation.

C l i n i c a l Management Appliance and Hygiene Control

The key e lement in the or thodont ic management of adult patients with periodontal complica- tions is to eliminate, or reduce, plaque accumulation, and gingival inflammation. This implies great emphasis on oral hygiene instruction, appliance construct ion, and periodical checkups throughout treatment.

To counteract the tendency of or thodont ic appliances to increase the accumulation of plaque on the teeth, at tempts should be made to keep the appliances and mechanics simple, and avoid hooks, elastomeric rings, and excess flash a round the bracket bases. ~4 The use of steel ligatures is r e c o m m e n d e d on all brackets, even the tooth- colored brackets (Fig 2), because elastomeric rings have been shown to attract significantly more plaque than steel ties. 25 Bonds are prefer- rable to bands. 26 Bonded molars show less plaque accumulation, gingivitis, and loss of a t tachment interproximally than do banded molars dur ing the or thodont ic t rea tment of adults. 24-26 How- ever, bonding is more complicated in adult patients than in adolescents. Many adults have

crown-and-bridge restorations made of porcelain or precious metals, in addition to amalgam restorations on molar teeth. Until recently, it was inconceivable that clinically acceptable bond strengths could be achieved with surfaces other than enamel, particularly in the mandibular posterior region. Following the introduction of a wide variety of new techniques and materials, it is now feasible to bond or thodont ic brackets, buc- cal tubes, and retainer wires to artificial surfaces, including amalgam, 27,2s porcelain, and gold, 27 and clinical experience with bonding to all different artificial tooth surfaces has proven to be excellent.

After the 4 to 6 months observation period after per iodontal t reatment, a careful clinical examinat ion and recording of status is necessary before or thodont ic t rea tment is initiated. This examinat ion should consist of probing every tooth, mobility check, check for bleeding points and exudation, and also include standardized intraoral radiographs. Renewed oral hygiene instruction and motivation is made after the p lacement of the or thodont ic appliances. Dur- ing the t reatment period professional tooth cleaning by a dental hygienist or periodontist may be pe r fo rmed at 3-month intervals, 26,29 or after regular examinat ion updates at 6 and 12 month intervals, depend ing on the situation. The reex- aminations should include recordings of probing depths, mobility, bleeding on probing, suppuration, gingival recessions, bone levels, and any other indicator of potential problems. Profes- sional scaling may be particularly indicated during active intrusion of elongated maxillary incisors, and when new a t tachment attempts are made, 32,33 because or thodont ic intrusion may shift supragingival plaque to a subgingival loca- tion. 3°,3I If efforts at maintaining excellent-to- good oral hygiene are unsuccessful, or thodont ic t rea tment should be terminated, a4

Following appliance removal, reinstruction in oral hygiene measures should be given to pre- vent subsequent labial gingival recession occur- ring as the result of overzealous toothbrushing, since cleaning is now easier to per form.

Periodontal Condition in Adult Orthodontic Patients

It is evident that or thodont ic tooth movemen t can be p e r f o r m e d in adults with reduced but

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healthy per iodont ium without further periodontal deterioration. 29,s5,36 Figures 2 to 5 show the periodontal status of three different adult orthodontic patients with advanced periodontitis. The findings of no significant further periodontal breakdown in these patients depended on the prerequisites outlined previously.

There exist few well-controlled studies on groups of adults with advanced periodontitis, who have received a full period of orthodontic fixed-appliance treatment. The most comprehen- sive study was carried out by Boyd et a129 al- though their material was limited. Ten adults with generalized periodontitis received preorth- odontic periodontal treatment including surgery, and then regular maintenance at 3-month intervals during a 2-year orthodontic treatment period. Six of the patients had 10 teeth severely compromised with probing depths of 6 mm

a n d / o r furcation involvement. Plaque, gingivitis, bleeding on probing, and pocket depths were assessed at 3-month intervals and probing depths and probing at tachment levels were measured at the start of treatment and at 3 months posttreatment. Ten control adults were used who had normal periodontal tissues and who received no periodontal maintenance during their orthodontic treatment. Also 20 adolescents served as reference patients. The results showed that:

1. Adults were more effective than adolescents in removing plaque, especially late in treatment.

2. Tooth movement in adults with reduced but healthy periodontium did not result in further significant loss of at tachment (none of the adults had mean loss of at tachment of more than 0.3 mm).

Figure 2. Adult female patient with advanced periodontal breakdown before (A-C,G), during (E-F), and after (D,H) 6 months of orthodontic treatment of the maxillary arch only. Note extensive destruction of bone around maxillary first molars, both of which show through-and-through furcation involvement (lure in B and C). In addition, the right molar has an extensive mesial infrabony pocket (white arrow in B). Orthodontic treatment was performed without bracket- ing the molars, and included extensive mesiodis- tal recontouring of all teeth mesial to the molars, and realigning of the teeth. Note in E and F that steel ties were used for hygienic reasons also on the tooth colored brackets. The posttreatment result was stabilized by means of a flexible spiral wire retainer (RW) bonded to each of six anterior teeth.

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Figure 3. Adult male patient with advanced periodontal destruction and marked pathological migration of the maxillary anterior teeth before (A-C) and after (D-F) orthodontic fixed-appliance treatment for 2 years. The patient was treated periodontally and orthodontically according to the new concepts outlined in the text. Note in C aggressive periodontitis and extensive periapical inflammation of three teeth where endodontic treatment was performed. Clinical appearance of the dentition and face is dramatically improved after treatment (D). The radiographic appearance of maxillary (E) and mandibular (F) anterior region 7 years after removal of the orthodontic appliances show markedly reduced but healthy periodontal tissues with no progression of periodontal destruction (small arrows) compared with the initial (B and C). More clinical information of the same patient is shown in Figure 4.

3. Adults with teeth that did not have healthy periodontal tissues may experience further breakdown and tooth loss because of ab- scesses during orthodontic treatment.

In another study by J~rtun and Urbye, 36 the effects of fixed orthodontic treatment was assessed radiographically on 24 patients (aged 20 to 65 years) who had advanced loss of marginal bone and pathological tooth migration. Follow- ing periodontal treatment, active appliance therapy was not started until inflammation had been eliminated, and the level of oral hygiene was high. Treatment was limited to realignment of the front teeth in one arch, and lasted for an average of only 7 months. Bone level measure- ments on radiographs indicated that the major-

it,/ of sites showed little or no loss of bone support. However, a few sites showed pro- nounced bone loss, indicating imperfect plaque control, and 35% bone loss occurred in one site.

"Hopeless Teeth"

According to the old concepts of peridontal disease being a generalized phenomenon , the retention of teeth diagnosed as periodontally "hopeless" would accelerate the destruction of the adjacent interproximal periodontium. Such teeth were therefore frequently extracted in the past, resulting in bone constriction in the area. However, in view of the concepts of site-specificity, the theoretic rationale for such extractions would seem unsupported. Indeed, recent fol-

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low-up studies have shown that r e t a i n e d p e r i o d o n - tally " h o p e l e s s " t ee th do n o t s ignif icant ly affect the i n t e r p r o x i m a l p e r i o d o n t i u m o f ad j acen t tee th fo l lowing t h e r a p y ) 74°

T h e c l in ical i m p l i c a t i o n o f these resul ts for o r t h o d o n t i c pa t i en t s wou ld be to advise de l ay ing the ex t r ac t i on o f t ee th for p e r i o d o n t a l r easons un t i l a l a te r s tage o f the disease p rocess t han h a d b e e n advoca t ed p rev ious ly ) 9,4° This does n o t m e a n tha t m u l t i r o o t e d tee th with extens ive verti- cal loss o f b o n e s u p p o r t o r t h r o u g h - a n d - t h r o u g h fu rca t ions n e e d to be i n c l u d e d in the o r t h o d o n - tic hook-up . F igure 2 i l lustrates the p r inc ip l e o f r e t a i n i n g several " h o p e l e s s " t ee th d u r i n g or th - o d o n t i c t r e a t m e n t w i thou t a t t e m p t i n g to move them, or i n c l u d e t h e m in the a n c h o r a g e units ,

Figure 4. Intraoral photo- graphs pretreatment (T0 and posttreatment (T2) of same patient as in Figure 3. The improved dental result is retained by means of a bonded lingual retainer (RW). On the left side, a two-unit br idge was con- structed (D). Some inter- dental recession was un- avoidable in the mandibular anterior region (C), but it does not show much clinically (compare Fig 3D).

d u r i n g a 6 -mon th t r e a t m e n t p e r i o d l imi t ed to the 10 a n t e r i o r tee th .

Retention

Rationale

T h e m i g r a t i o n o f t ee th assoc ia ted with p e r i o d o n - tal b r e a k d o w n a r o u n d the incisors in adul ts is usual ly b l a m e d on i n f l a m m a t o r y swell ing o r the tongue . However, a c c o r d i n g to Proffi t , 41 two m a j o r p r i m a r y factors a re involved in the equi l ib- r i um tha t d e t e r m i n e s the f inal pos i t i on o f teeth. These are the res t ing pressures o f l ip o r c h e e k a n d tongue , a n d forces p r o d u c e d by me tabo l i c activity wi th in the p e r i o d o n t a l m e m b r a n e . Wi th

Figure 5. Posttreatment clinical (A) and radiographic (C) appearance of adult male patient with advanced periodontitis [see situation at start of orthodontic treatment in B] after periodontal and orthodontic treatment, and many years later (D). One lower incisor was extracted as part of therapy. A six-unit bonded lingual retainer (RW) was used to stabilize the treatment result. The bonded wire will act both as an invisible and neat orthodontic retainer and as a periodontal splint, which would appear advantageous in cases where the destruction is as advanced as in this patient. Note signs of improvement of peridontal condition 8 years after removal of the orthodontic appliances, with marked crestal lamina dura (LD) contours. Some incisors in (C) had so little bone support that if the bonded retainer had not been used, they would probably have been lost over time.

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an intact p e r i o d o n t i u m , i m b a l a n c e d tongue- l ip forces are no rma l ly coun te rac t ed by forces f rom the pe r iodon ta l m e m b r a n e . However, when the p e r i o d o n t i u m breaks down, its stabil izing func- t ion can n o longe r exist, and the incisors beg in to move. If this hypothesis is correct , a conse- q u e n c e would be that persons with advanced pe r iodon ta l disease and tooth migra t ion would n e e d p e r m a n e n t r e t en t ion after the o r t hodon t i c correct ion.

Design The opt imal long- te rm re ta iner for adults with r educed p e r i o d o n t i u m is the flexible spiral wire (FSW) re ta ine r b o n d e d l ingual ly on each tooth in a segment . 42-44 The fabr icat ion and long- te rm

evaluat ion of such re ta iners is descr ibed else- where. 44 Figures 1 to 5 show di f ferent designs of FSW retainers in the maxil la a n d the m a n d i b l e in several patients. At the same t ime it works as a reliable invisible o r t hodon t i c retainer , 42-44 it con- comi tant ly acts as a nea t and hygienic pe r iodontal splint, which allows the individual teeth within the spl int to move physiologically. As long as the re ta ine r r emains intact, small spaces migh t o p e n up distal to, bu t n o t within, the retainer . 36,44

Effects

Ramfjord 1 c la imed that sp l in t ing may no t be

n e e d e d for most teeth with increased mobil i ty after pe r iodon ta l therapy. However, r educe d mobility of teeth after c o m b i n e d pe r iodon ta l a n d o r thodon t i c t r e a tmen t by us ing a FSW re ta iner would seem to be of cons iderab le benefi t . If a b o n d e d re ta ine r is no t used, bu t ins tead a remov- able plate or spr ing re ta ine r is used at n igh t on a long- te rm basis, there is a risk for o n g o i n g j igg l ing of the teeth because of the relapse t endency d u r i n g the day. 4x Exper imen ta l studies in animals indica te that j igg l ing forces may facilitate the progress of a t t a c h m e n t loss in per iodont i t is , 45,46 or at least result in more b o n e resorpt ion. 47 Also, more connect ive tissue reat- t a c h m e n t a n d b o n e r egene ra t i on may occur a r o u n d non- j igg led teeth. 4s Monkey experi - ments have shown that when expe r imen ta l j ig- gl ing of teeth was s topped, a s ignif icant gain of alveolar b o n e occurred. 47 Recently, Burget t et a149 n o t e d that the hea l ing fol lowing pe r iodon ta l therapy may be more advantageous in pat ients who received occlusal ad ju s tmen t than in n o n a d -

j u s t ed patients . Figures 3 a n d 5 show the excellent long- term per iodonta l react ion when b o n d e d FSW reta iners were used in two cases with severely advanced pe r iodon ta l b reakdown in the incisor areas. Several years ( > 7 to 8 years) after t e r m i n a t i o n of the o r thodon t i c t rea tment , the pe r iodon ta l cond i t i on a r o u n d the incisors ap- pears u n c h a n g e d or improved.

References

1. Ramfjord SP. Changing concepts in periodontics. J Pros- thet Dent 1984;52:781-786.

2. Axelsson E Lindhe J. Effects of controlled oral hygiene procedures on caries and periodontal disease in adults. Results after 6 years.J Clin Periodonto11981;8:239-248.

3. Axelsson P, Lindhe J, Nystr6m B. On the prevention of caries and periodontal disease. Results of a 15-year longitudinal study in adults. J Clin Periodontol 1991;18: 182-189.

4. Ramfjord SP, Morrison EC, Burgett FG, et al. Oral hygiene and maintenance of periodontal support. J Periodontol 1982;53:26-30.

5. Socransky SS, Haffajee AD, Goodson JM, et al. New concepts of destructive periodontal disease. J Clin Peri- odontol 1984;11:21-32.

6. Listgarten MA. A perspective on periodontal diagnosis. J Clin Periodontol 1986;13:175-181.

7. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: Current concepts. J Periodontol 1992;63:322-331.

8. Jeffcoat MK. Current concepts in periodontal disease testing.JAm Dent Assoc 1994;125:1071-1078.

9. Badersten A, Nilveus R, EgelbergJ. Effect of nonsurgical periodontal therapy. II. Severely advanced periodontitis. J Clin Periodontol 1984;11:63-76.

10. Badersten A, Nilveus R, EgelbergJ. Effect of nonsurgical periodontal therapy. III. Single versus repeated instrumentation. J Clin Periodontol 1984;11:114-124.

11. H/immerle CHF, Joss A, Lang NP. Short-term effect of initial periodontal therapy (hygienic phase). J Clin Peri- odonto11991;18:233-239.

12. Pedrazzoli V, Kilian M, Karring T, et al. Effect of surgical and nonsurgical periodontal treatment on periodontal status and subgingival microbiota. J Clin Periodontol 1991; 18:598-604.

13. Renvert S, Nilveus R, Dahl6n G, et al. Five-year follow up of periodontal intraosseous defects treated by root planing or flap surgery. J Clin Periodontol 1990;17:356-363.

14. Lindhe J, Nyman S. Scaling and granulation tissue removal in periodontal therapy.J Clin Periodontol 1985; 12:374-388.

15. Claffey N. Decision making in periodontal therapy. The re-evaluation.J Clin Periodonto11991;18:384-389.

16. Page R. Frontiers in periodontics. Pac Coast Soc Orth- odont Bull 1991;63:39-41.

17. Listgarten MA, Lai CH, Young V. Microbial composition and pattern of antibiotic resistance in subgingival microbial samples from patients with refractory periodontitis. J Periodontol 1993;64:155-161.

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subgingival microbial samples from patients with refractory

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