Effects of adjacent periodontitis on osseointegrated dental implants

Effects of adjacent periodontitis on osseointegrated dental implants | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Effects of adjacent periodontitis on osseointegrated dental implants Keun-Soo Ryoo, Kyung-Hwa Kim, Young-Dan Cho, Yang-Jo Seol, Young Ku This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-2847235/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract This study aimed to investigate whether newly emerged periodontitis or apical periodontitis on the adjacent teeth affects osseointegrated dental implants in a beagle dog model. The mandibular second and fourth premolars on both sides of three beagles were extracted. Two months after extraction, four bone-level implant fixtures, two on both sides of each mandible, were placed in each beagle. Six weeks after implant surgery, healing abutments were connected. After sufficient osseointegration, plaque control was performed in the control group, while periodontitis and apical periodontitis were induced in the experimental groups. The beagles were euthanized for histological analyses five months after induction of experimental periodontitis. The implants in the control and apical periodontitis groups were well-maintained, while those in the periodontitis group showed clinical signs of inflammation with bone resorption. The bone-to-implant contact (BIC) and bone area (BA) values in the periodontitis group were lower than those in the other groups. The distance between the implant shoulder and the first BIC was significantly greater in the periodontitis group than in the control group. Unlike apical periodontitis, periodontitis of the teeth surrounding dental implants can induce peri-implantitis. Periodontal healthcare is essential for long-term dental implant survival. Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Osseointegration of dental implants results in stable anchorage with direct bone-to-implant contact. 1 The concept of osseointegration was first proposed by Brånemark et al., who observed firm anchorage of intra-osseous titanium implants in the rehabilitation of masticatory function in dogs. 2 Although the long-term survival rate of implants has been reported to be over 95%, 3,4 a number of factors can cause implant failure. These failures are classified into early and late failures depending on whether they occur before or after the development of osseointegration. 5 Early implant failures occur before or at abutment connection because of inadequate osseointegration due to interference in the healing process. 6 The main reason for such failures is the predominance of fibrous tissue formation between the implant surface and surrounding bone over osseointegration. 7 – 11 According to a prospective multicenter study on dental implants in partially edentulous patients, early failures were clustered in patients with high dental plaque and gingivitis indices. 12 Among the various etiologic factors of early failure, microorganisms are a common cause of failure of osseointegration, 12 – 14 while occlusal overloading or peri-implantitis are common reasons for late implant failure. 14 Several previous studies have reported that patients with a history of periodontitis may show more implant loss due to greater marginal bone loss and peri-implantitis than patients without a history of periodontitis. 15 – 17 In addition, we have previously shown that untreated experimental periodontitis was correlated with compromised osseointegration of dental implants. 18 Conversely, periodontitis after dental implantation may also affect implant survival; however, studies on this topic are still rare. Therefore, this study attempted to investigate whether newly emerging periodontitis or apical periodontitis of adjacent teeth affects osseointegrated dental implants in a beagle dog model. Results Clinical findings In the control and the apical periodontitis groups, all implant sites showed uneventful healing without significant inflammation (Fig. 1 d and 1 f). However, in the periodontitis group, the implants showed signs of inflammation with gingival swelling, redness, and pus discharge on the peri-implant mucosa (Fig. 1 e). One of the implants had failed at the time of euthanasia. Histologic findings Direct contact of the bone with the implants was observed in all groups (Fig. 2 ). Typical trabecular bone patterns surrounding the implants were observed in all groups, and osteocytes were embedded in the lacunae. No marked inflammatory cells were detected in the control (Fig. 2 a) and apical periodontitis (Fig. 2 c) groups. Furthermore, the marginal bone was intact for most of the implants in the control (Fig. 2 a) and apical periodontitis (Fig. 2 c) groups. However, the periodontitis group showed prominent marginal bone loss and infiltrated connective tissue (Fig. 2 b) as well as complete loss of the surrounding bone near the failed implant. Histometric analyses The BICs in the periodontitis group (mesial, 42.46% ± 28.82%; distal, 46.56% ± 33.20%) were lower than those in the control group (mesial, 65.49% ± 10.50%; distal, 74.82% ± 7.91%) and apical periodontitis group (mesial, 67.97% ± 9.35%; distal, 75.26% ± 9.86%), although the differences were not statistically significant (Table 1 ). Likewise, the BAs in the periodontitis group (mesial, 29.77% ± 29.94%; distal, 17.84% ± 33.23%) were lower than those in the control group (mesial, 65.89 ± 24.49; distal, 66.95% ± 4.33%) and the apical periodontitis group (mesial, 69.31% ± 21.40%; distal, 69.20% ± 12.76%); however, the differences were not statistically significant. The distal IS-fBIC value in the periodontitis group (distal, 4138.98 µm ± 3118.95 µm) was significantly higher than that in the control group (distal, 70.24 µm ± 65.60 µm) (P < 0.05). The BIC and BA of the failed implant were both considered 0%, while its IS-fBIC was counted as 8500 µm for the statistical analyses. Table 1 BIC, BA, and IS-fBIC values BIC (%) BA (%) IS-fBIC (µm) Control Mesial 65.49 ± 10.50 65.89 ± 24.49 75.80 ± 87.11 Distal 74.82 ± 7.91 66.95 ± 4.33 64.68 ± 129.35* Periodontitis Mesial 42.46 ± 28.82 29.77 ± 29.94 3495.78 ± 3567.63 Distal 46.56 ± 33.20 17.84 ± 33.23 4138.98 ± 3118.95* Apical periodontitis Mesial 67.97 ± 9.35 69.31 ± 21.40 210.90 ± 174.06 Distal 75.26 ± 9.86 69.20 ± 12.76 178.57 ± 178.31 BIC, Bone-to-Implant Contact from the first BIC (fBIC) at coronal part of implant to bottom BA, Bone Area surrounding implant in the region of the coronal 3.0 mm IS-fBIC, Distance between Implant Shoulder (IS) to the fBIC * P-value less than 0.05 by post hoc comparison using Kruskal-Wallis test with Bonferroni correction Discussion In the present study, the osseointegrated implants adjacent to teeth with experimentally induced periodontitis showed progressive bone loss along with inflammation on the peri-implant mucosa, while apical periodontitis did not have any notable effect on the peri-implant supporting bone during the experimental period. The average IS-fBIC values in the periodontitis group were the highest, and the distal IS-fBIC value in the periodontitis group was significantly higher than that in the control group. In the histological assessments, one of the osseointegrated implants in the periodontitis group failed due to progressive loss of the supporting bone. These results indicate that periodontitis induced in adjacent teeth can further affect the implant, resulting in peri-implantitis. One possible explanation for these findings could be the transmission of periodontopathic microbiota from teeth adjacent to implants. In one study investigating the correlation between periodontopathic bacteria in periodontal pockets and implant sulcus within individuals using polymerase chain reaction (PCR) detection, the authors reported that colonization of P. gingivalis and A. actinomycetemcomitans (A.a) between the periodontal pockets and the implant sulcus showed statistically significant correlation. 19 Another study reported that the colonization of periodontopathic bacteria such as A.a , F. nucleatum , Prevotella intermedia , P. gingivalis , and Treponema denticola at the implant sulcus was associated with the microbiota in the gingival crevice of the adjacent teeth instead of the contralateral and occluding teeth. 20 Our results showing that peri-implantitis was induced at implants adjacent to the teeth with periodontitis but not in those with apical periodontitis or in the control group is in line with the findings of previous studies regarding the transmission of microorganisms. On the other hand, several studies have reported the effects of periapical lesions on teeth adjacent to implants in relation to retrograde peri-implantitis, which is a distinct condition from peri-implantitis. 21 – 24 Retrograde peri-implantitis is defined as a symptomatic lesion presenting with progressive bone loss at the apex of the implants with intact peri-implant bone in the coronal portion. 25 Even though multiple etiological factors such as excess heat during osteotomy, 26 the presence of a pre-existing microbial pathology, 27 and residual lesions of extracted teeth 28 have been suggested, periapical lesions on neighboring teeth have been frequently mentioned. 22 According to a retrospective analysis, the prevalence of retrograde peri-implantitis is reported to be 1% in implants without endodontic pathology in adjacent teeth. However, the percentage increased to 25%, with an odds ratio of 8.0, when endodontic pathology was present in adjacent teeth. 22 Another retrospective study reported a prevalence of 7.8% with implants placed adjacent to endodontically treated teeth, suggesting that the presence of pre-existing inflammation in adjacent teeth may cause retrograde peri-implantitis. 23 However, the results of the present study showed no correlation between periapical lesions and retrograde peri-implantitis. In this experiment, periodontitis and apical periodontitis showed different outcomes, and the mechanism underlying these differences may be related to the distance between the teeth and implants. Regrettably, however, the underlying mechanisms were not investigated in this study, and we hope to address this topic in future studies. Methods Three experimental groups, namely, control, periodontitis, and apical periodontitis groups, were defined on the basis of the presence of experimental periodontitis or apical periodontitis, and one beagle dog was randomly assigned to each group. Animals All animal experiments were performed in accordance with the principles of the 3Rs (Replacement, Reduction, and Refinement) and under the Laboratory Animal Act established by the Ministry of Food and Drug Safe of Republic of Korea. This study was approved by the KNOTUS Institutional Animal Care and Use Committee of Incheon, Republic of Korea (KNOTUS IACUC 21-KE-1015), and all authors complied with the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines. Three male beagles aged 1–2 years and weighing 11–12 kg were used for the study. The beagle dogs were fed appropriately under standard laboratory conditions with ad libitum access to water and housed individually at an ambient temperature of 23°C ± 3°C and relative humidity of 55% ± 15%. The entire surgical procedure was performed under general anesthesia induced using intravenous alfaxalone 3 mg/kg (Alfaxan; Jurox, Kansas City, USA) and maintained with isoflurane 1–3% (Terrell; Kyongbo Pharmaceutical, Ansan, Republic of Korea). Local anesthesia at the surgical sites was induced by injecting 2% lidocaine hydrochloride with 1:100,000 epinephrine. Surgical procedures The experimental schedule and the surgical procedure are presented in Figs. 1 and 3 , respectively. The mandibular second and fourth premolars on both the left and right sides were extracted (Fig. 1 a). The teeth were cut in a buccolingual direction in the furcation region using a high-speed handpiece with a diamond point bur. The roots were extracted individually to minimize damage to the alveolar bone. Eight weeks after extraction, an incision was made in the midcrestal area in the edentulous sites on both the left and right sides, and full-thickness flaps were raised. Four implants, two implant fixtures on each side, were placed in each beagle (Fig. 1 b). The implants used for this study were internal-type bone-level implants (TSIII; Osstem Implant Co., Seoul, Korea) with a diameter of 3.5 mm and height of 8.5 mm. The surface of the implants was sandblasted with large grit and acid-etched (SLA), with an average surface roughness of Ra 2.0–3.0 µm. The screws were connected to the fixtures and the flaps were sutured with 5 − 0 nylon (Ethilon; Ethicon, Cornelia, USA). After 8 weeks of healing, full-thickness flaps were raised, and the cover screws were disconnected. Healing abutments with a diameter of 4.0 mm and a height of 3.0 mm were connected to the fixtures (Fig. 1 c). Induction of experimental periodontitis and apical periodontitis Ten weeks after implant placement, experimental periodontitis and apical periodontitis were induced in the experimental groups and oral hygiene care was provided to the control group. In the control group, oral hygiene care with scaling and plaque control procedures was performed monthly, and healthy periodontal conditions were confirmed clinically (Fig. 1 d) and radiographically (Fig. 4 a). Experimental periodontitis was induced using gingival retraction cords. Gingival retraction cords were soaked in a suspension of Porphyromonas gingivalis (P. gingivalis , ATCC 33277), ligatured at the cervical area of the mandibular first premolar (1P1), third premolar (3P3), and first molar (1M1), and packed into the gingival pocket. The condition of the retraction cords was routinely checked, and P. gingivalis was applied monthly. After approximately 20 weeks, experimental periodontitis was confirmed on the basis of clinical signs of gingival inflammation (Fig. 1 e) and radiographs showing alveolar bone loss (Fig. 4 b). Experimental apical periodontitis was induced at 1P1, 3P3, and 1M1 on both sides of the mandible. The pulp was exposed using a carbide round bur, and a suspension of P. gingivalis was injected into the pulp and sealed with a temporary restorative material (Caviton; GC, Tokyo, Japan) (Fig. 1 f). The procedure was performed monthly until the periapical lesion could be clearly verified on periapical radiographs (Fig. 4 c). The beagles were euthanized 20 weeks after the induction of experimental and apical periodontitis. Histologic examination and histometric analysis The mandibles of the beagles were retrieved and placed in 10% neutral buffered formalin. Tissue blocks, each containing the implant and surrounding soft and hard tissues, were prepared using a diamond saw (Exakt; Kulzer, Germany). Ground sectioning was performed according to previously described methods. 29 The specimens were dehydrated in increasing concentrations of ethanol and embedded in acrylic resin (Technovit 7200 VLC resin; Kulzer, Germany). Each block was sectioned mesiodistally parallel to the implant axis. Two sections were obtained near the center of the implant, and each section was reduced to approximately 50 µm by microgrinding. One was stained with Masson–Goldner’s trichrome and the other with hematoxylin and eosin. Digital images of the sections were obtained using a digital slide scanner (Panoramic 250 Flash III; 3DHistech, Hungary). Histological and histomorphometric analyses were performed using image analysis software (CaseViewer; 3DHistech, Hungary and Image-Pro Plus; Media Cybernetics, USA). The following data were obtained from the mesial and distal sides of each implant: 1) the percentage of bone-to-implant contact (BIC) from the first BIC (fBIC) at the coronal part of the implant to the bottom (Fig. 5 a); 2) the percentage of bone area (BA) in the areas of interest between the threads 30 in the region of the coronal 3.0 mm (Fig. 5 b); and 3) the distance between the implant shoulder (IS) and fBIC (IS-fBIC) (Fig. 5 c). Statistical analysis Mean values and standard deviations were calculated for each group. A normal distribution could not be assumed because of the sample size. The Kruskal–Wallis test was performed to compare the three groups, with Bonferroni correction for multiple comparisons. The significance level was set at a p-value of less than 0.05. Statistical analyses were performed using SPSS version 25.0 (IBM Software, Armonk, NY, USA). Declarations *These authors contributed equally to this study. Data availability statement The datasets used and/or analysed during the current study available from the corresponding author on reasonable request. Acknowledgments This study was supported by grant no. 07-2021-0009 from the SNUDH Research Fund and the Ministry of Science and ICT of Korea (NRF-2020R1C1C1005830), and the Bio & Medical Technology Development Program of the National Research Foundation (NRF) and funded by the Korean government (MSIT) (No. 2022M3A9F3082330). Author contribution Conceptualization: Y.-D.C., Y.K.; formal analysis: K.-S.R., K.-H.K.; investigation: data: K.-S.R., K.-H.K., Y.-D.C.; curation: K.-S.R., Y.-J.S.; methodology: Y.-D.C., Y.K., Y.-J.S.; project administration: Y.-D.C., Y.K.; writing – original draft preparation: K.-S.R; writing – review & editing: K.-S.R., K.-H.K., Y.-D.C., Y.-J.S., Y.K. All authors have read and agreed to the published version of the manuscript. Competing interests The authors declare no competing interests. References Albrektsson, T. & Johansson, C. Osteoinduction, osteoconduction and osseointegration. European spine journal 10 , S96-S101 (2001). Brånemark, P.-I. et al. Intra-osseous anchorage of dental prostheses: I. Experimental studies. Scandinavian journal of plastic and reconstructive surgery 3 , 81-100 (1969). Buser, D. et al. 10‐year survival and success rates of 511 titanium implants with a sandblasted and acid‐etched surface: a retrospective study in 303 partially edentulous patients. Clinical implant dentistry and related research 14 , 839-851 (2012). Fischer, K. & Stenberg, T. Prospective 10‐year cohort study based on a randomized controlled trial (RCT) on implant‐supported full‐arch maxillary prostheses. Part 1: sandblasted and acid‐etched implants and mucosal tissue. Clinical implant dentistry and related research 14 , 808-815 (2012). Esposito, M., Hirsch, J. M., Lekholm, U. & Thomsen, P. Biological factors contributing to failures of osseointegrated oral implants,(I). Success criteria and epidemiology. European journal of oral sciences 106 , 527-551 (1998). Manor, Y., Oubaid, S., Mardinger, O., Chaushu, G. & Nissan, J. Characteristics of early versus late implant failure: a retrospective study. Journal of Oral and Maxillofacial Surgery 67 , 2649-2652 (2009). Alsaadi, G., Quirynen, M., Komárek, A. & Van Steenberghe, D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. Journal of clinical periodontology 34 , 610-617 (2007). Olson, J. W. et al. Dental endosseous implant assessments in a type 2 diabetic population: a prospective study. International Journal of Oral & Maxillofacial Implants 15 (2000). Shernoff, A. F. et al. Implants for type II diabetic patients: Interim report. Implant dentistry 3 , 183-185 (1994). Kronström, M. et al. Humoral immunity host factors in subjects with failing or successful titanium dental implants. Journal of clinical periodontology 27 , 875-882 (2000). Kronström, M., Svenson, B., Hellman, M. & Persson, G. R. Early implant failures in patients treated with Brånemark System titanium dental implants: a retrospective study. International Journal of Oral & Maxillofacial Implants 16 (2001). van Steenberghe, D. et al. The Applicability of Osseointegrated Oral Implants in the Rehabilitation of Partial Edentulism: A Prospective Multicenter Study on 558 Fixtures. International Journal of Oral & Maxillofacial Implants 5 (1990). van Steenberghe, D., Quirynen, M. & Naert, I. in European Workshop on Periodontology, Date: 1999/01/01-1999/01/01. Quirynen, M. & Teughels, W. Microbiologically compromised patients and impact on oral implants. Periodontology 2000 33 , 119-128 (2003). Kim, Y.-K. et al. The seven-year cumulative survival rate of Osstem implants. Journal of the Korean Association of Oral and Maxillofacial Surgeons 40 , 68 (2014). Ferreira, S., Silva, G. M., Cortelli, J. R., Costa, J. & Costa, F. Prevalence and risk variables for peri‐implant disease in Brazilian subjects. Journal of clinical periodontology 33 , 929-935 (2006). Karoussis, I. K. et al. Long‐term implant prognosis in patients with and without a history of chronic periodontitis: a 10‐year prospective cohort study of the ITI® Dental Implant System. Clinical oral implants research 14 , 329-339 (2003). Lee, D. et al. Effects of Untreated Periodontitis on Osseointegration of Dental Implants in a Beagle Dog Model. J. Periodontol. 87 , 1141-1148, doi:10.1902/jop.2016.160121 (2016). Sumida, S., Ishihara, K., Kishi, M. & Okuda, K. Transmission of periodontal disease-associated bacteria from teeth to osseointegrated implant regions. International Journal of Oral & Maxillofacial Implants 17 (2002). Aoki, M. et al. Transmission of periodontopathic bacteria from natural teeth to implants. Clinical implant dentistry and related research 14 , 406-411 (2012). Sarmast, N. D., Wang, H. H., Sajadi, A. S., Angelov, N. & Dorn, S. O. Classification and clinical management of retrograde peri-implantitis associated with apical periodontitis: a proposed classification system and case report. Journal of Endodontics 43 , 1921-1924 (2017). Lefever, D., Van Assche, N., Temmerman, A., Teughels, W. & Quirynen, M. Aetiology, microbiology and therapy of periapical lesions around oral implants: a retrospective analysis. Journal of clinical periodontology 40 , 296-302 (2013). Zhou, W. et al. Endodontic treatment of teeth induces retrograde peri‐implantitis. Clinical oral implants research 20 , 1326-1332 (2009). Sarmast, N. D. et al. A novel treatment decision tree and literature review of retrograde peri‐implantitis. Journal of periodontology 87 , 1458-1467 (2016). Quirynen, M., Gijbels, F. & Jacobs, R. An infected jawbone site compromising successful osseointegration. Periodontology 2000 33 , 129-144 (2003). Piattelli, A., Scarano, A., Balleri, P. & Favero, G. A. Clinical and histologic evaluation of an active" implant periapical lesion": a case report. International Journal of Oral & Maxillofacial Implants 13 (1998). El Askary, A. S., Meffert, R. M. & Griffin, T. Why do dental implants fail? Part I. Implant dentistry 8 , 173-185 (1999). Ayangco, L. & Sheridan, P. J. Development and treatment of retrograde peri-implantitis involving a site with a history of failed endodontic and apicoectomy procedures: a series of reports. International Journal of Oral & Maxillofacial Implants 16 (2001). Donath, K. & Breuner, G. A method for the study of undecalcified bones and teeth with attached soft tissues* The Säge‐Schliff (sawing and grinding) Technique. Journal of Oral Pathology & Medicine 11 , 318-326 (1982). Vignoletti, F. et al. Early healing of implants placed into fresh extraction sockets: an experimental study in the beagle dog. De novo bone formation. Journal of Clinical Periodontology 36 , 265-277 (2009). Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-2847235","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":197499514,"identity":"2aa1a107-f614-43a1-ae01-df066068f821","order_by":0,"name":"Keun-Soo Ryoo","email":"","orcid":"","institution":"Seoul National University and Seoul National University Dental Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Keun-Soo","middleName":"","lastName":"Ryoo","suffix":""},{"id":197499515,"identity":"f2cc373d-0f5f-4bcd-a638-bd0fe015ab4e","order_by":1,"name":"Kyung-Hwa Kim","email":"","orcid":"","institution":"Seoul National University and Seoul National University Dental Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Kyung-Hwa","middleName":"","lastName":"Kim","suffix":""},{"id":197499516,"identity":"bdb32cea-a019-490d-a852-e4fdcab75661","order_by":2,"name":"Young-Dan Cho","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAuklEQVRIiWNgGAWjYLACHgYJORjbgFgtFsYka6lIbCBaC3/74YcP3uZIpM+f3WPA8KOGwdi8gYAWiTNpxoZzt0nkbrhzxoCx5xiDmcwBAloMGHLYpHlBWiRyDBh4GxhsJAg5zID/DVhLuvyMHAPGv0RpkYDYksBwI8eAGWiLGUEtEjeegf1iuOFGWsFhmWMSxgS18PcnA0NsW528/IzkjQ/f1NgYziCkBQUcANpKkoZRMApGwSgYBTgAAGRpNfYgURA3AAAAAElFTkSuQmCC","orcid":"","institution":"Seoul National University and Seoul National University Dental Hospital","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Young-Dan","middleName":"","lastName":"Cho","suffix":""},{"id":197499517,"identity":"9e1493a8-6064-4491-b0de-0358e6ebf9b6","order_by":3,"name":"Yang-Jo Seol","email":"","orcid":"","institution":"Seoul National University and Seoul National University Dental Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Yang-Jo","middleName":"","lastName":"Seol","suffix":""},{"id":197499518,"identity":"4d86fe9c-b796-4504-9d50-f15bc906ceaf","order_by":4,"name":"Young Ku","email":"","orcid":"","institution":"Seoul National University and Seoul National University Dental Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Young","middleName":"","lastName":"Ku","suffix":""}],"badges":[],"createdAt":"2023-04-22 03:14:15","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-2847235/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-2847235/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":36708097,"identity":"ff340780-eb1c-4e76-ba63-54c09cfb862d","added_by":"auto","created_at":"2023-05-08 14:40:00","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":3372992,"visible":true,"origin":"","legend":"\u003cp\u003eClinical photos of the experimental procedure\u003c/p\u003e\n\u003cp\u003e(a) At 8 weeks after tooth extraction, the ridge had healed well. (b) The first implant operation to place the fixtures was performed in the healed ridge. (c) At 6 weeks after implant placement, the second implant operation to connect healing abutments was performed. (d-f) At 2 weeks after healing abutment connection, scaling and plaque control were performed in the control group, and experimental periodontitis and apical periodontitis were induced in the experimental groups. At 20 weeks after induction of the experimental conditions, the control (d) and apical periodontitis (f) groups showed a favorable gingival condition, but the periodontitis group showed gingival inflammation (e).\u003c/p\u003e","description":"","filename":"figure1..png","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/b7a7b97021e91faf6f5103da.png"},{"id":36708096,"identity":"3805cf73-258f-4851-b3f7-2d01e935d4b5","added_by":"auto","created_at":"2023-05-08 14:39:59","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":1985082,"visible":true,"origin":"","legend":"\u003cp\u003eHistologic images of all groups\u003c/p\u003e\n\u003cp\u003e(a) Control, (b) periodontitis, (C) apical periodontitis. Scale bar = 2.0 mm\u003c/p\u003e","description":"","filename":"figure2..png","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/8091724ab6051488576ffd84.png"},{"id":36708098,"identity":"42183b8f-9e95-4b07-8af9-9f52fbf451e6","added_by":"auto","created_at":"2023-05-08 14:40:00","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":19618,"visible":true,"origin":"","legend":"\u003cp\u003eExperimental procedure\u003c/p\u003e\n\u003cp\u003eImplants were placed eight weeks after tooth extraction in all groups. Healing abutments were connected at 8 weeks after implant placementin all groups. After two weeks of healing, abutment connection, scaling, and plaque control were performed in the control group, and experimental periodontitis and apical periodontitis were induced in groups 2 and 3, respectively. All beagles were euthanized 20 weeks after the induction of periodontitis.\u003c/p\u003e","description":"","filename":"figure3..png","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/8e89d0dde54270844a14f7c5.png"},{"id":36708099,"identity":"ce37fbc7-bb0a-40bf-9d29-0048d15ee11d","added_by":"auto","created_at":"2023-05-08 14:40:00","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":925778,"visible":true,"origin":"","legend":"\u003cp\u003eRadiographs obtained before and after induction of experimental periodontitis and apical periodontitis\u003c/p\u003e\n\u003cp\u003eThe left column shows the radiographs obtained before the induction of periodontitis, and the right column shows the radiographs obtained 20 weeks after induction. (a) Control, (b) periodontitis, and (C) apical periodontitis\u003c/p\u003e","description":"","filename":"figure4..png","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/718b3af5b778de9a9dfea5b5.png"},{"id":36708914,"identity":"5e3c0320-224e-4d47-820c-68d6315cfce2","added_by":"auto","created_at":"2023-05-08 14:48:00","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":2966077,"visible":true,"origin":"","legend":"\u003cp\u003eMethods for histometric analysis\u003c/p\u003e\n\u003cp\u003e(a) The length of the bone-to-implant contact was measured from the mesial and distal sides of the implant surface, and the percentage of BIC was calculated from these lengths. (b) The area within the implant threads and the reproduced mirror area were chosen as the area of interest for analyzing BAs. (c) IS and fBIC measurements were used to evaluate marginal bone loss.\u003c/p\u003e","description":"","filename":"figure5..png","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/9d397b826c8478a4e2b4e56d.png"},{"id":36761896,"identity":"6602c1e6-497d-489e-9597-c36cf60ea52e","added_by":"auto","created_at":"2023-05-10 02:14:36","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2618827,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-2847235/v1/34f672e9-4e5f-4070-b5b3-84d37bca3112.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Effects of adjacent periodontitis on osseointegrated dental implants","fulltext":[{"header":"Introduction","content":"\u003cp\u003eOsseointegration of dental implants results in stable anchorage with direct bone-to-implant contact.\u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u003c/sup\u003e The concept of osseointegration was first proposed by Br\u0026aring;nemark et al., who observed firm anchorage of intra-osseous titanium implants in the rehabilitation of masticatory function in dogs.\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u003c/sup\u003e Although the long-term survival rate of implants has been reported to be over 95%,\u003csup\u003e3,4\u003c/sup\u003e a number of factors can cause implant failure. These failures are classified into early and late failures depending on whether they occur before or after the development of osseointegration.\u003csup\u003e\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e\u003c/sup\u003e Early implant failures occur before or at abutment connection because of inadequate osseointegration due to interference in the healing process.\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e The main reason for such failures is the predominance of fibrous tissue formation between the implant surface and surrounding bone over osseointegration.\u003csup\u003e\u003cspan additionalcitationids=\"CR8 CR9 CR10\" citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u003c/sup\u003e According to a prospective multicenter study on dental implants in partially edentulous patients, early failures were clustered in patients with high dental plaque and gingivitis indices.\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e Among the various etiologic factors of early failure, microorganisms are a common cause of failure of osseointegration,\u003csup\u003e\u003cspan additionalcitationids=\"CR13\" citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e while occlusal overloading or peri-implantitis are common reasons for late implant failure.\u003csup\u003e\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eSeveral previous studies have reported that patients with a history of periodontitis may show more implant loss due to greater marginal bone loss and peri-implantitis than patients without a history of periodontitis.\u003csup\u003e\u003cspan additionalcitationids=\"CR16\" citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e\u003c/sup\u003e In addition, we have previously shown that untreated experimental periodontitis was correlated with compromised osseointegration of dental implants.\u003csup\u003e\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e\u003c/sup\u003e Conversely, periodontitis after dental implantation may also affect implant survival; however, studies on this topic are still rare. Therefore, this study attempted to investigate whether newly emerging periodontitis or apical periodontitis of adjacent teeth affects osseointegrated dental implants in a beagle dog model.\u003c/p\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eClinical findings\u003c/h2\u003e \u003cp\u003eIn the control and the apical periodontitis groups, all implant sites showed uneventful healing without significant inflammation (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ed and \u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ef). However, in the periodontitis group, the implants showed signs of inflammation with gingival swelling, redness, and pus discharge on the peri-implant mucosa (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ee). One of the implants had failed at the time of euthanasia.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eHistologic findings\u003c/h2\u003e \u003cp\u003eDirect contact of the bone with the implants was observed in all groups (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Typical trabecular bone patterns surrounding the implants were observed in all groups, and osteocytes were embedded in the lacunae. No marked inflammatory cells were detected in the control (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea) and apical periodontitis (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ec) groups. Furthermore, the marginal bone was intact for most of the implants in the control (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea) and apical periodontitis (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ec) groups. However, the periodontitis group showed prominent marginal bone loss and infiltrated connective tissue (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eb) as well as complete loss of the surrounding bone near the failed implant.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eHistometric analyses\u003c/h2\u003e \u003cp\u003eThe BICs in the periodontitis group (mesial, 42.46% \u0026plusmn; 28.82%; distal, 46.56% \u0026plusmn; 33.20%) were lower than those in the control group (mesial, 65.49% \u0026plusmn; 10.50%; distal, 74.82% \u0026plusmn; 7.91%) and apical periodontitis group (mesial, 67.97% \u0026plusmn; 9.35%; distal, 75.26% \u0026plusmn; 9.86%), although the differences were not statistically significant (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Likewise, the BAs in the periodontitis group (mesial, 29.77% \u0026plusmn; 29.94%; distal, 17.84% \u0026plusmn; 33.23%) were lower than those in the control group (mesial, 65.89\u0026thinsp;\u0026plusmn;\u0026thinsp;24.49; distal, 66.95% \u0026plusmn; 4.33%) and the apical periodontitis group (mesial, 69.31% \u0026plusmn; 21.40%; distal, 69.20% \u0026plusmn; 12.76%); however, the differences were not statistically significant. The distal IS-fBIC value in the periodontitis group (distal, 4138.98 \u0026micro;m\u0026thinsp;\u0026plusmn;\u0026thinsp;3118.95 \u0026micro;m) was significantly higher than that in the control group (distal, 70.24 \u0026micro;m\u0026thinsp;\u0026plusmn;\u0026thinsp;65.60 \u0026micro;m) (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05). The BIC and BA of the failed implant were both considered 0%, while its IS-fBIC was counted as 8500 \u0026micro;m for the statistical analyses.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eBIC, BA, and IS-fBIC values\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eBIC (%)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eBA (%)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eIS-fBIC (\u0026micro;m)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMesial\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e65.49\u0026thinsp;\u0026plusmn;\u0026thinsp;10.50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e65.89\u0026thinsp;\u0026plusmn;\u0026thinsp;24.49\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e75.80\u0026thinsp;\u0026plusmn;\u0026thinsp;87.11\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDistal\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e74.82\u0026thinsp;\u0026plusmn;\u0026thinsp;7.91\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e66.95\u0026thinsp;\u0026plusmn;\u0026thinsp;4.33\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e64.68\u0026thinsp;\u0026plusmn;\u0026thinsp;129.35*\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003ePeriodontitis\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colspan=\"1\" nameend=\"c4\" namest=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMesial\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e42.46\u0026thinsp;\u0026plusmn;\u0026thinsp;28.82\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e29.77\u0026thinsp;\u0026plusmn;\u0026thinsp;29.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e3495.78\u0026thinsp;\u0026plusmn;\u0026thinsp;3567.63\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDistal\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e46.56\u0026thinsp;\u0026plusmn;\u0026thinsp;33.20\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e17.84\u0026thinsp;\u0026plusmn;\u0026thinsp;33.23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e4138.98\u0026thinsp;\u0026plusmn;\u0026thinsp;3118.95*\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eApical periodontitis\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMesial\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e67.97\u0026thinsp;\u0026plusmn;\u0026thinsp;9.35\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e69.31\u0026thinsp;\u0026plusmn;\u0026thinsp;21.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e210.90\u0026thinsp;\u0026plusmn;\u0026thinsp;174.06\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDistal\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e75.26\u0026thinsp;\u0026plusmn;\u0026thinsp;9.86\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e69.20\u0026thinsp;\u0026plusmn;\u0026thinsp;12.76\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e178.57\u0026thinsp;\u0026plusmn;\u0026thinsp;178.31\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eBIC, Bone-to-Implant Contact from the first BIC (fBIC) at coronal part of implant to bottom\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eBA, Bone Area surrounding implant in the region of the coronal 3.0 mm\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eIS-fBIC, Distance between Implant Shoulder (IS) to the fBIC\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003e* P-value less than 0.05 by post hoc comparison using Kruskal-Wallis test with Bonferroni correction\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn the present study, the osseointegrated implants adjacent to teeth with experimentally induced periodontitis showed progressive bone loss along with inflammation on the peri-implant mucosa, while apical periodontitis did not have any notable effect on the peri-implant supporting bone during the experimental period. The average IS-fBIC values in the periodontitis group were the highest, and the distal IS-fBIC value in the periodontitis group was significantly higher than that in the control group. In the histological assessments, one of the osseointegrated implants in the periodontitis group failed due to progressive loss of the supporting bone. These results indicate that periodontitis induced in adjacent teeth can further affect the implant, resulting in peri-implantitis.\u003c/p\u003e \u003cp\u003eOne possible explanation for these findings could be the transmission of periodontopathic microbiota from teeth adjacent to implants. In one study investigating the correlation between periodontopathic bacteria in periodontal pockets and implant sulcus within individuals using polymerase chain reaction (PCR) detection, the authors reported that colonization of \u003cem\u003eP. gingivalis\u003c/em\u003e and \u003cem\u003eA. actinomycetemcomitans (A.a)\u003c/em\u003e between the periodontal pockets and the implant sulcus showed statistically significant correlation.\u003csup\u003e\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e\u003c/sup\u003e Another study reported that the colonization of periodontopathic bacteria such as \u003cem\u003eA.a\u003c/em\u003e, \u003cem\u003eF. nucleatum\u003c/em\u003e, \u003cem\u003ePrevotella intermedia\u003c/em\u003e, \u003cem\u003eP. gingivalis\u003c/em\u003e, and \u003cem\u003eTreponema denticola\u003c/em\u003e at the implant sulcus was associated with the microbiota in the gingival crevice of the adjacent teeth instead of the contralateral and occluding teeth.\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e Our results showing that peri-implantitis was induced at implants adjacent to the teeth with periodontitis but not in those with apical periodontitis or in the control group is in line with the findings of previous studies regarding the transmission of microorganisms.\u003c/p\u003e \u003cp\u003eOn the other hand, several studies have reported the effects of periapical lesions on teeth adjacent to implants in relation to retrograde peri-implantitis, which is a distinct condition from peri-implantitis.\u003csup\u003e\u003cspan additionalcitationids=\"CR22 CR23\" citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u003c/sup\u003e Retrograde peri-implantitis is defined as a symptomatic lesion presenting with progressive bone loss at the apex of the implants with intact peri-implant bone in the coronal portion.\u003csup\u003e\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e\u003c/sup\u003e Even though multiple etiological factors such as excess heat during osteotomy,\u003csup\u003e\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e\u003c/sup\u003e the presence of a pre-existing microbial pathology,\u003csup\u003e\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e and residual lesions of extracted teeth\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e have been suggested, periapical lesions on neighboring teeth have been frequently mentioned.\u003csup\u003e\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u003c/sup\u003e According to a retrospective analysis, the prevalence of retrograde peri-implantitis is reported to be 1% in implants without endodontic pathology in adjacent teeth. However, the percentage increased to 25%, with an odds ratio of 8.0, when endodontic pathology was present in adjacent teeth.\u003csup\u003e\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u003c/sup\u003e Another retrospective study reported a prevalence of 7.8% with implants placed adjacent to endodontically treated teeth, suggesting that the presence of pre-existing inflammation in adjacent teeth may cause retrograde peri-implantitis. \u003csup\u003e\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e\u003c/sup\u003e However, the results of the present study showed no correlation between periapical lesions and retrograde peri-implantitis.\u003c/p\u003e \u003cp\u003eIn this experiment, periodontitis and apical periodontitis showed different outcomes, and the mechanism underlying these differences may be related to the distance between the teeth and implants. Regrettably, however, the underlying mechanisms were not investigated in this study, and we hope to address this topic in future studies.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eThree experimental groups, namely, control, periodontitis, and apical periodontitis groups, were defined on the basis of the presence of experimental periodontitis or apical periodontitis, and one beagle dog was randomly assigned to each group.\u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eAnimals\u003c/h2\u003e \u003cp\u003e All animal experiments were performed in accordance with the principles of the 3Rs (Replacement, Reduction, and Refinement) and under the Laboratory Animal Act established by the Ministry of Food and Drug Safe of Republic of Korea. This study was approved by the KNOTUS Institutional Animal Care and Use Committee of Incheon, Republic of Korea (KNOTUS IACUC 21-KE-1015), and all authors complied with the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines. Three male beagles aged 1\u0026ndash;2 years and weighing 11\u0026ndash;12 kg were used for the study. The beagle dogs were fed appropriately under standard laboratory conditions with \u003cem\u003ead libitum\u003c/em\u003e access to water and housed individually at an ambient temperature of 23\u0026deg;C\u0026thinsp;\u0026plusmn;\u0026thinsp;3\u0026deg;C and relative humidity of 55% \u0026plusmn; 15%. The entire surgical procedure was performed under general anesthesia induced using intravenous alfaxalone 3 mg/kg (Alfaxan; Jurox, Kansas City, USA) and maintained with isoflurane 1\u0026ndash;3% (Terrell; Kyongbo Pharmaceutical, Ansan, Republic of Korea). Local anesthesia at the surgical sites was induced by injecting 2% lidocaine hydrochloride with 1:100,000 epinephrine.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eSurgical procedures\u003c/h2\u003e \u003cp\u003eThe experimental schedule and the surgical procedure are presented in Figs.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e and \u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e, respectively. The mandibular second and fourth premolars on both the left and right sides were extracted (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea). The teeth were cut in a buccolingual direction in the furcation region using a high-speed handpiece with a diamond point bur. The roots were extracted individually to minimize damage to the alveolar bone. Eight weeks after extraction, an incision was made in the midcrestal area in the edentulous sites on both the left and right sides, and full-thickness flaps were raised. Four implants, two implant fixtures on each side, were placed in each beagle (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eb). The implants used for this study were internal-type bone-level implants (TSIII; Osstem Implant Co., Seoul, Korea) with a diameter of 3.5 mm and height of 8.5 mm. The surface of the implants was sandblasted with large grit and acid-etched (SLA), with an average surface roughness of Ra 2.0\u0026ndash;3.0 \u0026micro;m. The screws were connected to the fixtures and the flaps were sutured with 5\u0026thinsp;\u0026minus;\u0026thinsp;0 nylon (Ethilon; Ethicon, Cornelia, USA). After 8 weeks of healing, full-thickness flaps were raised, and the cover screws were disconnected. Healing abutments with a diameter of 4.0 mm and a height of 3.0 mm were connected to the fixtures (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ec).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eInduction of experimental periodontitis and apical periodontitis\u003c/h2\u003e \u003cp\u003eTen weeks after implant placement, experimental periodontitis and apical periodontitis were induced in the experimental groups and oral hygiene care was provided to the control group. In the control group, oral hygiene care with scaling and plaque control procedures was performed monthly, and healthy periodontal conditions were confirmed clinically (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ed) and radiographically (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ea). Experimental periodontitis was induced using gingival retraction cords. Gingival retraction cords were soaked in a suspension of \u003cem\u003ePorphyromonas gingivalis (P. gingivalis\u003c/em\u003e, ATCC 33277), ligatured at the cervical area of the mandibular first premolar (1P1), third premolar (3P3), and first molar (1M1), and packed into the gingival pocket. The condition of the retraction cords was routinely checked, and \u003cem\u003eP. gingivalis\u003c/em\u003e was applied monthly. After approximately 20 weeks, experimental periodontitis was confirmed on the basis of clinical signs of gingival inflammation (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ee) and radiographs showing alveolar bone loss (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eb). Experimental apical periodontitis was induced at 1P1, 3P3, and 1M1 on both sides of the mandible. The pulp was exposed using a carbide round bur, and a suspension of \u003cem\u003eP. gingivalis\u003c/em\u003e was injected into the pulp and sealed with a temporary restorative material (Caviton; GC, Tokyo, Japan) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ef). The procedure was performed monthly until the periapical lesion could be clearly verified on periapical radiographs (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ec). The beagles were euthanized 20 weeks after the induction of experimental and apical periodontitis.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eHistologic examination and histometric analysis\u003c/h2\u003e \u003cp\u003eThe mandibles of the beagles were retrieved and placed in 10% neutral buffered formalin. Tissue blocks, each containing the implant and surrounding soft and hard tissues, were prepared using a diamond saw (Exakt; Kulzer, Germany). Ground sectioning was performed according to previously described methods.\u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u003c/sup\u003e The specimens were dehydrated in increasing concentrations of ethanol and embedded in acrylic resin (Technovit 7200 VLC resin; Kulzer, Germany). Each block was sectioned mesiodistally parallel to the implant axis. Two sections were obtained near the center of the implant, and each section was reduced to approximately 50 \u0026micro;m by microgrinding. One was stained with Masson\u0026ndash;Goldner\u0026rsquo;s trichrome and the other with hematoxylin and eosin. Digital images of the sections were obtained using a digital slide scanner (Panoramic 250 Flash III; 3DHistech, Hungary). Histological and histomorphometric analyses were performed using image analysis software (CaseViewer; 3DHistech, Hungary and Image-Pro Plus; Media Cybernetics, USA). The following data were obtained from the mesial and distal sides of each implant: 1) the percentage of bone-to-implant contact (BIC) from the first BIC (fBIC) at the coronal part of the implant to the bottom (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ea); 2) the percentage of bone area (BA) in the areas of interest between the threads\u003csup\u003e\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e\u003c/sup\u003e in the region of the coronal 3.0 mm (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003eb); and 3) the distance between the implant shoulder (IS) and fBIC (IS-fBIC) (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ec).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eMean values and standard deviations were calculated for each group. A normal distribution could not be assumed because of the sample size. The Kruskal\u0026ndash;Wallis test was performed to compare the three groups, with Bonferroni correction for multiple comparisons. The significance level was set at a p-value of less than 0.05. Statistical analyses were performed using SPSS version 25.0 (IBM Software, Armonk, NY, USA).\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e*These authors contributed equally to this study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and/or analysed during the current study available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study was supported by grant no. 07-2021-0009 from the SNUDH Research Fund and the Ministry of Science and ICT of Korea (NRF-2020R1C1C1005830), and the Bio \u0026amp; Medical Technology Development Program of the National Research Foundation (NRF) and funded by the Korean government (MSIT) (No. 2022M3A9F3082330).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003eAuthor contribution\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eConceptualization: Y.-D.C., Y.K.; formal analysis: K.-S.R., K.-H.K.; investigation: data: K.-S.R., K.-H.K., Y.-D.C.; curation: K.-S.R., Y.-J.S.; methodology: Y.-D.C., Y.K., Y.-J.S.; project administration: Y.-D.C., Y.K.; writing \u0026ndash; original draft preparation: K.-S.R; writing \u0026ndash; review \u0026amp; editing: K.-S.R., K.-H.K., Y.-D.C., Y.-J.S., Y.K. All authors have read and agreed to the published version of the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAlbrektsson, T. \u0026amp; Johansson, C. Osteoinduction, osteoconduction and osseointegration. \u003cem\u003eEuropean spine journal\u003c/em\u003e \u003cstrong\u003e10\u003c/strong\u003e, S96-S101 (2001).\u003c/li\u003e\n\u003cli\u003eBr\u0026aring;nemark, P.-I.\u003cem\u003e et al.\u003c/em\u003e Intra-osseous anchorage of dental prostheses: I. Experimental studies. \u003cem\u003eScandinavian journal of plastic and reconstructive surgery\u003c/em\u003e \u003cstrong\u003e3\u003c/strong\u003e, 81-100 (1969).\u003c/li\u003e\n\u003cli\u003eBuser, D.\u003cem\u003e et al.\u003c/em\u003e 10‐year survival and success rates of 511 titanium implants with a sandblasted and acid‐etched surface: a retrospective study in 303 partially edentulous patients. \u003cem\u003eClinical implant dentistry and related research\u003c/em\u003e \u003cstrong\u003e14\u003c/strong\u003e, 839-851 (2012).\u003c/li\u003e\n\u003cli\u003eFischer, K. \u0026amp; Stenberg, T. Prospective 10‐year cohort study based on a randomized controlled trial (RCT) on implant‐supported full‐arch maxillary prostheses. Part 1: sandblasted and acid‐etched implants and mucosal tissue. \u003cem\u003eClinical implant dentistry and related research\u003c/em\u003e \u003cstrong\u003e14\u003c/strong\u003e, 808-815 (2012).\u003c/li\u003e\n\u003cli\u003eEsposito, M., Hirsch, J. M., Lekholm, U. \u0026amp; Thomsen, P. Biological factors contributing to failures of osseointegrated oral implants,(I). Success criteria and epidemiology. \u003cem\u003eEuropean journal of oral sciences\u003c/em\u003e \u003cstrong\u003e106\u003c/strong\u003e, 527-551 (1998).\u003c/li\u003e\n\u003cli\u003eManor, Y., Oubaid, S., Mardinger, O., Chaushu, G. \u0026amp; Nissan, J. Characteristics of early versus late implant failure: a retrospective study. \u003cem\u003eJournal of Oral and Maxillofacial Surgery\u003c/em\u003e \u003cstrong\u003e67\u003c/strong\u003e, 2649-2652 (2009).\u003c/li\u003e\n\u003cli\u003eAlsaadi, G., Quirynen, M., Kom\u0026aacute;rek, A. \u0026amp; Van Steenberghe, D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. \u003cem\u003eJournal of clinical periodontology\u003c/em\u003e \u003cstrong\u003e34\u003c/strong\u003e, 610-617 (2007).\u003c/li\u003e\n\u003cli\u003eOlson, J. W.\u003cem\u003e et al.\u003c/em\u003e Dental endosseous implant assessments in a type 2 diabetic population: a prospective study. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e15\u003c/strong\u003e (2000).\u003c/li\u003e\n\u003cli\u003eShernoff, A. F.\u003cem\u003e et al.\u003c/em\u003e Implants for type II diabetic patients: Interim report. \u003cem\u003eImplant dentistry\u003c/em\u003e \u003cstrong\u003e3\u003c/strong\u003e, 183-185 (1994).\u003c/li\u003e\n\u003cli\u003eKronstr\u0026ouml;m, M.\u003cem\u003e et al.\u003c/em\u003e Humoral immunity host factors in subjects with failing or successful titanium dental implants. \u003cem\u003eJournal of clinical periodontology\u003c/em\u003e \u003cstrong\u003e27\u003c/strong\u003e, 875-882 (2000).\u003c/li\u003e\n\u003cli\u003eKronstr\u0026ouml;m, M., Svenson, B., Hellman, M. \u0026amp; Persson, G. R. Early implant failures in patients treated with Br\u0026aring;nemark System titanium dental implants: a retrospective study. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e16\u003c/strong\u003e (2001).\u003c/li\u003e\n\u003cli\u003evan Steenberghe, D.\u003cem\u003e et al.\u003c/em\u003e The Applicability of Osseointegrated Oral Implants in the Rehabilitation of Partial Edentulism: A Prospective Multicenter Study on 558 Fixtures. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e5\u003c/strong\u003e (1990).\u003c/li\u003e\n\u003cli\u003evan Steenberghe, D., Quirynen, M. \u0026amp; Naert, I. in \u003cem\u003eEuropean Workshop on Periodontology, Date: 1999/01/01-1999/01/01.\u003c/em\u003e\u003c/li\u003e\n\u003cli\u003eQuirynen, M. \u0026amp; Teughels, W. Microbiologically compromised patients and impact on oral implants. \u003cem\u003ePeriodontology 2000\u003c/em\u003e \u003cstrong\u003e33\u003c/strong\u003e, 119-128 (2003).\u003c/li\u003e\n\u003cli\u003eKim, Y.-K.\u003cem\u003e et al.\u003c/em\u003e The seven-year cumulative survival rate of Osstem implants. \u003cem\u003eJournal of the Korean Association of Oral and Maxillofacial Surgeons\u003c/em\u003e \u003cstrong\u003e40\u003c/strong\u003e, 68 (2014).\u003c/li\u003e\n\u003cli\u003eFerreira, S., Silva, G. M., Cortelli, J. R., Costa, J. \u0026amp; Costa, F. Prevalence and risk variables for peri‐implant disease in Brazilian subjects. \u003cem\u003eJournal of clinical periodontology\u003c/em\u003e \u003cstrong\u003e33\u003c/strong\u003e, 929-935 (2006).\u003c/li\u003e\n\u003cli\u003eKaroussis, I. K.\u003cem\u003e et al.\u003c/em\u003e Long‐term implant prognosis in patients with and without a history of chronic periodontitis: a 10‐year prospective cohort study of the ITI\u0026reg; Dental Implant System. \u003cem\u003eClinical oral implants research\u003c/em\u003e \u003cstrong\u003e14\u003c/strong\u003e, 329-339 (2003).\u003c/li\u003e\n\u003cli\u003eLee, D.\u003cem\u003e et al.\u003c/em\u003e Effects of Untreated Periodontitis on Osseointegration of Dental Implants in a Beagle Dog Model. \u003cem\u003eJ. Periodontol.\u003c/em\u003e \u003cstrong\u003e87\u003c/strong\u003e, 1141-1148, doi:10.1902/jop.2016.160121 (2016).\u003c/li\u003e\n\u003cli\u003eSumida, S., Ishihara, K., Kishi, M. \u0026amp; Okuda, K. Transmission of periodontal disease-associated bacteria from teeth to osseointegrated implant regions. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e17\u003c/strong\u003e (2002).\u003c/li\u003e\n\u003cli\u003eAoki, M.\u003cem\u003e et al.\u003c/em\u003e Transmission of periodontopathic bacteria from natural teeth to implants. \u003cem\u003eClinical implant dentistry and related research\u003c/em\u003e \u003cstrong\u003e14\u003c/strong\u003e, 406-411 (2012).\u003c/li\u003e\n\u003cli\u003eSarmast, N. D., Wang, H. H., Sajadi, A. S., Angelov, N. \u0026amp; Dorn, S. O. Classification and clinical management of retrograde peri-implantitis associated with apical periodontitis: a proposed classification system and case report. \u003cem\u003eJournal of Endodontics\u003c/em\u003e \u003cstrong\u003e43\u003c/strong\u003e, 1921-1924 (2017).\u003c/li\u003e\n\u003cli\u003eLefever, D., Van Assche, N., Temmerman, A., Teughels, W. \u0026amp; Quirynen, M. Aetiology, microbiology and therapy of periapical lesions around oral implants: a retrospective analysis. \u003cem\u003eJournal of clinical periodontology\u003c/em\u003e \u003cstrong\u003e40\u003c/strong\u003e, 296-302 (2013).\u003c/li\u003e\n\u003cli\u003eZhou, W.\u003cem\u003e et al.\u003c/em\u003e Endodontic treatment of teeth induces retrograde peri‐implantitis. \u003cem\u003eClinical oral implants research\u003c/em\u003e \u003cstrong\u003e20\u003c/strong\u003e, 1326-1332 (2009).\u003c/li\u003e\n\u003cli\u003eSarmast, N. D.\u003cem\u003e et al.\u003c/em\u003e A novel treatment decision tree and literature review of retrograde peri‐implantitis. \u003cem\u003eJournal of periodontology\u003c/em\u003e \u003cstrong\u003e87\u003c/strong\u003e, 1458-1467 (2016).\u003c/li\u003e\n\u003cli\u003eQuirynen, M., Gijbels, F. \u0026amp; Jacobs, R. An infected jawbone site compromising successful osseointegration. \u003cem\u003ePeriodontology 2000\u003c/em\u003e \u003cstrong\u003e33\u003c/strong\u003e, 129-144 (2003).\u003c/li\u003e\n\u003cli\u003ePiattelli, A., Scarano, A., Balleri, P. \u0026amp; Favero, G. A. Clinical and histologic evaluation of an active\u0026quot; implant periapical lesion\u0026quot;: a case report. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e13\u003c/strong\u003e (1998).\u003c/li\u003e\n\u003cli\u003eEl Askary, A. S., Meffert, R. M. \u0026amp; Griffin, T. Why do dental implants fail? Part I. \u003cem\u003eImplant dentistry\u003c/em\u003e \u003cstrong\u003e8\u003c/strong\u003e, 173-185 (1999).\u003c/li\u003e\n\u003cli\u003eAyangco, L. \u0026amp; Sheridan, P. J. Development and treatment of retrograde peri-implantitis involving a site with a history of failed endodontic and apicoectomy procedures: a series of reports. \u003cem\u003eInternational Journal of Oral \u0026amp; Maxillofacial Implants\u003c/em\u003e \u003cstrong\u003e16\u003c/strong\u003e (2001).\u003c/li\u003e\n\u003cli\u003eDonath, K. \u0026amp; Breuner, G. A method for the study of undecalcified bones and teeth with attached soft tissues* The S\u0026auml;ge‐Schliff (sawing and grinding) Technique. \u003cem\u003eJournal of Oral Pathology \u0026amp; Medicine\u003c/em\u003e \u003cstrong\u003e11\u003c/strong\u003e, 318-326 (1982).\u003c/li\u003e\n\u003cli\u003eVignoletti, F.\u003cem\u003e et al.\u003c/em\u003e Early healing of implants placed into fresh extraction sockets: an experimental study in the beagle dog. De novo bone formation. \u003cem\u003eJournal of Clinical Periodontology\u003c/em\u003e \u003cstrong\u003e36\u003c/strong\u003e, 265-277 (2009).\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-2847235/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-2847235/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThis study aimed to investigate whether newly emerged periodontitis or apical periodontitis on the adjacent teeth affects osseointegrated dental implants in a beagle dog model. The mandibular second and fourth premolars on both sides of three beagles were extracted. Two months after extraction, four bone-level implant fixtures, two on both sides of each mandible, were placed in each beagle. Six weeks after implant surgery, healing abutments were connected. After sufficient osseointegration, plaque control was performed in the control group, while periodontitis and apical periodontitis were induced in the experimental groups. The beagles were euthanized for histological analyses five months after induction of experimental periodontitis. The implants in the control and apical periodontitis groups were well-maintained, while those in the periodontitis group showed clinical signs of inflammation with bone resorption. The bone-to-implant contact (BIC) and bone area (BA) values in the periodontitis group were lower than those in the other groups. The distance between the implant shoulder and the first BIC was significantly greater in the periodontitis group than in the control group. Unlike apical periodontitis, periodontitis of the teeth surrounding dental implants can induce peri-implantitis. Periodontal healthcare is essential for long-term dental implant survival.\u003c/p\u003e","manuscriptTitle":"Effects of adjacent periodontitis on osseointegrated dental implants","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-05-08 14:39:55","doi":"10.21203/rs.3.rs-2847235/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"f0cabd49-8931-4553-925e-48b529256a10","owner":[],"postedDate":"May 8th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2023-05-10T02:14:24+00:00","versionOfRecord":[],"versionCreatedAt":"2023-05-08 14:39:55","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-2847235","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-2847235","identity":"rs-2847235","version":["v1"]},"buildId":"rHA-KDH7Qsr4HCuvH75dn","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}