Introduction

The alveolar ridge resorption can restrict dental implant placement [1]. Usually, the bone resorption occurs as a consequence of tooth loss, trauma, and pathologies [2]. Therefore, augmentation procedures are performed to provide adequate bone volume for dental implant placement [3]. Residual alveolar ridges according to the main resorbed region are classified as horizontal, vertical, or combined defects. This classification guides the surgeon to the adequate diagnosis and support the treatment decision [4]. Different techniques are available to reconstruct and/or regenerate atrophic alveolar ridges, including ridge split crest, bone block graft, biomaterials, distraction osteogenesis, and guided bone regeneration [5,6,7,8,9,10,11].

The autogenous bone is the gold standard for graft procedures due to osteogenesis, osteoinduction, and osteoconduction features. It is used as a block and/or particulate graft [6, 12, 13]. However, the autogenous grafts have some disadvantages including: requirement of a donor site, high morbidity, potential graft resorption, and difficulty to adaptation. Therefore, alternative bone materials from different origins are available, represented by allogenic bone graft (derived from human cadavers), xenogenous bone graft (derived from other animal species), and bone graft substitutes (completely synthetic) [14,15,16].

The xenogenous bone is used for alveolar ridge augmentation with reliable results, low morbidity, and decreased complication rate [14, 17, 18]. Also, they show a good long-term stability due to the slow resorption characteristic [19]. It is important to highlight that any bone substitute material has osteoinductive feature similar to autogenous bone. Actually, the bone substitute materials support the bone healing process by the osteoconductive characteristic [16, 18,19,20]. Furthermore, the efficiency of bone substitute materials in augmentation procedures is proved in many studies [17, 19, 21].

The aim of this study was to perform a systematic review of literature on horizontal ridge augmentation using xenogenous bone graft for dental implant placement, to evaluate the bone gain, graft resorption, complication rate, and success.

Materials and methods

This systematic review was directed in accordance for the PRISMA statement (Preferred Reporting Items for Systematic Review and Meta-Analysis) [22], and aimed to answer the following question: In implant patients, treated with xenografts for horizontal ridge augmentation, what would be the outcomes in terms of bone gain, bone resorption, implant survival, and complication rates?

Search strategy and selection criteria

The search strategy was performed in MEDLINE (Medical Literature Analysis and Retrieval System Online, via PubMed), ELSEVIER (via Scopus), and Cochrane Library databases. All possible combinations of the following descriptors were searched: “xenograft,” “Xenogenous,” “bone augmentation,” “bone reconstruction,” “bone particulate,” “bone block,” “bone augmentation,” “bone reconstruction,” “bone particulate,” “bone block,” “lateral augmentation,” “ridge augmentation,” and “horizontal augmentation”.

Three independent reviewers (GC, GST, LBM) analyzed titles and/or abstracts according to the following inclusion criteria: specific studies that evaluated horizontal ridge augmentation using xenogenous bone grafts, studies on humans, reported in the English language, no time restriction regarding to publication date, and study types: case series, retrospective, or prospective clinical trials. The inclusion criteria were broad to bring general results. Technical variations, use of membranes, or type of prosthetic rehabilitation were not considered. Furthermore, bone grafts used in sinus lift procedure or vertical augmentation were not included on this study.

After the initial selection, the researchers evaluated the full-text of the selected articles according to the same inclusion criteria to define the final included studies. Any disagreements between the reviewers were settled by additional discussion.

Data extraction

Data from the included studies was extracted by the reviewers, including the following variables: type of study; augmentation procedure (bone block and/or particulate graft, xenogenous or xenogenous-autogenous mixture); number of patients, age, and gender; number of bone grafts; anatomic region of augmentation; horizontal bone gain; resorption rate; complications; implant viability; and success rate. Again, disagreements between reviewers were solved by further discussion. Data were analyzed by descriptive statistics and horizontal bone gain was evaluated by the confidence interval (95%) from the data.

Quality evaluation

All included studies were evaluated using the PRISMA statement [22] criteria to define the scientific evidence for the clinical decision-making process. This evaluation classifies the potential risk of bias of each study, analyzing the following criteria: random sample selection, definition of inclusion and/or exclusion criteria, report of losses to follow-up, validated measurements obtained, and statistical analysis. Studies meeting all criteria were classified as low risk of bias, those that did not meet one of the criteria were classified as moderate risk of bias, and those that did not meet two or more criteria were classified as high risk of bias.

Results

The electronic search was performed by two authors (GC and GST) in March 04, 2017 resulting in 2160 articles. After duplicate removal and the reading of titles and/or abstracts, 69 articles were selected. The full-text of all the selected articles was reviewed for the inclusion criteria. Thus, 37 articles did not meet one or more inclusion criteria in title and/or abstract, and three articles were excluded after full reading. Therefore, 29 articles were included in the final selection. A flowchart of the selection and inclusion process is present in Fig. 1.

Fig. 1
figure 1

Flowchart of systematic review process, according to the PRISMA statement

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All the included articles ranged between 2001 and 2017. Among them, 18 studies were prospective, 10 were retrospective, one was case-control, and one was case series. Table 1 shows the quality assessment and bias risk of the selected papers.

Table 1 PRISMA quality assessment of bias from selected papers
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Table 2 presents the extracted data for each reviewed article. The mean of horizontal bone gain was 4.44 mm, ranging from 0.11 to 7.72 mm (Fig. 2). In contrast, 18 studies reported resorption data, in millimeters and/or percentage. The means of resorption rate were 1.29 ± 1.11 mm and 24.4 ± 11.04%. The complication rate was 7.95%, and membrane exposure was the most frequent reported one. Furthermore, the achieved horizontal volume allowed implant placement with a success in 96.93% of the cases.

Table 2 Data extraction of included papers after full reading screening
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Fig. 2
figure 2

Horizontal bone gain (in millimeters), 95%CI according to available data

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Discussion

This study aimed to aggregate qualified scientific information about horizontal ridge augmentation using xenogenous bone grafts to clarify and discuss its advantages, indications, and complications. In total, 610 patients were submitted to 853 augmentation procedures, involving both the maxilla and mandible. The xenogenous bone grafts were used in different forms, 73.0% of studies used xenografts as particulate graft, alone or associated with autogenous bone. Furthermore, usually, the grafts were covered by a membrane. Most of the studies used absorbable membrane [2, 14, 23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40], and few studies used titanium mesh [41,42,43]. Moreover, two studies applied a fibrin sealant—containing fibrinogen, aprotinin, and thrombin—to the grafted area [44, 45]. The application of barriers probably decreases the resorption rates, but the type is not relevant for bone gain [3, 7, 10, 23, 24, 29].

This systematic review was not limited to clinical trials to achieve more data about the use of xenografts. Thus, it was observed that particulate xenograft was the most frequently used, followed by the mixture between autogenous and xenogenous particulate grafts.

Some disadvantages of autogenous bone such as high rates of resorption, harvesting surgery morbidity, and limited amount of volume, stimulated researchers to investigate about bone material substitutes as feasible alternatives [46,47,48]. Furthermore, most of the studies are from the last 10 years, revealing that this subject is recent and there is a lack of absolute information. The autogenous graft seems to have a significant higher resorption rates when compared with xenografts. In our review, the average resorption for xenografts was 24.4%, while the literature report average resorption rates varying from 10 to 49% for autogenous bone grafts [14, 49,50,51,52].

Regarding complications, 13 studies did not report any type [1, 2, 26, 28, 30, 31, 33, 36, 37, 40, 42, 53]. On the other hand, the remaining studies demonstrate dehiscence as the most common complications, however not leading to major problems. Another common complication was membrane exposure with no need of surgical interventions. However, seven studies reported graft infection, failure, and need re-operation.

Horizontal augmentation procedures using xenografts are feasible, presenting significant bone gain and low rates of complications. Esposito et al. [18] published a systematic review evaluating the efficacy of both horizontal and vertical augmentation procedures. However, they found few evidences about horizontal augmentation, with only one clinical trial. In our review, 18 studies were prospective and seven of them presented low risk of bias.

Wessing et al. (2018) [54] published a similar review; however, they have considered any kind of grafts, as fresh frozen bone grafts, autogenous grafts, or xenografts. Beyond our analysis considered only graft procedures with presence of anorganic bone materials, we found a similar treatment success rate, 99.13% (CI, 97.23–99.96) in the Wessing et al. study and 96.43% (CI, 95.43–97.43) in our study.

According to the reviewed studies, xenogenous graft provides proper amount of bone augmentation in thickness (mean 4.44 mm), and high rates of success for implant placement. Just one study presented lower success for implant placement (64%) [14]. However, this study was the only one that used bone blocks from equines and showed 50% of graft loss, which is not reported in any other study [14].

The highest thickness gain was shown by Urban et al. [37] and Gultekin et al. [30], both using a combination of autogenous and xenogenous particulate grafts. These findings agree with the hypothesis that anorganic xenogenous graft could slow the resorption of autogenous bone [7, 25, 30] increasing the volume to the grafted area [1, 2, 27, 52].

The study with the greatest sample size was Kolerman et al. [38] and achieved a mean gain of 3.5 mm (SD 0.93 mm) using a combined technique of split crest and interpositional particulate graft.

The limitation of this systematic review was the impossibility to perform meta-analysis due to the variability and lack of standardization of data. Moreover, despite the number of studies included, only one of them was a randomized clinical trial. Therefore, future studies should explore this lack of clinical trials about the use of bone substitutes in augmentation procedures, especially for horizontal augmentation.

The xenogenous bone grafts, regardless of form of use, presented high success rate without major complications. Those procedures allowed implant placement in 96.63% of the cases. Autogenous block grafts show success rates from 92 to 100% [55]. However, there are few data about implant installation in grafted areas. Therefore, it is possible to conclude that xenografts are a feasible alternative to autogenous bone grafts in horizontal augmentation. Additionally, we encourage researchers to perform controlled randomized clinical trial in this area due to the lack of strong evidence about implant insertion torque, initial stability, and osseointegration failures in grafted areas.