Journctl af Clinical Periodontoiogy 1983; 10: 206-22i

Key words: Atiactied gingiva - keralinized gmgifa - perludonial heatlli - perhdonlat surgery - wound heating.Accepled for pubUcation July 1, I3fi2

Role of attached gingiva for maintenance ofperiodontal health

Healing following excisional and grafting procedures in dogs

JAN WENNSTROM and JAN LINDHE

Department of Periodontology, School of Dentistry, University of Gothenburg, Gothenburg, Sweden

Abstract. The present study was undertaken to analyze ih^ ro\e of attached gingiva iot the. maintenanceof periodonta! health in sites with normal and reduced height ofthe supporting apparatus. Furthermore,the effect of excision and grafting of gingiva on some parameters describing dimensions and location ofthe periodontal tissues was evaluated. 7 beagle dogs were used. A baseline examination comprisedassessments of dental plaque, gingivai conditions, attachment level, position of the gingival margin andwidth of the keratinized and the attached gingiva. In the right side of tbe jaws (experimental side) a 6-month period of periodontal tissue breakdown was followed by surgical excision ofthe entire zone of thegingiva. After another 4-month period of healing with daily plaque control, a gingival graft was insertedin one quadrant of the experimental side to regain a zone of attached gingiva while the other quadrant ofthe experimental side was left ungrafted. In the left side of the jaws (control side), the teeth weresubjected to daily meticulous pjaque control during the entire study. In one of the control quadrants theentire zone of the keratinized and attached gingiva was excised at a time point corresponding to thegrafmg procedure in the experimental side, while the gingiva in the remaining control jaw quadrant wasleft unoperated. Clinicai examinations of all control and experimental tooth units were repeated atcertain time intervals during the course ofthe study. The fmal examination was carried ont 4 monthsafter grafting.

The results ofthe experiment showed that in sites exposed to careful plaque control measures gingivalhealth couid be established and maintained without sign of recession of the gingival margin or loss ofattachment, independent of (1) presence or absence of attached gingiva, (2) width of keratinized gingivaor (3) height of the supporting attachment apparatus. Following surgical excision of the entire gingiva,all buccal sites regained a zone of keratinized gingiva, but most sites were lacking attached gingiva.Furthermore, grafting of gingival tissue significantly increased the width of the keratinized and theattached gingiva but had no obvious effect on the position of the gingival margin or the level of theattachment.

The attached gingiva is a dense, collagenous in humans is a loose, elastic connective tissueconnective tissue firmly hnked to the underlying covered by a non-keratinized epitheliumalveolar bone and root surface, and covered by (Orban 1948).a keratinized epithelium. Ciinically, the width It has been suggested that the presence of aof the attached gingiva is determined as the certain zone of attached gingiva is essential fordistance between the gingival margin and the (I) the maintenance of gingival health, (2)mucogingival junction reduced with the prob- prevention of gingival recession and (3) un-ing depth. Thus, the attached gingiva separates altered levels of the connective tissue attach-the free gingiva from the fl/veo/arm«co5a which ment (e.g. Gartreil & Matthews 1976, Schmid

ATTACHED GINGIVA - PERIODONTAL HEALTH 207

1976). In a clinical trial by Lang & Loe (1972) itwas demonstrated that in areas with less than 1mm of attached gingiva inflammation persisteddespite optima! piaque control. Numerous sur-gical procedures have been developed to correctso-called mucogingival "deficiencies" (for re-view sec Nery & Davies 1976).

Recent observations by Miyasato et al.(1977), Dorfman et al. (1980) and de Trey &Bernimoulin (1980), however, have questionedthe concept that there is a need for attachedgingiva for the maintenance of gingivai health.In the studies referred to it was demonstratedthat non-inflamed marginal soft tissue can beestablished and maintained in areas with aminimal zone of, or lack of, attached gingivaand, in addition, that in the presence of plaquesuch areas are not more susceptible to inflam-mation than areas with an "adequate" width ofattached gingiva.

Also the concept that a zone of attachedgingiva is necessary for the prevention of gin-gival recession and loss of attachment hasrecently been questioned. In a clinical trialcomprising 92 human subjects Dorfman et al.(1980) placed free autogenous gingival grafts inone of bilateral buccal sites with "inadequate"zones of attached gingiva. The oral hygieneof the patients was carefully supervised overa 2-year period. Reexaminations performed atvarious intervals after surgery revealed thatneither grafted nor non-grafted sites demon-strated further attachment loss or recessionof the "soft tissue margin" (i.e. gingival margin).Hangorsky & Bissada (1980) performed a simi-lar study and confirmed in most respects thefindings by Dorfman et al. (1980). Lindhe &Nyman (i980) examined the alterations of theposition of the "soft tissue margin" on thebuccal surface of teeth in patients who followingtreatment for advanced periodonta! disease hadbeen enrolled in a meticulous maintenance careprogram for 10-11 years. In all patients thedistance between the cementoenamel junctionand the soft tissue margin was assessed on allbuccal surfaces of all teeth treated. In addition

the presence or absence of keratinized gingivaon the buccai surfaces was determined. Theauthors reported that no apical displacement ofthe position of the "soft tissue margin" occurredduring the observation period, either in areaswith, or in areas without, a zone of keratinizedgingiva. On the contrary, in both types of areasa small coronal regrowth of the gingival marginoccurred during 10-11 years of observation.

In a study by Wennstrom et al. (1981) anexperimental model was developed in beagledogs which enabled the establishment of dif-ferent types of dentogingival units. Followingextensive, experimentally produced, break-down of the periodontal tissues the diseasedsites were treated surgically by techniques inwhich the keratinized gingiva was either pre-served or completely removed. After healing itwas observed that 2 different categories ofgingival units had been estabiished, namely (1)regenerated gingival units accompanied by awide zone of keratinized gingiva with a com-paratively thick keratin layer of the coveringepithelium and (2) regenerated gingival unitsaccompanied by a narrow zone of, or with lackof, keratinized gingiva including an oral epithe-lium with a comparatively thin keratin layer. Inboth types of gingival units non-inflamed con-ditions could be established and maintained byproper plaque control measures. When bac-terial plaques were allowed to accumulate onthe tooth surfaces of the dogs, the free gingivalunits associated with wide or narrow zones ofkeratinized gingiva responded to the microbialcolonization by an inflammatory reaction, thelocation and extension of which did not varywith the width of the keratinized gingiva(Wennstrom et al. 1982). It was concluded thatthe capacity for inflammatory response of themarginal soft tissue against piaque infectionwas unrelated to the absence or presence orwidth of the keratinized gingiva.

The aim of the present study was to analyzefurther the role of an attached gitigiva for themaintenance of periodontal health in sites withnormal or reduced height of the supporting

208 WENNSTROM AND LINDHE

apparatus. Furthermore, the effect of excisionand grafting of gingiva on some parametersdescribing dimensions and location of theperiodonta! tissues was evaluated.

Material and MethodsThe study was performed in 7 female beagledogs, aged around 2 years at the beginning ofthe experiment. The dogs were fed a soft dietallowing the accumulation of large amounts ofDental plaque. A clinical and radiographicalexamination at the start of the study revealedthe presence of dental plaque, calculus andgingival inflammation in the premoiar andmolar regions of the dentition, but no ioss ofconnective tissue attachment or alveolar bone.

Small amalgam restorations were placed incavities prepared in the buccai surface of themaxillary and the mandibular second, third andfourth premolars and the mandibular firstmolars. The apica! border of the amalgamrestorations which were placed coronaliy to themesial and the distal roots served as a referencefor the clinical assessments.

At each clinical examination performedduring the course of the study the followingparameters were assessed at the buccai surfaceof each root of the maxillary (buccai roots) andmandibuiar second, third and fourth premolars('''4,3,2r'2',3,4) and the mandibular first molars(iMi):

1. Plaque Index (Pll) - according to Silness &Loe (1964).

2. Gingiva! Index (GI) - according to Loe &Silness (1963) and Loe (1967).

3. Gingival Exudate (GE) - according to theorifice technique described by Loe & Holm-Pedersen (1965). The stained area of thefilter paper strips used was measured to thenearest 0.5 mm with the use of a slidingcaliper.

4. Probing depth (PD).5. Clinical attachment level (AL) - i.e. the

probing depth assessed from the apicalborder of the amalgam restoration.

6. Position of the gingival margin (GM) - i.e.the distance between the amalgam restora-tion and the "soft tissue margin".

7. Width of the keratinized gingiva (KG) - i. e.the distance between the "soft tissue margin"and the mucogingival junction after stainingthe alveolar mucosa with Schiller's iodinesolution (Fasske & Morgenroth 1958).

8. Width of the attached gingiva (AG) - i.e.KG reduced with the probing depth.

All linear distances were measured with acalibrated periodontal probe, which had adiameter of 0.4 mm and 1 mm gradings.

The design of the experiment is outlined inFig. 1. Following a Baseline examination (Day0) the teeth in the left side of the jaws (controlside) were carefully scaled and polished anddaily, during the subsequent 420 days, subjectedto meticulous plaque removal by the use oftoothbrush and dentifrice.

In the right side of the jaws (experimental side)periodontal tissue breakdown was induced ac-cording to a technique described by Lindhe &Fricsson (1978). Cotton floss ligatures wereplaced in a subgingival position around theneck of all experimental teeth and plaque wasaiiowed to accumulate. To enhance the rate ofbreakdown, the cotton floss ligatures wereexchanged every 3 weeks. After 120 days theligatures were removed but plaque was allowedto accumulate for another 60 days (Fig. 1).

Subsequent to the clinical examination onDay 180 the inflamed periodontal tissuesaround the teeth in the experimental side wereremoved using a surgical procedure. An inci-sion was made around I mm apical to themucogingival junction and a full thickness flapwas elevated on the buccai side of the teeth. Asimilar procedure was performed on the lingualside of the teeth in the mandible, while agingivectomy procedure was used on the palatalside in the maxilla. The soft tissue portion,coronal to the incision line, which included not

ATTACHED GINGIVA - PERIODONTAL HEALTH 209

EXPERIMENTAL DESIGN

LEFTSIDE

I I I H i 1-300 330 360

EXP.PERIODONTAL BREAKDOWN

RIGHT

HEALING

LIGATUREPLACEMENT

I I I

HEALING

PlaQue conlrol

TRANSP.OFKER GINGIVA(one jgw)

• PB-£<c/sed"PB-Grafted-

EXAMINATIONS:

X X X

Fig, 1. Experimental design. In the left side of the jaws a careful plaque control program was maintainedthroughout the study. On Day 300 the entire zone of gingiva was removed in one jaw quadrant (N-excised). Inthe right side of the jaws periodontal breakdown was induced and progressed for 180 days by ligature placement(Day 0-120) and plaque accumulation (Day 0-180). Surgical treatment including removal of the entire zone ofgingiva was performed on Day 180. Thereafter, meticulous tooth cleaning was carried out daily for theremaining part of the study. On Day 300 a gingival graft was inserted in one jaw quadrant (PB-grafted). CUnicaiexaminations were carried out at indicated time intervals.Ptanung und Organisation der Studie. Wdhrend der gesamten Versuehszeit wurde an den linken Kieferseiten einsorgfdltiges Flaque-Konlrollprogramm administriert. Am Versuehstage 300 wurde an einem Quadramen dieGingiva in ihrer Gesamtheit exzidiert (N-exzidiert). Auf den rechten Kieferseiten wurde parodontale Destruktioninduziert und 180 Tage lang durch Anbringen von Eigaturen (Versuehstag 0-120) und das Ansammeln von Flaque(Versuchstag 0-180) aufrechterhalten. Die ehirurgische Behandlung, die aus der Entfernung der Gingiva in ihrerGesamtheit bestand. wurde an dem Versuehstag 180 vorgenommen, Danach wurde wdhrend der noch verbleibendenVersuchszeil taglich sorgfdltige Zahnreinigung durchgefuhrt. Am Versuehstage 300 wurde in einen der Kiefer-quadranten ein gingivales Transplanlat inserierl (PB-iransplantiert). An indizierten Zeitpunkten wurden klinischeNachuntersuchungen vorgenommen,Protocole experimental, Du cote gauche (left side) des machoires, un programme d'elimination soigneuse de laplaque (plaque control) a ete maintenu pendant lout Ie courxde f etude. Au Jour 300. la lotalite de la zone de gencivekeratinisee a ete supprimee dans un des quadrants (sites normaux avee excision = N-exeised). I'autre servant detemoin (N-eonlrol), Du cote droit (right side), une desirueiion parodontale (periodontalbreakdown) a eteprovoqueeet a evolue pendant 180 fours a la suite de la pose de ligatures (four 0-120) et de I aeeumulation de la plaque (Jour0-180), Un traitemeni chirwgieal comporiani I'elimination de la zone de gencive keraiiiiisee a eie cffcctuc au Jour180. Un nettoyage mcticuleux des dents (plaque eontrol) a ensuite eti execute lous les fours pendant le resie deI'eiude. Au Jour 300. une greffegingivale a eteplaeee dans un des quadrants (FB-grafted). Lesexamens eliniques ontete effeetues aux imervalles indiques par le tableau (examinations).

only the inflamed periodontal tissues but alsothe entire zone of the keratinized and attachedgingiva, was removed together with the under-

lying periosteum. The exposed portions of theroots were carefully scaled and planed. Themucosal flaps were moved in coronal direction.

210 WENNSTROM AND LINDHE

placed against the tooth surfaces and secured inthis position with interproximal and interrad-icular sutures to achieve complete coverage ofthe surgically denuded alveolar bone. No sur-gical dressing was applied. Starting on the dayof surgery the teeth of both sides of the jawswere subjected to plaque controi by the use ofchlorhexidine digluconate (0.2%) washings(twice daily for 1 week) and mechanical means,tooth brushing (once daily) from Day 187 toDay 300 (Fig. 1).

The position of the gingival margin (GM) andthe width of the keratinized gingiva (KG) wereassessed after 2 and 4 weeks of healing (Days195 and 210).

On Day 300, i.e. after 120 days of healing(Fig. 1), the clinical examination was repeated.A gingival graft was subsequently placed in onequadrant in the right side of the jaws (experi-mental side) in order to increase the zones ofattached and keratinized gingiva. In 3 dogs thegrafting procedure was performed in the maxi!-iaryjawandin4dogsin themandibularjaw. Anincision was made at the mucogingiva! junctionof the recipient sites in the experimental sideand the marginally located tissue was excised. Aspht flap was elevated leaving the periosteum onthe alveolar bone surface. The marginal edge ofthe flap was moved in an apical direction to alevel around 5 mm apical of the marginal bonecrest. The flap was secured in this position andsutured to the periosteum. From the oppositeside of the maxilla or mandible {the left side ofthe Jaws) the entire portion of the keratinizedgingiva was removed in one quadrant (thedonor site) and immediately transplanted tothe recipient site. The autograft was secured inits new position with interproximal sutures andfor 5 min pressed against the recipient bed. Thegraft was covered with a periodontal dressing(Coe-Pac®) resting in a custom-made acrylicstent which was kept in piace for 6 days. In thedonor sites the denuded alveolar bone wascovered by a coronaily sliding flap preparedfrom the alveolar mucosa.

Six days after grafting the sutures were re-

moved and a new periodontal dressing wasapplied and retained for further 7 days. During2 weeks of initial heaiing plaque control wasmaintained by chlorhexidine washings. Sub-sequently mechanical tooth cleaning was exer-cised once a day. Clinical examinations werecarried out after 30, 60 and 120 days of healing;i. e. experimental days 330, 360 and 420 (Fig. 1).

At the end of the study, in each dog 4 differenttypes of "dentogingival" units had been estab-lished (Figs. 1 and 2), namely:

1. Normal non-operated gingiva! units withwide zones of keratinized (KG) and attachedgingiva (AG) and with normal height of thesupporting apparatus (N-control), i.e. thejaw quadrant in the left side where thegingiva was left unoperated (Fig. 2D).

2. Regenerated gingival units with narrowzone oi KG, but without AG, and withnormal height of the supporting apparatus(N-excised), i. e. the donor site of the left jawquadrants (Fig. 2B).

3. Regenerated gingival units with narrowzone of KG, but without AG and withreduced height of the supporting apparatus(PB-excised), i.e. the ungrafted jaw quad-rant in the right side (Fig. 2A).

4. Regenerated gingival units with wide zonesof KG and AG. and with reduced height ofthe supporting apparatus (PB-grafted), i.e.the recipient site of the right side (Fig. 2C),.

Percentage distribution of Plaque and Gingiva!Index scores 0,1,2 and 3 was calculated for eachjaw quadrant and dog. For all other parametersindividual mean values representing each quad-rant and dog were calculated. Statistical analy-sis of the data was performed using Student's t-test and analysis of variance.

ResultsOral hygiene and gingival conditionAt the start of the experiment aimost all buccaltooth surfaces in the posterior dentition of the

ATTACHED GINGIVA - PERIODONTAL HEALTH 211

Fig- 2. Clinical photographs illustrating the various "dentogingival" units established in the4 jaw quadrants. A.PB-excised units. B. N-excised units. C. PB-grafted units. D. N-controi units.Die klinisehen Fotograften veransehaulichen die verschiedenen "demogingivalen" Einheiten der 4 Kiefer-quadranten. A. FB-exzidierte Einheiten. B. N-exzidierte Einheiten. C. FB-tran.splantierte Einheiten. D. N-Kontroll-einheiten.Fhotographies cliniques illustratit les differents sites "gingivo-dentaires" etablis dans les 4 quadrants. A. sites FB-excises (FB-exeisedj. B. sites N-excises (N-excised). C. sites FB-avec greffes (FB-grafted). D. sites N-temoins (N-control).

dogs harboured dental plaque and calculus andtbe adjacent gingiva showed ciinical signs ofinflammation (Day 0; Figs. 3, 4). Around 50%of the tootb surfaces in each quadrant had grossamounts of dental deposits, while only around

7% were free frotn plaque. Between 15-28% ofthe gingiva! units showed marked signs ofinflammation (GI score^2). The remainingunits displayed only shght change in colour andtexture (GI score=l). From all buecal units

WENNSTROM AND LINDHE

PLAQUE INDEX SCORES

N-Co

N-Ex

PB-E

xPB

-Gr

:•:•::':': ?:^§:'

1

1 V//

//////M

W////////A\

N-Cc

PB-E

xPB

-Gr

N-Co

N-Ex

PB-E

xPB

-Gr

1O K lU 13

U LiJ 1 11 1 m m

Z Z Q. D.

W Score 3K Score 2^ Score 1^ Score 0

DAY 0 DAY 180 DAY 300 DAY 420Fig. 3. Mean percentage of buccai tooth surfaces with Plaque Index scores 0 , 1 , 2 and 3 on Days 0, 180, 300 and420 for the N-control , N-excised, PB-excised and PB-grafted units.

Mittlere Anzahl bukkaler Zahnoberfldchen (in Prozent) mit den Plaqueindex-Scores 0, I, 2 und 3 an denVersuchstagen 0. 180, 300 und 420 bei N-Kontroll-, N-exzidierten-. PB-exzidierten- und PB-transplanticrtenEinheiten.Pourcentage tnoyen defaces vestibulaires ayant pour I'Indice de Plaque les scores 0, 1, 2et3 aux Jours 0, 180. 300 et420 pour les sites N-control. N-excised, PB~excised et PB-grafted.

GINGIVAL INDEX SCORES

DAY 0

i^SS

DAY 180 DAY 300 DAY 420

Score 3

Score 3

So ore 1

Score 0

Eig. 4. Mean percentage of gingival units with Gingival Index scores 0,1,2 and 3 on Days 0,180, 300 and 420 forthe N-contro!, N-excised, PB-excised and PB-grafted units.Mittlere Anzahl gingivaler Einheiten (in Prozent) mit den Gingivalindex-Scores 0. 1. 2 und 3 an den Versuchstagen0, 180, 300 und 420 bei N-Kontroll-. N-exzidierten-, PB-exzidierten- und PB-transplantierten Einheiten.

Pourcentage moyen de sites ayant pour I'Indice Gingiva! les scores 0. I,2et3 aux Jours 0. 180, 300 et 420 pour lessites N-control, N-excised, PB-excised et PB-grafted.

ATTACHED GINGIVA - FERIODONTAL HEALTH 113

Table 1. Amount of Gingiva] Exudate at the various examination intervals. Mean value (mm) and standarddeviationDie Menge gingivalen Exsudates bei den verschiedenen Untersuehungsintervallen. Mittelwert (mm) undStandard-abweichungQuantites d'exsudat gingival aux differents examens, Valeur moyenne (mm) et ecart-type

Units

N-ControlN-ExcisedPB-ExcisedPB-Grafted

Day 0

2.9±1.03.2±1.43.0+i. l3.4±1.7

Day 180

0.9 + 0.51.2+1.58.7 + 2.78.9 + 3.7

Day 300

0.3±0.20.1+0.20.4+0.50.3±0.5

Day 420

0.2±0.20.3 + 0.20.1±0.20.2±0:2

N-Control (N-Kontrolle, N-temoin), N-«xcised (N-exzidiert, N-excise), PB-grafted {PB-transplantiert, FB-avee greffe).

Gingival Exudate could be collected, and themean amounts obtained from the 4 jaw quad-rants varied between 2.9 and 3.4 mm (Table 1).

As a consequence of the plaque controlmeasures on the left side of the faws (N-controiand N-excised) clinical examinations performedon Days 180, 300 and 420 revealed the presenceof clean tooth surfaces (Fig. 3) and in com-parison to Day 0 improved gingiva] conditions.Thus, on Day 180 - 83%, Day 300 - 94% andDay 420 - 97% of the gingival units examinedwere considered healthy (Fig. 4). The meanamounts of Gingival Exudate also decreasedduring the observation period and were foundto be close to zero on Days 300 and 420(Table I).

On the right side of ihe jaws (PB-excised andPB-grafted) the placement of ligatures resultedin gross accumulation of bacteria! deposits (Fig.3) and pronounced signs of gingival inflamma-tion (Fig. 4). At the reexamination on Day 180the frequency of Gingival Index score 3 wasaround 50% (Fig. 4) and from ali gingival unitslarge amounts of Gingival Exudate could becollected (mean values 8.7-8.9 mm; Table 1).The surgical excision of the inflamed tissuesfollowed by scaling and daily performed plaquecontrol measures resulted in an improvement ofthe conditions of the marginal gingiva. Thus,the reexamination performed at the end of thehealing period (Day 420) revealed that all toothsurfaces examined were free from plaque (Fig.3) and that almost all gingiva! units (98%) were

classified as clinically healthy (Fig. 4). Theremaining gingival units showed only minutesigns of inflammation (Gl score—]). In addi-tion, only minute amounts of Gingival Exudatecould be collected (Table 1).

Attachment level and probing depthThe results from the assessments of the clinicalattachment level are presented in Fig. 5 andTable 2. In the non-operated "plaque-free"

ALTERATIONS IN ATTACHMENT LEVELS

mmLoss

-t—I-0 laO 300 330 420 Days

Fig. 5. Alterations in attachment levels forthe varioustypes of'dentogiugivai" units during the course of thestudy.Verdnderungen der Attaehmentniveaus bei den ver-schiedenen Typen "deniogingivaler" Einheiten wdhrenddes Versuehsablaufes,Modifications des niveaux de I'attache dam les dif-ferentes categories de sites "gingivo-dentaires"pendantle eours de I'etude,

WENNSTROM AND LINDHE

Table 2, Alterations of clinical attachment levels between the baseline examination (Day 0) and tbe variousexamination intervals. Mean value (mm) and standard deviationVerdnderungen klinischer Attachmentniveaus zwischen der Ausgangsuntersuchung (Versuchstag 0) und den ver-schiedenen Untcrsuchungsintervallen. Mittelwert (mm) und StandardabwcichungModifications des niveaux cllniques de I'attache entre I'examen intitial (Jour 0) et les differents examens.Valeur moyenne (mm) et ecart-type

Units Day 180 Day 300 Day 330 Day 420

N-ControlN-ExcisedPB-ExcisedPB-Grafted

+ 0.!±0.20.0±0.2

-3.6±0.2-4.2±0.5

+ 0- 0- 3- 4

.I±0.2

.l±0.2

.5±0.2

.2±0.4

+ 0.1±0.I-0.6±0.1-3.6 + 0.4-4.2+0.5

0.0±0.2-0.6±0.3-3.5±0.2-4.0±0.4

control quadrant (N-control) the clinical at-tachment level was maintained unaltered duringthe entire observation period. In the right sideof the jaws the 180 days of experimental peri-odonta! tissue breakdown (PB) resulted in apronounced loss of attachment (on the average3.9 mm; Fig. 5; PB-excised and PB-grafted).This level of attachment was maintained un-altered during the remaining part of the study.Thus, neither surgical excision of the inflamedperiodontal tissues (on Day 180) nor grafting(on Day 300) had a significant effect on theclinical attachment level. In the healthy sites(the left side of the jaws) from which the entirezone of keratinized gingiva was removed onDay 300 (N-excised) a significant loss of attach-ment was observed 30 days following surgery(mean loss 0.5 mm;P<0.01). Between Days 330and 420 no further loss of clinical attachmentoccurred.

The mean probing depths at the differentexamination intervals are shown in Table 3. At

the initial examination (Day 0) the averageprobing depth values varied between 1.5-1.6mm. At the reexamination on Day 180, theprobing depth in the right side of the jaws hadincreased (PB-excised and PB-grafted meanvalues 2.1-2.2 mm; P < 0.01). No pockets with aprobing depth exceeding 3 mm were found. Thesurgical treatment performed in the right side ofthe jaws on Day ISO, followed by daily plaquecontrol, resulted in a reduction of the probingdepth. The probing depth of the regeneratedgingival units of the N-excised quadrants wasshallower on Days 330 and 420 than during thepresurgical phase (Days 0, 180, 300), 1.2 mm vs1.7 mm (F<O.Ol; Table 3).

Width of keratinized (KG) and attached gingiva(AG)The variations observed regarding the width ofthe KG are presented in Fig. 6 and Table 4.Changes which occurred regarding the width ofthe AG are illustrated in Fig. 7. The measure-

Table 3, Probing depth at the various examination intervals. Mean value (mm) and standard deviationSondierungstiefe bei den verschiedenen Untersuchungsintervallen. Mittelwert (mm) und StandardabweichungProfondeur de sondage aux differents examens. Valeur moyenne (mm) et ecart-type

Units Day 0 Day 180 Day 300 Day 330 Day 420

N-ControlN-ExcisedPB-ExcisedPB-Grafted

1.6 + 0.2L6±0.2i.6±0.21.5±0.2

i.7+0.2L7±0.22.1 ±0.3**2.2±0.5**

L7±0.21.8 + 0.21.6+0.21.8±0.2

1.6±0.21.2±0.2**1.7 ±0.21.9±0.3

L6±0.2L3±0.21.7±0.2L9±0.2

** Signifies a statistical difference (/'<0.01) from tbe value obtained at the previous examination (bezeichneteinen statistisch abgesieherten Unterschied(PKO.OI) zu dem Wert der vorhergehenden Untersuchung, differencestatistique (P< 0,01) par rapport a la valeur obtenue a I'examen precedent).

ATTACHED GINGIVA - PERIODONTAL HEALTH 215

WIDTH OF KERATINIZED GINGIVA WIDTH OF ATTACHED GINGIVA

N-ConUQlN-EXCIBBO

t 1 I

mm

4-

3-

2-

1 -a N-CD• N-Ex

300 330 420 Days

180 2 ID 300 330 3S0 420 Days

\

•4-300 330 360 420

Fig. 6. Alterations of the mean width of keratinizedgingiva for the various types of "dentogingival'" unitsduring the course of the study.Verdnderungen der mittleren Breite keratinisierter Gin-giva bei den versehiedenen Typen "dentogingivaler"Einheiten wdhrend des Ablaufes der Studie.Modifieations de la largeur moyenne de la zone degencive keratinisce dans les differentes categories desites "gingivo-dentaires" pendant ie cours de l'etude.

PB-e»c(ssdPB-Graflea

Fig. 7. Alterations of the mean width of attachedgingiva for the various types of "dentogingiva!" unitsduring the course of the study.Verdnderungen der mittleren Breite angewachsenerGingiva bei den verschiedenen Typen "dentogingivaler"Einheiten wdhrend des Ablaufes dieser Studie.Modifications de la largeur moyenne de la zone degeneive attachee dans les diffe.rentes eategories de sites"gingivo-dentaires" pendant le cours de l'etude.

Table 4. Width of the keratinized gingiva at the various examination intervals. Mean value (mm) andstandard deviationDie Breite der keratinisierten Gingiva bei den versehiedenen Untersuchungsintervalien. Mittelwert (mm) undStandardabweichungLargeur de la zone de gencive keratinisce aux differents examens. Vateur moyenne (mm) et ecart-type

Units DayO Day i80 Day 210 Day 300 Day 330 Day 360 Day 420

N-ControlN-ExcisedPB-ExcisedPB-Grafted

4.5 + 0.44.3±0.24.4+0.84.3+0.2

4.4 + 0.74,3 + 0.43.2±0.42.8±0.6

4.5 + 0.74.3+0.4l . l±0.21.0±0.2

4.4±0.84.3±0.4i.7 + 0.21.7±0.5

4.4+0.71.2 + 0.2I.6±0.24.6±0.4

4,4+0.8i.3±0.4].6±0.24.8±1.I

4.3±0.81.5 + 0.41.6±0.24.9+0.9

Size of gingiva] graft inserted on Day 300 in PB-grafted units; 5.8±0.8 {die Grosse des am Versuehstage 300eingepassten Transplantates PB-transplaittierter Finheiten; 5,S±0.8. grandeur des greffes gingivales placees auJour 300 dans les sites FB-grafted: 5,8±0,8).

WENNSTROM AND LINDHE

Table 5. Width of attached gingiva at the various examination intervals. Mean value (mm) and standarddeviationDie Breite der angewachsenen Gingiva an den verschiedenen Untersuchungsintervallen. Mittehvert (mm) undStan dardab weichungLargeur de la zone de gencive attachee aux differents examens. Valeur moyenne (mm) et ecart-type

Units Day 0 Day 180 Day 300 Day 330 Day 420

N-ControlN-ExcisedPB-ExcisedPB-Grafted

2.9 + 0.62.7±0.52.8±0.82.6+0.5

2.8 + 0.62.6±0.5l.l±0.50.7±0.6

2.7±0.72.6+0.4O.!±0.20.1 + 0.1

2.8±0.90.2±0.20.1 ±0.22.9±0.7

2.7±0.80.2+0.40.1 ±0.23.0±1.0

merits made at the start of the study revealedthat the KG had an average width of 4.3-4.5mm in the different jaw quadrants. 2.6-2.9 mmof this zone were considered to belong to theattached gingiva (Table 5). These dimensions ofthe gingival tissue were maintained unchangedin the N-control quadrants during the 420 daysof observation. The period of periodontal tissuebreakdown in the right side of the jaws {PB-excised and PB-grafted) resulted in a significantdecrease of the width of the AG (mean decrease1.8 mm; PKO.Ql; Fig. 7) while the decrease ofthe zone of the KG amounted to 1.3 mm(P<O.OV, Fig. 6).

Following the surgical treatment of the peri-odontal tissues, including excision of the entirezone of keratinized gingiva (Day 180; PB-excised and PB-grafted), the soft tissue re-generated to form a new zone of keratinizedgingiva. Thus, the reexamination performed120 days after surgery (Day 300) revealed that azone, on the average 1.7 mm wide, of KG hadreformed (PB-excised and PB-grafted; Fig. 6;Tabie 4). However, no portion of this regen-erated gingiva was attached to the underlyingbone or root and consequently the width of AGwas considered to be zero (Fig. 7; Tabte 5). OnDay 300 the keratinized gingiva was excisedalso in one ofthe control quadrants (N-excised).The heaiing pattern in this jaw quadrant wassimilar to that of the experimental quadrants.Hence, 120 days after surgery KG had a meanwidth of 1.5 mm, while no AG was observed.

In one quadrant in the right side of the jaws, agingival graft was placed in order to regain a

zone of AG and to increase the zone of KG (PB-grafted). The mean width of the grafts insertedwas 5.8 mm (±0.8). The reexamination carriedout 30 days after grafting (Day 330} revealed thepresence of a 4.6 mm wide zone of KG. Theattached portion made up 2.9 mm of thisgingiva. During the remaining part ofthe studyonly minor and statistically insignificantchanges occurred regarding the width of KGand AG. At the end of the observation periodthe dimensions of the PB-grafted units weresimilar to those of the non-operated N-contro!units (Figs. 6, 7).

Position of the gingival marginThe alterations which occurred in the positionof the "soft tissue margin" (i.e. the gingivalmargin (GM)) are illustrated in Fig. 8 and Table6. In the control tooth regions (N-control) nochange of the position of GM occurred duringthe 420 days of observation. In the right side ofthe jaws (PB-excised and PB-grafted) there wasa pronounced apical displacement of the gin-gival margin between Days 0 and 180 (X=:3.4mm). The clinical examination performed 30days after surgery (i.e. experimental Day 210)revealed a further 0.8 mm apical displacementof the gingival margin. Between Days 210 and300, however, a small (X —0.5 mm) coronalregrowth of the soft tissue occurred.

Measurements performed immediately aftergrafting showed that the coronal edge of thegrafts was located approximately 1 mm coronalof the presurgical level of the gingival margin(PB-grafted; Fig. 8). However, 2 weeks after

ATTACHED GINGIVA - PERIODONTAL HEALTH 217

ALTERATIONS IN POSITION OF GINQIVAL MARGIN

I N-ConlfOlN-e«cisaaPB-EjcrsDdPB-Grafled

Eig. 8. Alterations of the position of the gingivalmargin (="soft tissue margin") for the various typesof "dentogingival" units during the course of thestudy.Verdnderungen der Lage des Gingivalsaumes (~"wetehgeweblichcr Saum") bei den verschiedencn Ty-pen "dentogingivaler" Einheiten wdhrend des Ablaufesdieser Studie.Modifications de la position du rebord gingival (—"rebord de tissu mou'') dans les difjerentes categories desites "gingivo'dentaires" pendant le cours de I'etude.

grafting the gingiva] margin was located at alevel similar to the presurgicai position. Duringthe remaining observation period no furthersignificant changes occurred.

The surgical excision of the gingival tissue onthe left side of the jaws (N-excision) resulted inan apical shift of the soft tissue margin ofaround 1 mtn (Fig. 8; Table 6), and this position

was maintained unaltered until the end of thestudy.

DiscusstonThe present study was performed in order toevaluate the role of an attached gingiva for themaintenance of periodontal health in sites withnormal and reduced heights of the attachmentapparatus. The method used to establish dif-ferent types of soft tissue margins was similar tothe experimental procedure previously de-scribed by Wennstrom et al. (1981). Thus, inone side of the jaws a period of experimentallyproduced periodontal breakdown which re-sulted in pronounced loss of attachment, wasfollowed by surgical excision of the inflamedgingiva including removal of the entire zone ofthe keratinized and attached gingiva. Subse-quent to healing ali buccal sites had regained azone of keratinized gingiva (KG), but most siteswere lacking attached gingiva (AG). Thesefindings corroborate and extend observationsreported by Karring et al. (1971) and Wenn-strom et al. (1981) regarding the regenerativepotential of the gingiva following differentexcisional procedures. However, while in thepresent study no gingival units without KGcould be established, Wennstrom etal. (1981) ina similar experiment observed that some of theregenerated gingival units following "gingivec-tomy" (<10%) were devoid of KG. Lindhe &Nyman (!980) reported from a retrospectivestudy in humans that 2 months after surgical

Table 6. Alterations of the position of the gingival margin between the baseline examination (Day 0) and thevarious examination intervals. Mean value (mm) and standard deviationAnderungen der Eage des Gingivalsaumes zwischen der Ausgangsuntersuehung (Versuchtstag 0) und d/^nverschiedenen Untersuchungsintervallen. Mlttelwert (mm) und StandardabweichungModifications de la position du rebord gingival entre l'examen initial (Jour 0) et les differents examens. Valeurmoyenne (mm) et ecart-type

Units Day 180 Day 195 Day 210 Day 300 Day 315 Day 330 Dav 420

N-ControlN-ExcisedPB-ExcisedPB-Graftcd

+ 0.I±0.2 +0.1±0.1+ O.3±0.2 +0.1 + 0.2-3.1±0.2 -3.7±0.7-3.7±0.2 -4.2±0.5

+ 0.1+0.2 0.0+0.2 0.0±0.2 +0.1+0.2 +0.1+0.2+ 0.1±0.2 +0.1+0.2 -1.0±0.2 -1.1 + 0.2 -1.0 + 0.2-4.0±0.5 -3.5±0.2 -3.5 + 0.3 -3.5 + 0.4 -3.4+0.2-4.4±0.5 -4.0±0.7 -4.0±0.7 -3.9±0.5 -3.8±0.7

WENNSTROM AND LINDHE

treatment (apically repositioned flap) 52% ofthe buccal sites in the premolar regions werelacking KG. However, at a reexamination 10-11 years later the frequency of units devoid ofKG had significantly decreased. The differencesobserved in the studies referred to, regardingthe frequency of soft tissue units without KG,raay be reiated to the technique used to deter-mine presence and position ofthe mucogingivalborder. Since the keratin layer of the oralepithelium of the gingiva which regeneratesfollowing excision is often thin (Wennstrom etal. 1981), it may be difficuit by clinical inspec-tion only to detect the presence of KG. In thepresent study, but not in the studies by Lindhe& Nyman (1980) and Wennstrom et al. (1981),the alveolar mucosa was stained with SchiUer'siodine solution, which facilitated the visualiza-tion of the mucogingival line. With improvedmaturation of the regenerated gingival tissuethe thickness ofthe keratin layer increases andconsequently it becomes easier in a clinicalassessment to distinguish between gingiva andalveolar mucosa. This may explain why Lindhe& Nyman (1980) noted a significant decrease ofbuccal units devoid of KG between the 2-monthpostoperative examination and the final exam-inations 10-11 years after active therapy.

Since most regenerated gingival units weredevoid of attached gingiva a gingival graft wasinserted in one of the experimental jaw quad-rants (PB-grafted) in order to regain a zone ofAG and to increase the width of KG. Thereexamination 4 months after grafting revealedthat on the average a 3 mm wide zone of AG hadbeen estabhshed (Fig. 7). This finding is inaccordance with e.g. Dorfman et al. (1980), deTrey & Bernimouiin (1980), Hangorsky & Bis-sada (1980), and shows that the use of gingivalgrafts is an effective and predictable means ofestablishing (or widening) the zone of keratin-ized and attached gingiva.

Measurements performed 2 weeks aftergrafting revealed that the width of the keratin-ized gingiva, compared with the width of thegraft, had decreased with around 20% (Fig. 6).

This finding is in agreement with previousreports on healing of gingival transplants indogs (Staffileno & Levy 1969) and humans (EgHet al. 1975). Since the degree of apical displace-ment of the "soft tissue margin" (gingivaimargin) following initial healing was similar tothe reduction of the width of the graft, it seemsreasonable to assume that the part of the graftwhich was placed to cover the exposed rootsurfaces was lost during initial healing. Thisassumption is validated by findings presentedby Staffileno & Levy (1969). They performed aclinical and histologic study of gingival trans-plants in dogs and claimed that the risk forpartial or total necrosis ofthe graft increased ifthe graft was placed over an avascular area suchas a root surface.

Concomitantly with the attachment lossduring the period of experimentally producedperiodontal breakdown the "soft tissue margin"was displaced in apical direction (Fig. 8). As aresult of this displacement no buccal pocketswere found with a probing depth exceeding 3mm (Table 3; Day 180). Tlie subsequent sur-gical treatment of the inflamed tissues did notinfluence the position of the clinical attachment(Fig. 5; Days 300-330). However, in the "nor-mal" side of the jaws, where the tissues at thetime of surgery were healthy, the use ofthe samesurgical procedure resulted in a small butstatistically significant loss of attachment (Fig.5; Days 300-330; 0.5 mm; P<0.0\). Thesefindings are interesting in view of results fromrecent studies showing that periodontal surgeryin buccal sites and sites with shallow pockets(less than 4 mm), always results in loss ofclinical attachment (Ramfjord et ai. 1975, Ros-ling et al. 1976, Knowles et al. 1979, Lindhe etal. 1982). Since the probing depths in thepresent study were similar in both sides of thejaws (<3 mm), the differences observed re-garding attachment loss between the healthyand the diseased sites must be related to thedegree of inflammation in the soft tissues. Thus,differences in the condition of the soft tissueprior to therapy must be taken into account

ATTACHED GINGIVA - PERIODONTAL HEALTH 219

when determining loss or gain of attachmentfollowing surgical intervention in sites withvarying probing depths (Listgarten et al. 1976,Armitage et al. 1977, Robinson & Vitek 1979).

During the 4-8 month period of dailymechanical tooth cleaning the areas lackingattached gingiva (N-excised and PB-excised)were maintained healthy and without recessionof the "soft tissue margin" (Fig. 8). On thecontrary, a smail («=0.5 mm) coronal regrowthof the "soft tissue margin" occurred. Suchgingiva] remodelling, aiso called "creeping at-tachment" (Goldman & Cohen 1964), has beenreported to take place following different typesof periodontal surgical procedures, such as softtissue grafting (Bell et al. 1978), gingivectomy(Afshar-Mohajer & Stahl 1977) and flap proce-dures (Lindhe & Nyman 1980), and is probablythe result of improved tissue maturation andimproved resistance of the tissue to clinicalprobing.

The present study in the beagle dog clearlydemonstrated that with daily performed me-chanical plaque control gingival health could beestablished and maintained without sign ofrecession of the "soft tissue margin" or attach-ment loss, independent of (1) presence or ab-sence of attached gingiva, (2) width of keratin-ized gingiva or (3) height of the periodontalsupport. Furthermore, soft tissue grafting wasfound to be an effective and predictable meansto increase the width of the keratinized andattached gingiva, but did not otherwise improvethe condition ofthe periodontium.

enthielt die Beurteilung der vorhandenen dentalenPlaquemenge, der gingivalen Gesundheit, des Attaeh-mentniveaus, der Lage des Gingivairandes und derBreite der keratinisierten sowie der angewachsenenGingiva. An der rechten Kieferseite (Versuchsseite)wurde nach einer 6-nionatlichen Periode parodon-taler Destruktion die Gingiva in ihrer Gesamibreiteexzidiert. Nach einer dann folgenden Heilungsperi-ode wurde, bei tagJicher Plaquekontrolle, an einemQuadranten der Versuchsseite Gingiva transpiantierl,wahrend der andere Quadrant der Versuchsseiteunbehandelt verblieb. An der linken Kieferseite (Kon-trollseite), wurde wahrend der gesamten Versuchs-dauer eine tagliclie sorgfaltige Plaquekontrolle vor-genommen. Zu etwa dem gleichen Zeitpunkt, an demdie Transplantationsbehandiung an der Versuchsseitevorgenommen wurde, wurde an einem der Kontroll-quadranten die Gesamtflache der keratinisierten undangewachsenen Gingiva exzidiert. An dem verblei-benden Kieferkontrollquadranten wurde kein Ein-gnff vorgenommen. Wahrend des Versuehsablaufeswurden die Kaueinheiten der Kontroll- und Versuchs-seiten in gewissen Zeuabstanden laufend untersuchi.Die den Versuch abschliessende Untersuchung wurdedann 4 Monate nach der Transplantation vorge-nommen.

Die Resultaie dieses Versuches zeigen, dass -unabhangig von (1) dem Vorhandensein oder nicht-Vorhandensein angewachsener Gingiva, (2) der Brei-te keratinisierter Gingiva oder (3) der Hohe desHalteapparates - die gingivale Gesundheit in Regi-onen in denen sorgfaltige Plaquekontrolle durch-gefiihrt worden war, ohne Anzcichen von Rezessiondes Zahnfleischsaumes oder von Attachmentverlust,erreicht und aufrechterhahen werden konnte. Nachchirurgischer Exzision der Gesamtgingiva regene-ricne an alien bukkaien Regionen ein keratinisierterBereich. in den meisten dieser Regionen entstandjedoch keine angewachsene Gingiva. Weiterhin er-hohten die transplantierten gingivalen Gewebe dieBreite der keratinisierten und angewachsenen Gin-giva - sie hatten jedoch keinen offenbaren Einflussauf die Lage des Zahnfleischsaumes oder des Attaeh-mentniveaus.

Zusammenfassung

Die Bedeutung der angewachsenen Gingiva fur dieAufrechterhaltung parodontaler GesundheiiDie vorliegende Studie wurde konz.ipiert, um dieRolle der angewachsenen Gingiva bei der Erhaltungparodontaler Gesundheit in Regionen mit normaierund reduzierter Hohe des Halteapparates zu anaiy-sieren. Weiterhin wurde die Folge gingivaler Exzisionund Transplantation auf einige, die Abmessung unddie Lokalisation parodontaler Gewebe beschreiben-de. Parameter beurteilt. 7 Beagies-Hunde wurden furdiese Studie angewendet. Die Ausgangsuntersuchung

Resume

Role de la gencive atiachee pour le maintien de ta santedu parodonteLa presente etude a ete entreprise dans le but d'ana-lyser le rolede \d.gencive attaehee pQ\ir \t maintien dela sante du parodonte au niveau de localisations ou lahauteur de Fappareil de soutien est soit normale soitreduite. Nous avons en outre evalue I'effet de I'exci-sion et de greffes gingivales sur certains parametresqui definissent les dimensions et la position des tissusparodontaux. L'etude a ete faite sur 7 chiens briquets.

220 WENNSTROM AND LINDHE

A rexamen initial, on enregistrait la plaque dentaire,l'etat gingiva], le niveau de Tattache, la position durebord gingivaJ et la largeur de la zone de gencivekeratinisee et de la zone de gencive attachee. Du cotedroit de.s machoires (cote experimental), apres uneperiode de 6 mois ou on provoquait ia destruction destissus parodontaux, on a pratique i'exdsion chirur-gicale de la totalitc de la zone gingivale. Apres uneperiode de cicatrisation de 4 mois, oil en eliminait laplaque tous ies jours, on a ensuite pratique une greffegingivale dans un des quadrants du cote experimentalpour reconstituer une zone de gencive attachee, tandisque I'autre quadrant ne recevait pas de greffe. Du cotegauche des machoires (cote temoin), les dents ont etesoumises lous les jours a une elimination meticuieusede la plaque pendant tout ie cours de I'etude. Dans undes quadrants temoins, la totalite de la zone degencive keratinisee et atiachee a ete excisee a unmoment correspondant a i'execution de la greffe ducote experimental, tandis que I'autre quadrant temoinne subissait pas d'intervention chirurgicale. Des exa-mens cliniques de toutes les localisations dentairestemoins et experimentaies ont etc repetes a certainsintervalles pendant le cours de I'etude. L'examen finala ete pratique 4 mois apres la greffe.

Les resultats de celte experience ont montre que,dans des localisations soumises a une eliminationsoigneiise de la plaque, la sante gingivaie pouvait etreobtenue et maintenue sans signe de relrait du rebordgingival ni pene d'attache, independamment de (1) lapresence ou I'absence de gencive attachee, (2) lalargeur de !a zone de gencive keratinisee ou (3) lahauteur de l'appareil de soutien. Apres l'excisionchirurgicale de la totaiite de la gencive, toutes ieslocalisations vestibulaires ont regagne une zone degencive keratinisee, mais la gencive attachee man-quait dans la plupart de ces localisations. De pltis, lesgreffes de tissti gingivai augmentaient significative-ment Ia hauteur de la gencive keratinisee et de lagencive attachee, mais n'avait pas d'action nettesur laposition du rebord gingival ou le niveau de I'attache.

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Address;

Jan WennstromDepartment of PeriodontologySchool of DentistryUtiiversity of GothenburgBox 33070S-40Q 33 GothenburgSweden