Influence of Grafting on Pocket Depth and Dentin Hypersensitivity Around Third Molar Extraction Sites: A Split-Mouth Randomized Controlled Trial

Removal of an impacted third molar (3M) is a common oral surgical procedure.¹ Adequate management of impacted mandibular third molars poses a great challenge to clinicians. One concern is the health and condition of the periodontium around the impacted 3M. Studies have shown that a completely erupted second molar (2M) in close proximity to the impacted 3M has highly compromised periodontal health.^2,3 The type of impaction also has been studied for its association with periodontal disease. Horizontal and mesioangular impactions have been found to have more predisposition toward periodontal disease development.⁴ Difficulty in maintaining proper oral hygiene in this hard-to-access region results in overall increase in dental plaque, increased pocket depth, progressive attachment loss along the distal root of the 2M, and resultant dentin hypersensitivity around the 2M.^5,6 Persistent or progressive periodontal defect on the distal aspect of the mandibular 2M following surgical removal of the 3M compromises the treatment outcome considerably.^7-11

To overcome this postoperative periodontal pocket development, some authors have considered modifying the surgical technique and studied its effects on subsequent probing depths.¹² Karaca et al have also reviewed the influence of various flap designs on the health of the periodontium after mandibular 3M surgery.¹³ With the advent of regenerative procedures with advanced bone graft materials, a variety of bone substitutes have also been used to overcome the attachment loss in periodontal defects.¹⁴ Therefore, this study assesses the use of a bone graft substitute at 3M extraction sockets and its effect on periodontal measures in relation to the 2M.

The trial was carried out at the Faculty of Dentistry, SEGi University, Malaysia, under the approval of the institutional ethics committee, SEGi University (SEGiUni/VC/RIMC/41-2014) between 2015-2017. Inclusion criteria included patients willing for removal of bilaterally impacted mandibular third molars with pocket depth of ≥4 mm at either the distolingual or distobuccal sites around the mandibular second molars. Patients with history of smoking (≥10 cigarettes/day), systemic diseases that could affect periodontitis including diabetes mellitus, and who were on regular use of antimicrobial mouthrinses were excluded from the trial. Twenty-seven (n = 27) healthy patients with bilateral horizontally impacted 3Ms in the age group of 19 to 29 years (mean age 24 years) were included in the study. Assessment of the impacted 3Ms included a detailed clinical examination and orthopantomogram (OPG) (Figure 1). One oral surgeon was involved in screening, recruiting, and treating the patients for the trial to ensure that cases with similar anatomical position and surgical difficulty were selected.¹⁵

A computer-generated simple randomization sheet was used to allocate the extracted sites into either grafting sites (experimental) or nongrafting sites (control). The placement of bone grafts into one of the extracted sites was hidden from the patient and the clinician/periodontist involved in measurement of periodontal parameters (SSR). The split-mouth simple randomization design, screening, recruitment, treatment, and follow-up of the patients according to the CONSORT (Consolidated Standards of Reporting Trials) guidelines is represented in Figure 2.¹⁶

The primary outcome for the clinical trial was the changes in the pocket depth distal to the 2M at 6 months following surgical removal of the 3M. Secondary outcomes included feedback from the patients regarding dentin hypersensitivity at 3 and 6 months. A comprehensive periodontal examination and six-point periodontal charting was performed on the mandibular second molars. All periodontal measurements were carried out by a single calibrated assessor (SSR) using a University of North Carolina (UNC)-15 probe.¹⁷ Scaling and root debridement was performed by a single calibrated periodontist (SSR). Sensitivity testing was performed by applying air stimulus on the distal surface of the 2M for 1 second from a triple air dental syringe to assess the presence or absence of dentin hypersensitivity at 3 and 6 months. Voluntary response of a request to withdraw the stimulus was considered as presence of sensitivity, whereas no response was considered as absence of sensitivity.¹⁷ A participant questionnaire was used to register feedback from patients regarding dentin hypersensitivity.^18,19

The oral surgeon performed the surgical procedure following the standard operating technique agreed by the researchers and described as follows. Inferior alveolar nerve block, lingual nerve block, and long buccal nerve block injections were administered prior to 3M removal using 2% lignocaine hydrochloride with vasoconstrictor (1:80,000). A universal mucoperiosteal flap was elevated to gain proper access to the surgical site (Figure 3). A round 023 carbide bur was used with a straight surgical handpiece with copious 0.9% saline irrigation to remove the bone on the buccal and distal aspects of the 3M to achieve proper access. Tooth elevation and sectioning of the crown and/or roots was carried out when indicated under copious saline irrigation to ensure that defect morphology was not altered during the process of extraction (Figure 4).

Alloplast bone graft (Osteon^™ II synthetic resorbable bone graft material, Genoss, genoss.com) was placed in one of the randomly chosen extraction sockets following surgical removal of the 3M (Figure 5). Bone graft was mixed with the patient's own blood available from the surgical site, and bone grafts were condensed into the sockets using surgical instruments. 4-0 silk sutures were used to approximate the flaps (Figure 6).

Patients were provided with postoperative instructions on maintenance and possible complications in both verbal and written form. All patients were prescribed capsule amoxicillin 500 mg every 8 hours for 5 days, and metronidazole 400 mg every 8 hours for 5 days. Pain control was achieved by tablet etoricoxib 120 mg once daily for 2 days in all patients. Patients were recalled after 10 days for review and suture removal.

Subsequent OPGs were taken at the 6-month review visit (Figure 7). Pocket depth around the 2M was measured at baseline and at 3 months and 6 months after removal of the impacted 3M.

Sample size estimation was carried out before the initiation of the study using the power calculations and effect size as follows. To achieve a power of 80%, with a two-sided alpha level of 0.05 and to detect an effect size of reduction of 1 mm of pocket depth, at least 17 sites per arm were needed. Keeping in mind the possibility of dropouts in the trial, it was decided to enroll at least 20 patients. All the data regarding pocket depth reduction was statistically analyzed using paired t-test (P < .0001). The data concerning reduction in dentin hypersensitivity was statistically analyzed using chi-square test (P < .05). (Statistics were done using MedCalc^® software 18.2.1 [MedCalc, medcalc.org].)

At the preoperative stage there were no significant differences in pocket depth between the distolingual and distobuccal sites around the 2Ms in cases and control sites. Mean pocket depth at distolingual pocket was 5.81 mm at grafted sites and 5.77 mm at nongrafted sites; distobuccal pocket depth was measured as 5.59 mm at both grafted and nongrafted sites.

At 3 months post-treatment, pocket depths were measured for both cases and controls at distobuccal and distolingual sites of the 2Ms. Mean pocket depth distolingually was 3.40 mm at grafted sites and 3.60 mm at nongrafted sites. At the distobuccal aspect the mean pocket depth was found to be 3.22 mm at grafted sites and 3.29 mm at nongrafted sites. Grafted sites showed better results for decrease in pocket depth especially in the distolingual aspect; however, the results were not statistically significant (P = .0213) (Table 1). The decrease in the mean pocket depth distobuccally was better in the grafted site but not statistically significant (P = .5372).

After 6 months, mean pocket depth distolingually was 2.29 mm at grafted sites and 3.51 mm at nongrafted sites. At the distobuccal aspect the mean pocket depth was found to be 2.11 mm at grafted sites and 3.29 mm at nongrafted sites. Grafted sites showed better results in comparison to the nongrafted sites in both the distolingual and distobuccal aspects with statistically significant results (P < .0001) (Table 1).

The association of grafting with the presence of dentin hypersensitivity in relation to 2Ms post 3M surgery showed that at 3 months 19% (n = 5) of grafted sites had dentin hypersensitivity versus 63% (n = 17) in nongrafted sites. At 6 months, none of the grafted sites had dentin hypersensitivity compared with 48% (n = 13) of nongrafted sites. This indicates that grafting is associated with reduced dentin hypersensitivity in 2Ms, which was statistically significant at 3 months (P = .002) and 6 months (P = .0001) (Table 2 and Table 3).

Surgical extraction of impacted third molars is associated with several complications. The most often encountered complication is the formation of a periodontal pocket at the distal aspect of the second molar. This is considered to be a result of dental plaque accumulation and progressive bacterial colonization, which contribute to the periodontal destruction distal to the second molar and development of periodontitis resulting in dentin hypersensitivity and bone loss. Blakey et al assessed the change in periodontal status in asymptomatic third molars and made an important observation that a baseline periodontal pocket depth of ≥4 mm in the third molar region showed an increase in periodontal probing depth of ≥2 mm at annual follow-up visit.³ Horizontal and mesioangular impactions are seen with higher prevalence of increased pocket depth. White et al observed increased pocket depth and attachment loss around the second molar region in younger individuals with median age of 28 years.²⁰ Kugelberg et al have shown pocket depth of ≥7 mm in 43% of cases following third molar removal.^8-10 In order to minimize the chances of formation of periodontal defects at the distal aspect of second molars, various treatment modalities have been considered. Enhanced plaque control measures with proper postoperative oral hygiene care has shown to considerably decrease the prevalence of pocket formation during the initial healing phase. These benefits, however, were lost after 1 year, and oral hygiene measures did not influence the prevalence of intrabony defects.⁹

In the present study, for measurement of periodontal parameters, a single calibrated periodontist examined all the patients using a UNC-15 probe, which is the most commonly used probe in periodontal research. Studies have shown that probings with a manual probe are reproducible and showed less interexaminer variability compared to the Florida probe.^21,22 Additionally, the manual probe is inexpensive and easily available compared to constant-pressure probes. All patients included in the present study were treated with scaling and root debridement. This procedure was done to eliminate pseudo-pockets present around the teeth, while simultaneously it prepared the tissues for the subsequent minor surgical procedure. To reduce the chances of infection, following surgical removal of the impacted mandibular third molar, patients were treated with a combination of amoxicillin and metronidazole. None of the patients reported any adverse events following use of the combination of amoxicillin and metronidazole.²³

Leung et al studied the effects of root debridement on the distal surface of the second molar as an adjunctive procedure during the removal of the third molar and found a significant control in plaque accumulation at 6 months with reduction in residual pocket depth.⁶ Osborne et al, however, reported root debridement of the distal aspect of second molars after extraction of impacted third molars did not provide any significant benefits.²² Modification in flap design and tooth sectioning techniques have also been considered with regard to controlling the complication of distal osseous periodontal defect on the second molar.¹³ Newer regenerative methods and various bone graft materials, including autografts, xenografts, allografts, and alloplasts, along with their benefits for improving periodontal health, have also been studied, with their effects on periodontal pocket depth reduction and osseous defect fill being compared. All of these materials have their own limitations, and the search for an ideal graft material and technique is still ongoing. The use of autograft is limited with factors being morbidity at the donor site, limited volume availability, and a prolonged healing phase.²⁴ Newer alloplasts are now available that have low duration of remodeling and high potential for osseous regeneration.

The bone graft material used in this study (Osteon II) is a commercially available synthetic osteoconductive alloplast containing hydroxyapatite and β-tricalcium phosphate at a ratio of 30:70. The bone graft material is supplied in vials with a grain size of 0.5 mm to 1 mm with an overall volumetric porosity of approximately 77%. The pore size of the bone graft is around 250 µm. The bone graft was mixed with blood available in the nearby area, which may contain growth factors and may add osteoinductive potential to the graft.²⁵ (Authors' note: The authors recognize that epithelial downgrowth into the defect area could impair periodontal regeneration. However, due to the additional cost of using a membrane, the present study was limited to placement of bone grafts into the defect. Future studies should evaluate the benefits of membranes around these defects.)

This split-mouth randomized study design examined the bone graft material's use at third molar extraction sites and its subsequent effects on the distal periodontal pocket depth and dentin hypersensitivity of second molars. The outcome measures included decrease in the distal periodontal probing depth at the second molar and subjective evaluation of the effect of grafting on dentin sensitivity at the second molar. The density of bone fill was also studied using an orthopantomogram at follow-up visits at 10 days, 3 months, and 6 months postoperative.

All cases in the current study had a mean baseline pocket depth of 5.5 mm in the distobuccal (DB) and 5.8 mm in the distolingual (DL) sites of the second molars. The results of this study showed that at 3 months the mean pocket depth at the DL² and DB sites of second molars was 3.40 mm and 3.22 mm, respectively, which was slightly less, or better, than nongrafted sites, which were 3.60 mm and 3.29 mm at DL and DB aspects, respectively. These results, however, were not statistically significant. Statistically significant (P < .0001) results were observed at 6 months with DL and DB sites showing reduction of 2.29 mm and 2.11 mm, respectively, in the grafted sites. This suggests that grafting gives better healing of the periodontal defect in the long term as seen in the present cases at 6 months; at 3 months, however, no benefits were observed. These findings are similar to the Sammartino et al study in which bone grafts as well as bone grafts with membrane resulted in reduction of pocket depth and gain in clinical attachment level compared to the nongrafted site.²⁶

Hassan et al studied the risk for the development of periodontal defects distal to the mandibular second molar after impacted third molar extraction among patients aged 30 to 35 years with anorganic xenograft plus membrane.¹⁴ They reported that after 1 year, there was a statistically significant gain in the clinical attachment level and a reduction in the probing depth in the grafted sites compared with the nongrafted sites. The results of the present study are similar to the results of the Hassan et al study. The patient age group in the present study was from 19 to 29 years (mean 23 years), with statistically significant improvement in pocket depths at 6 months. Similar results were reported by Throndson et al, who studied 14 patients in whom surgical removal of bilateral impacted third molars was performed and observed that grafting sites had improvement in probing depths and statistically significant gain in clinical attachment levels distal to the second molars.²³ The authors, however, reported no significant increase in bone formation when comparing the grafted and nongrafted sites at 1 year. In the present study, similar results were noticed with respect to pocket depth.

Patient-reported outcomes are being collected in clinical trials and are considered to be an important means to assess the success of therapeutics/techniques.²⁷ Dentin hypersensitivity is a significant concern specifically after removal of a third molar that closely abuts the second molar as in class 2 level A impactions.⁴ In the present study, dentin hypersensitivity was assessed subjectively by blowing air over the second molar at the operated site during the follow-up visit at 3 months and 6 months. This study showed a considerably lower number of sites with dentin hypersensitivity following grafting versus sites without grafting, with only five grafted sites (19%) at 3 months and none at 6 months with statistically significant results. This may be concluded to be the dentin exposure that occurs following the surgical removal of a third molar that closely abuts the distal aspect of an erupted second molar, which tends to be covered adequately enough in the healing phase by grafting.

Alloplastic bone grafting at the osseous defect site following third molar removal showed statistically significant improved outcomes in pocket depth distal to second molars at 6 months. Grafting also showed decreased dentin hypersensitivity in relation to the second molar at both 3 and 6 months. Within the limitations of this study, horizontally impacted mandibular third molars with a pocket depth of ≥5.5 mm in the distal aspect of the second molar may benefit from reduction of pocket depth and reduced chance of dentin hypersensitivity.

The authors thank the Research and Innovation Management Centre, SEGi University, Malaysia, for its generous grant to conduct this study. The authors also thank Datuk Dr. Khairiyah Abd Muttalib for providing permissions for necessary radiographs during the study. The authors had no conflict of interest to report.

Haydar Majid, BDS, MDSc
Lecturer, Faculty of Dentistry, SEGi University, Petaling Jaya, Malaysia; Diplomate, International Congress of Oral Implantolgists

Srinivas Sulugodu Ramachandra, BDS, MDS
PhD Student, School of Dentistry, The University of Queensland, Herston, Australia

Saurabh Kumar, BDS, MDS
Senior Lecturer, Faculty of Dentistry, SEGi University, Petaling Jaya, Malaysia

Myint Wei, BDS, MDSc, DipMedEd
Senior Lecturer, Faculty of Dentistry, SEGi University, Petaling Jaya, Malaysia; Fellow, International College of Continuing Dental Education

Kalyan C. Gundavarapu, BDS, MDPH, DDPH RCS
Consultant, Dentospital, Ongole, Andhra Pradesh, India

1. Blondeau F, Daniel NG. Extraction of impacted mandibular third molars: postoperative complications and their risk factors. J Can Dent Assoc. 2007;73(4):325.

2. Barbato L, Kalemaj Z, Buti J, et al. Effect of surgical intervention for removal of mandibular third molar on periodontal healing of adjacent mandibular second molar: a systematic review and Bayesian network meta-analysis. J Periodontol. 2016;87(3):291-302.

3. Blakey GH, Jacks MT, Offenbacher S, et al. Progression of periodontal disease in the second/third molar region in subjects with asymptomatic third molars. J Oral Maxillofac Surg. 2006;64(2):189-193.

4. Stella PEM, Falci SGM, Oliveira de Medeiros LE, et al. Impact of mandibular third molar extraction in the second molar periodontal status: a prospective study. J Indian Soc Periodontol. 2017;21(4):285-290.

5. Krausz AA, Machtei EE, Peled M. Effects of lower third molar extraction on attachment level and alveolar bone height of the adjacent second molar. Int J Oral Maxillofac Surg. 2005;34(7):756-760.

6. Leung WK, Corbet EF, Kan KW, et al. A regimen of systematic periodontal care after removal of impacted mandibular third molars manages periodontal pockets associated with the mandibular second molars. J Clin Periodontol. 2005;32(7):725-731.

7. Richardson DT, Dodson TB. Risk of periodontal defects after third molar surgery: an exercise in evidence-based clinical decision-making. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100(2):133-137.

8. Kugelberg CF. Periodontal healing two and four years after impacted lower third molar surgery. A comparative retrospective study. Int J Oral Maxillofac Surg. 1990;19(6):341-345.

9. Kugelberg CF, Ahlström U, Ericson S, et al. Periodontal healing after impacted lower third molar surgery in adolescents and adults. A prospective study. Int J Oral Maxillofac Surg. 1991;20(1):18-24.

10. Kugelberg CF, Ahlstrom U, Ericson S, et al. The influence of anatomical, pathophysiological and other factors on periodontal healing after impacted lower third molar surgery. A multiple regression analysis. J Clin Periodontol. 1991;18(1):37-43.

11. Aloy-Prosper A, Garcia-Mira B, Larrazabal-Moron C, Penarrocha-Diago M. Distal probing depth and attachment level of lower second molars following surgical extraction of lower third molars: a literature review. Med Oral Patol Oral Cir Bucal. 2010;15(5):e755-e759.

12. Chang HH, Lee JJ, Kok SH, Yang PJ. Periodontal healing after mandibular third molar surgery-a comparison of distolingual alveolectomy and tooth division techniques. Int J Oral Maxillofac Surg. 2004;33(1):32-37.

13. Karaca İ, Şimşek Ş, Uğar D, Bozkaya S. Review of flap design influence on the health of the periodontium after mandibular third molar surgery. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104(1):18-23.

14. Hassan KS, Marei HF, Alagl AS. Does grafting of third molar extraction sockets enhance periodontal measures in 30- to 35-year-old patients? J Oral Maxillofac Surg. 2012;70(4):757-764.

15. Mahdey HM, Arora S, Wei M. Prevalence and difficulty index associated with the 3(rd) mandibular molar impaction among Malaysian ethnicities: a clinico-radiographic study. J Clin Diagn Res. 2015;9(9):ZC65-ZC68.

16. Schulz KF, Altman DG, Moher D, CONSORT Group. CONSORT 2010 statement: updated guidelines for reporting parallel group randomized trials. Ann Intern Med. 2010;152(11):726-732.

17. Mason S, Kingston R, Shneyer L, Harding M. Clinical study to monitor dentinal hypersensitivity with episodic use of a desensitising dentifrice. BDJ Open. 2017;3:17011.

18. Dell-Kuster S, Sanjuan E, Todorov A, et al. Designing questionnaires: healthcare survey to compare two different response scales. BMC Med Res Methodol. 2014;14:96.

19. Baker SR, Gibson BJ, Sufi F, et al. The dentine hypersensitivity experience questionnaire: a longitudinal validation study. J Clin Periodontol. 2014;41(1):52-59.

20. White RP Jr, Madianos PN, Offenbacher S, et al. Microbial complexes detected in the second/third molar region in patients with asymptomatic third molars. J Oral Maxillofac Surg. 2002;60(11):1234-1240.

21. Kour A, Kumar A, Puri K, et al. Comparative evaluation of probing depth and clinical attachment level using a manual probe and Florida probe. J Indian Soc Periodontol. 2016;20(3):299-306.

22. Osborne WH, Snyder AJ, Tempel TR. Attachment levels and crevicular depths at the distal of mandibular second molars following removal of adjacent third molars. J Periodontol. 1982;53(2):93-95.

23. Throndson RR, Sexton SB. Grafting mandibular third molar extraction sites: a comparison of bioactive glass to a nongrafted site. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2002;94(4):413-419.

24. Ramachandra SS, Rana R, Reetika S, Jithendra KD. Options to avoid the second surgical site: a review of literature. Cell Tissue Bank. 2014;15(3):297-305.

25. Bae JH, Kim YK, Kim SG, et al. Sinus bone graft using new alloplastic bone graft material (Osteon)-II: clinical evaluation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109(3):e14-e20.

26. Sammartino G, Tia M, Bucci T, Wang HL. Prevention of mandibular third molar extraction-associated periodontal defects: a comparative study. J Periodontol. 2009;80(3):389-396.

27. McGuire MK, Scheyer ET, Gwaltney C. Commentary: incorporating patient-reported outcomes in periodontal clinical trials. J Periodontol. 2014;85(10):1313-1319.