Scarring of gingiva and alveolar mucosa following apical surgery: visual assessment after one year

O R I G I N A L A R T I C L E

Scarring of gingiva and alveolar mucosa following apical surgery:visual assessment after one yearT. von Arx1, G.E. Salvi2, S. Janner1 & S.S. Jensen3

1Department of Oral Surgery and Stomatology2Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland3Department of Oral & Maxillofacial Surgery, Copenhagen University Hospital, Glostrup, Denmark

Abstract

Aim: (1) To visually assess scarring of the gingiva and alveolar mucosa 1year following apical surgery in the aesthetic zone; and (2) to evaluatewhether scarring correlated with patient-related or surgical parameters.Material and methods: The material included 72 cases in the anteriormaxilla. Three observers, who were blinded to the incision and flap design,independently assessed scar formation of the soft tissues. Each observerdetermined a pretreatment and a 1-year follow-up score of scarring, andmean changes were calculated.Results: With regard to the gingiva, the type of incision had a significant(P = 0.0013) influence on scar formation; that is, submarginal incisions andpapilla-saving incisions produced more scarring than intrasulcular andpapilla-base incisions. Scarring of the alveolar mucosa was significantly(P = 0.0108) influenced by the type of surgery (first-time vs. re-surgery)and by gender (P = 0.0496); that is, less scar formation of the alveolarmucosa was observed in re-surgery than in first-time cases as well as in malecompared with female patients.Conclusions: Scar formation of the gingiva appeared to be influenced bythe incision technique and use of antibiotics, whereas scar formation ofthe alveolar mucosa was correlated with gender and type of surgery.Possible scar formation should be discussed with the patient beforesurgery.

Key words:alveolar mucosa, apical surgery, gingiva,

scarring

Correspondence to:Professor Dr T von Arx

Department of Oral Surgery and Stomatology

School of Dental Medicine, University of Bern

Freiburgstrasse 7

CH-3010 Bern

Switzerland

Tel.: +41 31 632 25 66

Fax: +41 31 632 98 84

email: [email protected]

Accepted: 26 October 2008

doi:10.1111/j.1752-248X.2008.00039.x

Clinical relevance

Scientific rationale for study: Apical surgery mayresult in healing of the apical lesion, but may createan unsightly scar of the gingiva or of the alveolarmucosa.Principal findings: In two thirds of the assessed cases,scar formation was observed, with more substantialscarring of the alveolar mucosa than of the gingiva.Scarring of the gingiva was influenced by the type ofincision and the use of antibiotics, whereas scarring ofthe alveolar mucosa was correlated with gender andtype of surgery.Practical implications: Scar formation should beaddressed during examination of the patient.

Introduction

Apical surgery is often a last resort to save a toothwith a non-healing or recurrent periapical lesion.Although conventional endodontic re-treatmentshould be evaluated first, the recent advances inapical surgery, that is, the introduction of microsurgi-cal principles, have made apical surgery a valuabletreatment option1. Apical surgery should be consid-ered in cases where conventional re-treatment isnot feasible, is associated with risks or is declined bythe patient. A common example is a tooth withacceptable endodontics and a new post and crownrestoration, but with a persistent or enlargingperiapical lesion2.

Oral Surgery ISSN 1752-2471

178 Oral Surgery 1 (2008) 178–189. © 2008 John Wiley & Sons A/S

mailto:[email protected]

In evaluating the treatment outcome after apicalsurgery, the majority of published studies focus onclinical and radiographic signs of periapical healing.In contrast, information concerning soft tissue healingfollowing apical surgery is scarce, in particular withregard to scar formation. In apical surgery, intentionalsurgical injury is performed to correct pathologicalinjury. The surgery includes incisional wounding,dissectional wounding and osseous excisionalwounding3–5. In clinical studies, osseous healing isjudged by the resolution or reduction of the formerradiolucency and absence of clinical signs and symp-toms6. However, no parameters have been defined todescribe healing of the incisional (and dissectional)wounds. With regard to gingival and mucosal healing,the patient may complain about scar formation that wasnotpresentbeforesurgery.

Normal wound healing includes a complex, well-orchestrated series of events involving resident andmigratory cells and the extracellular matrix7. Scar for-mation is a frequent finding in dermal wound healing,but can also be observed in oral mucosal wound healing.A scar is defined as a macroscopic disturbance of thenormal structure of tissue architecture, and is histologi-cally characterised by the lack of specific organisation ofcellular and matrix elements when compared withuninjured skin7. Hypertrophic scars and keloids areexamples of fibroproliferative disorders with excessaccumulationofcollagenwithinthewound8.

Kramper and co-workers9 evaluated the clinical andhistological features of wound healing of three types ofsurgical flap designs used in apical surgery. The studywas performed in beagle dogs and the observationlasted up to 60 days. Flaps included (1) a semilunarincision of the alveolar mucosa; (2) a submarginalincision within the attached gingiva; and (3) anintrasulcular incision of the attachment apparatus andpapillae. Inflammatory changes persisted longer in thesemilunar and intrasulcular incisions and retardedwound healing. Loss of alveolar bone occurred with theintrasulcular incision. Visible scarring was observed inthe submarginal and semilunar incisions. Harrisonand Jurosky3 histologically assessed the wound healingresponses to incisional wounding in apical surgery inrhesus monkeys. An intrasulcular triangular flap and asubmarginal rectangular flap showed essentially nodifference in healing progress at 14 and 28 days post-surgery. No data were reported with regard to scarring.

Clinical data on scar formation of the gingiva andalveolar mucosa following apical surgery are also scarce.Chindia and Valderhaug10 compared a trapezoidal flap(intrasulcular incision) with a semilunar flap (incision2 mm from the attached gingiva). Patients were ran-

domly assigned to either flap procedure. The trapezoidalflap produced less noticeable scarring than the semilu-nar flap. Velvart11 described use of the papilla-base inci-sion for recession-free healing of the interdental papillaafter apical surgery in 20 patients. The visual observa-tion, 1 month post-operatively, demonstrated a visibleincision defect in four papillae, a partially detectableincision defect in seven papillae and perfect healing innine papillae. A follow-up study by the same author12

with a 1-year observation period did not address scar-ringwithrespect to thepapilla-base incision.

From an aesthetic point of view, the risk of scarringmust be considered in patients with a high smile line.Such patients display their maxillary anterior teeth intheir entirety as well as a significant portion of thesupporting soft tissues13. In implant dentistry, the posi-tion of the upper lip on smiling has become an impor-tant diagnostic factor for aesthetic risk assessment14. Aspatients’ treatment expectations tend to increase, itappears appropriate to also include these aspects intreatment planning and when informing patients priorto apical surgery.

The aims of the present clinical study were (1) tovisually assess scarring of the gingiva and the alveolarmucosa 1 year following apical surgery in the aestheticzone; and (2) to evaluate whether scarring correlatedwith patient-related or surgical parameters.

Materials and methods

The initial material comprised 107 consecutive casesincluding 123 teeth with apical surgery or re-surgeryperformed in the aesthetic zone (maxillary incisors,canines and first premolars). A total of 35 patients with51 teeth were excluded for various reasons (Table 1).The final number of patients and teeth was 72, includ-ing 32 central incisors, 21 lateral incisors, four canines

Table 1 Excluded and drop-out cases

n patients n teeth

Initial material 107 123

Excluded cases Multiple treated teeth within

same flap

15 31

Facial bone plate missing 6 6

Data set not complete 9 9

Drop-out cases Tooth extracted, not related to

apical surgery

2 2

Patient could not be located for

1-year follow up

1 1

Patient not willing to come for

1-year follow-up

2 2

Final material 72 72

von Arx et al. Apical surgery and scarring of soft tissues

179Oral Surgery 1 (2008) 178–189. © 2008 John Wiley & Sons A/S

and 15 first premolars. The mean age of these 72patients was 49.2 years (range 11–80 years). In 63 cases(87.5%), apical surgery was a first-time surgery, and in9 cases (12.5%) it was a re-surgery.

Surgical technique

Patients were fully informed about the surgical proce-dure, post-operative care, follow-up examinations andalternative treatment options. Each patient signed aconsent form based on the principles defined in theDeclaration of Helsinki. All surgeries were performedby one surgeon (T. v. A.).

Apical surgery was carried out under local anaes-thesia. The choice of incision and flap design wasbased on criteria described in a previous article15. Inre-surgery cases, the incision line did not necessarilyconcur with the previous incision line. Followingelevation of a full-thickness mucoperiosteal flap, bonewas removed from the apical area to gain access to thelesion and the root end. Affected roots were thenresected approximately 3 mm from the apex. Follow-ing debridement of the pathological tissue, haemostasisof the bony crypt was achieved. The surgical area wasstained with methylene blue and the root end wasinspected for the presence of fractures, cracks or isth-muses using a rigid endoscope. Root-end cavities wereprepared with sonic-driven microtips and were retro-filled with either SuperEBA (Staident International,Staines, UK) or MTA (Mineral Trioxide Aggregate,Dentsply Tulsa Dental, Tulsa, OK, USA). Alternatively,a shallow concavity was prepared in the cut root faceusing round diamond burs, with subsequent placementof dentin-bonded resin composite (Retroplast, Retro-plast Trading, Rorvig, Denmark). After the wound areawas cleaned, wound closure was accomplished withsutures and gauze was applied for slight compression.All patients were given non-steroidal analgesics andwere instructed to rinse with 0.1% chlorhexidine-digluconate twice a day for 10 days. Antibiotics wereprescribed in cases with a history of acute infection, inpatients presenting with clinical signs and symptoms,and in patients who required antibiotics for medicalreasons. Sutures were removed normally within 4–7days after surgery. Patients were recalled 1 year post-surgically for clinical and radiographic re-examination.

Biographical and surgical parameters

The biographical parameters included age (<45 years,�45 years), gender (male, female), gingival biotype(thin-scalloped, thick-flat)16 and smoking (no, yes).The surgical parameters comprised the type of surgery

(first-time surgery, re-surgery), use of antibiotics(no, yes), type of incision (intrasulcular, sub-marginal, papilla-base, papilla-saving)15, type of flap(trapezoidal = mesial and distal release incisions;triangular-mesial = a single mesial release incision;triangular-distal = a single distal release incision),duration of surgery (<60 min, �60 min), timing ofsuture removal (4–5 days, �6 days), post-operativehealing complications (no, yes) and radiographichealing at the 1-year follow-up (healed, not healed).The latter were classified according to the radiographichealing criteria established by Rud et al.17 and Molvenet al18. Complete and incomplete (‘scar tissue’) radio-graphic healing of the former radiolucency were cat-egorised as ‘healed’, whereas cases with uncertain orunsatisfactory radiographic healing were categorisedas ‘not healed’.

Visual assessment

Scarring of the gingiva and of the alveolar mucosa (ofthe treated and adjacent teeth) was visually assessed bythree independent observers: a periodontist (G. E. S.),an oral surgery graduate student (S. J.), and an oral andmaxillofacial surgeon (S. S. J.). The three observerswere trained and calibrated by means of samplephotographs. The observers were not involved inthe surgeries and were blinded to the type of incisionand flap used; the only information disclosed to themwas the tooth treated. Each observer was providedwith an identical set of photographs taken at theinitial examination (pretreatment photos) and at there-examination (1-year follow-up photos). All photo-graphs were taken by the same person with a digitalcamera (Nikon D100, Nikkor Medical Objective andMacro Speedlight, Nikon Corporation, Tokyo, Japan).The camera settings were identical for pretreatmentand follow-up photographs. Each observer determineda pretreatment score and a follow-up score (Table 2).Changes in scar formation were subsequently com-puted (‘follow-up score’ minus ‘pretreatment score’).In cases of disagreement between the observers, thefollowing rules were applied: when at least twoobservers denoted the same score, this score was

Table 2 Definition of score categories of scarring

Score Definition

0 No scar

1 Fine scar line or tissue indentation (width of scar <1 mm)

2 Broad scar line or tissue indentation (width of scar �1 mm)

Apical surgery and scarring of soft tissues von Arx et al.


used irrespective of the third score; when each of theobservers denoted a different score, the ‘middle’ score(=score 1) was used.

Statistics

In order to assess the inter-rater agreement, weightedkappa values were computed according to the proce-dure of Fleiss and Cohen19. In addition, the concor-dance between each observer and the consensus wascomputed. Fisher’s exact test was performed for allbiographical and surgical parameters to determine ifthere were non-random associations between theseparameters and scar formation. Because of the explor-atory type of the study, no P-value correction for mul-tiple comparisons was performed. Statistical tests werecarried out for gingiva and alveolar mucosa separately.All analyses were performed with SAS version 9.1 (SASInstitute, Cary, NC, USA).

Results

Kappa values of inter-examiner agreement and con-cordance between each examiner and the consensusare shown in Table 3. Pair-wise comparisons betweenthe three examiners were rated as fair to moderate, anda moderate-to-almost-perfect concordance was foundbetween examiner and consensus ratings.

The pretreatment and the 1-year follow-up scores ofscarring are summarised in Table 4. Before surgery,the majority of cases presented with neither gingival(87.5%) nor mucosal (84.7%) scarring. At the 1-yearfollow up, the number of cases with no scar haddropped considerably (P < 0.001 for both gingiva andalveolar mucosa) and was similar for the gingiva(23.6%) and the alveolar mucosa (20.8%). However,the number of cases with substantial scarring was morepronounced in the alveolar mucosa (23 cases) com-pared with the gingiva (12 cases) (P = 0.7334).

Table 3 Range of computed kappa values (inter-examiner agreement and concordance between observer and consensus) for scoring of scar formation of

gingiva and alveolar mucosa

Kappa values for

rating of gingiva

Kappa values for rating

of alveolar mucosa

Pretreatment Inter-examiner agreement 0.55–0.62 0.69–0.80

Concordance between observer and consensus 0.75–0.90 0.78–0.91

1-year follow-up Inter-examiner agreement 0.22–0.54 0.32–0.71

Concordance between observer and consensus 0.46–0.84 0.52–0.85

Table 4 Distribution of scores of scarring

(n = 72)

Score of scarring

Gingiva Alveolar mucosa

Pretreatment 1-year follow-up Pretreatment 1-year follow-up

0 (no scar) 63 87.5% 17 23.6% 61 84.7% 15 20.8%

1 (mild scar) 4 5.6% 43 59.7% 4 5.6% 34 47.2%

2 (substantial scar) 5 6.9% 12 16.7% 7 9.7% 23 31.9%

Table 5 Distribution of changes in scarring for

gingiva and alveolar mucosa (n = 72)Pretreatment score → 1-year

follow-up score Gingiva Alveolar mucosa

No change (+0) 0 → 0 17 23.6% 15 20.8%

1 → 1 2 2.8% 2 2.8%

2 → 2 5 6.9% 7 9.7%

Subtotal 24 33.3% 24 33.3%

Mild change (+1) 0 → 1 41 56.9% 32 44.4%

1 → 2 2 2.8% 2 2.8%

Subtotal 43 59.7% 34 47.2%

Substantial change (+2) 0 → 2 5 6.9% 14 19.4%

Subtotal 5 6.9% 14 19.4%



With regard to the calculated changes of scarringover time, an equal number of cases (33.3%) presentedwithout any change for the gingiva and the alveolarmucosa (Table 5). Mild changes tended to be morefrequent in the gingiva (59.7%) than in the alveolarmucosa (47.2%) (P = 0.1812). Significantly (P =0.0466) more substantial changes of scarring wereobserved in the alveolar mucosa (19.4%) comparedwith the gingiva (6.9%).

The correlation of changes of scarring with the bio-graphical and surgical parameters is reported sepa-rately for the gingiva (Table 6) and the alveolar mucosa(Table 7). Computed P-values for non-random asso-ciations between parameters and scar formation areshown in Table 8.

Scarring of gingiva

With respect to biographical parameters, no significantdifferences were noted across the subgroups of theparameters ‘age’, ‘gender’, ‘smoking habit’ and ‘bio-

type’. However, smokers tended to produce less gingi-val scarring than non-smokers.

With regard to surgical parameters, the type of inci-sion was found to have a significant (P = 0.0013)influence on gingival scarring. Intrasulcular andpapilla-base incisions never yielded substantial changesof gingival scarring, in contrast to submarginal incisions(in 9.7%) and papilla-saving incisions (in 25%). Also,the use of antibiotics had a significant (P = 0.0138)effect on scarring of the gingiva. Cases treated withantibiotics never showed substantial scarring of thegingiva compared with 17.9% of cases without anti-biotic coverage. Other surgical parameters were notsignificant factors for gingival scar formation.

Scarring of alveolar mucosa

With respect to biographical parameters, gender(P = 0.0496) was found to significantly influence scar-ring of the alveolar mucosa, that is, a substantialchange of scarring was observed in 27.5% of female

Table 6 Correlation of changes in scarring of the gingiva with biographical and surgical parameters (n = 72)

Parameter Subgroups n

0 (no change in

scarring)

1 (mild change

in scarring)

2 (substantial change

in scarring)

Age <45 years 25 8 32.0% 16 64.0% 1 4.0%

�45 years 47 16 34.0% 27 57.5% 4 8.5%

Gender Male 32 12 37.5% 19 59.4% 1 3.1%

Female 40 12 30.0% 24 60.0% 4 10.0%

Smoking No 63 18 28.6% 40 63.5% 5 7.9%

Yes 9 6 66.7% 3 33.3% 0 0%

Biotype Thin 38 12 31.6% 24 63.2% 2 5.3%

Thick 34 12 35.3% 19 55.9% 3 8.8%

Surgery First-time 63 19 30.2% 39 61.9% 5 7.9%

Re-surgery 9 5 55.6% 4 44.4% 0 0%

Antibiotics No 28 9 32.1% 14 50.0% 5 17.9%

Yes 44 15 34.1% 29 65.9% 0 0%

Incision ISI1 12 7 58.3% 5 41.7% 0 0%

SMI2 31 4 12.9% 24 77.4% 3 9.7%

PBI3 21 12 57.1% 9 42.9% 0 0%

PSI4 8 1 12.5% 5 62.5% 2 25.0%

Flap Trapezoidal 16 3 18.8% 11 68.8% 2 12.5%

Triangular-mesial 39 14 35.9% 24 61.5% 1 2.6%

Triangular-distal 17 7 41.2% 8 47.1% 2 11.8%

Duration of surgery <60 min 32 9 28.1% 19 59.4% 4 12.5%

�60 min 40 15 37.5% 24 60.0% 1 2.5%

Suture removal After 4–5 days 26 8 30.8% 17 65.4% 1 3.8%

After �6 days 46 16 34.8% 26 56.5% 4 8.7%

Healing complications No 67 23 34.3% 39 58.2% 5 7.5%

Yes 5 1 20.0% 4 80.0% 0 0%

1-year radiographic healing Healed 66 23 34.8% 38 57.6% 5 7.6%

Not healed 6 1 16.7% 5 83.3% 0 0%

ISI1, intrasulcular incision; PBI3, papilla-base incision; PSI4, papilla-saving incision; SMI2, submarginal incision.



patients compared with 9.4% of male patients. Nochange of scarring was noted in 46.9% of the malepatients compared with 22.5% of the female patients.The smoking habit had a tendency (P = 0.0779) toinfluence scarring of the alveolar mucosa, with 33.3%

of smokers showing a change of scarring (mild or sub-stantial) compared with 71.4% of non-smokers. ‘Age’and ‘biotype’ were not relevant parameters in relationto scar formation of the alveolar mucosa.

With regard to surgical parameters, the type ofsurgery proved to be significant (P = 0.0108), with nochange of scarring in 77.8% of re-surgery cases but27.0% in first-time surgery cases. The other surgicalparameters were not significantly associated with scarformation of the alveolar mucosa. However, cases withsuture removal after �6 days (mean 8.46 days, range6–20 days) tended to demonstrate more substantialscarring of the alveolar mucosa (26.1%) comparedwith cases with suture removal after 4–5 days (mean4.19 days, 7.7%, P = 0.1019). Also, cases with post-operative healing complications tended (P = 0.0940) toshow more substantial scarring (60%) compared withcases with uneventful healing (16.4%).

Discussion

The present study assessed scarring of the gingiva andalveolar mucosa following apical surgery in the

Table 7 Correlation of changes in scarring of the alveolar mucosa with biographical and surgical parameters (n = 72)

Parameter Subgroups n

0 (no change

in scarring)

1 (mild change

in scarring)

2 (substantial change

in scarring)

Age <45 years 25 7 28.0% 12 48.0% 6 24.0%

�45 years 47 17 36.2% 22 46.8% 8 17.0%

Gender Male 32 15 46.9% 14 43.7% 3 9.4%

Female 40 9 22.5% 20 50.0% 11 27.5%

Smoking No 63 18 28.6% 32 50.8% 13 20.6%

Yes 9 6 66.7% 2 22.2% 1 11.1%

Biotype Thin 38 14 36.8% 17 44.7% 7 18.4%

Thick 34 10 29.4% 17 50.0% 7 20.6%

Surgery First-time 63 17 27.0% 32 50.8% 14 22.2%

Re-surgery 9 7 77.8% 2 22.2% 0 0%

Antibiotics No 28 8 28.6% 15 53.6% 5 17.9%

Yes 44 16 36.4% 19 43.2% 9 20.5%

Incision ISI1 12 5 41.7% 3 25.0% 4 33.3%

SMI2 31 9 29.0% 17 54.8% 5 16.1%

PBI3 21 9 42.9% 10 47.6% 2 9.5%

PSI4 8 1 12.5% 4 50.0% 3 37.5%

Flap Trapezoidal 16 4 25.0% 7 43.8% 5 31.3%

Triangular-mesial 39 12 30.8% 21 53.8% 6 15.4%

Triangular-distal 17 8 47.1% 6 35.3% 3 17.6%

Duration of surgery <60 min 32 8 25.0% 18 56.3% 6 18.8%

�60 min 40 16 40.0% 16 40.0% 8 20.0%

Suture removal After 4–5 days 26 8 30.8% 16 61.5% 2 7.7%

After �6 days 46 16 34.8% 18 39.1% 12 26.1%

Healing complications No 67 23 34.3% 33 49.3% 11 16.4%

Yes 5 1 20.0% 1 20.0% 3 60.0%

1-year radiographic healing Healed 66 23 34.8% 32 48.5% 11 16.7%

Not healed 6 1 16.7% 2 33.3% 3 50.0%

ISI1, intrasulcular incision; PBI3, papilla-base incision; PSI4, papilla-saving incision; SMI2, submarginal incision.

Table 8 Summary of P-values for biographical and surgical parameters

Parameter P-value gingiva

P-value alveolar

mucosa

Age 0.7950 0.7228

Gender 0.5237 0.0496*

Smoking 0.1007 0.0779

Bio-type 0.8078 0.8197

Type of surgery 0.3400 0.0108*

Use of antibiotics 0.0138* 0.7356

Type of incision 0.0013* 0.2665

Type of flap 0.2502 0.4561

Duration of surgery 0.2452 0.3678

Timepoint of suture removal 0.7947 0.1019

Post-operative healing

complications

0.7566 0.0940

1-year radiographic healing 0.6221 0.1639

*Significant at the usual 0.05 level.



aesthetic zone. Scarring has been defined as a macro-scopic disturbance of the normal structure and functionof the mucosa architecture, resulting from the endproduct of a healed wound. The healing processincludes haemostasis, inflammation, proliferation andremodelling. Scar formation occurs when dysregula-tion of the normal physiological processes occurs,resulting in altered growth factor, cytokine, proteolyticand cellular profiles7. Scarring may manifest itself as anelevated or depressed site, with an alteration of mucosatexture, colour, reflectance and biomechanical proper-ties20. These macroscopic changes undoubtedly resultfrom histological alterations in the involved epithelialand submucosal elements. With regard to appraisal ofscarring, it has been suggested to assess scarring noearlier than 1 year after wounding20.

In this study, three observers rated the pretreatmentand 1-year follow-up photographs using a descriptivescore system of pre-existing and post-surgical scarringwith three categories. Comparison of the inter-examiner agreement showed better agreement forassessment of mucosal compared with gingival scarring,as well as better inter-examiner agreement for pre-treatment compared with follow-up assessment ofscarring in both gingival and mucosal sites. Presumably,assessment of the gingiva was more difficult thanassessment of the alveolar mucosa, and the follow-upevaluation was more problematic compared with thepretreatment evaluation. Substantial to almost perfectconcordance was noted between observer and consen-sus ratings for all evaluations, and this concordance wasalwaysgreater thanthe inter-examineragreement.

The majority of cases presented without scarring atthe beginning of the study; exceptions were cases withprevious surgery or trauma in the area. For this reason,the change in scarring (from pretreatment status tofollow-up status) and not the scar present at the 1-yearfollow-up was considered to be the factor of interest.Although the calculated total percentage (66.7%) ofchanges of scarring was equal for gingiva and alveolarmucosa, a significantly (P < 0.05) higher percentage ofsubstantial change of scarring was observed in thealveolar mucosa (19.4%) compared with the gingiva(6.9%). Based on these data, the alveolar mucosaappears to be more prone to scarring than the gingivafollowing apical surgery. Possible contributing factorsmight include increased mobility, elevated risk ofwound dehiscence and greater dissection area of thealveolar mucosa compared with the gingiva. Pretreat-ment and follow-up photos of four cases are shown tohighlight the differences in scarring between gingivaand alveolar mucosa (Figs 1–4). The concept of a sepa-rate assessment of scarring of gingiva and alveolar

mucosa is based on the patient’s different perception ofthese two tissues, in particular, with regard to the levelof the smile line. Scarring of the alveolar mucosa mightonly become visible in the case of a very high positionof the upper lip when smiling, whereas scarring of thegingiva might be perceived also in patients with lowersmile lines.

In the present study, changes of scarring were alsocorrelated with various biographical and surgicalparameters, which will be discussed separately.

Age

No correlation was found between the parameter ‘age’(cut-off point, 45 years) and change of scarring. Woundhealing in the dermis of aged individuals has beenreported to occur with minimal scarring and delayedinflammatory responses21. The phenomenon of better

(A)

(B)

Figure 1 A 60-year-old male patient with apical surgery of maxillary left

first premolar. (A) The pretreatment photo shows no scarring of the gingiva

(score 0) and alveolar mucosa (score 0) in this area but an erythematous

mucosa presenting in this region. (B) The follow-up photo, 1 year after

surgery, shows no scarring of the gingiva (score 0) and alveolar mucosa

(score 0) in the treated area. A papilla-base incision had been used with a

release incision at the mesial line angle of the canine.



scar quality with aging may be related to the increasedformation of type III collagen over time22. No informa-tion on oral mucosal healing in relation to age wasfound in the literature.

Gender

Female patients had a tendency towards more sub-stantial changes of scarring of the gingiva (10%) thanmale patients (3.1%), but this difference was not sta-tistically significant. In contrast, in the alveolar mucosa,a significant difference was found (females 27.5%compared with males 9.4%; P < 0.05). We can onlyspeculate that healing mechanisms in females mightdiffer (hormonal modulation?) from those in males,resulting in increased scar formation in the alveolarmucosa. It is known from studies on scarring after burnwounds that female patients tend to produce morepathological scar tissue than male patients23.

Smoking

An interesting finding was that smokers tended to havefewer changes in scarring in the gingiva (P = 0.1007) aswell as in the alveolar mucosa (P = 0.0779) comparedwith non-smokers. However, these results must bejudged with caution, since only nine patients (12.5%)were smokers. The percentage of mild and substantialchange of scarring was 71.4% in non-smokers com-pared with 33.3% in smokers for both gingiva andalveolar mucosa. As scar formation is associated withstimulation of fibroblastic activity, it is plausible thatthe cytotoxic effect of nicotine upon various fibroblastpopulations might indirectly prevent or reduce gingivaland mucosal scarring24,25.

(A)

(B)

Figure 2 A 59-year-old female patient with first-time apical surgery of

maxillary left lateral incisor. (A) The pretreatment photo shows no scarring

of the gingiva (score 0) and alveolar mucosa (score 0). (B) The follow-up

photo 1 year after surgery shows mild scarring of the gingiva (score 1) and

alveolar mucosa (score 1) in the treated area. A submarginal incision had

been used with a release incision at the mesial aspect of the flap.

(A)

(B)

Figure 3 A 63-year-old female patient with apical re-surgery of the max-

illary left lateral incisor. (A) The pretreatment photo shows no scarring of

the gingiva (score 0) but substantial scarring of the alveolar mucosa

(score 2). (B) The follow-up photo 1 year after re-surgery shows mild

scarring of the gingiva (score 1) and persistent substantial scarring of the

alveolar mucosa (score 2) in the treated area. A submarginal incision had

been used with a release incision at the mesial aspect of the flap. In the

meantime, two implants had also been placed in the maxillary left pos-

terior segment.



Gingival biotype

Gingival (or periodontal) biotypes have been describedas either thin-scalloped or thick-flat. They react differ-ently to surgical or prosthetic interventions16,26,27. Thethin, scalloped periodontium reacts with soft tissuerecession, apical migration of attachment and loss ofunderlying alveolar bone volume. The thick, flatperiodontium resists recession and reacts with pocketformation, and may be predisposed to formation ofunsightly notches and scars due to the fibrotic tissuenature. However, in the present study, no differenceswere found between the two gingival biotypes withregard to scar formation following apical surgery.

Type of surgery

First-time surgery cases (73%) had significantly(P < 0.02) more changes in scarring of the alveolar

mucosa than re-surgery cases (22.2%). With regard tothe gingiva, a similar but statistically not significantcorrelation was observed. These data seem plausible asthe previous surgery in re-surgery cases had alreadyresulted in some sort of scarring.

Use of antibiotics

The benefit of antibiotic coverage in apical surgery hasnot been clarified yet. Only two clinical studies6,28 haveaddressed the effect of antibiotics on the outcome afterapical surgery with no significant difference whetherantibiotics were given or not. In a recent randomisedcontrolled clinical trial29, no positive effect of antibiotictherapy with regard to initial 4-week healing wasobserved. Although these studies assessed the overallhealing, the present study focused on scar formation,and interestingly, cases with antibiotics demonstratedsignificantly less substantial scarring of the gingivacompared with cases without antibiotics. The benefit ofantibiotics with regard to reduction of scarring might beexplained by lower numbers of fibroblast-stimulatingcytokines and inflammatory cells20,30. However, thepresent study was not designed to evaluate the effect ofantibiotics on scarring, and only selected cases receivedantibiotics. Therefore, confounding factors were notaccounted for, and the beneficial effect of antibioticsneeds further investigation.

Type of incision

The choice of incision technique is always a challengingand debatable aspect of apical surgery. A variety offactors must be considered when choosing a specificincision technique, particularly in the anterior maxilla.These factors include status of the marginal periodon-tium, width of free and attached gingiva, location andextent of periapical lesions, presence of a restorationmargin and the patient’s aesthetic demands15. In thepresent study, the parameter ‘type of incision’ signifi-cantly (P < 0.002) influenced the change in scarring ofthe gingiva (but not of the alveolar mucosa). The sub-marginal and papilla-saving incisions resulted in morechanges in scarring of the gingiva compared with thepapilla-base incision and the intrasulcular incision, andthese changes were also more substantial. Therefore,patients who expose the gingiva should be informedabout the risk of gingival scarring before using a sub-marginal or papilla-saving incision. In a randomisedclinical trial, Chindia and Valderhaug10 described lessscar formation with an intrasulcular (trapezoidal)incision compared with a submarginal (semilunar)incision; however, no specific clinical assessment of

(A)

(B)

Figure 4 A 57-year-old female patient with first-time apical surgery of the

maxillary left lateral incisor. (A) The pretreatment photo shows no scarring

of the gingiva (score 0) and alveolar mucosa (score 0). (B) The follow-up

photo 1 year after surgery shows substantial scarring of the gingiva (score

2) and mild scarring of the alveolar mucosa (score 1) in the treated area. A

trapezoidal, papilla-saving incision had been used for surgical access.



scar formation was performed. Similar findings werereported in an experimental dog study that evaluatedthree commonly used incision techniques in apicalsurgery9. Very little, if any, scarring was evident withthe intrasulcular incision. However, scarring was quiteevident with the submarginal and semilunar incisions.

Type of flap

This parameter included three types of flap design: atrapezoidal access flap with two release incisions, a tri-angular access flap with a single, mesial release incisionand a triangular access flap with a single, distal releaseincision. The trapezoidal design appeared to producemore substantial changes in scarring of the alveolarmucosa, but this parameter did not prove significant.From a clinical point of view, it is plausible that a trap-ezoidal flap might result in more scarring (in particularof the alveolar mucosa) due to the fact that a trapezoi-dal flap has three wound edges, compared with onlytwo edges for a triangular flap.

Duration of surgery

It has been advocated that in a prolonged surgical pro-cedure, especially when a high degree of haemostasishas been achieved, there is a risk that the tissues willdry out with subsequent shrinkage of the flap31.However, in the present study, the duration of surgery(cut-off point 60 min) was not significantly correlatedwith scarring of gingiva and alveolar mucosa.

Timing of suture removal

Atrend(P = 0.1019) towards less scarringof thealveolarmucosa was observed when sutures were removedwithin 4–5 days without increasing the risk of wounddehiscence. In contrast, sutures left in place for a longerperiod might elicit an inflammatory reaction withfibroblast stimulationandsubsequentscar formation.

Post-operative healing complications

In five patients (7%), wound infection was treatedwith incision and drainage for several days. This treat-ment led to considerably more substantial scarring ofthe alveolar mucosa (in 60%) compared with caseswith uneventful healing (16.4%). However, because ofthe small number of cases with a post-operative infec-tion, this difference was not statistically significant(P = 0.0940).

Radiographic healing at 1-year follow-up

Only six cases (8%) were classified as ‘not healed’ withregard to the 1-year radiographic assessment. Fiftypercent of these cases showed substantial scarringof the alveolar mucosa compared with only 16.7% ofradiographically ‘healed’ cases. However, because ofthe small number of ‘not healed’ cases, this differencewas not statistically significant (P = 0.1639).

Although scarring seldom results in a painful condi-tion or impaired function in the anterior maxilla,patients may complain about compromised aesthetics.Patients may also be worried about gingival recessionaround crown margins. However, a recent clinicalstudy about changes of periodontal parameters follow-ing apical surgery found no significant influence forthe presence and type of restorations32. Scarring ofthe supporting soft tissues is of particular concern inpatients with a so-called high smile line. The latter isdefined as exposure of the total cervico-incisal length ofthe maxillary anterior teeth and of a contiguous bandof gingiva33. Jensen and co-workers13 evaluated theposition of the smile line on the basis of standardisedphotographs in a total of 733 subjects. The researchersfound that younger females (�35 years) presentedwith higher smile lines than older males (>35 years)(P < 0.01). In Germanic Caucasian subjects, a highsmile line was observed in 33% of the younger (�35years) and 29% of the older (>35 years) females com-pared with 25% and only 6% of males, respectively(P < 0.01). A trend for slightly higher smile lines (butstatistically not significant) was found in Asian subjectswhen compared with Caucasians.

A similar, gender-related, vertical lineament of lipposition was reported by Peck and co-workers34 in atotal of 86 subjects. The upper lips of the females werepositioned, on average, 1.5 mm more superiorly atmaximum smile line than those of the males (P < 0.01).In contrast, males exhibited a longer upper lip (meandifference was 2.2 mm) than females (P < 0.001). Tjanet al. (1984)33 also described a preponderance of highsmile lines in females (13.8%) compared with males(6.8%; P < 0.05). Because change of scarring wasfound to be more frequent in females than in males inthe present study, the parameters ‘gender’ and ‘smileline’ should be considered when examining possiblecandidates for apical surgery in the aesthetic zone, andin particular, females with a high lip line and high aes-thetic demands. In the present study, neither the levelof the lip line nor the patients’ attitude towards thepretreatment and follow-up gingival aesthetics wasassessed. It would be interesting to evaluate howpatients’ and surgeons’ attitudes would concur.



To date, the extent of scar formation has been attrib-uted to operator skill, to tension placed on woundmargins and sutures, to the patient’s capacity of con-nective tissue remodelling8 and to the use of a surgicalmicroscope35. Local inflammation, infection, wounddehiscence and foreign bodies are considered impor-tant contributory factors7. One difference that emergesas a major causative factor in scar-free or scar-forminghealing is the extent and type of inflammation at thewound site and hence, the growth factor profile of thehealing wound20. It has also been demonstrated thatsignificantly lower levels of macrophage, neutrophiland T-cell infiltration, as well as less inflammatorycytokine production, were observed in oral versusdermal wounds. These findings may explain thatdiminished inflammation is a key feature of the pri-vileged repair of oral mucosa30. Other researchershave reported phenotypic characteristics (‘non-scarring phenotype) of oral mucosal fibroblasts thatmay mediate the preferential healing36,37. In hyper-trophic scars, the principal causes are local, resultingfrom excessive wound tension because of inappropri-ate wound closure or post-operative infection. Thesefactors prolong inflammatory cell migration andcytokine release at the wound, and therefore, result inoverproduction of extracellular matrix38. Attemptsshould therefore aim at avoiding tension to woundmargins and preventing wound infection to reducescarring of oral mucosa.

The findings of the present study demonstrate thatadditional parameters such as gender, type of surgeryand most importantly, type of incision, point to a mul-tifactorial aetiology of soft tissue scarring followingapical surgery.

Conclusions

1 More substantial scarring was noted in the alveolarmucosa compared with the gingiva following apicalsurgery.2 The only statistically significant parameters associ-ated with change in gingival scarring were the type ofincision and the use of antibiotics.3 With regard to change in scarring within the alveo-lar mucosa, two parameters proved significant: genderand type of surgery.

Acknowledgements

The authors thank Dirk Klingbiel, Rahel Studer andGabriel Fischer, Institute of Mathematical Statistics andActuarial Science, University of Bern, for the statisticalanalysis.

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Scarring of gingiva and alveolar mucosa following apical surgery: visual assessment after one year