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JFBJournal of Functional Biomaterials
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18 August 2022

A Narrative Review on the Effectiveness of Bone Regeneration Procedures with OsteoBiol® Collagenated Porcine Grafts: The Translational Research Experience over 20 Years

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1
Department of Medical, Oral and Biotechnological Sciences, “G. d’Annunzio” University of Chieti-Pescara, 66013 Chieti, Italy
2
Center for Advanced Studies and Technology-CAST, “G. d’Annunzio” University of Chieti-Pescara, 66013 Chieti, Italy
3
Department of Medical, Surgical, and Dental Sciences, University of Milan, 20122 Milan, Italy
4
Department of Interdisciplinary Medicine, University of Bari “Aldo Moro”, 70124 Bari, Italy
J. Funct. Biomater.2022, 13(3), 121;https://doi.org/10.3390/jfb13030121
This article belongs to the Special Issue Selected Reviews in Biomaterials: Development, Applications and Challenges
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Abstract

Over the years, several bone regeneration procedures have been proposed using natural (autografts, allografts, and xenografts) and synthetic (i.e., metals, ceramics, and polymers) bone grafts. In particular, numerous in vitro and human and animal in vivo studies have been focused on the discovery of innovative and suitable biomaterials for oral and maxillofacial applications in the treatment of severely atrophied jaws. On this basis, the main objective of the present narrative review was to investigate the efficacy of innovative collagenated porcine bone grafts (OsteoBiol®, Tecnoss®, Giaveno, Italy), designed to be as similar as possible to the autologous bone, in several bone regeneration procedures. The scientific publications were screened by means of electronic databases, such as PubMed, Scopus, and Embase, finally selecting only papers that dealt with bone substitutes and scaffolds for bone and soft tissue regeneration. A total of 201 papers have been detected, including in vitro, in vivo, and clinical studies. The effectiveness of over 20 years of translational research demonstrated that these specific porcine bone substitutes are safe and able to improve the biological response and the predictability of the regenerative protocols for the treatment of alveolar and maxillofacial defects.

1. Introduction

Bone regeneration procedures are surgical techniques developed to restore the jaw defects provoked by tissue damage, infections, tooth loss, neoplasms, or local trauma [1,2,3]. Many different protocols have been adopted in accordance with the defect type (horizontal/vertical augmentation) [4,5,6,7], the local anatomy (anterior/posterior region of maxilla/mandibula) [8,9,10,11], the defect extension, and the planned rehabilitation [4,12,13,14]. The rationale of these procedures is to obtain a durable regeneration of the hard/soft tissue interface after the organization of a blood clot, which promotes the local new bone formation [15,16,17]. The use of xenografts and alloplastic bone substitutes represents a useful and safe technique that takes advantage of the high manageability of these products, avoiding the need for a donor site for autologous graft retrieving [17,18,19]. The effectiveness of these products has been evaluated by different studies conducted in various research centers around the world. These studies have been developed on a progressive scale, starting from in vitro studies on cell cultures, proceeding with in vivo studies on animal models, and finally with human studies, which allow for strengthening the 20-year work experience in translational research activity. In particular, both the histological and histomorphometric investigations performed at the microscopic level are able to reveal the bone response to the graft, providing strong knowledge about the bone scaffold behavior, the resorption process, the local bone neoformation, and the long-term persistent response of the regenerated tissues. Moreover, these methodologies have been associated with other techniques, such as Scanning Electron Microscopy (SEM), Transmission Electron Microscopy (TEM), Atomic Force Microscopy (AFM) and Synchrotron Micro-CT, in order to improve the biomaterial surface characterization and information about the physicochemical and biological compositions. This methodological approach steers clinicians towards the correct choice of the scaffold shape (i.e., particulate/block), the surgical procedure, and the graft manipulation and stabilization techniques, in order to increase the predictability of the procedure. In these terms, the aim of the present review was to describe the effectiveness of several protocols for the alveolar/maxillofacial bone and soft tissue regeneration using different OsteoBiol® innovative collagenated porcine bone grafts.

2. Materials and Methods

The screening of the studies was performed using the electronic databases PubMed, Scopus, and Embase, through the research of specific keywords: Piattelli A AND porcine bone biomaterials; Piattelli A AND porcine bone biomaterials AND jawbone regeneration; Piattelli A AND porcine granules; Piattelli A AND porcine bone blocks; Piattelli A AND porcine collagen bone barriers; Piattelli A AND porcine collagen membranes; OsteoBiol® AND porcine bone biomaterial; OsteoBiol® AND jawbone regeneration; OsteoBiol® AND maxillofacial regeneration; OsteoBiol® AND porcine granules; OsteoBiol® AND porcine bone blocks; OsteoBiol® AND porcine collagen bone barriers; OsteoBiol® AND porcine collagen membranes.
The manuscripts were then evaluated through a qualitative synthesis.

2.1. Inclusion Criteria

The studies published up to January 2021 were evaluated with no language restrictions. The identified studies were limited to papers that dealt with collagenated porcine bone substitutes and scaffolds for bone and soft tissue regeneration during the last 20 years. No restrictions about the use of barrier membranes were applied to the systematic research process. The inclusion criteria considered human studies, in vitro research and reports, and animal model investigations. The off-topic publications were excluded from the investigation. The articles were then classified in accordance with the surgical procedure and the study design.

2.2. Selection of the Studies

The screening of the study data and papers was performed independently by two calibrated and expert reviewers (M.T. and A.P.). After a first check, all the abstracts of the identified papers were evaluated as the 1st level of screening. The reviews and book chapters were excluded from the qualitative analysis. A description of the reasons for exclusion was drafted, concerning not considered articles. The full text of the included papers was obtained, and then, they were classified for the qualitative synthesis. For this purpose, a specially designed data form was used (Excel Office Microsoft, Redmond, WA, USA).
A total of 1375 manuscripts have been detected by the electronic database research. A total of 266 duplicates have been removed, and 1109 papers have been considered for the full-text eligibility evaluation. A total of 44 literature reviews, five book chapters, 87 papers written in non-English grammar, and 772 off-topic manuscripts were excluded. In the end, a total of 201 papers have been included in the final analytical synthesis (Figure 1).
Figure 1. PRISMA Flowchart of the study design and manuscript-selection process.

2.3. Description of the Porcine Grafts

Figure 2 and Figure 3 report the characteristics and the clinical applications of the different biomaterials (OsteoBiol®, Tecnoss®, Giaveno, Italy) used and cited in the selected papers. All of them are porcine collagenated xenografts and show high biocompatibility and osteoconductive properties [20,21]. A dedicated product has been developed for every clinical indication, trying to provide the best handling, granulometry, and consistency, in order to achieve ideal regenerative results [22]. In particular, the dual-phase heterologous bone matrix granules are composed of a mineral phase and a xenogenic collagen phase, which is able to provide the best biocompatibility, a chemical composition similar to autogenous bone, gradual resorption of the bone matrix with the replacement by the newly formed bone at re-entry time, and a high angiogenic potential [23,24,25,26]. These elements are critical for a successful bone regeneration procedure that sometimes can be further improved with the association of some of these xenografts.
Figure 2. Description of the characteristics regarding OsteoBiol® products.
Figure 3. Description of the clinical applications of OsteoBiol® products.

3. Results

The main effective results for each biomaterial used alone or in combination have been schematically divided and summarized in the tables below [Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7 and Table 8], on the basis of the clinical indication they have been specifically designed for.
Table 1. Bone regeneration procedures with collagenated porcine xenografts: Alveolar Regeneration (ALR) and Alveolar Regeneration/Dehiscences and Fenestrations (ALR/DEH).
Table 2. Bone regeneration procedures with collagenated porcine xenografts: Dehiscences and Fenestrations (DEH) and Dehiscences and Fenestrations/Lateral Access Sinus Lift (DEH/LASL).
Table 3. Bone regeneration procedures with collagenated porcine xenografts: Crestal Access Sinus Lift (CASL), Lateral Access Sinus Lift (LASL) and Lateral Access Sinus Lift/Horizontal Augmentation (LASL/HOR).
Table 4. Bone regeneration procedures with collagenated porcine xenografts: Horizontal Augmentation (HOR), Vertical Augmentation (VER), Horizontal and Vertical Augmentation (HOR/VER) and Vertical Augmentation/Lateral Access Sinus Lift (VER/LASL).
Table 5. Bone regeneration procedures with porcine xenografts: Maxillofacial (MAX).
Table 6. Bone regeneration procedures with collagenated porcine xenografts: Periodontal Regeneration (PER) and Soft Tissue Augmentation (TIS).
Table 7. Bone regeneration procedures with collagenated porcine xenografts: Laboratory Tests (in vitro studies) (LAB), Laboratory Tests/Experimental Studies (LAB/EXP) and Laboratory Tests/Lateral Access Sinus Lift (LAB/LASL).
Table 8. Bone regeneration procedures with collagenated porcine xenografts: Experimental Studies (EXP).
In summary, all the in vitro, experimental, and clinical results described in Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7 and Table 8 suggested that, during the last 20 years, the OsteoBiol® collagenated biomaterials have shown reliable outcomes in terms of biocompatibility, morbidity, new bone formation, and bone and soft tissue regeneration, according to expert surgeons’ experience.

4. Discussion

The number of studies reporting surgical techniques for bone regeneration and the clinical effectiveness of bone substitutes and xenografts has greatly increased over the last years, with high predictability and stability of the regenerated alveolar bone ridges [9,18,219]. The treatment of bone defects represents a clinical occurrence that requires optimal management of the three-dimensional stability of the grafts and regenerative spaces. In this way, blood-clot stability plays a key role in new bone formation and the morphological restoration of the atrophied bone ridge [220].
The effectiveness of graft implantation is affected by a biunivocal biological relationship between the host tissue and the bone substitutes that has been investigated by numerous histological studies on retrieved biopsies [221].
In many ex vivo studies conducted by using porcine graft specimens, the histologic and histomorphometric evaluations reported newly formed bone in contact with the scaffolds and an evident presence of cells in the osteocyte lacunae [7,24,25,27,222].
This evidence has been corroborated by the clinical success of these biomaterials, which confirmed the histologic and histomorphometric findings and showed an intimate apposition of newly formed bone in contact with the porous porcine-derived biomaterials, especially in maxillary sinus augmentation procedures [28,85,89,90,93,97,99,100,101,110,111,116,117,119].
In addition, the results obtained from ex vivo and clinical data have been supported by in vitro studies, which demonstrated the osteoblast differentiation and bone regeneration capabilities together with the angiogenic potential of the OsteoBiol® bone matrix [21,23,26,178,183,184,185,194,197].
With reference to graft resorption, many studies revealed the nearly complete substitution of membranes and the ongoing resorption of collagenated bone particles within 6 months. Especially, Wachtel et al. [123] reported that the biodegradation of the cortical bone Lamina® was almost complete after 6 months, with varying degrees of residual graft particles. Cardaropoli et al. [30] confirmed the presence of a marginal residual graft rate (24.5%) of Gen-Os® biomaterial, covered by Evolution® collagen membrane to preserve the bone socket, just after 4 months from implant insertion. Additionally, another clinical study [95] reported a high resorption rate of mp3®, with 13.55% of residual grafting material after 5 months, that reached 12.3% within 12 months [24]. Considering that the limit for the residual volume of bone grafts for successful implant placement is set at 40% [223], these values are considerably lower.
Regarding the aforementioned residual graft limit, it should be considered that only Apatos Cortical® showed a higher residue percentage (around 30%) after many years from the surgery, although it stayed within 40%, comparable to the different types of xenografts present in the market [96,224].
However, these histological findings allow for adequate preservation of the grafted volume and do not appear to negatively affect the predictability of regenerative procedures and the survival rate of the dental implant in regenerated sites [225].
Overall, based on the data discussed, it appears clear that, due to the unique properties of these xenografts, an adequate preservation of graft volume and an improved new bone formation have been achieved.
In addition, the literature proved that OsteoBiol® materials could be used alone or in combination both for the regeneration of bone defects and soft tissue augmentation. For example, in the latter case, membranes, such as Derma, can be used alone as an alternative to connective tissue graft to improve the quality of keratinized tissues [166,171,172,173,174]. Apatos®, instead, is a universal filler that can be employed to treat peri-implant defects and two-wall defects [68,74]. Moreover, thanks to its granulometry, Apatos® fits well in big sockets, e.g., after molar extractions [41]. For this reason, sinus lift procedures (with crestal or lateral access) [85,91] can be performed with Apatos® as a bone substitute, as well as surgeries for horizontal regenerations. Finally, as an example of a combination of materials, Apatos® grafts can be protected with Evolution membrane [59] to reach a better ridge preservation compared to non-preserved size.
Although the effectiveness of using these biomaterials has been summarized in the results (Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7 and Table 8) and discussed in this section, it is necessary to recognize that this narrative review has potential weaknesses. The main limitations include: (i) the manuscript does not contain all the reports in the field of “effectiveness of bone regeneration procedures with collagenated porcine grafts”, but only some selected publications that concern OsteoBiol® biomaterials; (ii) the collected articles come from studies not only conducted by the authors of this review, but also by several other authors; (iii) the manuscript describes the individual works but does not quantify the results, and no statistical analysis is performed here; (iv) the manuscript does not compare the effectiveness of OsteoBiol® products with other competitors, which are also successfully used for bone and soft tissue regeneration within the craniofacial area. However, our main goal was to summarize the achievements of these specific materials over the years.
Despite these limitations, we can conclude that the 20-year translational research experience showed the safety of these specific porcine bone substitutes and demonstrated their capability to improve the biological response and predictability of regenerative protocols for the treatment of alveolar and maxillofacial defects. For future perspectives, it will certainly be useful to extend the number of included studies, analyze and compare the success rate of each product, and perform longer-term histological and histomorphometric studies in order to better understand the resorption times of all these biomaterials. In this way, a systematic review could be performed to better highlight the advantages of using OsteoBiol® collagenated porcine bone grafts with respect to other porcine substitutes.

Author Contributions

Conceptualization, A.P. and N.D.P.; validation, G.I. and L.M.; investigation, M.T., G.I. and A.P.; writing—original draft preparation, T.R., N.D.P., F.I. and M.T.; writing—review and editing, M.P. and P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All the data supporting reported results regarding publications cited in this review are available contacting the corresponding author upon request.

Conflicts of Interest

The authors declare no conflict of interest.

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Laboratory Fracture Resilience of Hybrid Abutments Used in Oral Rehabilitation: A Systematic Review
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