Evaluation of deproteinised bovine bone matrix combined with absorbable biofilm for the preservation of extraction sites of mandibular impacted wisdom teeth

Abstract

BACKGROUND:

Bone defects and deep periodontal pockets often exist distal to the second molar after mandibular third molar extraction, seriously threatening the periodontal health of the second molar.

OBJECTIVE:

To evaluate the effect of socket preservation with bone substitute materials on alveolar bone resorption and prevention of the distal periodontal defect of the adjacent tooth after mandibular impacted third molar extraction compared with natural healing.

METHODS:

Ninety-nine patients with mandibular impacted teeth, treated in our hospital from January 2018 to December 2020, were randomly divided into the control and experimental groups. The experimental group underwent minimally invasive tooth extraction and socket preservation using the deproteinised bovine bone mineral, Bio-Oss and the bioabsorbable collagen membrane, Bio-Gide. The control group healed naturally after minimally invasive tooth extraction. The alveolar ridge dimension of the extraction sites, the probing depth, tooth mobility and gingival index on the distal aspect of the mandibular second molars were examined and recorded before and six months after the operations.

RESULTS:

There was a significant difference between the experimental group and the control group in the alveolar bone width ( $P<$ 0.05) and height ( $P<$ 0.05) before and after surgery. The probing depth of the extraction sites in both groups was reduced.

CONCLUSION:

Using Bio-Oss and Bio-Gide to preserve extraction sites of impacted teeth can promote recovery more effectively than natural healing on the height of the distal alveolar bone and the width of the alveolar crest of the second molar and thus improve the periodontal status of the adjacent second molar.

Keywords

Impacted mandibular third molar second molar alveolar bone socket preservation

1. Introduction

Bone defects and deep periodontal pockets often exist distal to the second molar after mandibular third molar extraction [1], seriously threatening the periodontal health of the second molar. The degree of periodontal destruction is closely related to the patient’s age and preoperative periodontal status. For patients under 25 years, the probing depth of the periodontal pocket after surgery can be controlled to within 4 mm, but this is difficult in patients over 25 years. When the initial probing depth is more than 7 mm in older patients, the remaining periodontal pocket is usually 5 cu. mm. Several methods have been used to promote periodontal tissue regeneration distal to the second molar [2, 3, 4]. Using various bone replacement materials or barrier membranes within the extraction fossa has significantly improved periodontal health distal to the second molar, reducing probing depth; improving the gingival index, clinical attachment level and local alveolar bone mass; and increasing bone mineral density [5, 6, 7, 8]. There is no consensus about the kind of bone substitute material and barrier membrane that can achieve the best clinical effect. The application of various supporting materials still requires clinical research.

Site preservation, often used before implant repair, is the simultaneous implantation of bone substitutes in the extraction pit to guide and promote local bone regeneration and to maximise the preservation of tissue conditions conducive to repair and implant [8]. Several studies have confirmed that preserving extraction sites is beneficial for maintaining or reconstructing the three-dimensional alveolar ridge morphology [9]. Bio-Oss bone powder and Bio-Gide membranes are commonly used in various bone defect repair and site preservation procedures and have a definite effect on increasing bone mass and reducing bone resorption [10, 11]. However, applying these two materials for site preservation after extracting an impacted third molar has rarely been reported.

This study aimed to investigate the effect of Bio-Oss and Bio-Gide on periodontal health and alveolar bone dimensions, analyse the factors affecting the clinical outcome, and provide a basis for preserving the extraction site of impacted wisdom teeth.

2. Materials and methods

The hospital’s Medical Ethics Committee approved the study (Ethics no. 2018YLSLYZ01). All subjects signed the informed consent form.

2.1 Study subjects and grouping

Patients attending the Department of Stomatology at the Changping District Hospital from January 2018 to December 2020 were included. Ninety-nine patients aged 18 to 55 years with impacted wisdom teeth were enrolled. Bio-Oss and Bio-Gide were used to preserve the extraction sites in the trial group. The control group healed naturally after tooth extraction.

The inclusion criteria were: (1) patients with good general health or well-controlled hypertension without any contraindication to tooth extraction; (2) impacted wisdom tooth in the mesial part of the mandible, with severe alveolar bone resorption distal to the second molar but with a minimum residual height of the bone wall $\geqslant$ 3 mm; (3) patients with good oral hygiene and good compliance after periodontal therapy; (4) patients who had stopped smoking or smoked less than ten cigarettes per day before and after periodontal therapy.

The exclusion criteria were: (1) patients less than 18 years of age or more than 55 years; (2) patients with an acute tooth infection, (3) patients who smoked more than ten cigarettes per day, (4) patients who were pregnant, lactating or planning a pregnancy; (5) patients on long-term non-steroidal anti-inflammatory drugs, bisphosphonates, corticosteroids, tetracyclines, immunosuppressants or other drugs affecting bone metabolism or bone healing; (6) a history of head and neck radiotherapy; and (7) those with missing second molars or requiring simultaneous removal of the second molars.

Ninety-nine patients were enrolled in this study, including 49 in the trial and 50 in the control groups.

2.2 Experimental materials and methods

2.2.1. Materials and equipment included Bio-Oss, Bio-Gide, minimally invasive dental extraction instruments and cone beam computed tomography (CBCT) software (3D CBCT, Synod, Germany).

Figure 1.

Operation procedure of experimental group. a: Preoperative local oral radiography; b. Open the mucoperiosteal flap; c–d: Removal of a small number of blocking bone plates and tooth extraction; e: Bio-Oss bone meal was filled in the extraction fosse. f: Cover Bio-Gide film; g: Tight suture.

2.2.2. Surgical approach (Fig. 1)

In the control group, the wisdom teeth were extracted as follows. A corner incision was made after local infiltration anaesthesia with primrose hemp and towel preparation with iodophor. The gingiva was separated, and a mucoperiosteal flap was opened. The tooth was separated with the help of a turbine, protecting the alveolar bone wall during the surgery to minimise its destruction. The tooth was loosened and pulled out gently with tooth forceps. The extraction pit was scraped to clean the infected and other pathological tissues. The distal calculus of the adjacent tooth was removed if necessary. Tension sutures were used to close the periosteum. Two tablets of LOFN codeine (0.2 g of ibuprofen, 12.5 mg of codeine) and one tablet of cefaclor (0.375 g) were administered half to one hour before surgery. Postoperatively, oral cefaclor was prescribed for seven days (0.375 g twice daily). Oral rinsing with compound chlorhexidine solution for two weeks was advised from the second day after surgery (for one minute, four times daily). Sutures were removed one week after the operation.

Guided bone regeneration (GBR) was performed in the trial group. Fresh blood was collected and mixed with Bio-Oss powder for implantation in the extraction pit such that the bone graft material was at least 0.5 mm above the alveolar crest. The Bio-Gide collagen membrane was sheared, and the surface of the bone graft was covered with the edge located on the normal bone surface. Preoperative and postoperative medications were the same as in the control group. Sutures were removed two weeks after the operation.

2.2.3. Evaluation method

The same radiologist performed the CBCT using the same machine (Sirona, Orthophos XG 3D Ceph) in all the patients. The acquired images were processed, and 3D reconstruction was done using the DICOM3.0 software. A series of isometric CBCT images were obtained from the coronal and sagittal images with 1 mm intervals. Preoperative and six-month postoperative measurements were made by overlapping preoperative and postoperative photographs of the same location to ensure angular consistency. The specific indicators were as follows:

•

The height was measured from the middle buccal, lingual and central enamel cementum boundaries of the second molar to the superior margin of the alveolar bone (Fig. 2).

Figure 2.

Schematic diagram of measuring the height of autogenous bone (buccal side for example). a: The height from the enamel-dentin junction to the crest of the alveolar ridge of the maxillary second premolar before extraction is 7.54 mm. b: Six months after implantation of bone powder and membrane at the same time as the extraction of impacted tooth, the height from enamel-dentin junction to the crest of the alveolar ridge of the maxillary second premolar in the distal-central zone is 0.56 mm.

The bone widths of the autogenous bone were noted at 1 mm, 4 mm, 7 mm and 10 mm around the enamel cementum boundary (Fig. 3).

Figure 3.

Diagram of measuring the width of autogenous bone. After six months of the impacted tooth extraction, the bone width from the enamel-dentin junction to the root in the distal-central area of the maxillary second premolar was measured at 1 mm, 4 mm, 7 mm, and 10 mm depths.

The distal probing depth, tooth mobility and gingival index of second molars were recorded before and at six months after surgery.

2.2.4. Statistical analysis

The data was entered into Excel 2019 software and analysed by the SPSS Statistics for Windows, version 23.0. software package (IBM Corp., Armonk, New York). The chi-square test compared the baseline information of the intervention and control groups. The $t$ -test or non-parametric tests were used to compare the related indexes at baseline and after the treatment depending on the data distribution.

3. Results

3.1 Patients’ baseline data

Ninety-nine patients were enrolled in the study, including 49 in the trial and 50 in the control groups. There were significant differences in age and sex distribution between the two groups ( $P<$ 0.05). However, there was no significant difference between the two groups in the location of the third molar in the bone, the follow-up duration and the number of teeth on the left or right sides ( $P>$ 0.05) (Table 1).

Table 1
Patients’ baseline data

Demographic index	Group	control group ( $n=$ 50)	experimental group ( $n=$ 49)	$X^{2}$	$p$ value
Years	$\leqslant$ 25	28(57.1)	14(28.6)	8.16	0.004
	$\geqslant$ 26	21(42.9)	35(71.4)
Follow-up months	$\leqslant$ 6	13(26.0)	10(20.4)	0.96	0.617
	7–20	30(60.0)	34(69.4)
	$\geqslant$ 21	7(14.0)	5(10.2)
Dental position	48	21(42.0)	24(49.0)	0.49	0.486
	38	29(58.0)	25(51.0)
Position	Low	13(26.0)	12(24.5)	0.10	0.593
	Middle	27(54.0)	26(53.1)
	High	10(20.0)	11(22.4)
Sex	Female	32(64.0)	17(34.7)	8.50	0.004
	Male	18(36.0)	32(65.3)

3.2 The changes and resorption of alveolar bone

Changes in alveolar bone width: there was a significant difference between the trial and control groups ( $P<$ 0.05) in terms of the difference between the alveolar bone width before and after surgery at the 1 mm root of the enamel cementum boundary (Table 2). Age-related analysis of alveolar bone width showed no significant difference in alveolar bone width between the two groups when the patients were older than 26 years. When patients were $\leqslant$ 25 years of age, the application of bone replacement materials and barrier membranes significantly increased the alveolar bone width at 1 mm and 4 mm below the enamel cementum boundary in the distal second molar (Table 3).

Table 2
Total evaluation of the changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm of enamel cementum boundary in experimental group and control group after extraction of impacted wisdom teeth ( $\bar{x}$ $\pm$ $s$ )

Group	1 mm	4 mm	7 mm	10 mm
Experimental group ( $n=$ 49)	0.01 $\pm$ 1.8	$-$ 0.19 $\pm$ 1.8	$-$ 0.10 $\pm$ 1.1	$-$ 0.04 $\pm$ 0.6
Contral group ( $n=$ 50)	$-$ 1.38 $\pm$ 2.6	$-$ 0.52 $\pm$ 1.3	$-$ 0.40 $\pm$ 1.8	$-$ 0.05 $\pm$ 0.5
$t$ value	2.15	1.05	0.98	0.12
$p$ value	0.04	0.30	0.33	0.90

Changes in alveolar bone height: overall, there were significant differences in the alveolar bone height in the distal buccal (HB), central (HO) and lingual (HL) positions preoperatively and postoperatively in the trial and control groups ( $P<$ 0.01 and $P<$ 0.05, respectively) (Table 4).

3.3 Changes of periodontal probing

There was a significant difference between the two groups ( $P<$ 0.01), but there was no significant difference ( $P>$ 0.05) between the two groups at the midpoint and lingual sites (Table 5).

Bleeding index and tooth mobility: there was no significant difference between the two groups ( $P$ > 0.05) (Table 6).

4. Discussion

More significant periodontal destruction, including increased probing depth, loss of attachment and loss of alveolar bone, tends to occur in the distal part of the second molar after extraction of the impacted

Table 3
The changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm after extraction of wisdom teeth in different age groups ( $\bar{x}$ $\pm$ $s$ )

Group	1 mm		4 mm		7 mm		10 mm
	$\leqslant$ 25 years	$\geqslant$ 26 years	$\leqslant$ 25 years	$\geqslant$ 26 years	$\leqslant$ 25 years	$\geqslant$ 26 years	$\leqslant$ 25 years	$\geqslant$ 26 years
Experimental group ( $n=$ 49)	0.15 $\pm$ 1.1	$-$ 0.11 $\pm$ 2.3	0.47 $\pm$ 0.9	$-$ 0.45 $\pm$ 1.9	$-$ 0.02 $\pm$ 0.5	$-$ 0.13 $\pm$ 1.3	$-$ 0.09 $\pm$ 0.3	$-$ 0.02 $\pm$ 0.7
Contral group ( $n=$ 50)	$-$ 0.84 $\pm$ 1.1	$-$ 2.73 $\pm$ 4.3	$-$ 0.15 $\pm$ 1.0	$-$ 1.08 $\pm$ 1.5	$-$ 0.07 $\pm$ 0.5	$-$ 0.84 $\pm$ 2.7	$-$ 0.10 $\pm$ 0.5	0.02 $\pm$ 0.6
$t$ value	2.31	1.77	1.99	1.21	0.28	1.35	0.13	$-$ 0.21
$p$ value	0.03	0.09	0.05	0.23	0.78	0.18	0.90	0.83

third molar [12]. A systematic review showed that site preservation could effectively reduce the distal probing depth of the second molar after wisdom tooth extraction [5].

Table 4

Comparison of HB, HO, HL between the experimental group and the control group ( $\bar{x}$ $\pm$ $s$ mm)

Group	HB difference	HO differernce	HL difference
Experimental group ( $n=$ 49)	$-$ 2.20 $\pm$ 2.6	$-$ 4.46 $\pm$ 3.0	$-$ 2.63 $\pm$ 2.8
Control Group ( $n=$ 50)	$-$ 0.88 $\pm$ 2.4	$-$ 2.09 $\pm$ 2.2	$-$ 1.51 $\pm$ 1.7
$t$ value	$-$ 2.64	$-$ 4.50	$-$ 2.38
$p$ value	0.01	0.00	0.02

Note: HB:buccal; HO: cenral; HL: lingual.

Table 5

Comparison of the difference of periodontal probing (PD) before and after tooth extraction in all impacted patients ( $\bar{x}$ $\pm$ $s$ ) mm

Group	HB difference	HO difference	HL difference
Experimental group ( $n=$ 49)	$-$ 2.20 $\pm$ 2.6	$-$ 4.46 $\pm$ 3.0	$-$ 2.63 $\pm$ 2.8
Control Group ( $n=$ 50)	$-$ 0.88 $\pm$ 2.4	$-$ 2.09 $\pm$ 2.2	$-$ 1.51 $\pm$ 1.7
$t$ value	$-$ 2.64	$-$ 4.50	$-$ 2.38
$p$ value	0.01	0.00	0.02

Table 6

Comparison of gingival bleeding index before and after tooth extraction in all impacted patients

Different stages	Bleeding index	Control group ( $n=$ 50)	Experimental group ( $n=$ 49)	Total	$X^{2}$	$p$ value
Distal preoperation	0	23(46.0)	16(32.7)	39(39.4)	2.75	0.25
	1	18(36.0)	18(36.7)	36(36.4)
	2	9(18.0)	15(30.6)	24(24.2)
Distal postoperative	0	13(26.0)	20(40.8)	33(33.3)	2.48	0.29
	1	26(52.0)	21(42.9)	47(47.5)
	2	11(22.0)	8(16.3)	19(19.2)

This study comprehensively analysed the clinical effects of site preservation of the alveolar fossa of the impacted wisdom tooth using the GBR technique combined with Bio-Oss bone meal and Bio-Gide membrane.

4.1 The healing of impacted mandibular third molars after extraction and site preservation using Bio-Oss bone powder and Bio-Gide membrane for guided bone regeneration, alveolar bone changes and periodontal status in the distal portion of the adjacent second molars were evaluated. The results showed that the width of the alveolar bone in the experimental group was greater compared with the control group at the root of the enamel cementum boundary at 1 mm, which indicated that the effect of the implant-bone substitute was better than that of the natural healing at the top of the alveolar ridge. However, there was no significant difference in the jaw base. It should be noted that this effect was most pronounced in patients younger than 25 years but not in patients older than 26 years, showing that age has a specific impact on efficacy.

Both natural healing and Bio-Oss plus Bio-Gide site preservation effectively increased the distal bone height of adjacent teeth. Bone graft intervention was more effective in restoring bone height than in the control group, and the difference was significant. At the same time, both natural healing and bone grafting can improve the depth of periodontal probing. Bone grafting can make the periodontal pocket shallower in the distal buccal side of adjacent teeth, which is significantly different from natural healing.

Periodontal probing depth was influenced by alveolar bone height and gingival groove depth. The measurement of bone mass height showed that site preservation resulted in a significant increase in bone mass in the distal middle of the second molar compared with natural healing. Still, there was no significant difference in the improvement of probing depth between the second molar’s distal midpoint and lingual side, suggesting that in addition to bone mass changes, local gingival thickness also changes, resulting in a non-significant difference in probing depth. Previous studies have found that soft-tissue thickening occurs after tooth extraction in aesthetic areas due to absorption of the bone edges [13]. A 2020 randomised-controlled study showed that site preservation significantly increased local bone height but caused thinner soft tissue after restoration in the maxillary premolar region compared with natural healing after tooth extraction [14]. The latter was 1.16 mm thinner than the former. Therefore, the thickness of soft tissue caused by natural healing after tooth extraction and the thinness of soft tissue caused by site preservation make the changes in probing depth and the alveolar bone height insignificant. Thinner soft tissue is a disadvantage for sites where implant restoration may be required. The second molar’s improved distal alveolar ridge height is more critical for this study.

4.2 Factors affecting the results of the study

Migration of the tissue flap to close the extraction wound, combined with the labial mucosal flap, reduces the width of the gingiva’s distal keratinisation, resulting in the risk of gingival recession. After the close suture of the extraction wound, the tooth and soft tissue are adjacent but not completely closed. The premise of GBR is the initial closure and maintenance of soft tissue. An intact soft-tissue barrier should be present on the barrier membrane to reduce the interference of external mechanical factors and microorganisms during alveolar bone regeneration [15]. A meta-analysis showing a mean bone gain of 3.01 mm in unexposed and 0.56 mm in exposed cases suggests that exposure of the barrier membrane significantly impacts the therapeutic efficacy of GBR [16]. On the other hand, some soft tissue dehiscence caused by tissue oedema, membrane exposure and loss of bone graft material is not conducive to bone regeneration. Hence, the increase in the bone cannot be maintained. Simion et al. [17] showed that bone regeneration is substantially reduced with exposure to a non-absorbable barrier and that collagen membrane exposure may reduce new bone formation by approximately 20%.

4.3 Discussion on avoiding adverse factors of operation

An improved surgical incision and gingival groove relaxation reduce the risk of gingival recession. Most of the mandibular wisdom teeth in this study were extracted and preserved through the gingival groove incision and achieved the same effect as an angular incision.

Bone-filling materials currently include collagen plugs, bone collagen, and growth factors. Among these materials, collagen plugs and bone collagen that block tooth extraction and GBR wounds are simple, quick and easy to obtain. The effect of the GBR technique on site preservation has been demonstrated.

4.4 Limitations of the study

According to the current research, Bio-Oss and Bio-Gide are essential in preserving the extraction site of impacted mandibular wisdom teeth. However, this filling material can not completely prevent the loss of alveolar bone after tooth extraction, and more research on implant materials is needed. Because the decreased thickness of the soft tissue is unfavourable to implant repair, a more in-depth study is required to solve this problem. Further research is needed on protecting adjacent teeth more effectively after extraction of impacted teeth.

5. Conclusion

After extraction of impacted wisdom teeth, Bio-Oss and Bio-Gide were used for site preservation and were beneficial in increasing the distal bone height of adjacent teeth, improving the depth of periodontal probing and protecting the adjacent teeth. Therefore, impacted wisdom teeth should be pulled out as soon as possible. Compared with natural healing, site preservation can promote the recovery of the distal alveolar bone height and the width of the alveolar crest, improve the probing depth in the distal buccal position of the second molar, and protect the adjacent teeth more effectively. At the same time, the age of the patients, the classification of the impacted wisdom teeth and the presence of chronic inflammation are also important factors affecting the distal periodontitis of adjacent teeth.

Ethics statement

This study was conducted in accordance with the Declaration of Helsinki. This study was conducted with approval from the Ethics Committee of Beijing Changping District Hospital. Written informed consent was obtained from all participants.

Competing interest

The authors declare that they have no competing interests.

Funding

Not applicable.

Author contributions

(I) Conception and design: MJ; (II) Administrative support: JNN; (III) Provision of study materials or patients: MJ and WJY; (IV) Collection and assembly of data: CXL and ZMX; (V) Data analysis and interpretation: JNN, CXL and ZMX. All authors helped write the manuscript and approved the final version.

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

Footnotes

Acknowledgments

Special thanks to Professor Li Xingming, Capital University of Medical Sciences Public Health, for supporting the data of this study.

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Evaluation of deproteinised bovine bone matrix combined with absorbable biofilm for the preservation of extraction sites of mandibular impacted wisdom teeth

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Materials and methods

2.1 Study subjects and grouping

2.2 Experimental materials and methods

3.1 Patients’ baseline data

Table 1 Patients’ baseline data

Table 2 Total evaluation of the changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm of enamel cementum boundary in experimental group and control group after extraction of impacted wisdom teeth ( x ¯ ± s )

4. Discussion

Table 3 The changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm after extraction of wisdom teeth in different age groups ( x ¯ ± s )

Ethics statement

Competing interest

Funding

Author contributions

Availability of data and materials

Footnotes

Acknowledgments

References

Table 1
Patients’ baseline data

Table 2
Total evaluation of the changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm of enamel cementum boundary in experimental group and control group after extraction of impacted wisdom teeth ( $\bar{x}$ $\pm$ $s$ )

Table 3
The changes of alveolar bone width at 1 mm, 4 mm, 7 mm, 10 mm after extraction of wisdom teeth in different age groups ( $\bar{x}$ $\pm$ $s$ )