Stability of Periodontal Healing Distal to the Mandibular Second Molar After Third Molar Coronectomy: A 3-Year Follow-Up Study

Accepted Manuscript Stability of periodontal healing distal to the second mandibular molar after third molar coronectomy: A 3-year follow-up study Elisabetta Vignudelli, DDS, MSc. PHD Student, Giuseppe Monaco, DDS, Maria Rosaria Antonella Gatto, MD, PhD, Tommaso Costi., DDS, Claudio Marchetti, MD, DDS, Giuseppe Corinaldesi, MD, DDS PII:

S0278-2391(18)30992-3

DOI:

10.1016/j.joms.2018.08.027

Reference:

YJOMS 58437

To appear in:

Journal of Oral and Maxillofacial Surgery

Received Date: 23 November 2017 Revised Date:

27 August 2018

Accepted Date: 27 August 2018

Please cite this article as: Vignudelli E, Monaco G, Antonella Gatto MR, Costi. T, Marchetti C, Corinaldesi G, Stability of periodontal healing distal to the second mandibular molar after third molar coronectomy: A 3-year follow-up study, Journal of Oral and Maxillofacial Surgery (2018), doi: 10.1016/ j.joms.2018.08.027. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Title: Stability of periodontal healing distal to the second mandibular molar after third molar coronectomy: A 3-year follow-up study

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Authors: 1. Elisabetta Vignudelli, DDS, MSc. PHD Student. Unit of Oral and Maxillofacial Surgery.

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Department of Oral and Maxillofacial Surgery (DIBINEM), University of Bologna, Italy

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2. Giuseppe Monaco, DDS. Visiting Professor. Unit of Oral and Maxillofacial Surgery. Department of Oral and Maxillofacial Surgery (DIBINEM), University of Bologna, Italy

3. Maria Rosaria Antonella Gatto MD,PhD, Researcher. Unit of Periodontology. Unit of Oral and Maxillofacial Surgery. Department of Oral and Maxillofacial Surgery (DIBINEM),

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University of Bologna, Italy.

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4. Tommaso Costi. DDS. Clinical fellow. Unit of Oral and Maxillofacial Surgery. Department

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of Oral and Maxillofacial Surgery (DIBINEM), University of Bologna, Italy

5. Claudio Marchetti, MD, DDS. Professor of Maxillofacial Surgery. Unit of Oral and Maxillofacial Surgery. Department of Oral and Maxillofacial Surgery (DIBINEM), University of Bologna, Italy

6. Giuseppe Corinaldesi, MD, DDS Assistant Professor. Unit of Oral and Maxillofacial Surgery. Department of Oral and Maxillofacial Surgery (DIBINEM), University of Bologna, Italy

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Corresponding author: Dr. Elisabetta Vignudelli

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Department of Oral and Maxillofacial Surgery, DIBINEM, University of Bologna Via San Vitale 59, 40125, Bologna, Italy

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Tel.: 0039-051-2088155

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Fax: 0039-051-225208

[email protected] (fax and e-mail can be published)

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Funding

Keywords

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The authors declare no sources of support in the form of grants.

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Periodontal healing, coronectomy, third molar, extraction.

ACCEPTED MANUSCRIPT ABSTRACT Purpose: The stability of the periodontal attachment distal to the second mandibular molar after coronectomy of the third molar is still unclear. This study addressed the question of

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whether periodontal measures are stable over time among patients undergoing coronectomy. Methods: This prospective cohort study enrolled 30 patients treated at the Unit of Oral and Maxillofacial Surgery of the University of Bologna. The predictor variables were the probing

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pocket depth (PPD), the distance between the marginal crest (MC) and the bottom of the osseous defect (BOD), and the distance between the cemento-enamel junction (CEJ) and the

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BOD. Three points on the distal surface of the second molar were recorded: the disto-buccal (DB), disto-medial (M), and disto-lingual (DL) sites. The DB site was used as the statistical unit. The Wilcoxon test for paired data and Kendall’s tau-b were used to evaluate all variables. The significance level was set at P < 0.05.

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Results: The 3-year follow-up was completed by 27 patients (7 males, 20 females; mean age 28 ± 7 years) with 30 third molars. At 3 years, the PPD was 4 ± 1.25 mm; no significant changes in PPD were recorded for all sites from 9 months to 3 years. For MC–BOD and

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CEJ–BOD, significant reductions were evident between preoperative values and those at 9–

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36 months (p = 0.001) and between values at 9 and at 36 months (p = 0.02). Conclusion: A clinical healthy periodontium distal to the second molar was observed 36 months after coronectomy. However, further studies are necessary to confirm these preliminary clinical results.

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ACCEPTED MANUSCRIPT Introduction Coronectomy is a recognized surgical option for the treatment of third molars close to the inferior alveolar nerve (IAN)

1-3

. Several outcomes of the technique have been analyzed and

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compared to complete extraction; these include the immediate post-operative complication rates, long-term complication rates, and the fate of the remaining roots 1,4-6.

Several authors have recently focused on periodontal healing after coronectomy

7-9

. This

topic is also relevant to third molar extractions because of the possibility of incomplete post-

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, residual post-surgical intrabony defects 15-16 and related

. In addition, several studies have investigated how to manage and improve post-

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risks

10-14

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extraction periodontal healing

extraction periodontal healing distally to the second mandibular molars using bioabsorbable or non-resorbable membranes, grafting materials, or root planning 10-18.

After coronectomy, periodontal healing seems to be good in the short term

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particularly

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when the GBR technique is employed 8-9, but long-term data are lacking. The authors earlier published the findings of a prospective cohort study evaluating

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modifications to the periodontal indices distal to the second mandibular molar 9 months after coronectomy of the third molar 7. In this study, we performed follow-up on periodontal

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healing in the same patients for up to 3 postoperative years. The purpose of the present study was to analyze periodontal healing distal to the mandibular second molar at 3 years after coronectomy of the mandibular third molar. The specific aims were to record changes in the periodontal indexes measured distal to the second mandibular molar at 36 months after coronectomy of the third molar. Differences in the indexes between 9 and 36 months were also analyzed.

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ACCEPTED MANUSCRIPT Materials and Methods

A prospective cohort study was carried out on a study population consisting of all

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consecutive healthy patients referred to the Unit of Oral and Maxillofacial Surgery, Department of Biomedical and Neuromotor Science, University of Bologna, from November 2011 to June 2012, for the extraction of mandibular third molars. The patients underwent coronectomy in the same department from November 2011 to June 2012. Data on periodontal

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healing at 9 months were published in 2017 7; the results of the present study prolong the

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follow-up to 3 years (Fig 1 and 2) .

The study was explained to the patients, who provided written informed consent before any study-related procedure. The medical protocols of this study followed the Declaration of Helsinki, and this research was approved by the Ethics Committee AUSL Città di Bologna,

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Italy (CE: 12098).

The study was carried out in accordance with the current standards recommended for

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the reporting of observational studies in epidemiology (the STROBE statement).

The inclusion criteria for the original study were as follows: aged between 18 and 70

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years old, ASA 1 status according to the American Society of Anesthesiologists (ASA) physical classification system, presence of at least one third mandibular molar that needed extraction because of previous episodes of pericoronitis, the presence on a panoramic radiograph of at least one radiographic marker that was considered highly predictive of close contact between the IAN and third molar roots (e.g., increased radiolucency, narrowing or diversion, and interruption of the radiopaque border), and direct contact between the roots

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ACCEPTED MANUSCRIPT and the mandibular canal, due to the absence of cortical bone, as evaluated by cone-beam computed tomography (CBCT). Patients were excluded for the following reasons: systemic conditions that precluded

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surgical treatment, the use of antibiotics or anti-inflammatory agents within 14 days before surgery, third molars with caries, endodontic disease or premature apexes, tobacco use (>10 cigarettes per day), history of head or neck radiotherapy, poor oral hygiene (full-mouth

displaying plaque), and poor oral hygiene motivation.

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plaque score >25% calculated as a percentage of all surfaces (four aspects per tooth)

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The present follow-up study included all of the patients of the original study who completed 3 years of follow-up.

Study Variables

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Predictor Variable

The predictor variable was time: preoperative, 9 months and 36 months after coronectomy of

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the mandibular third molar.

Primary Outcome Variables and Assessment

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The primary outcomes variables used to assess periodontal healing were probing pocket depth (PPD), the distance between the marginal crest of the second molar (MC) and the bottom of the osseous defect (BOD), i.e., MC–BOD, and the distance between the cementoenamel junction (CEJ) of the second molar and the BOD , i.e., CEJ–BOD. -

PPD: The distance between the gingival margin and the bottom of the pocket, measured before surgery and after 36 months.

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MC–BOD: The distance between the MC and the BOD. The MC of the second molar was chosen as a reference point instead of the CEJ because the gingival margin typically did not permit visualizing the CEJ of the second molar. This was evaluated

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after third molar crown removal and 36 months later using bone sounding after local anesthesia to avoid underestimation of the defect depth, due to impact between the probe and the third molar’s crown.

CEJ–BOD: The distance between the CEJ of the second molar and the BOD. This was

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-

evaluated during surgery, after third molar crown removal, and 9 months after surgery.

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These measurements were recorded with the aid of a resin template, on three points of the distal surface of second molar: the disto-buccal (DB), disto-medial (M), and disto-lingual (DL) sites. In addition, to ensure correct measurements at 3 years after surgery, if gingival tissue covered the CEJ after the healing phase, the second molar crown’s vertical dimension

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(H) was measured (the distance between the MC and the CEJ). This measurement enabled evaluation of the CEJ–BOD according to the difference between MC–BOD and H (CEJ–BC

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= MC–BC).

Other Patient and Outcome Variables

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Other variables were grouped into logical categories including demographic variables, radiographic/clinical variables, and postoperative outcomes. The demographic variables were patient age (years) and sex (male/female). The radiographic/clinical variables were M3 impaction pattern (fully or partially impacted), M3 impaction type (vertically impacted if the inclination of the third molar axis was <25° relative to the axis of the mesial tooth or horizontally impacted if the inclination of the third molar axis was >25° relative to the axis of the mesial tooth). 5

ACCEPTED MANUSCRIPT Postoperative outcomes were measures of post-extraction complications. Subjects with one or more of the diagnoses outlined below were defined as having post-extraction complications: any subjective postoperative sensory change; a failed coronectomy (presenting as intra-

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operative root mobilization), any second surgery (reason and type) and any infection (diagnosed based on swelling, pain, and pus).

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Preoperative, Intraoperative and Postoperative Care

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Clinical Care and Operative Techniques

Patient age, third molar impaction pattern and type and PPD distal to the second molar, measured using a calibrated 15 University of North Carolina color-coded probe, were recorded in the preoperative assessment. All operations were performed as previously

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described using a standardized surgical protocol7,19. All procedures were performed, and all measurements made, by a single operator. Preoperative, intraoperative and post-operative

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care were provided as previously described in this journal, in 2017 7.

Data Management and Analyses

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Data management

We employed a data collection form and data management system using Excel 2011 software (Microsoft Corp, Redmond, WA) and Windows, ver. 14.0.0). Data were entered by a single operator. Before entry, data were evaluated for accuracy and completeness; logical consistency was verified and the range of quantitative data was computed. A hard copy of the data entered was verified and stored in individual coronectomy files. Data were analyzed using the SPSS software (ver. 11.5; SPSS, Inc., Chicago, IL). 6

ACCEPTED MANUSCRIPT For the quantification of migration, manually developed periapical radiographs (DF55 Ultra Speed, 2.4 × 4 cm; Kodak, Tokyo, Japan) were transformed into computed images using a Perfection V750 scanner (Epson, Nagano, Japan) to obtain 40,800 × 56,160-pixel images at

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4800-dpi resolution. During scanning, a piece of millimeter paper was inserted under each radiograph to permit calibration. Radiographs were saved in JPEG format and analyzed using

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the Digora imaging software (Soredex, Helsinki, Finland) by an external examiner.

Statistical Analyses

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On the basis of a precision of 0.5 mm and an estimated standard deviation of 1.32 mm 18 with a 95% confidence limit, a minimum of 27 patients was necessary The DB site represented the statistical unit of analysis. All quantitative variables differed significantly from a Gaussian distribution (Kolmogorov-Smirnov test with Lilliefors continuity correction, p < 0.05), except

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for the CEJ-BOD distance.

Proportions, medians and interquartile ranges, and median/interquartile range and mean/ standard deviation ratios were obtained for nominal and quantitative scale data. A Friedman

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test was used to compare PPD by time point. A Mann-Whitney test was used to compare PPD by sex, smoking history, and third molar impaction pattern and type; Kendall’s tau-b was

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used to evaluate the association between PPD and age. The Wilcoxon test for paired data was used to compare PPD, MC–BOD, CEJ–BOD between 0 and 9 months, 0 and 36 months, and 9 and 36 months; the alpha level was reduced to 0.02 by applying Bonferroni’s correction for multiple comparisons. Linear regression analysis of PPD, MC–BOD, and CEJ–BOD was used to quantify the degree of variation in the main outcomes and radicular migration between baseline and 9 and 36 months. The influence of the third molar impaction pattern and type on MC–BOD were evaluated using bootstrapping, given the small size of the 7

ACCEPTED MANUSCRIPT groups. Bias-corrected and accelerated (BCa) 95% confidence intervals were determined and the Mann-Whitney exact test was used for comparisons between the groups. The significance

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level was set at 0.05.

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ACCEPTED MANUSCRIPT Results We initially included 30 patients with 34 high-risk mandibular third molars (9 males, 21 females) and a mean age of 28 ± 7 years (range: 17–56 years). Of the 34 coronectomies, 31

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completed the 9-month follow-up and the results were published in 2017 7. Among the initial sample of 30 patients with 34 high-risk mandibular third molars, 27 patients (7 males, 20 females), with a mean age of 28 ± 7 (range, 17–56) and 30 third molars,

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completed 3 years of follow-up. Of the 30 coronectomies, 16 were fully impacted and 14 were partially impacted. Additionally, 13 were vertically impacted and 17 were horizontally

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impacted.

At 3 years, the PPD was 4 ± 1.25 mm. The reductions in PPD, from the preoperative values to those at 9–36 months, were statistically significant (p = 0.002 and 0.004, respectively), but

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no significant changes were noted between 9 months and 3 years (Table 1).

At 3 years, the MC-BODs were 7 ± 2. The values for the DB sites and CEJ-BODs were 0 ± 1.

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For MC-BOD and CEJ-BOD, significant reductions were seen between the preoperative values and those at 9–36 months (p = 0.001), and between 9 and 36 months (p = 0.001 and p

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= 0.002). Post-extraction complications were evaluated in a previous paper 7. The between-group variation in PPD, MC-BOD, and CEJ-BOD over time is shown in Table 1; the largest reduction was for PPD, and the reductions were similar between MC-BOD and CEJ-BOD.

No significant relationships were observed among age, sex, smoking history, third molar impaction pattern and type, and PPD reduction (Table 2); however, significant relationships 9

ACCEPTED MANUSCRIPT were determined between third molar impaction type and MC-BOD reduction at 0–36 months (p = 0.045; Table 3); between third molar impaction pattern and CEJ-BOD at 9–36 months (p = 0.038), and between third molar impaction pattern and CEJ-BOD at 0–36

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months (p = 0.045; Table 4).

All retained roots, as observed radiographically, migrated (with statistical significance; p =

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0.001) away from the mandibular canal during the first 9 months. The median root migration was 2.9 ± 2.5 mm. There was no statistically significant correlation between the MC-BOD

was detected from 9 to 36 months.

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reduction and the degree of root migration (p > 0.05). No statistically significant migration

At 9 months, second surgeries were required in four (11.8%) patients, no such surgeries were needed to remove or correct retained roots from 9 to 36 months. No infections were recorded

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from 9 to 36 months.

Discussion

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Coronectomy is today considered to be an alternative surgical procedure for the treatment of high-risk mandibular third molars 1, 4, 6, 19-24. The technique has been extensively investigated

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in terms of the short-term outcomes and complications, and also the long-term fate of retained root fragments

1, 4, 5, 9 20- 25

. The purpose of the present study was to analyze the

stability of periodontal healing distal to the mandibular second molar 3 at years after coronectomy of the mandibular third molar. While some authors have focused on periodontal healing in regions distal to the second mandibular molar after third molar coronectomy, longterm follow-up data are lacking and only short-term data are available7-9.

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ACCEPTED MANUSCRIPT In our patients, a clinically healthy periodontium distal to the second mandibular was confirmed at 36 months after coronectomy of the third molars. Compared to the 9-month data, increased PPD stability and slight improvements in the MC–BOD and CEJ–BOD were

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evident, reflecting completion of periodontal healing by 9 months, followed by stable maintenance over time. It is not possible to compare our data with those of other studies, because studies with similar follow-up durations are lacking.

Periodontal healing after

complete extraction and coronectomy (with or without a GBR procedure) has been

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investigated using the same bone variables, but with shorter follow-up times 10,11, 13,14, 26,27. A

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recent randomized clinical pilot trial 9 compared periodontal healing after coronectomy with or without GBR by evaluating the PPDs of the distal area

7, 26-31

. The 12-month PPD values

were normal in patients who did and did not undergo GBR; no significant difference was apparent.

GBR performed after coronectomy appears to inhibit root migration 9. Such

and root anatomy

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migration is common the distances range from 2 to 4 mm 7, 32. Migration is influenced by sex , and is more marked soon after surgery, becoming less, and finally

ceasing, over some years 22. The authors recorded a root migration distance of 2.9 ± 2.5 mm

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at 9 months but no more thereafter. Such migration caused us to extract three retained roots fragments to prevent neurological damage. However, it has been suggested 9 that migration

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of a mesially oriented retained root might damage the periodontal attachment of the second molar. GBR can be used to reduce the rate of second surgery to extract retained roots that have migrated. However, membrane placement might complicate second surgery if such surgery were ever necessary. In addition, root migration may reduce the risk of iatrogenic nerve injury during a second surgery to extract a retained root. In fact, even if a retained root is asymptomatic and alive, extraction is sometimes necessary because of infection or troublesome symptomatology 6. Regarding the fate of the retained root fragments, no further 11

ACCEPTED MANUSCRIPT complications were recorded from 9 to 36 months. As noted in our previous report 7, the final second surgery rate was 11.8% (four extractions; one due pulpitis and three due to root migration) and there were no complications after 12 months 7. However, Leung and Cheung

Thus, longer-term follow-up is essential.

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recently reported that some retained roots required extraction between 36 and 60 months 6.

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Despite our positive results, the present study had several limitations. First, all included patients had a low risk of periodontal problems. Second, this study did not include a control

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group with which to confirm and compare these preliminary results.

Additionally, periodontal healing was evaluated by calculating the mean values; the percentage of sites exhibiting residual periodontal defects was not evaluated. In fact, as shown by Kugelberg

15-16

many patients may exhibit residual periodontal defects after third

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molar extraction. Further studies with larger sample are necessary to evaluate residual periodontal defects of second mandibular molars after third molar coronectomy without GBR 8,9

.

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In conclusion, after coronectomy, satisfactory periodontal healing distal to the second molar and restoration of a normal periodontium were obtained and maintained for 36 months after

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surgery. Future studies with a large sample of patients with a high risk of developing second molar periodontal defects are necessary to evaluate any residual periodontal defects of the second mandibular molar after third molar coronectomy and to compare periodontal healing between coronectomy and complete extraction.

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ACCEPTED MANUSCRIPT The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see:

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http://www.textcheck.com/certificate/9JVMGj

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28. Kim HY, Yi SW, Choi SH, Kim CK: Bone probing measurement as a reliable evaluation of the bone level in periodontal defects. J Periodontol 71 :729-735, 2000 17

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coronectomy. J Oral Maxillofac Surg.

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protecting the inferior alveolar nerve:

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ACCEPTED MANUSCRIPT Caption to illustrations

Fig. 1 Radiograph at 36 months after surgery. The post-operative and 9 months radiograph of

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the same case was previous published on this journal in 2017. Fig. 2 Clinical healing at 36 months after surgery. The post-operative and 9 months photos of

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the same case was previous published on this journal in 2017

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ACCEPTED MANUSCRIPT Tables Table 1. Within and between groups change of PPD, MC-BOD and CEJ-BOD

PPD*

Within groups reduction

2 (3.5)

Friedman test: p=0.001

p=0.002

0 (1)

P=0.004

P=0.684

4 (4.5)

6 (5)

Friedman test: p=0.001

p=0.001

p=0.001

CEJ-BOD**

4.5 (2.3) p=0.001

Between groups variation

-0.05 (0.017)$ P=0.004

0 (2)

-0.143 (0.028)$

p=0.001

P=0.001

5.7 (2.9)

1.2 (1.9)

-0.134 (0.014)$

p=0.001

p=0.002

P=0.001

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MC-BOD*

Friedman test: p=0.001

Between groups reduction

2 (4)

0-9-36 months

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.

9-36 months

0-36 months

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0-9 months

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*Median (Interquartile range) ** Mean ± S.D in mm $Regression coefficient (standard error)

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ACCEPTED MANUSCRIPT Table 2 PPD reductions (mm) within preoperative and 9-36 months and between 9-36 months by demographic and clinical parameters. Median (Interquartile range)

M

0-36 months

9-36 months

1.5 (5.50)

1 (5.75)

0 (0.75)

2 (2.75)

2 (3.50)

0 (1)

p=0.413

p=0.336

p=0.051

Yes

1.4 (2.75)

2 (3.75)

0 (1)

No

1(0)

0.5(0)

-0.5 (0)

p=0.112

p=0.313

p=0.270

Partial

2 (4)

2 (5)

0 (1)

Total

2 (4)

2 (5)

0 (1)

p=0.874

p=0.892

p=0.923

Vertical

2 (2)

2 (3)

0 (1)

Horizontal

2 (5)

F

M AN U

Smoke

Third molar impaction

impaction type

1 (6)

0 (1)

p=0.790

p=0.560

0.175

0.160

-0.142

P=0.461

0.513

0.490

AC C

Kendall’s tau

EP

p=0.874

Age (years)

TE D

pattern

Third molar

SC

Gender

RI PT

0-9 months

21

ACCEPTED MANUSCRIPT Table 3.MC-BOD reductions (mm) within preoperative and 9-36 months and between 9-36 months by demographic and clinical parameters. Median (Interquartile range) 0-9 months

0-36 months

9-36 months

M

4 (4)

6 (6)

-1 (5)

F

3 (5)

5 (5)

0 (2)

p=0.893

p=0.676

p=0.218

Yes

4 (4.25)

5.5 (5)

0 (2)

No

2.5(4)

4.5(6.7)

-3 (4.7)

p=0.257

p=1.00

p=0.081

Partial

5 (4.5)

5 (5.7)

0 (1)

Total

3 (5.2)

5.5 (4.27)

-0.5 (2.5)

p=0.646

p=0.391

p=0.08

Vertical

3 (3.2)

3.5 (3.5)

0 (1.5)

Horizontal

6 (5)

M AN U

Third molar impaction pattern

type

p=0.128

-0.08 p=0.586

7 (4.2)

-1 (2)

p=0.045

p=0.203

0.04

-0.05

p=0.799

p=0.751

AC C

Kendall’s tau

EP

Age (years)

TE D

Third molar impaction

SC

Smoke

RI PT

Gender

22

ACCEPTED MANUSCRIPT Table 4. CEJ-BOD reductions (mm) within preoperative and 9-36 months and between 9-36 months by demographic and clinical parameters. Mean (Standard deviation) 0-9 months

0-36 months

9-36 months

M

4.3 (2.2)

6 (3.3)

1.7 (2.7)

F

4.4 (2.5)

5.4 (2.9)

1.0 (.71)

p=0.872

p=0.676

p=0.522

Yes

4.6 (2.4)

5.5 (2.9)

0.95 (1.8)

No

3(2.2)

5.7(3.8)

2.7 (2.6)

p=0.182

p=1.00

p=0.124

4.7 (2.5)

5.3 (3.3)

0.6 (1.8)

4 (2.2)

5.8 (2.7)

1.8(2.0)

p=0.689

p=0.391

p=0.038

Vertical

3.6 (2.5)

4.3 (3)

0.7 (1)

Horizontal

3.7 (2.2)

Partial

M AN U

Third molar impaction pattern Total

type

p=0.084

0.175 P=0.461

6.6 (2.6)

1.6 (2.2)

p=0.045

p=0.174

0.160

-0.142

0.513

0.490

AC C

Kendall’s tau

EP

Age (years)

TE D

Third molar impaction

SC

Smoke

RI PT

Gender

23

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT