Efficacy of bone ring grafts for the reconstruction of alveolar ridge deficiencies: A systematic review. Part I: Clinical trials

Abstract

Background:

Bone ring (BR) grafts have been introduced to reconstruct alveolar ridge defects with simultaneous implant placement, but its clinical effectiveness remains undetermined. This systematic review aimed to comprehensively investigate BR grafts in diverse scenarios of ridge defect with simultaneous or staged implant placement.

Methods:

Electronic retrieval of MEDLINE, Embase, Cochrane Library(CENTRAL), Web of Science, Scopus, and citation search until August 3, 2023, was used to identify relevant clinical articles that utilized BR grafts for ridge defect reconstruction. The quality of evidence in the studies reviewed was assessed with the Joanna Briggs Institute Critical Appraisal tool. The protocol was registered in Prospective Register of Systematic Reviews (CRD42023453943).

Results:

Fourteen studies with 251 BRs were identified, of which 8 studies were for alveolar ridge augmentation, 4 studies were for extraction socket augmentation, and 2 studies were for sinus floor elevation. Reported sources of BRs included autografts, allografts, and xenografts. The follow-up period ranged from 4 months to 4.7 years. Regarding the primary outcomes, the utilization of BR grafts demonstrated favorable bone gain along with acceptable graft absorption and marginal bone loss. Regarding the secondary outcomes, satisfactory bone mineral density and implant stability were confirmed, accompanied by a recorded incidence of postoperative complications (20 cases) and an implant failure rate of 5.58%.

Conclusions:

BR grafting with simultaneous or staged implant insertion is an effective approach for reconstructing alveolar ridge deficiencies. The BR grafts demonstrate favorable bone remodeling and osteointegration with the alveolar bone and implant; however, its success may be compromised by complications. Future studies should further investigate the clinical efficacy of BR grafting comparing to other bone augmentation techniques in diverse scenarios.

1. Introduction

Following exodontia, the extraction socket undergoes a series of bone reconstruction processes, leading to a significant reduction dimension.^[1] A systematic review^[2] revealed that within 6 months after tooth loss, horizontal and vertical ridge absorption reached 29% to 63% and 11% to 22%, respectively. These undesirable events complicate the optimal implant positioning and compromise the long-term prognosis.

Alveolar bone augmentation is often necessary to counteract ridge resorption, with the aim of placing the implant in the prosthetic-driven position.^[3] Various treatment modalities have been developed for horizontal/vertical bone augmentation, including guided bone regeneration, onlay/inlay bone grafting, and distraction osteogenesis.^[4] However, overly invasive augmentation procedures often require staged implant placement, resulting in increased discomfort during secondary approaches and prolonged overall treatment duration.^[5]

To this end, Fukuda et al^[6] introduced bone ring (BR) grafts, allowing ring-shape autogenous bone blocks for simultaneous implant placement. The mechanism of this technique is to combine a ring-shape bone scaffold with a primary stability with the mean of a dental implant instead of titanium screws.^[7] The BR grafts can be securely stabilized through implants, ensuring an intimate fit of BR into the defective area (Fig. 1).^[8] Autogenous BR grafts can be harvested from the chin, in situ, or ramus of the mandible. Their dimensions are determined by the diameter of the implant and defect size to ensure adequate primary implant stability.^[9] To avoid the comorbidity of autogenous BR, commercial allogeneic/xenograft BR grafts have also been utilized.^[10] They are prefabricated into several standard dimensions for adapting implants and have good biocompatibility with alveolar bone and implants.

Figure 1.

Diagram of bone ring graft with simultaneous implant placement.

Although several clinical cases have reported the safety and efficacy of this technique in bone augmentation,^[7,11,12] concerns remain regarding the failure of implant osseointegration due to cracked BR and inadequate implant/BR stability.^[10,13] Currently, scientific evidence supporting the application of BR grafts for alveolar ridge reconstruction in humans is scarce, despite a limited number of animal trials providing some crucial evidence.^[14–18]

To our knowledge, no comprehensive systematic review has been conducted to assess clinical outcomes of bone reconstruction using BR grafts, including horizontal and vertical ridge augmentation, socket augmentation, and sinus floor augmentation. Therefore, the objective of this systematic review was to assess the available clinical evidence regarding the utilization of BR grafts for alveolar ridge reconstruction and propose clinical considerations for their implementation. The specific aim of this study was to investigate the bone remodeling and osseointegration performance of BR grafts under different scenarios.

2. Materials and methods

2.1. Protocol and registration

The protocol was elaborated and registered in the International Prospective Register of Systematic Reviews under registration number CRD42023453943. The systematic review was developed and followed according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses statement (2020)^[19] and Assessing the Methodological Quality of Systematic Reviews guidelines.^[20]

2.2. Focus question and PIO criteria

The focus question was developed according to the population, intervention, and outcome: “In patients exhibiting alveolar ridge defects and being in need of reconstruction surgery, what is the efficacy of bone remodeling and osseointegration in procedures utilizing BR grafts?”

Population (P): Participants with alveolar defects requiring ridge reconstruction surgery.

Intervention (I): Ridge reconstruction surgery employing the BR grafts.

Outcomes (O): Primary outcomes (horizontal/vertical ridge gain, graft resorption, marginal bone loss) and secondary outcomes (bone density, implant stability, implant failure, and postoperative complication).

2.3. Search strategy

Two authors (H.L. and M.C.) searched for relevant studies in the MEDLINE (via PubMed), Embase, Cochrane Library (CENTRAL), Web of Science, and Scopus databases by using the search strategy shown in Table 1. Databases were searched from the date of their inception to August 3, 2023. Moreover, the authors independently searched the citations of relevant articles to locate any potentially eligible studies.

Table 1.

The search strategy used for each database.

Databases	Search strategy	Records
MEDLINE (PubMed)	((“bone regeneration”[MeSH Terms] OR (“bone augmentation”[Title/Abstract] OR “ridge augmentation”[Title/Abstract] OR “socket augmentation”[Title/Abstract] OR “sinus augmentation”[Title/Abstract] OR “bone graft”[Title/Abstract])) AND (“bone ring”[Title/Abstract] OR “ring block”[Title/Abstract] OR “ringbone”[Title/Abstract])) AND (humans[Filter])	14
Embase	(“bone regeneration”/exp OR “bone regeneration” OR “bone augmentation”/exp OR “bone augmentation” OR “ridge augmentation” OR “socket augmentation” OR “sinus augmentation”/exp OR “sinus augmentation” OR “bone graft”/exp OR “bone graft”) AND (“bone ring” OR “ring block” OR “ringbone”) AND (“human”/exp OR human OR “clinical trial”/exp OR “clinical trial”) AND “article”/it	21
Web of Science	(“bone regeneration” OR “bone augmentation” OR “ridge augmentation” OR “socket augmentation” OR “sinus augmentation” OR “bone graft”) AND (“bone ring” OR “ring block” OR “ringbone”) AND (human OR “clinical trial”)	27
Scopus	(“bone regeneration” OR “bone augmentation” OR “ridge augmentation” OR “socket augmentation” OR “sinus augmentation” OR “bone graft”) AND (“bone ring” OR “ring block” OR “ringbone”) AND (human OR “clinical trial”) AND (LIMIT-TO (DOCTYPE, “ar”)) AND (LIMIT-TO (LANGUAGE, “English”))	78
Cochrane Library (CENTRAL)	(“bone regeneration” OR “bone augmentation” OR “ridge augmentation” OR “socket augmentation” OR “sinus augmentation” OR “bone graft”) AND (“bone ring” OR “ring block” OR “ringbone”) in Title Abstract Keyword	3

2.4. Selection criteria

The inclusion criteria were as follows: prospective/retrospective case series, cohort studies (CSs), controlled clinical trials (CCTs), randomized clinical trials with a minimum of 4 patients in good general health; at least one of the specific outcome variables were assessed and recorded; studies in which alveolar ridge reconstruction procedures (e.g., horizontal and/or vertical ridge augmentation, extraction socket augmentation, and maxillary sinus floor elevation).

The exclusion criteria were as follows: no outcomes of interest; published in a language other than English; inappropriate study design (i.e., review, protocol, preclinical trial, and conference article); <4 patients; patients with compromised systematic health.

2.5. Data collection

After the initial retrieved publications were identified, 2 independent reviewers (H.L. and M.C.) screened the studies as follows: deleted duplicate studies, read the titles and abstracts, reviewed full texts, and determined eligibility for inclusion.

The following data were extracted from the included studies: author, year of publishing, study design, number of patients, mean year, male/female, characteristics of defects, number of implants, type of surgery, origin of BR grafts, follow-up period, surgery procedure, timing of implant placement, and outcomes were recorded. Then, unmatched information was cross-checked and verified to exclude literature not fulfilling the inclusion criteria.

2.6. Risk of bias in individual studies

Two independent reviewers (X.X. and Z.Y.) evaluated the methodological quality of the eligible studies independently. The quality of case series, CSs, and CCTs was assessed with the standardized Joanna Briggs Institute Critical Appraisal tool, which is divided into 2-categorized question checklists (10-question checklist for case series and 11-question checklists for CSs and CCTs). Each question was responded to with “yes,” “no,” or “unclear.” The criteria for evaluating the risk of bias were as follows: a low risk of bias was indicated when ≥50% of responses were marked as “yes,” a high risk of bias when ≥50% were marked as “no,” and uncertain if ≥50% were marked as “unclear.”

2.7. Data synthesis

Due to the considerable heterogeneity of the included studies in terms of study design, surgical protocols, follow-up time, and outcome variables, quantitative analyses were not feasible. The qualitative evaluation employed descriptive analysis, specifically focusing on alveolar ridge augmentation, extraction socket augmentation, and maxillary sinus elevation achieved through BR grafts.

3. Results

3.1. Inter-reviewer agreement

The inter-reviewer Kappa statistic between the 2 independent reviewers (H.L. and M.C.) was 0.92 for searching and 0.94 for data collection. Moreover, the inter-reviewer Kappa statistic between the 2 independent reviewers (X.X. and Z.Y.) was 0.90 for risk of bias assessment. Therefore, inter-reviewer agreement was considered perfect. The intervention of a third reviewer for consensus purposes was not needed.

3.2. Study selection

The initial database search identified 14 records in MEDLINE via PubMed, 21 in Embase, 27 in Web of Science, and 78 in Scopus, 3 in the Cochrane Library(CENTRAL). The citation search located 5 additional articles.^{[6,8,21–23]} Out of a total of 147 articles, 43 duplicate articles were discarded. After conducting title and abstract screening as well as citation search, the full text of 19 articles was reviewed. Following the exclusion of 5 articles (Table 2), a total of 14 articles were ultimately included for inclusion in this systematic review.^{[6,8,21–35]} Figure 2 illustrates the search and screening process.

Table 2.

Studies excluded after full-text review.

Excluded studies	Reasons for exclusion
Giesenhagen et al[10]	Review
Giesenhagen et al[7]	Insufficient patients
Mehmet et al 2023[24]	Preclinical trial
Zhou et al 2022[25]	Preclinical trial
Sadiq et al 2013[26]	Abstract

Figure 2.

PRISMA (2020) flowchart of the search process. PRISMA = Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

3.3. Study characteristics

The 14 articles included 6 case series,^{[6,22,27–29,32]} 3 retrospective CSs,^[8,23,30] 3 prospective CSs,^[21,34,35] and 2 CCTs.^[31,33] All studies were published between 2000 and 2023, and the mean follow-up period ranged from 4 months to 3.1 years. The types of alveolar ridge reconstruction using BR grafts included horizontal and/or vertical alveolar ridge augmentation,^{[6,8,27–32]} extraction socket augmentation,^[21,33–35] and sinus floor elevation.^[22,23] A total of 195 patients with 203 sites received BR grafts. Tables 3 and 4 provides critical information about the included studies.

Table 3.

Characteristics of clinical studies employing BR grafts.

Author	Study design	No. of patients (mean year; M/F)	Characteristics of defects	No. of implants	Type of surgery	Origin of BRs	Follow-up period	Surgery procedure	Timing of implant placement
(a) Alveolar ridge augmentation
El Chaar et al[27]	Retrospective case series	8 (61.6; 4/4)	Siebert class II and III ridge deficiency, ≥4 mm apical to the native bone, and ≥1 mm of interproximal bone	8	Horizontal and vertical augmentation	Allograft	7 mo	BR grafts, gap with particulate allograft, covering with 2 collagen resorbable membranes	Simultaneously
Chen et al[28]	Retrospective case series	15 (35; 9/6)	Single central maxillary incisor loss with 2–3 wall defects	15	Horizontal and vertical augmentation	Autogenous (10 in situ and 5 from the chin)	4 mo–3 y	BR grafts, bovine bone substitute, covering with resorbable collagen membrane	Simultaneously
Ding et al[8]	Retrospective cohort study	11 (49.91 ± 12.95; 8/3), 12 augmented sites	Class III–IV alveolar ridge defects	12	Horizontal augmentation	Xenograft	12 mo	BR grafts, bovine bone substitute, covering with resorbable collagen membrane	Simultaneously
Fukuda et al[6]	Case series	9	Insufficient alveolar bone height in the anterior maxilla	14	Vertical augmentation	Autogenous (from the chin)	3.1 y (1.5–4.7)	BR grafts with cancellous bone chips	Simultaneously
Flanagan[29]	Case series	8	Single tooth partial edentulism with atrophic facial cortices	8	Horizontal and vertical augmentation	Allograft	4 mo	BR grafts, 50–50 mix of particulate allograft and calcium sulfate, covering with collagen membrane	Simultaneously
Nord et al[30]	Retrospective cohort study	51 (58.8 ± 11.7; 21/30)	Vertical bone defects (54 in maxilla, 27 in mandible)	81	10 cases were extraction augmentation; 41 cases were vertical augmentation	Allograft	12 mo	BR grafts, mixture of autologous bone particles and bovine bone graft particles, coving with porcine pericardium barrier membrane	Simultaneously
Wychowanski et al[31]	Clinical controlled trial	Test: 15 Control: 15	Vertical bone defects (premolar or molar area in the mandible)	Test: 30 Control: 30	Vertical augmentation	Autogenous (from the chin)	24 mo	Test: BR grafts, xenograft, covering collagen membrane Control: Tunnel xenograft	Test: Simultaneously Control: Staged
Yawale et al[32]	Case series	15	Siebert class II and/or class III defects	16	Horizontal and vertical augmentation	Autogenous (in situ)	6 mo	BR grafts, osseograft particles, covering a barrier membrane	Simultaneously
(b) Extraction socket augmentation
Chandra et al[33]	Controlled clinical trial	34 (32.60 ± 10.22; 17/17) Test: 17 1 patient lost, 2 sites osseintegration failed Control: 17 1 site lacked implant primary stability	Single incisor or premolar in a type II socket	Test: 14 Control: 16	Horizontal and vertical socket augmentation	Autogenous (from the chin)	12 mo	Test: BR grafts, autogenous bone particles Control: sticky bone with a membrane	Staged
Giraddi and Saifi[21]	Prospective cohort study	14 patients (30.35 ± 7.13; 7/7) 15 augmented sites	7 in maxilla, 8 in mandible	15	Vertical socket augmentation	Autogenous (from the chin)	15 mo	BR grafts, autogenous spongious bone, covering with PRF membrane	Simultaneously
Omara et al[34]	Prospective cohort study	10 patients (31; 6/4) 12 augmented sites	Severe buccal defects in the mandibular premolar molar region	12	Horizontal socket augmentation	Autogenous (from the chin)	6 mo	BR grafts	Simultaneously
Yuce et al[35]	Prospective cohort study	8 patients (42.63; 3/5) 12 augmented sites	Maxillary anterior region	12	Horizontal and vertical socket augmentation	Autogenous BRs from the chin	18 mo	BR grafts	Simultaneously
(c) Sinus floor elevation
Rizzo et al[22]	Case series	4 (62; 1/3)	Extremely resorbed bone crests (≤3 mm)	4	Vertical sinus augmentation	Allograft	—	BR grafts, covering a resorbable membrane	Simultaneously
Sindel et al[23]	Retrospective cohort study	10 (57.8; 6/4)	Severe alveolar ridge atrophy with Schneiderian membrane perforation	10	Vertical sinus augmentation	Autogenous (from the chin)	24.3 mo	BR grafts	Simultaneously

BR = bone ring, M/F = male/female.

Table 4.

Methodological quality of case series by means of the JBI.

Author	Outcome reported
	Primary	Secondary
(a) Alveolar ridge augmentation
El Chaar et al[27]	• Marginal bone loss: 7 mo: mesial: 0.26 ± 0.52 mm, distal: 0 mm, average: 0.13 ± 0.38 mm 16.13 mo: mesial: 0.31 ± 0.55 mm, distal: 0.14 ± 0.21 mm, average: 0.22 ± 0.39 mm	• Implant failure: 0 • Postoperative complications: 0
Chen et al[28]	• Ridge width gain (4 mo): 4.73 ± 0.7 mm (P < .05) • Ridge height gain (4 mo): 5.55 ± 0.87 mm (P < .05) • Horizontal graft resorption: 4 mo: 1.66 ± 2.85 mm; 1 y: 2.44 ± 2.85 mm; 2 y: 2.69 ± 2.77 mm; 3 y: 2.72 ± 3.18 mm (P < .05)	• Implant failure: 0 • Postoperative complications: 1 BR exposed
Ding et al[8]	Ridge width gain (12 mo): 0 mm plane: 1.95 ± 0.19 mm; 1 mm plane: 2.39 ± 0.38 mm; 2 mm plane: 2.91 ± 0.56 mm; 3 mm plane: 3.28 ± 0.63 mm Marginal bone loss (12 mo): buccal: 1.46 ± 0.38 mm Horizontal graft resorption (12 mo): 0 mm plane: 0.45 ± 0.28 mm (17.78 ± 9.03%); 1 mm plane: 0.41 ± 0.36 mm (13.86 ± 10.55%); 2 mm plane: 0.43 ± 0.31 mm (13.02 ± 8.85%); 3 mm plane: 0.48 ± 0.31 mm (12.96 ± 8.36%)	Implant failure: 0 Postoperative complications: 1 fracture of the wound
Fukuda et al[6]		• Implant failure: 0 • Postoperative complications: 1 exposed chin bone necrosed
Flanagan[29]		• Implant failure: 0 • Postoperative complications: 0
Nord et al[30]	• Vertical graft resorption: 6 wk: 5.6% ± 9.7%; 6 mo: 8.0% ± 11.8%; 12 mo: 8.6% ± 8.3%	• Implant failure: 5 • Postoperative complications: 3 periimplant bone loss 2–3 mm
Wychowanski et al[31]	• Ridge height gain: Test: 4.3 ± 1.3 mm Control: 4.4 ± 1.5 mm	• Implant stability (PTV): Primary: Test: −3.2 ± 1.3 Control: −1.2 ± 1.6 24 mo: Test: −3.7 ± 1.1 Control: −3.6 ± 1.2 • Implant failure: Test: 4 Control: 1 • Postoperative complications: Test: 3 poor healing Control: 0
Yawale et al[32]	• Marginal bone loss: 3 mo: mesial: 0.70 ± 0.06 mm, distal: 1.22 ± 0.16 mm 6 mo: mesial: 0.69 ± 0.07 mm, distal: 1.14 ± 0.13 mm	• Implant failure: 1 • Postoperative complications: 0
(b) Extraction socket augmentation
Chandra et al[33]	• Ridge height gain (6 mo): Buccal plate: Test: 3.09 ± 1.6 mm Control: 1.90 ± 0.94 mm (P < .01) Palatal/lingual plate: Test: 3.31 ± 2.66 mm Control: 1.99 ± 1.22 mm (P < .01)	• Bone density (HU, 6 mo): Test: 659.6 ± 133.8 Control: 552.1 ± 65.6 (P = .042) • Implant stability (ISQ, 6 mo): Test: 61.60 ± 8.9 Control: 45.02 ± 6.33 (P = .034) • Implant failure: Test: 2 Control: 0 • Postoperative complications: Test: 3 soft tissue dehiscence, 3 pain and swelling Control: 1 soft tissue dehiscence, 3 pain and swelling
Giraddi and Saifi[21]	• Ridge width gain (9 mo): Mesial: 3.70 ± 1.10 mm, distal: 3.69 ± 1.10 mm • Marginal bone loss: 6 mo: mesial: 0.67 ± 0.34 mm, distal: 0.64 ± 0.21 mm 9 mo: mesial: 0.76 ± 0.38 mm, distal: 0.78 ± 0.23 mm	• Implant failure: 1 • Postoperative complications: 1 soft tissue dehiscence
Omara et al[34]	• Marginal bone loss: 6 mo: 0.26 ± 0.87 mm (P = .321) • Vertical graft resorption: 6 mo: 0.26 ± 0.87 mm (1.89% ± 6.41%) (P = .328)	• Bone density (HU, 6 mo): Ring-implant interface: mesial: 393.21 ± 421.52 (P = .008), distal: 282.60 ± 457.48 (P = .056), buccal: 429.69 ± 571.12 (P = .024), lingual: 263.86 ± 505.57 (P = .098); Ring-alveolus interface: mesial: 420.43 ± 360.66 (P = .002), distal: 325.28 ± 272.45 (P = .002) • Implant failure: 0 • Postoperative complications: 2 transient numbness of the lower lip, 1 cracked BR
Yuce et al[35]		• Implant failure: 0 • Postoperative complications: 1 BR infection
(c) Sinus floor elevation
Rizzo et al[22]		• Implant failure: 0 • Postoperative complications: 0
Sindel et al[23]	• Marginal bone loss (5 implants): 2.4 ± 0.49 mm	• Implant failure: 1 • Postoperative complications: 1 soft tissue dehiscence

BR = bone ring, Hu = Hounsfield Unit, ISQ = implant stability quotient, PTV = Periotest value.

3.4. Risk of bias

According to the Joanna Briggs Institute, 3 case series^[27,28,32] exhibited a low risk of bias, 2^[6,29] exhibited an uncertain risk of bias, and 1^[22] exhibited a high risk of bias. Four CSs^[8,21,30,34] and 2 CCTs^[31,33] indicated a low risk of bias, while 2 CSs^[23,35] indicated an uncertain risk of bias (Tables 5 and 6).

Table 5.

Methodological quality of case series by means of the JBI.

	El Chaar et al[24]	Chen et al[25]	Fukuda et al[6]	Flanagan[26]	Yawale et al[29]	Rizzo et al[22]
Were there clear criteria for inclusion in the case series?	Y	Y	N	N	Y	N
Was the condition measured in a standard, reliable way for all participants included in the case series?	Y	Y	N	?	Y	?
Were valid methods used for identification of the condition for all participants included in the case series?	Y	Y	?	?	Y	N
Did the case series have consecutive inclusion of participants?	?	?	?	?	?	N
Did the case series have complete inclusion of participants?	Y	?	?	?	?	N
Was there clear reporting of the demographics of the participants in the study?	Y	Y	N	N	N	Y
Was there clear reporting of clinical information of the participants?	?	Y	?	?	Y	Y
Were the outcomes or follow up results of cases clearly reported?	Y	Y	Y	Y	Y	Y
Was there clear reporting of the presenting site(s)/clinic(s) demographic information?	Y	Y	N	N	N	N
Was statistical analysis appropriate?	Y	Y	?	?	Y	?
Overall appraisal	Low	Low	Uncertain	Uncertain	Low	High

? = unclear or not applicable, JBI = Joanna Briggs Institute Critical Appraisal tool, N = no, Y = yes.

Table 6.

Methodological quality of CSs and CCTs by means of the JBI.

	Ding et al[8]	Nord et al[27]	Wychowanski et al[28]	Chandra et al[30]	Giraddi and Saifi[21]	Omara et al[31]	Yuce et al[32]	Sindel et al[23]
Were the 2 groups similar and recruited from the same population?	N	N	Y	Y	N	N	N	N
Were the exposures measured similarly to assign people to both exposed and unexposed groups?	N	N	Y	Y	N	N	N	N
Was the exposure measured in a valid and reliable way?	Y	Y	Y	Y	Y	Y	Y	Y
Were confounding factors identified?	?	?	?	?	?	?	?	?
Were strategies to deal with confounding factors stated?	?	?	?	?	?	?	?	?
Were the groups/participants free of the outcome at the start of the study (or at the moment of exposure)?	Y	Y	Y	Y	Y	Y	Y	Y
Were the outcomes measured in a valid and reliable way?	Y	Y	Y	Y	Y	Y	?	Y
Was the follow-up time reported and sufficient to be long enough for outcomes to occur?	Y	Y	Y	Y	Y	Y	Y	Y
Was follow up complete, and if not, were the reasons to loss to follow up described and explored?	Y	Y	Y	Y	Y	Y	Y	Y
Were strategies to address incomplete follow-up utilized?	?	?	?	Y	?	?	?	?
Was appropriate statistical analysis used?	Y	Y	N	Y	Y	Y	N	N
Overall appraisal	Low	Low	Low	Low	Low	Low	Uncertain	Uncertain

? = unclear or not applicable, CCTs = controlled clinical trials, CSs = cohort studies, JBI = Joanna Briggs Institute Critical Appraisal tool, N = no, Y = yes.

3.5. Characteristics of BR grafts

The origins of BR grafts included autograft, allograft, and xenograft. The autogenous BR was harvested from the chin bone and in situ. The allogeneic and xenogeneic BRs were commercial prefabricated products. The inner and outer diameters of these BRs usually respond to the implant’s diameter and the recipient site’s shape, respectively.

3.6. Characteristics of surgical interventions and treatment outcomes

3.6.1. Alveolar ridge augmentation.

In 7 single-CSs, alveolar ridge augmentation (4 for horizontal and vertical and 2 for vertical) was performed using autogenous BRs (3 studies, 39 patients), allogeneic BRs (3 studies, 57 patients), and xenogeneic BRs (1 study, 11 patients). The follow-up period ranged from 4 months to 4 years.

Only 1 comparative study evaluated simultaneous implantation of autogenous BRs with collagen membrane (15 patients, 30 implants) versus staged implantation of tunnel techniques (15 patients, 30 implants) for vertical ridge augmentation.

3.6.1.1. Primary outcomes.

The average increase in alveolar ridge width was 4.73 ± 0.7 mm,^[28] while alveolar ridge height was 4.3 ± 1.3 mm^[31] and 5.55 ± 0.87 mm^[28] using BR grafts, which exhibited a significant augmentation compared to the initial ridge size (P < .05). Ding et al^[8] reported that the ridge width gain at 0, 1, 2, and 3 mm planes after a 12-month follow-up period was 1.95 ± 0.19, 2.39 ± 0.38, 2.91 ± 0.56, and 3.28 ± 0.63 mm, respectively. The mean marginal bone loss (MBL) around the implant using BR grafts exhibited variations across multiple angles and time points.^[8,27,32] The horizontal graft resorption was 1.66 ± 2.85, 2.44 ± 2.85, 2.69 ± 2.77, and 2.72 ± 3.18 mm at 4 months, 1 year, 2 years, and 3 years, respectively.^[28] The vertical graft resorption rate was 5.6% ± 9.7%, 8.0% ± 11.8%, and 8.6% ± 8.3% at 6 weeks, 6 months, and 12 months, respectively.^[30]

3.6.1.2. Secondary outcomes.

A total of 5 implants were reported failure during follow-up, giving an overall failure rate of 5.49%, of which the data from Nord et al^[30] were not counted due to different types of recipient sites. BR exposure, donor site necrosis, and poor healing of the recipient site were found to be postoperative complications, with an overall incidence of 7.14%. The mean primary implant stability (Periotest value) was −3.2 ± 1.3, and the 24-month implant stability was −3.7 ± 1.1.^[31]

3.6.2. Extraction socket augmentation.

For extraction sockets, BR grafts were used to either reconstruct buccal dehiscence type defects or to augment insufficient ridge height. In 3 prospective single-CSs, bone augmentation of vertical socket defects (14 patients, 15 implants)^[21] and horizontal and vertical socket defects (18 patients, 24 implants) was performed using autogenous BRs.^[34,35] The implants were nested within the BRs and placed in the extraction socket, ranging from 6 to 18 months follow-up.

A comparative study^[33] evaluated the use of autogenous BRs (14 patients, 14 implants) versus sticky bone with membrane (16 patients, 16 implants) for socket augmentation with staged implant placement.

3.6.2.1. Primary outcomes.

The mean ridge width gain was 3.7 ± 1.1 and 3.69 ± 1.1 mm in the mesial and distal, respectively.^[21] The mean increase of ridge height in the buccal and palatal/lingual was 3.09 ± 1.6 and 3.31 ± 2.66 mm, respectively,^[33] which was significantly higher than that in the control group (P < .05). The vertical graft absorption/rate was 0.26 ± 0.87 mm and 1.89 ± 6.41% at 6 months.^[34] The mean MBL was 0.26 ± 0.87 mm at 6 months and 0.76 ± 0.38 and 0.78 ± 0.23 mm at 9 months.^[21]

3.6.2.2. Secondary outcomes.

A total of 3 implants were reported failure during follow-up, with an overall failure rate of 5.7%. Postoperative complications included soft tissue dehiscence (4), transient numbness of the lower lip (2), pain and swelling (3), BR crack (1), and BR infection (1), with an incidence of 20.7%. Bone density was significantly higher at both the ring-implant interface and the ring-alveolar interface than immediately after grafting (P < .05).^[34] Compared with the control group (552.1 ± 65.6 Hounsfield units), bone density in the BR group (659.6 ± 133.8 Hounsfield units) increased significantly (P = .042). In terms of implant stability, the implant stability quotient (ISQ) of the BR group was 61.60 ± 8.9 after 6 months, which was higher than 45.02 ± 6.33 in the control group (P < .05).^[33]

3.6.3. Sinus floor elevation.

Two single-CSs employed BR grafts to augment the height of severely atrophic maxillary posterior areas via a lateral window approach with different surgical protocols. Rizzo et al^[22] obtained the fresh mineralized, frozen, homologous BR grafts using trephine burs, which were subsequently attached to the implant neck in vitro and then grafted into the recipient area with a covering resorbable membrane (4 patients, 4 implants). Sindel et al^[23] harvested BR grafts from the chin and placed them at the base of the maxillary sinus. The BR grafts inside the sinus cavity were locked to both the implant apex and alveolar crest by leveraging rotational forces of the implant insertion (10 patients, 10 implants).

3.6.3.1. Primary outcomes.

The mean MBL of 5 implants calculated by Sindel et al^[23] was 2.4 ± 0.49 mm, and the other 5 implants were not evaluated.

3.6.3.2. Secondary outcomes.

One implant failure and 1 postoperative complication of soft tissue dehiscence and crest resorption were reported by Sindel et al.^[23]

4. Discussion

4.1. Summary of evidence

This present review investigated the clinical efficacy of BR grafts in ridge dimension change, BMD, implant prognosis, and postoperative complications in the case of alveolar ridge augmentation, extraction socket augmentation, and sinus floor elevation. The findings demonstrated a favorable impact of BR grafts on bone remodeling and periimplant osseointegration during simultaneous implant placement under various bone augmentation procedures.

Autogenous BRs harvested from the chin were initially considered due to their osteogenic, osteoinductive, and osteoconductive capabilities. However, some disadvantages occurred, including prolonged operative time, secondary surgery for the donor site, and neurosensory disturbances.^[36] A more favorable alternative is in situ BRs collected from the apical area of the implant bed. Nevertheless, the chin can still be considered if there is insufficient bone volume in situ.^[28] In cases where partial edentulism requires a larger volume of BR grafts, prefabricated allogeneic or xenogeneic BR grafts made of cylindrical blocks cut by presized trephines may serve as an alternate approach.^[29] These BR grafts support periimplant osteogenic space without posing a physical barrier to rapidly in growing local vessels.^[34]

During the initial healing phase, achieving revascularization and bone increment is crucial for the stability of both the implant and BR graft.^[13,27] The stability of the BR graft relies on precise fit with the inner diameter of the implant and the outer diameter of the recipient site. Meanwhile, an apical native bone length of 3 to 4 mm ensures stability for the implant.^[7,27] Additionally, El Chaar et al^[27] suggested maintaining at least 1 mm of periimplant interproximal bone adjacent to teeth to promote blood supply and preserve papilla.

A retrospective cohort study^[8] evaluated the effectiveness of xenogeneic BR grafts for horizontal ridge augmentation and simultaneous implant placement. Radiological outcomes based on 4 parallel planes below the implant neck platform demonstrated good stability and spatial support performance of the xenograft BRs, resulting in a bone width of at least 1.5 and <1 mm horizontal absorption. This result was analogous to that of Chen et al,^[28] who reported stable bone width change 1 year after surgery with an average horizontal bone gain of 4.73 ± 0.7 mm. Similar encouraging results were also observed in extraction socket augmentation surgery, where the mesial side yielded 3.7 ± 1.1 mm and the distal side yielded 3.69 ± 1.1 mm.^[21] Compared to horizontal ridge defects, 2-to 3-wall ridge defects of the extraction socket provided better anchoring for BR due to its partially profiled fit with the socket wall.^[28]

In the context of reconstructing Siebert class II or class III defects, the utilization of BR grafts resulted in a significant increase in vertical defect height, ranging from 3.0 to 6.42 mm. A systematic review also reported similar findings, with a vertical bone gain of approximately 4 mm.^[9] Notably, the majority of these results were attributed to the combined influence of BR graft and implant. Nevertheless, Chandra et al^[33] conducted an evaluation on the efficacy of 6-month healing with BR grafts alone and found that both buccal (3.09 ± 1.6 mm) and lingual/palatal bones (3.31 ± 0.66 mm) exhibited significantly greater height compared to the control group using sticky bone and barrier membranes. Based on available evidence, BR grafts with simultaneous or staged implant placement can be expected to augment ridge volume; however, adopting a simultaneous protocol may reduce overall treatment duration, as demonstrated by animal studies from Nakahara et al.^[17,18]

The absorption of BR grafts influences the ultimate bone gain. The observed horizontal and vertical absorption patterns of BR grafts in the reviewed studies generally aligned with previously reported values for autograft, allograft, and xenograft materials.^[8,30,34] Factors such as the structure of BRs, utilization of collagen membranes, and supplementation with graft particles may contribute to some of the differences.

In studies involving ridge augmentation surgery, the mean MBL at the implant sites increased over time; however, there was a specific variation in the data across different studies.^[8,27,32] This variability could be attributed to autogenous, allogeneic, and xenogeneic grafts exhibiting differences in degradation rate and bone formation.^[37] In our study, the mean MBL in the mesial, distal, and buccal sites was found to be <1.5 mm, which is higher compared to the 0.57 mm reported by Saez-Alcaide et al.^[9] However, it should be noted that his study only included data from 2 studies, limiting the ability to conclusively argue for the superiority of BR grafts over other GBR procedures.

In cases of maxillary posterior region atrophy, implant placement typically necessitates sinus floor elevation techniques (via lateral window or transalveolar approach) to enhance vertical bone volume.^[38] However, when severely resorbed crest (≤3 mm) or perforated Schneiderian membrane (>5 mm), the intricacy and risk of failure associated with bone grafting surgery are considerably high. Rizzo et al^[22] and Sindel et al^[23] employed BR grafts to devise creative methodologies enabling simultaneous implant placement during sinus floor lifting. The former approach briefly involved anchoring the implant to the BR in vitro and grafting them into a preprepared annular receiver area of the bone crest. In contrast, the latter method relied on locking the implant to both BRs of the alveolar crest and sinus cavity through interacting rotational forces. Notably, Sindel et al^[23] proposed an innovative solution for addressing extensive Schneider membrane perforation during inoperable bone increment surgery by utilizing an implant apex to secure support for a BR graft inside the sinus.

The results from both studies^[33,34] on bone density measurements demonstrated a statistical increase, indicating favorable angiogenesis and osteointegration at the interfaces between the ring-implant and ring-alveolus. It suggested that the structural BR as an osteoconductive scaffold for vascular and cellular ingrowth maintained a stable profile for continuous remodeling and adequate mineralization.^[33] Understandably, BR grafts exhibited significantly improved implant stability, with values comparable to those obtained for autografts by Ribeiro et al^[39] (ISQ = 57.9 ± 9.46). Additionally, their study found reliable evidence of implant stability with allografts (ISQ = 58.5 ± 5.76), providing valuable insights into the role of allogeneic BRs in enhancing implant stability.^[39]

Complications observed in the included studies following autogenous/allogenic BR grafting encompassed BR exposure/infection/cracked, donor osteonecrosis, soft tissue dehiscence, poor healing, wound pain/swelling, and temporary numbness of the lower lip. These complications have also been documented in prior investigations on onlay bone grafts,^[4,40] wherein high-risk factors for graft failure include exposure, infection, or cracking of grafts. Notably, the presence of soft tissue dehiscence and poor healing increases the susceptibility to infection during BR healing. Several crucial measures can potentially mitigate the occurrence of postoperative complications, including utilization of static navigation guidance,^[11,27] smoothing the sharp edges of the BR graft,^[10,28] and employing tension-free suture.^[10,28] Interestingly, in Chandra et al’s study,^[33] certain signs and symptoms such as pain and swelling, which are inherent in bone augmentation surgery, have been considered as complications. It is reasonable to include the severity of symptoms and signs like pain and swelling in postoperative complication statistics only if they significantly impact the patient’s quality of life or clinical outcomes.

During a follow-up period ranging from 4 months to 4.7 years, the failure rate of BR grafts was 5.58%, which aligned with the findings reported by Saez-Alcaide et al’s^[9] systematic review (5.03%). Intraoperative fracture of the BR is a significant concern due to the implant rotational insertion through the BR. To mitigate this risk, it is recommended to maintain a periimplant width of at least 1.5 mm or utilize tapping drills solely for providing a central osteotomy site of minimal difference to the implant diameter.^[34] In this sense, the absence of a standardized protocol concerning the preparation and transplantation of BR heightens the potential for intraoperative and postoperative adverse events to occur.

4.2. Limitations and further suggestions

Most studies on BR grafts primarily focus on providing data related to the amount of bone gain and implant success, while there is a scarcity of histomorphologic data concerning BR grafts with alveolar bone and implants. The high complication rate associated with BR grafts is only briefly mentioned without detailed analysis; few studies conduct an in-depth assessment of patient-reported outcomes. Providing histological and histomorphometric evidence, as well as exploring the interpretation, treatment, and prevention of complications, would be valuable for future research endeavors.

Despite the promising outcomes of BR grafts in alveolar ridge reconstruction, few studies have compared BR with other bone augmentation procedures, and the studies that have been published lack homogeneous surgical protocol and adequate follow-up period. The assessment of participants and confounding factors in the included studies is subject to uncertainty, which introduces a potential source of bias in the results. Consequently, there is insufficient evidence to draw firm conclusions as to the long-term predictability and superiority of BR grafts over alternative methods. The provision of well-designed controlled trials and homogeneous protocol of BR grafting would be useful in assessing the efficacy of BR grafting for bone remodeling and osseointegration.

5. Conclusions

BR grafting with simultaneous or staged implant placement is an effective method for reconstructing alveolar ridge defects. Stable bone gain and less graft resorption can be anticipated, but some of postoperative complications lead to the implant failure and so should be approached with care both in treatment protocol, paying patient characteristics due attention, and during the BR grafting procedure itself.

Many of the clinical studies on BR grafts focus on the clinical success of bone remodeling and osteointegration and do not compare them to conventional bone augmentation techniques. Further studies should compare the outcomes of the BR grafting with other bone augmentation techniques in various clinical scenarios and by doing so obtain comprehensive information to support its application in clinical practice.

Acknowledgments

The authors are thankful to Mr. Lang Xin for help with the methodological evaluation.

Author contributions

Methodology: Ruiming Zhao, Yi Wang.

Writing—original draft: Ruiming Zhao, Yi Wang, Jiaming Gong.

Data curation: Huijing Lin, Min Cao.

Formal analysis: Huijing Lin, Min Cao.

Validation: Xu Xu, Zhenfei Yuan.

Visualization: Xu Xu, Zhenfei Yuan.

Writing—review & editing: Jiaming Gong.