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      Periodontal and endodontic pathology delays extraction socket healing in a canine model

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          Abstract

          Purpose

          The aim of the present exploratory study was to evaluate extraction socket healing at sites with a history of periodontal and endodontic pathology.

          Methods

          The mandibular 4th premolar teeth in 5 adult beagle dogs served as experimental units. Periodontal and endodontic lesions were induced in 1 premolar site in each animal using wire ligatures and pulpal exposure over 3 months (diseased sites). The contralateral premolar sites served as healthy controls. The mandibular 4th premolar teeth were then extracted with minimal trauma, followed by careful wound debridement. The animals were sacrificed at days 1, 7, 30, 60, and 90 post-extraction for analysis, and the healing patterns at the healthy and diseased extraction sites were compared using radiography, scanning electron microscopy, histology, and histometry.

          Results

          During the first 7 days of healing, a significant presence of inflammatory granulation tissue was noted at the diseased sites (day 1), along with a slightly accelerated rate of fibrin clot resolution on day 7. On day 30, the diseased extraction sites showed a greater percentage of persistent fibrous connective tissue, and an absence of bone marrow formation. In contrast, healthy sites showed initial signs of bone marrow formation on day 30, and subsequently a significantly greater proportion of mature bone marrow formation on both days 60 and 90. Radiographs exhibited sclerotic changes adjoining apical endodontic lesions, with scanning electron microscopy showing collapsed Volkmann canals protruding from these regions in the diseased sites. Furthermore, periodontal ligament fibers exhibited a parallel orientation to the alveolar walls of the diseased sites, in contrast to a perpendicular arrangement in the healthy sites.

          Conclusions

          Within the limitations of this study, it appears that a history of periodontal and endodontic pathology may critically affect bone formation and maturation, leading to delayed and compromised extraction socket healing.

          Graphical Abstract

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          Most cited references19

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          Dimensional ridge alterations following tooth extraction. An experimental study in the dog.

          To study dimensional alterations of the alveolar ridge that occurred following tooth extraction as well as processes of bone modelling and remodelling associated with such change. Twelve mongrel dogs were included in the study. In both quadrants of the mandible incisions were made in the crevice region of the 3rd and 4th premolars. Minute buccal and lingual full thickness flaps were elevated. The four premolars were hemi-sected. The distal roots were removed. The extraction sites were covered with the mobilized gingival tissue. The extractions of the roots and the sacrifice of the dogs were staggered in such a manner that all dogs contributed with sockets representing 1, 2, 4 and 8 weeks of healing. The animals were sacrificed and tissue blocks containing the extraction socket were dissected, decalcified in EDTA, embedded in paraffin and cut in the buccal-lingual plane. The sections were stained in haematoxyline-eosine and examined in the microscope. It was demonstrated that marked dimensional alterations occurred during the first 8 weeks following the extraction of mandibular premolars. Thus, in this interval there was a marked osteoclastic activity resulting in resorption of the crestal region of both the buccal and the lingual bone wall. The reduction of the height of the walls was more pronounced at the buccal than at the lingual aspect of the extraction socket. The height reduction was accompanied by a "horizontal" bone loss that was caused by osteoclasts present in lacunae on the surface of both the buccal and the lingual bone wall. The resorption of the buccal/lingual walls of the extraction site occurred in two overlapping phases. During phase 1, the bundle bone was resorbed and replaced with woven bone. Since the crest of the buccal bone wall was comprised solely of bundle this modelling resulted in substantial vertical reduction of the buccal crest. Phase 2 included resorption that occurred from the outer surfaces of both bone walls. The reason for this additional bone loss is presently not understood. (c) Blackwell Munksgaard, 2005.
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            Dynamics of bone tissue formation in tooth extraction sites. An experimental study in dogs.

            The aim of the present experiment was to study events involved in the healing of marginal, central and apical compartments of an extraction socket, from the formation of a blood clot, to bone tissue formation and remodeling of the newly formed hard tissue. Nine mongrel dogs were used for the experiment. The fourth mandibular premolars were selected for study and were divided into one mesial and one distal portion. The distal root was removed and the socket with surrounding soft and mineralized tissue was denoted "experimental unit". The dogs were killed 1, 3, 7, 14, 30, 60, 90, 120 and 180 days after the root extractions. Biopsies including the experimental units were demineralized in EDTA, dehydrated in ethanol and embedded in paraffin. Serial sections 7 microm thick were cut in a mesio-distal plane. From each biopsy, three sections representing the central part of the socket were selected for histological examination. Morphometric measurements were performed to determine the volume occupied by different types of tissues in the marginal, central and apical compartments of the extraction socket at different intervals. During the first 3 days of healing, a blood clot was found to occupy most of the extraction site. After seven days this clot was in part replaced with a provisional matrix (PCT). On day 14, the tissue of the socket was comprised of PM and woven bone. On day 30, mineralized bone occupied 88% of the socket volume. This tissue had decreased to 15% on day 180. The portion occupied by bone marrow (BM) in the day 60 specimens was about 75%, but had increased to 85% on day 180. The healing of an extraction socket involved a series of events including the formation of a coagulum that was replaced by (i) a provisional connective tissue matrix, (ii) woven bone, and (iii) lamellar bone and BM. During the healing process a hard tissue bridge--cortical bone--formed, which "closed" the socket.
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              Ridge preservation with the use of Bio-Oss collagen: A 6-month study in the dog.

              In previous short-term studies, it was observed that while the placement of biomaterial in alveolar sockets may promote bone formation and ridge preservation, the graft may in fact also delay healing. The objective of the present experiment was to evaluate the more long-term effect on hard tissue formation and the amount of ridge augmentation that can occur by the placement of a xenogeneic graft in extraction sockets of dogs. Five beagle dogs were used. The third mandibular premolars were hemi-sected. The distal roots were carefully removed. A graft consisting of Bio-Oss collagen was placed in one socket while the contra-lateral site was left without grafting. After 6 months of healing, the dogs were euthanized and biopsies were sampled. From each experimental site, four ground sections - two from the mesial root and two from the healed socket - were prepared, stained and examined under a microscope. The placement of Bio-Oss collagen in the fresh extraction socket served as a scaffold for tissue modeling but did not enhance new bone formation. In comparison with the non-grafted sites, the dimension of the alveolar process as well as the profile of the ridge was better preserved in Bio-Oss-grafted sites. The placement of a biomaterial in an extraction socket may modify modeling and counteract marginal ridge contraction that occurs following tooth removal.
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                Author and article information

                Journal
                J Periodontal Implant Sci
                J Periodontal Implant Sci
                JPIS
                Journal of Periodontal & Implant Science
                Korean Academy of Periodontology
                2093-2278
                2093-2286
                June 2017
                28 June 2017
                : 47
                : 3
                : 143-153
                Affiliations
                [1 ]Department of Periodontology and Dental Research Institute, Seoul National University School of Dentistry, Seoul, Korea.
                [2 ]US Army Advanced Education Program in Periodontics, Ft. Gordon, GA, USA.
                [3 ]Department of Periodontology, Dankook University College of Dentistry, Cheonan, Korea.
                [4 ]Department of Oral Surgery, Universitätsklinikum Düsseldorf, Düsseldorf, Germany.
                [5 ]Laboratory for Applied Periodontal & Craniofacial Regeneration (LAPCR), Augusta University Dental College of Georgia, Augusta, GA, USA.
                Author notes
                Correspondence: Ki-Tae Koo. Department of Periodontology and Dental Research Institute, Seoul National University School of Dentistry, 101 Daehak-ro, Jongno-gu, Seoul 03080, Korea. periokoo@ 123456snu.ac.kr , Tel: +82-2-2072-0108, Fax: +82-2-744-0051
                Author information
                https://orcid.org/0000-0001-9875-297X
                https://orcid.org/0000-0002-9809-2630
                https://orcid.org/0000-0002-4671-8398
                https://orcid.org/0000-0002-8819-6858
                https://orcid.org/0000-0003-2275-7656
                https://orcid.org/0000-0002-7927-9838
                https://orcid.org/0000-0002-2041-8047
                https://orcid.org/0000-0002-5873-9903
                https://orcid.org/0000-0003-1607-0583
                Article
                10.5051/jpis.2017.47.3.143
                5494309
                be5e3d4e-1665-432f-9c03-aedd1e80cbae
                Copyright © 2017. Korean Academy of Periodontology

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( https://creativecommons.org/licenses/by-nc/4.0/).

                History
                : 02 April 2017
                : 21 May 2017
                Funding
                Funded by: National Research Foundation of Korea, CrossRef http://dx.doi.org/10.13039/501100003725;
                Award ID: 2012R1A1A1042670
                Categories
                Research Article

                Dentistry
                biological models,bone marrow,histology,wound healing
                Dentistry
                biological models, bone marrow, histology, wound healing

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