{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T00:34:20Z","timestamp":1792456460472,"version":"4.5.0"},"reference-count":45,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2025,1,2]],"date-time":"2025-01-02T00:00:00Z","timestamp":1735776000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"ARDEC Academy, Rimini, Italy"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Dentistry Journal"],"abstract":"<jats:p>Background: This investigation focused on the influence of collagen on the integrity of the Schneiderian membrane during maxillary sinus augmentation in a rabbit model. The aim of this study was to elucidate the relationship between membrane integrity and bone regeneration in augmented maxillary sinuses using collagenated and non-collagenated grafts, through detailed histological and histomorphometric analyses. Methods: In this forward-looking, randomized, split-mouth design, bilateral maxillary sinus augmentation was conducted on 12 rabbits. One sinus was filled with deproteinized bovine bone material (DBBM) as the grafting material (non-collagenated; control), while a combination of DBBM particles integrated with 10% porcine-derived type I collagen was used in the contralateral sinus (collagenated; test). Histological analyses were carried out following healing periods of 2 and 12 weeks. Results: At the 2-week time point, six sites of thinned mucosa (&lt;40 \u00b5m) and no perforations were observed in the collagenated group, while twenty-one thinned mucosa sites (p = 0.027 between test and control) and two perforations (p = 0.175 between test and control) were found in the non-collagenated group. After 12 weeks of healing, the number of sites with thinned mucosa was 20 in the collagenated group and 19 in the non-collagenated group, with four perforations observed in each group. These perforations were distributed across three sinuses in the collagenated group and two sinuses in the non-collagenated group. No statistically significant differences were found between the groups. Conclusions: The addition of 10% collagen to deproteinized bovine bone mineral initially provided protection against mucosal thinning and perforation after 2 weeks of healing. However, by week 12, this protective effect diminished, resulting in similar rates of mucosal thinning and perforations in both groups.<\/jats:p>","DOI":"10.3390\/dj13010019","type":"journal-article","created":{"date-parts":[[2025,1,2]],"date-time":"2025-01-02T06:05:10Z","timestamp":1735797910000},"page":"19","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Impact of Collagenated and Non-Collagenated Deproteinized Bovine Bone Mineral on Schneiderian Membrane Integrity in Rabbits"],"prefix":"10.3390","volume":"13","author":[{"given":"Rihito","family":"Yamada","sequence":"first","affiliation":[{"name":"Department of Oral Implantology, School of Dentistry, Osaka Dental University, 8-1 Kuzuhahanazonocho, Hirakata 573-1121, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7389-5886","authenticated-orcid":false,"given":"Samuel Porfirio","family":"Xavier","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery and Periodontology, Faculty of Dentistry of Ribeir\u00e3o Preto, University of S\u00e3o Paulo, Av. do Caf\u00e9-Subsetor Oeste-11 (N-11), Ribeir\u00e3o Preto 14040-904, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasushi","family":"Nakajima","sequence":"additional","affiliation":[{"name":"Department of Oral Implantology, School of Dentistry, Osaka Dental University, 8-1 Kuzuhahanazonocho, Hirakata 573-1121, Osaka, Japan"},{"name":"ARDEC Academy, 47923 Rimini, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3657-384X","authenticated-orcid":false,"given":"Erick Ricardo","family":"Silva","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Surgery and Periodontology, Faculty of Dentistry of Ribeir\u00e3o Preto, University of S\u00e3o Paulo, Av. do Caf\u00e9-Subsetor Oeste-11 (N-11), Ribeir\u00e3o Preto 14040-904, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2804-1632","authenticated-orcid":false,"given":"Daniele","family":"Botticelli","sequence":"additional","affiliation":[{"name":"Department of Oral Implantology, School of Dentistry, Osaka Dental University, 8-1 Kuzuhahanazonocho, Hirakata 573-1121, Osaka, Japan"},{"name":"ARDEC Academy, 47923 Rimini, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuki","family":"Teranishi","sequence":"additional","affiliation":[{"name":"Department of Oral Implantology, School of Dentistry, Osaka Dental University, 8-1 Kuzuhahanazonocho, Hirakata 573-1121, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shunsuke","family":"Baba","sequence":"additional","affiliation":[{"name":"Department of Oral Implantology, School of Dentistry, Osaka Dental University, 8-1 Kuzuhahanazonocho, Hirakata 573-1121, Osaka, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,1,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"384","DOI":"10.5114\/aoms\/174648","article-title":"Clinical evaluation of maxillary sinus floor elevation with or without bone grafts: A systematic review and meta-analysis of randomised controlled trials with trial sequential analysis","volume":"20","author":"Chen","year":"2024","journal-title":"Arch. Med. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1111\/prd.12165","article-title":"Sinus floor elevation procedures to enable implant placement and integration: Techniques, biological aspects and clinical outcomes","volume":"73","author":"Lundgren","year":"2017","journal-title":"Periodontol. 2000"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"506","DOI":"10.11607\/jomi.10600","article-title":"Single-Stage Lateral Sinus Floor Elevation Using Different Grafts: A Systematic Review of Controlled Clinical Trials","volume":"39","year":"2024","journal-title":"Int. J. Oral Maxillofac. Implant."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1034\/j.1600-0501.2002.130409.x","article-title":"Maxillary sinus augmentation model in rabbits: Effect of occluded nasal ostium on new bone formation","volume":"13","author":"Asai","year":"2002","journal-title":"Clin. Oral Implants Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1111\/j.1600-0501.2004.01003.x","article-title":"Grafting of deproteinized bone particles inhibits bone resorption after maxillary sinus floor elevation","volume":"15","author":"Xu","year":"2004","journal-title":"Clin. Oral Implants Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"902","DOI":"10.1111\/j.1600-0501.2011.02245.x","article-title":"Volumetric changes of the graft after maxillary sinus floor augmentation with Bio-Oss and autogenous bone in different ratios: A radiographic study in minipigs","volume":"23","author":"Jensen","year":"2012","journal-title":"Clin. Oral Implants Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1007\/s12663-013-0554-z","article-title":"Comparative, Histological and Histomorphometric Analysis of Three Anorganic Bovine Xenogenous Bone Substitutes: Bio-Oss, Bone-Fill and Gen-Ox Anorganic","volume":"13","author":"Manfro","year":"2014","journal-title":"J. Maxillofac. Oral Surg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1097\/ID.0000000000000187","article-title":"Comparison of two kinds of bovine bone in maxillary sinus augmentation: A histomorphometric study","volume":"24","author":"Moon","year":"2015","journal-title":"Implant Dent."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1111\/cid.12374","article-title":"Sinus Floor Augmentation Using Straumann\u00ae BoneCeramic\u2122 and Bio-Oss\u00ae in a Split Mouth Design and Later Placement of Implants: A 5-Year Report from a Longitudinal Study","volume":"18","author":"Mordenfeld","year":"2016","journal-title":"Clin. Implant Dent. Relat. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1111\/j.1600-0501.2010.02030.x","article-title":"Apical and marginal bone alterations around implants in maxillary sinus augmentation grafted with autogenous bone or bovine bone material and simultaneous or delayed dental implant positioning","volume":"22","author":"Sbordone","year":"2011","journal-title":"Clin. Oral Implants Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1111\/j.1600-0501.2009.01733.x","article-title":"Sinus augmentation analysis revised: The gradient of graft consolidation","volume":"20","author":"Busenlechner","year":"2009","journal-title":"Clin. Oral Implants Res."},{"key":"ref_12","first-page":"548","article-title":"Regenerative bone potential after sinus floor elevation using various bone graft materials: A systematic review","volume":"50","author":"Stumbras","year":"2019","journal-title":"Quintessence Int."},{"key":"ref_13","first-page":"562","article-title":"Bone regeneration in a human maxillary sinus following the use of Bio-Oss\u00ae or autogenous bone: A randomized controlled clinical trial","volume":"25","author":"Vallecillo","year":"2014","journal-title":"Clin. Oral Implants Res."},{"key":"ref_14","first-page":"587","article-title":"Bone Regeneration in the Maxillary Sinus with Collagenated and Non-collagenated Bone Grafts: A Histological Study in Rabbits","volume":"32","author":"Godoy","year":"2021","journal-title":"Clin. Oral Implants Res."},{"key":"ref_15","first-page":"365","article-title":"Maxillary sinus augmentation: A clinical study","volume":"24","author":"Boynes","year":"1980","journal-title":"Dent. Clin. N. Am."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0011-8532(22)02107-3","article-title":"Maxillary and sinus implant reconstruction","volume":"30","author":"Tatum","year":"1986","journal-title":"Dent. Clin. N. Am."},{"key":"ref_17","unstructured":"Summers, R.B. (1994). A new concept in maxillary implant surgery: The osteotome technique. Compendium, 15, quiz 162."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"773","DOI":"10.11607\/prd.1288","article-title":"Long-term implant survival in the grafted maxillary sinus: A systematic review","volume":"33","author":"Wallace","year":"2013","journal-title":"Int. J. Periodontics Restor. Dent."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1111\/j.1600-051X.2008.01272.x","article-title":"A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation","volume":"35","author":"Pjetursson","year":"2008","journal-title":"J. Clin. Periodontol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1111\/j.1600-0501.2009.01704.x","article-title":"Maxillary sinus floor elevation using the (transalveolar) osteotome technique with or without grafting material. Part I: Implant survival and patients\u2019 perception","volume":"20","author":"Pjetursson","year":"2009","journal-title":"Clin. Oral Implants Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e568","DOI":"10.4317\/medoral.26545","article-title":"Does sinus membrane thickness influence the risk of perforation during lateral sinus lift surgery for dental implants? a systematic review and meta-analysis","volume":"29","author":"Ke","year":"2024","journal-title":"Med. Oral Patol. Oral Cir. Bucal"},{"key":"ref_22","first-page":"517","article-title":"Complications of the lateral approach for sinus augmentation: A systematic review","volume":"30","author":"Kim","year":"2019","journal-title":"Clin. Oral Implants Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"681","DOI":"10.11607\/jomi.10048","article-title":"The Impact of Sinus Floor Elevation Techniques on Sinus Membrane Perforation: A Systematic Review and Network Meta-analysis","volume":"38","author":"Lee","year":"2023","journal-title":"Int. J. Oral Maxillofac. Implants"},{"key":"ref_24","first-page":"237","article-title":"Bone augmentation procedures in implant dentistry","volume":"24","author":"Chiapasco","year":"2009","journal-title":"Int. J. Oral Maxillofac. Implants"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Nakajima, Y., Botticelli, D., De Rossi, E.F., Ferreira Balan, V., Pires Godoy, E., Ricardo Silva, E., and Xavier, S.P. (2023). Schneiderian Membrane Collateral Damage Caused by Collagenated and Non-collagenated Xenografts: A Histological Study in Rabbits. Dent. J., 11.","DOI":"10.3390\/dj11020031"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"660","DOI":"10.11607\/jomi.8580","article-title":"Incidence of Sinus Mucosa Perforations During Healing After Sinus Elevation Using Deproteinized Bovine Bone Mineral as Grafting Material: A Histologic Evaluation in a Rabbit Model","volume":"36","author":"Miki","year":"2021","journal-title":"Int. J. Oral Maxillofac. Implant."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Favero, R., Apaza Alccayhuaman, K.A., Botticelli, D., Xavier, S.P., Ferreira Balan, V., Macchi, V., and De Caro, R. (2021). Sinus Mucosa Thinning and Perforations after Sinus Lifting Performed with Different Xenografts: A Histological Analysis in Rabbits. Dent. J., 10.","DOI":"10.3390\/dj10010002"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/s10006-021-00946-y","article-title":"Sinus mucosa thinning and perforation after sinus augmentation. A histological study in rabbits","volume":"25","author":"Kato","year":"2021","journal-title":"Oral Maxillofac. Surg."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Omori, Y., Botticelli, D., Migani, S., Ferreira Balan, V., Pires Godoy, E., and Xavier, S.P. (2022). Sinus Mucosal Damage Triggered by Synthetic or Xenogeneic Bone Substitutes: A Histological Analysis in Rabbits. J. Funct. Biomater., 13.","DOI":"10.3390\/jfb13040257"},{"key":"ref_30","first-page":"4383","article-title":"The influence of the surface characteristics of hydroxyapatite and beta-tricalcium phosphate on osteoblast behavior","volume":"26","author":"Hing","year":"2005","journal-title":"Biomaterials"},{"key":"ref_31","first-page":"516","article-title":"Use of collagenated and non-collagenated bovine bone grafts for sinus floor elevation: A histological study","volume":"26","author":"Alayan","year":"2015","journal-title":"J. Craniofac. Surg."},{"key":"ref_32","first-page":"1079","article-title":"Bone formation at implants in bone of different densities: An experimental study in dogs","volume":"25","author":"Lindhe","year":"2014","journal-title":"Clin. Oral Implants Res."},{"key":"ref_33","first-page":"170","article-title":"Strategies for the regeneration of periodontal tissues","volume":"32","author":"Sculean","year":"2005","journal-title":"J. Clin. Periodontol."},{"key":"ref_34","first-page":"47","article-title":"A potential novel strategy for bone tissue engineering: The role of collagen in implantable biomaterials","volume":"93","author":"Wong","year":"2010","journal-title":"J. Biomed. Mater. Res. B Appl. Biomater."},{"key":"ref_35","first-page":"932","article-title":"Ridge preservation with freeze-dried bone allograft and a collagen membrane: A 6-month study in humans","volume":"20","author":"Lindhe","year":"2009","journal-title":"Clin. Oral Implants Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e20230268","DOI":"10.1590\/1678-7757-2023-0268","article-title":"Clinical and radiographic evaluation of Bio-Oss granules and Bio-Oss Collagen in the treatment of periodontal intrabony defects: A retrospective cohort study","volume":"32","author":"Wang","year":"2024","journal-title":"J. Appl. Oral. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1111\/cid.13070","article-title":"Radiographic assessment of deproteinized bovine bone mineral (DBBM) and collagen-stabilized DBBM for transalveolar sinus floor elevation: A 2-year retrospective cohort study","volume":"24","author":"Wu","year":"2022","journal-title":"Clin. Implant Dent. Relat. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1111\/clr.12694","article-title":"A histomorphometric assessment of collagen-stabilized anorganic bovine bone mineral in maxillary sinus augmentation\u2014A prospective clinical trial","volume":"27","author":"Alayan","year":"2016","journal-title":"Clin. Oral Implants Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1111\/clr.12889","article-title":"Radiographic and histological evaluation of deproteinized bovine bone mineral vs. deproteinized bovine bone mineral with 10% collagen in ridge preservation. A randomized controlled clinical trial","volume":"28","author":"Nart","year":"2017","journal-title":"Clin. Oral Implants Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1002\/jbm.b.31529","article-title":"Physicochemical characterization of biomaterials commonly used in dentistry as bone substitutes\u2014Comparison with human bone","volume":"92","author":"Figueiredo","year":"2010","journal-title":"J. Biomed. Mater. Res. B Appl. Biomater."},{"key":"ref_41","first-page":"449","article-title":"Incidence, diagnosis, and treatment of sinus graft infection after sinus floor elevation: A clinical study","volume":"27","author":"Urban","year":"2012","journal-title":"Int. J. Oral Maxillofac. Implants"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Omori, Y., Botticelli, D., Ferri, M., Delgado-Ruiz, R., Ferreira Balan, V., and Porfirio Xavier, S. (2021). Argon Bioactivation of Implants Installed Simultaneously to Maxillary Sinus Lifting without Graft. An Experimental Study in Rabbits. Dent. J., 9.","DOI":"10.3390\/dj9090105"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"900","DOI":"10.4012\/dmj.2016-005","article-title":"Characterization and angiogenic potential of xenogeneic bone grafting materials: Role of periodontal ligament cells","volume":"35","author":"Rombouts","year":"2016","journal-title":"Dent. Mater. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1111\/clr.14123","article-title":"Mucosal adhesion phenomenon after maxillary sinus floor elevation: A preclinical study","volume":"34","author":"Nakajima","year":"2023","journal-title":"Clin. Oral Implants Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"879","DOI":"10.11607\/jomi.8226","article-title":"The Influence on Healing of Bony Window Elevated Inward in the Sinus Cavity as Cortical Bone Graft: A Histomorphometric Study in Rabbit Model","volume":"35","author":"Amari","year":"2020","journal-title":"Int. J. Oral Maxillofac. Implants"}],"container-title":["Dentistry Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-6767\/13\/1\/19\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T15:23:42Z","timestamp":1759850622000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-6767\/13\/1\/19"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,2]]},"references-count":45,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["dj13010019"],"URL":"https:\/\/doi.org\/10.3390\/dj13010019","relation":{},"ISSN":["2304-6767"],"issn-type":[{"value":"2304-6767","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,2]]}}}