Maxillary sinus floor augmentation comparing bovine versus porcine bone xenografts mixed with autogenous bone graft. A split-mouth randomized controlled trial

Pablo Galindo-Moreno, Dario Abril-García, Ana Belen Carrillo-Galvez, Federico Zurita, Natividad Martín-Morales, Francisco O'Valle, Miguel Padial-Molina, Pablo Galindo-Moreno, Dario Abril-García, Ana Belen Carrillo-Galvez, Federico Zurita, Natividad Martín-Morales, Francisco O'Valle, Miguel Padial-Molina

Abstract

Aim: To compare the effectiveness of two xenografts for maxillary sinus floor augmentation in terms of clinical, radiographical, histologic, and molecular outcomes.

Materials and methods: A split-mouth randomized clinical trial was conducted at the University of Granada. Ten consecutive patients in need of bilateral two-staged maxillary sinus floor augmentation were included. Each patient received both biomaterials (porcine bone mineral and anorganic bovine bone), which were randomly assigned for bilateral sinus augmentation. The maxillary autogenous bone scraped from the sinus access window was mixed with each xenograft at a 20:80 ratio. After a healing period of 6 months, bone biopsies were collected with a trephine during the implant placement in the regenerated area. Histologic, histomorphometrical, immunohistochemical, and molecular outcomes were analyzed. Clinical and radiographical data throughout the treatment phases were also evaluated.

Results: The resulting anatomic features were similar between both groups. After six months of graft consolidation, the graft resorption rates were similar between both biomaterials. The histologic, histomorphometrical, and immunohistochemical results showed no statistical differences between groups.

Conclusion: Anorganic bovine bone and porcine bone mineral combined with maxillary autogenous cortical bone show similar biologic and radiologic features in terms of biomaterial resorption, osteoconduction, and osteogenesis when used for maxillary sinus floor augmentation.

Keywords: anorganic bovine bone; bone biomaterial; implant dentistry; maxillary sinus augmentation; porcine bone mineral.

Conflict of interest statement

Pablo Galindo‐Moreno is a frequent speaker for Dentsply Sirona Implants at different events. Regardless, the authors declare no conflict of interest, either directly or indirectly, in any of the products listed in the manuscript.

© 2022 The Authors. Clinical Oral Implants Research published by John Wiley & Sons Ltd.

Figures

FIGURE 1
FIGURE 1
(a) Initial (semi‐transparent lines), post‐operative (dotted lines), and final (hard lines) heights of the crestal bone at the mesial, central, and distal sites of the graft. (b) Vertical graft resorption of the graft for either group. Note that this measure was calculated by subtracting the height at the 6 months follow‐up to the post‐operative height. (c) Crestal bone height gain, calculated by subtracting the height of the initial residual alveolar crest to the final height. (d) Bucco‐lingual sinus width at 5, 10, and 15 mm from the sinus floor. (e) Post‐operative (semi‐transparent colors), and final (solid colors) volumes of the areas grafted with ACB+ABB (orange) and ACB+PBM (green). (f) Volume of graft resorption after 6 months of healing. In all cases, orange is used for ACB+ABB, and green is used for ACB+PBM
FIGURE 2
FIGURE 2
Representative panoramic microphotograph of biopsies from the (a) ACB+PBM and the (b) ACB+ABB groups including pristine bone and grafted areas. Masson trichrome staining. Bar scale: 100 μm
FIGURE 3
FIGURE 3
Grafted area with active osteogenesis as determined by the presence of osteoblastic (*) and osteoid lines (**) in (a) ACB+ABB and (b) ACB+PBM groups. Masson trichrome staining. Original magnification 20×; bar scale: 100 μm. ABB, anorganic bovine bone; MT, mineralized tissue; nMT, non‐mineralized tissue; PBM, porcine bone mineral
FIGURE 4
FIGURE 4
Transmission electron microscopy images showing close connection between porcine bone mineral (PBM) (a) and anorganic bovine bone (ABB) (b) particles and newly mineralized tissue (MT). Colonization by cells in PBM (c) and ABB (d) particles can also be observed (white arrows). Bar scale: 1 and 5 μm
FIGURE 5
FIGURE 5
Similar immunohistochemical expression (in brown) of different markers in the grafted areas of a, c, e, g, and i) ACB+ABB and b, d, f, h, and j) ACB+PBM groups. (a,b) Osteopontin; (c,d) Musashi‐1; (e,f) CD68 (monocytes/macrophages/osteoclasts‐like cells); (g,h) TRAP (osteoclasts‐like cells); (i,j) CD34 (endothelial cells). Micropolymer conjugated with peroxidase staining method. Original magnification 20×; bar scale: 100 μm. ABB, anorganic bovine bone; MT, mineralized tissue; nMT, non‐mineralized tissue; PBM, porcine bone mineral

References

    1. Avila, G. , Wang, H. L. , Galindo‐Moreno, P. , Misch, C. E. , Bagramian, R. A. , Rudek, I. , Benavides, E. , Moreno‐Riestra, I. , Braun, T. , & Neiva, R. (2010). The influence of the bucco‐palatal distance on sinus augmentation outcomes. Journal of Periodontology, 81, 1041–1050.
    1. Avila‐Ortiz, G. , Neiva, R. , Galindo‐Moreno, P. , Rudek, I. , Benavides, E. , & Wang, H.‐L. (2012). Analysis of the influence of residual alveolar bone height on sinus augmentation outcomes. Clinical Oral Implants Research, 23, 1082–1088. 10.1111/j.1600-0501.2011.02270.x
    1. Avila‐Ortiz, G. , Wang, H.‐L. , Galindo‐Moreno, P. , Misch, C. E. , Rudek, I. , & Neiva, R. (2012). Influence of lateral window dimensions on vital bone formation following maxillary sinus augmentation. The International Journal of Oral & Maxillofacial Implants, 27, 1230–1238.
    1. Boeck‐Neto, R. J. , Artese, L. , Piattelli, A. , Shibli, J. A. , Perrotti, V. , Piccirilli, M. , & Marcantonio, E., Jr . (2009). VEGF and MVD expression in sinus augmentation with autologous bone and several graft materials. Oral Diseases, 15, 148–154. 10.1111/j.1601-0825.2008.01502.x
    1. Cassetta, M. , Perrotti, V. , Calasso, S. , Piattelli, A. , Sinjari, B. , & Iezzi, G. (2015). Bone formation in sinus augmentation procedures using autologous bone, porcine bone, and a 50: 50 mixture: A human clinical and histological evaluation at 2 months. Clinical Oral Implants Research, 26, 1180–1184. 10.1111/clr.12423
    1. Caubet, J. , Ramis, J. M. , Ramos‐Murguialday, M. , Morey, M. A. , Monjo, M. (2015). Gene expression and morphometric parameters of human bone biopsies after maxillary sinus floor elevation with autologous bone combined with Bio‐Oss®or BoneCeramic®. Clinical Oral Implants Research, 26(6), 727–735. 10.1111/clr.12380
    1. Galindo‐Moreno, P. , de Buitrago, J. G. , Padial‐Molina, M. , Fernández‐Barbero, J. E. , Ata‐Ali, J. , & O’Valle, F. (2018). Histopathological comparison of healing after maxillary sinus augmentation using xenograft mixed with autogenous bone versus allograft mixed with autogenous bone. Clinical Oral Implants Research, 29, 192–201. 10.1111/clr.13098
    1. Galindo‐Moreno, P. , Hernández‐Cortés, P. , Aneiros‐Fernández, J. , Camara, M. , Mesa, F. , Wallace, S. , & O’Valle, F. (2014). Morphological evidences of Bio‐Oss® colonization by CD44‐positive cells. Clinical Oral Implants Research, 25, 366–371.
    1. Galindo‐Moreno, P. , Hernández‐Cortés, P. , Mesa, F. , Carranza, N. , Juodzbalys, G. , Aguilar, M. , & O’Valle, F. (2013). Slow resorption of anorganic bovine bone by osteoclasts in maxillary sinus augmentation. Clinical Implant Dentistry and Related Research, 15, 858–866. 10.1111/j.1708-8208.2012.00445.x
    1. Galindo‐Moreno, P. , Hernandez‐Cortes, P. , Padial‐Molina, M. , Vizoso, M. L. , Crespo‐Lora, V. , & O’Valle, F. (2015). Immunohistochemical osteopontin expression in bone xenograft in clinical series of maxillary sinus lift. Journal of Oral Science & Rehabilitation, 1, 42–50.
    1. Galindo‐Moreno, P. , Moreno‐Riestra, I. , Avila, G. , Padial‐Molina, M. , Paya, J. A. , Wang, H.‐L. , & O’Valle, F. (2011). Effect of anorganic bovine bone to autogenous cortical bone ratio upon bone remodeling patterns following maxillary sinus augmentation. Clinical Oral Implants Research, 22, 857–864. 10.1111/j.1600-0501.2010.02073.x
    1. Galindo‐Moreno, P. , Moreno‐Riestra, I. , Ávila‐Ortiz, G. , Padial‐Molina, M. , Gallas‐Torreira, M. , Sánchez‐Fernández, E. , Mesa, F. , Wang, H.‐L. , & O’Valle, F. (2012). Predictive factors for maxillary sinus augmentation outcomes: A case series analysis. Implant Dentistry, 21, 433–440. 10.1097/ID.0b013e3182691959
    1. Galindo‐Moreno, P. , Padial‐Molina, M. , Fernández‐Barbero, J. E. , Mesa, F. , Rodríguez‐Martínez, D. , & O’Valle, F. (2010). Optimal microvessel density from composite graft of autogenous maxillary cortical bone and anorganic bovine bone in sinus augmentation: Influence of clinical variables. Clinical Oral Implants Research, 21, 221–227. 10.1111/j.1600-0501.2009.01827.x
    1. Galindo‐Moreno, P. , Padial‐Molina, M. , Lopez‐Chaichio, L. , Gutiérrez‐Garrido, L. , Martín‐Morales, N. , & O’Valle, F. (2020). Algae‐derived hydroxyapatite behavior as bone biomaterial in comparison with anorganic bovine bone: A split‐mouth clinical, radiological, and histologic randomized study in humans. Clinical Oral Implants Research, 31, 536–548. 10.1111/clr.13590
    1. Hallman, M. , Lundgren, S. , & Sennerby, L. (2001). Histologic analysis of clinical biopsies taken 6 months and 3 years after maxillary sinus floor augmentation with 80% bovine hydroxyapatite and 20% autogenous bone mixed with fibrin glue. Clinical Implant Dentistry and Related Research, 3, 87–96. 10.1111/j.1708-8208.2001.tb00236.x
    1. Hallman, M. , Sennerby, L. , & Lundgren, S. (2002). A clinical and histologic evaluation of implant integration in the posterior maxilla after sinus floor augmentation with autogenous bone, bovine hydroxyapatite, or a 20:80 mixture. International Journal of Oral and Maxillofacial Implants, 17(5), 635–643.
    1. Hallman, M. , Sennerby, L. , Zetterqvist, L. , & Lundgren, S. (2005). A 3‐year prospective follow‐up study of implant‐supported fixed prostheses in patients subjected to maxillary sinus floor augmentation with a 80:20 mixture of deproteinized bovine bone and autogenous bone: Clinical, radiographic and resonance frequency analysis. International Journal of Oral and Maxillofacial Surgery, 34, 273–280. 10.1016/j.ijom.2004.09.009
    1. Khosravi, N. , Maeda, A. , DaCosta, R. S. , & Davies, J. E. (2018). Nanosurfaces modulate the mechanism of peri‐implant endosseous healing by regulating neovascular morphogenesis. Communications Biology, 1, 72. 10.1038/s42003-018-0074-y
    1. Lee, J.‐S. , Shin, H.‐K. , Yun, J.‐H. , & Cho, K.‐S. (2017). Randomized clinical trial of maxillary sinus grafting using deproteinized porcine and bovine bone mineral. Clinical Implant Dentistry and Related Research, 19, 140–150. 10.1111/cid.12430
    1. Lee, J. H. , Yi, G. S. , Lee, J. W. , & Kim, D. J. (2017). Physicochemical characterization of porcine bone‐derived grafting material and comparison with bovine xenografts for dental applications. Journal of Periodontal & Implant Science, 47, 388–401. 10.5051/jpis.2017.47.6.388
    1. Li, S. , Chen, H. , & Yuen, D. (2014). Isolation and characterization of a porous carbonate apatite from porcine cancellous bone. Journal of Science, Technology, Innovation, 1, 13.
    1. Lundgren, S. , Cricchio, G. , Hallman, M. , Jungner, M. , Rasmusson, L. , & Sennerby, L. (2017). Sinus floor elevation procedures to enable implant placement and integration: Techniques, biological aspects and clinical outcomes. Periodontology, 73, 103–120. 10.1111/prd.12165
    1. Monje, A. , O’Valle, F. , Monje‐Gil, F. , Ortega‐Oller, I. , Mesa, F. , Wang, H.‐L. , & Galindo‐Moreno, P. (2017). Cellular, vascular, and histomorphometric outcomes of solvent‐dehydrated vs freeze‐dried allogeneic graft for maxillary sinus augmentation: A randomized case series. The International Journal of Oral & Maxillofacial Implants, 32, 121–127. 10.11607/jomi.4801
    1. Nomura, T. , Katz, J. L. , Powers, M. P. , & Saito, C. (2005). Evaluation of the micromechanical elastic properties of potential bone‐grafting materials. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 73, 29–34. 10.1002/jbm.b.30201
    1. O’Valle, F. , de Buitrago, J. G. , Hernández‐Cortés, P. , Padial‐Molina, M. , Crespo‐Lora, V. , Cobo, M. , Aguilar, D. , & Galindo‐Moreno, P. (2018). Increased expression of musashi‐1 evidences mesenchymal repair in maxillary sinus floor elevation. Scientific Reports, 8, 12243. 10.1038/s41598-018-29908-3
    1. Orsini, G. , Scarano, A. , Piattelli, M. , Piccirilli, M. , Caputi, S. , & Piattelli, A. (2006). Histologic and ultrastructural analysis of regenerated bone in maxillary sinus augmentation using a porcine bone‐derived biomaterial. Journal of Periodontology, 77, 1984–1990. 10.1902/jop.2006.060181
    1. Padial‐Molina, M. , Crespo‐Lora, V. , Candido‐Corral, C. , Martin‐Morales, N. , Abril‐Garcia, D. , Galindo‐Moreno, P. , Hernandez‐Cortes, P. , & O’Valle, F. (2021). Expression of musashi‐1 increases in bone healing. International Journal of Molecular Sciences, 22, 3395. 10.3390/ijms22073395
    1. Padial‐Molina, M. , de Buitrago, J. G. , Sainz‐Urruela, R. , Abril‐Garcia, D. , Anderson, P. , O’Valle, F. , Galindo‐Moreno, P. (2019). Expression of musashi‐1 during osteogenic differentiation of oral MSC: An in vitro study. International Journal of Molecular Sciences, 20(9), 2171. 10.3390/ijms20092171
    1. Saito, H. , Couso‐Queiruga, E. , Shiau, H. J. , Stuhr, S. , Prasad, H. , Allareddy, T. V. , Reynolds, M. A. , & Avila‐Ortiz, G. (2021). Evaluation of poly lactic‐co‐glycolic acid‐coated β‐tricalcium phosphate for alveolar ridge preservation: A multicenter randomized controlled trial. Journal of Periodontology, 92, 524–535. 10.1002/JPER.20-0360
    1. Salazar, V. S. , Gamer, L. W. , & Rosen, V. (2016). BMP signalling in skeletal development, disease and repair. Nature Reviews Endocrinology, 12, 203–221.
    1. Scarano, A. , Piattelli, A. , Perrotti, V. , Manzon, L. , & Iezzi, G. (2011). Maxillary sinus augmentation in humans using cortical porcine bone: A histological and histomorphometrical evaluation after 4 and 6 months. Clinical Implant Dentistry and Related Research, 13, 13–18. 10.1111/j.1708-8208.2009.00176.x
    1. Stegen, S. , & Carmeliet, G. (2020). Chapter 46 ‐ Vascular endothelial growth factor and bone–vascular interactions. In Bilezikian J. P., Martin T. J., Clemens T. L. & Rosen C. J. (Eds.), Principles of bone biology (Fourth Edition) (pp. 1141–1152). Academic Press. 10.1016/B978-0-12-814841-9.00046-4
    1. Tetè, S. , Zizzari, V. L. , Vinci, R. , Zara, S. , Di Tore, U. , Manica, M. , Cataldi, A. , Mortellaro, C. , Piattelli, A. , & Gherlone, E. (2014). Equine and porcine bone substitutes in maxillary sinus augmentation: A histological and immunohistochemical analysis of VEGF expression. The Journal of Craniofacial Surgery, 25, 835–839. 10.1097/SCS.0000000000000679
    1. Torrecillas‐Martínez, L. , Galindo‐Moreno, P. , Ávila‐Ortiz, G. , Ortega‐Oller, I. , Monje, A. , Hernández‐Cortés, P. , Aguilar, D. , & O’Valle, F. (2016). Significance of the immunohistochemical expression of bone morphogenetic protein‐4 in bone maturation after maxillary sinus grafting in humans. Clinical Implant Dentistry and Related Research, 18, 717–724. 10.1111/cid.12354
    1. Vimalraj, S. (2020). Alkaline phosphatase: Structure, expression and its function in bone mineralization. Gene, 754, 144855. 10.1016/j.gene.2020.144855

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