10.59987/ads/2020.1-4.02-09
Dentin has been an important topic of study for its potential use as a bone substitute because it has a higher mineral content than any material derived from bone. Furthermore, dentin is similar to autologous bone in two ways: it is both osteocompatible and osteoconductive, thus providing a physical matrix for the sediment of new bone. In this comparative study, we evaluated the osteoinductive and osteoconductive possibilities of various materials normally used in “socket preservation” or alveolar ridge preservation. From the results obtained, it can be seen that autologous dentin matrix and bovine-derived xenografts (Bio-Oss) achieved better bone regeneration with a greater amount of newly formed bone (expressed by the BV/TV parameter) and less fibrous bone, which has unfavorable characteristics for implant biomechanics.
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S. Mummolo
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Annali di stomatologia
osteoconductive
Clinical and histomorphometric comparison of autologous dentin graft versus a deproteinized bovine bone graft for Socket Preservation
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Original Article
2022-08-08
2022-08-08
2020-12-01
2023-12-04
02-09
Ann Stomatol (Roma)
S. Mummolo
2020
10.59987/ads/2020.1-4.02-09
02
Department of Life, Health and Environmental Sciences, University of L’Aquila, Italy
1971-1441
1-4
osteoconductive
en
09
Clinical and histomorphometric comparison of autologous dentin graft versus a deproteinized bovine bone graft for Socket Preservation
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                                                                                                        Original article


Clinical and histomorphometric comparison
of autologous dentin graft versus a deproteinized
bovine bone graft for Socket Preservation

Gallusi Gianni1                                                thickness to allow their insertion, primary stability, and os-
Quinzi Vincenzo1                                               seointegration. If such thickness is not present, implant
Grilli Filippo1                                                treatment may be possible only through regenerative
Memè Lucia2                                                    surgery techniques, the success of which is linked to an
Rasicci P.1                                                    accurate diagnosis involving the correct choice of graft
Mummolo Stefano1                                               material, which is crucial for adequate bone formation.
                                                               In current times, when implant placement is the favored
1
  Department of Life, Health and Environmental Scienc-         option for replacing a missing tooth, preservation of the
   es, University of L’Aquila, Italy                           alveolar ridge is vital. After tooth extraction, dimensional
2
  Università Politecnica delle Marche , Ancona, Italy          changes in the residual alveolar ridge are inevitable,
                                                               which pre-existing pathologies such as periodontal dis-
*Corresponding author:                                         ease and periapical lesions accelerate3.
Filippo Grilli: filippo.grilli@cc.univaq.it                    When a tooth is lost, the lack of stimulation of residual
Stefano Mummolo: stefano.mummolo@univaq.it                     bone causes a decrease in trabeculae and bone density
                                                               in the edentulous socket, along with a loss of width in the
                                                               buccal bone and a subsequent loss of height in the vol-
                                                               ume of the alveolar process. These risks are particularly
Abstract                                                       significant during the first 8 weeks4.
                                                               Within the first 6 months after tooth extraction, the alveo-
Dentin has been an important topic of study for its
                                                               lar ridge loses height and width ≥50%5-6. Therefore, to
potential use as a bone substitute because it has
                                                               maintain the bone volume useful for optimal functional
a higher mineral content than any material derived
                                                               and esthetic outcomes of a dental implant, it is neces-
from bone. Furthermore, dentin is similar to autolo-
                                                               sary to intervene conteporary or immediately after ex-
gous bone in two ways: it is both osteocompatible
                                                               traction. Placement of various grafting materials within
and osteoconductive, thus providing a physical ma-
                                                               the postextraction socket is supported by numerous
trix for the sediment of new bone.
                                                               studies as a “ridge preservation technique.” 5- 6-7-8-9
In this comparative study, we evaluated the osteoin-
                                                               Techniques for alveolar ridge preservation using autog-
ductive and osteoconductive possibilities of various
                                                               enous, allogeneic, and xenograft graft materials have
materials normally used in “socket preservation” or
                                                               been mentioned in the literature.
alveolar ridge preservation.
                                                               For most favorable results, an ideal bone graft should
From the results obtained, it can be seen that autol-
                                                               have the properties of osteoconduction, osteoinduction,
ogous dentin matrix and bovine-derived xenografts
                                                               and osteoproliferation10-11. Among all available op-
(Bio-Oss) achieved better bone regeneration with a
                                                               tions, allografts and xenografts demonstrate only osteo-
greater amount of newly formed bone (expressed by
                                                               conduction (except allograft with demineralized freeze-
the BV/TV parameter) and less fibrous bone, which
                                                               dried bone, which is osteoinductive). Considering that
has unfavorable characteristics for implant biome-
                                                               autologous bone possesses all three ideal properties,
chanics.
                                                               it is still considered the gold standard. However, infec-
                                                               tion hazard from the donor site, limited availability, and
Key words: dentin, socket preservation, osteocon-
                                                               marked resorption are some of the shortcomings of au-
ductive
                                                               tologous bone grafting.
                                                               Advances in tissue engineering and stem cell science
Introduction                                                   are leading to the development of new techniques for
The human body has intrinsic mechanisms that allow             bone regeneration in the maxillofacial area constituting
self-healing, but ‘restitutio ad integrum’ is not recurring,   an additional therapeutic possibility.
particularly in the oral cavity and at the level of the al-    Dentin has been an important topic of study for its poten-
veolar bone. Biomaterials can promote and enhance              tial use as a bone substitute because it has a higher min-
the natural capacity for healing and can be successfully       eral content than any material derived from bone. Further-
used to restore certain structures in the human body 1-2.      more, dentin is similar to autologous bone in two ways: it
Dental implants represent a method with predictable            is both osteocompatible and osteoconductive, thus pro-
results for rehabilitating chewing function in edentulous      viding a physical matrix for the sediment of new bone. For
patients as long as there is an adequate residual bone         the above reasons, dentin is considered an ideal bioac-

Annali di Stomatologia 2020; XI (1-4): 2-9                                                                                      2
    Clinical and histomorphometric comparison of autologous dentin graft versus a deproteinized bovine bone graft for Socket

    tive material for hard tissue regeneration 12-13-14.           As a quantitative technique, histomorphometry may also
    The literature agrees that proteins with a weight similar      find wider application in “measuring” the response of
    to bone morphogenetic proteins (BMPs) are abundant in          bone to biomaterials implanted during surgery. 29
    dental substance. BMPs help promote the differentiation
    of mesenchymal cells into odontoblasts and ameloblasts         Materials and methods
    15-16-17-18-19.
    These proteins can improve the osteoinductive proper-          In this comparative study, we evaluated the osteoinduc-
    ties of bone substitutes if they can be successfully re-       tive and osteoconductive possibilities of various mate-
    tained during the processing of the graft material. The        rials normally used in “socket preservation” or alveolar
    idea of being able to use the tooth as a bone substitute       ridge preservation. The study was carried out on a single
    dates back to studies on the identification of growth fac-     patient to get rid of all the variables that inevitably may
    tors known as bone morphogenetic proteins (Bmps). In           arise when evaluating a larger audience of subjects. The
    1967, U.S. orthopedic surgeon Marshall Urist, discov-          patient, a volunteer, of the present study, is a candidate
    erer of Bmps, first demonstrated their presence in dentin      for treatment and rehabilitation with implant-prosthetic
    as well. Subsequently, Bmps in the dentin matrix were          therapy at the Dental Clinic of the University of L’Aquila.
    isolated and characterized 17-18-19.                           In addition, the candidate patient required dental extrac-
    Autogenous dentin grafting has been developed and              tions for periodontal reasons. The patient included in the
    clinically applied in Korea from 2008 onward.                  study met the following exclusion criteria:
    The patient’s extracted tooth represents the ideal bioma-      - History of systemic disease that would make surgery
    terial because it is autologous, does not require a sec-            contraindicated
    ond harvest site, has high osteoconductive and osteoin-        - Long-term therapy with nonsteroidal anti-inflamma-
    ductive properties, and is remodeled and fully replaced             tory drugs
    by new bone.                                                   - Lack of antagonistic elements in the area being ex-
    The osteoinductive properties are due to the presence               tracted and thus of implant placement
    of significant amounts of Bmp within the dentin structure.     - Oral therapy with bisphosphonates
    These proteins are preserved even long after extraction        - Lack of elements adjacent to the site undergoing
    and are unaffected by storage conditions: consider that             therapy
    intact Bmps have been identified even in fossil human          - Inability to present at subsequent follow-ups
    teeth. The complete or partial demineralization treat-         - Subject smoker of more than 10 cigarettes per day.
    ment that is carried out by some of the current methods        Before participating in the study, the patient received
    increases the bioavailability of dentin Bmps, which are        clear explanations and signed the informed consent.
    otherwise constrained by the high degree of crystallinity      In addition, he or she was carefully evaluated through
    of hydroxyapatite. This makes dentin the most biologi-         analysis of diagnostic patterns and panoramic/periapical
    cal and osteoinductive material available, with the sole       radiographs, and data such as age, sex, smoking hab-
    exception of autologous bone. In this regard, it should        its, indication for dental extraction based on both clini-
    be kept in mind that in theory enamel also has good os-        cal and radiographic data, location of the tooth element,
    teoconductivity characteristics but, having a higher inor-     and presence/absence of adjacent teeth were acquired.
    ganic component (96% compared to 60-70% of dentin),            Once informed consent was performed, it was possible
    it is less easily resorbed even after demineralization 19.     to proceed with the surgical procedure.
    Many studies on the use of autogenous dentin as a graft        The clinical situation of the patient examined presented
    have shown good clinical and histological results 20-21-       the dental arches with edentulousness of numerous ele-
    22-23-24. However, there is a paucity of data supporting       ments.
    the use of autogenous tooth graft (ATG) in clinical ap-        To study the effectiveness of autogenous dentin in pre-
    plications.
                                                                   serving the alveolar ridge, the following experimental
    Avoiding autogenous bone harvesting by opening an-
                                                                   protocol was established.
    other surgical site is advantageous in all cases where
                                                                   The patient had extracted eight elements in the two
    the need to increase bone volumes is accompanied by
                                                                   arches.
    the extraction of dental elements. It also helps with the
                                                                   The post-extraction sites were divided into 3 groups:
    cost savings associated with the use of an autologous
                                                                   GROUP 1: in which the alveolus was filled with freshly
    material compared with those of animal or synthetic ori-
                                                                   prepared autologous dentin matrix;
    gin. 25-26-27-28
                                                                   GROUP 2: in which deproteinized bovine bone (Geistlich
    The primary objective of the present study is to evalu-
                                                                   Bio-Oss) was used;
    ate clinically and radiographically the efficacy of an au-
                                                                   GROUP 3: control, in which the alveolar bone defect was
    tologous dentin graft versus a deproteinized bovine bone
    graft in the technique of alveolar ridge preservation in       not filled, reproducing natural post-extraction conditions.
    post-extraction sites. The secondary purpose was to
    determine histologically the bone formation potential of       Surgical protocol
    ATG (Autogenous Tooth Graft).                                  -   Antibiotic prophylaxis.
    The data obtained were evaluated by histomorphometry,
                                                                   Following the latest guidelines about antibiotic prophy-
    or quantitative histology, which allows the acquisition of
                                                                   laxis in oral surgery, the patient received prophylactic an-
    the most important bone parameters, including the bone
                                                                   tibiotic therapy with 2g amoxicillin 1 hour before extrac-
    remodeling index. Indeed, suffice it to say that it is used
    for the diagnosis of metabolic diseases of the skeleton        tion and continued therapy in the postoperative period
    (on bicortical biopsies from the iliac crest).                 with 1g amoxicillin twice daily for 4 days.

3                                                                                       Annali di Stomatologia 2020; XI (1-4): 2-9
G. Gallusi et al.




Figure 1. Condition of the dental arches immediately following multiple extractions.



-    Anesthesia
Lidocaine-based local-regional and plexic anesthesia
was performed, with adrenaline 1:50000 where possible.

-    Dental extractions
Elements 1.4, 1.2, 2.2, 2.4, 3.4, 3.2, 4.2 and 4.4 were
extracted with manual syndesmotomes or extraction for-
ceps.
The atraumatic extraction and subsequent grafting for
the alveolar ridge preservation technique were per-
formed without dislodging a full-thickness flap using the
flapless technique.
Great care was taken to minimize trauma to the buccal
bone surface and to maintain the integrity of bone mor-
phology.

-    Curettage of the alveolus                                     Figure 2. Grinding and sorting process completed.
For proper performance of this study, it was necessary to
ensure the removal of all root fragments, fibers, and soft
tissues from the alveolus prior to the insertion of graft          The first step was to select teeth for treatment. Endodon-
material.                                                          tically treated elements were excluded.
Curettes were used to remove these tissues in the post-            A high-speed handpiece and an ultrasonic scaler were
extraction socket.                                                 used to remove all cavities, artificial materials (crowns
                                                                   or fillings of any kind, amalgam or composites), and de-
-    Preparation of autologous dentin matrix                       bris until completely clean elements remained. It was not
Parallel to curettage, according to the manufacturer’s             necessary to remove the crown or enamel.
recommendations, treatment of the extracted teeth for              The prepared teeth were dried and introduced into the
the creation of the autologous dentin matrix graft was             grinding chamber, they were then ground and sorted
performed.                                                         through the machine functions obtaining particles be-
The Smart Dentin Grinder manufactured by KometaBio                 tween 300 and 1200 microns in size. Particles smaller
was chosen for the preparation of the autologous material.         than 300 microns were discarded.

Annali di Stomatologia 2020; XI (1-4): 2-9                                                                                      4
    Clinical and histomorphometric comparison of autologous dentin graft versus a deproteinized bovine bone graft for Socket

                                                                   heal naturally. The graft material was condensed into the
                                                                   socket by gently pressing it while the patient’s blood was
                                                                   used as the preferred medium to blend it.
                                                                   The use of collagen membrane is mandatory to ensure
                                                                   the protection of the site from gingival proliferation (tent-
                                                                   ing effect) to allow graft rooting and osteogenesis, as
                                                                   well as to allow optimal retention of the material. For this
                                                                   purpose, the membrane was appropriately shaped ac-
                                                                   cording to the dimensions of the socket and then adapt-
                                                                   ed with the ends gently pushed underneath the adjacent
                                                                   soft tissues previously unglued (envelope technique).

                                                                   -    Sutures
                                                                   Mucosal margins were fixed in situ, using sutures with-
                                                                   out achieving complete soft tissue closure.
                                                                   Collagen membranes remained exposed to the oral cav-
                                                                   ity with healing by the second intention. Removal of the
                                                                   sutures was scheduled after 10 days.
    Figure 3. KometBio’s Smart Dentin Grinder with the ex-         The patient was recommended to continue antibiotic
    tracted and cleaned teeth inserted into the grinding cham-
    ber.                                                           prophylaxis and take, as an anti-inflammatory, naproxen
                                                                   sodium in 550 mg tablets twice daily as long as needed,
                                                                   in addition to the use of a chlorhexidine 0.2% mouth-
                                                                   wash twice daily.
    Drawer with particle sizes between 300 and 1200 mi-
    crons following the shredding and sorting process.             -    Sample
    Next, the sterilization step was carried out with substanc-    After about 6 months, the implants were placed by taking
    es provided by the manufacturer (NaOH with ethanol             the bone to be analyzed from the alveolar site by full-
    20%), respecting the timing and procedures.                    thickness flap and the use of core drills (hollow toothed,
    This process resulted in the organic residues dissolution      internally cooled, handpiece-mounted drills) in the area
    of, bacteria, and toxins in the dentin, leaving the dentin     where the biomaterial graft had been placed.
    particles ready for use.                                       Subsequently, the implant was placed.
                                                                   The patient received the same drug therapy at the time
    -    Grafting of biomaterials                                  of the initial surgery. The retrieval was left in a tube with
    In group 1, which includes the post-extraction sites of el-    a fixative for 9 days to preserve and stabilize its con-
    ements 1.2, 2.2, 3.2, and 4.2, the freshly prepared dentin     stituents.
    matrix was placed as an autogenous graft.                      The purpose of fixation is to prevent the postmortal de-
    In group 2 comprising sites 3.4 and 4.4, a deproteinized       generative processes that occur in tissues while preserv-
    bovine bone graft (Bio-Oss. Geistlich) was placed, and         ing their morphology, structure, and reactivity as best as
    in group 3, comprising sites 1.4 and 2.4, no graft was         possible by obtaining as extensive and truthful informa-
    placed and the postextraction socket was allowed to            tion as feasible about the “in vivo” condition of the tissue
                                                                   specimen under examination81.
                                                                   Indeed, the fixative allows instant blocking of enzyme
                                                                   activity, and preservation of all tissue components and
                                                                   does not alter the structure or allow tissue dislocation.
                                                                   In the present study, formaldehyde (or formalin) used in
                                                                   4% dilution pH7 was chosen as the fixative.
                                                                   This was followed by the inclusion step, which consists
                                                                   of allowing a substance to permeate the tissue under ex-
                                                                   amination, which, as it solidifies, allows it to be cut with
                                                                   a microtome into thin sections a few microns (μm) thick.
                                                                   The inclusion material chosen was methacrylate.
                                                                   The resulting piece was then placed for longitudinal cut-
                                                                   ting using the microtome.
                                                                   Histological sections, on the order of 5 microns (μm),
                                                                   were thus made for staining and analysis.
                                                                   The sections, arranged on object slides, were immersed
                                                                   in xylol, the inclusion solvent, to allow rehydration and
                                                                   subsequent staining.
                                                                   Once the slide was stained, depending on the need for
                                                                   investigation, the section was sealed using Canada bal-
                                                                   sam and coverslip.
    Figure 4. Drawer with particle sizes between 300 and 1200      Several sections were made of each sampling, of which,
    microns following the shredding and sorting process.           some were stained with methylene blue/blue II, for anal-

5                                                                                        Annali di Stomatologia 2020; XI (1-4): 2-9
G. Gallusi et al.




Figure 5. Placement of Group 1 grafting material (dentin) in the post-extraction socket.




ysis of structural parameters, and the remaining with              parameter) and less fibrous bone, which has unfavor-
TRAcP staining for analysis of bone cell parameters.               able characteristics for implant biomechanics.
                                                                   This assessment resulted not only from histomorpho-
-    Histomorphometric analysis                                    metric examination but also from histological sections
Histomorphometric analysis involved the entirety of the            analyzed by light microscopy.
    sectioned specimen, and the following were mea-                The percentage of residual material, examined by his-
    sured:                                                         tomorphometry, was also found to be higher for the
- osteoclast number/bone surface area (number/                     first two groups than for the third, an important finding
    mm2),                                                          to allow its replacement with newly formed bone tissue
- osteoclast surface area/bone surface area (percent),             (osteoconduction). For group I, with autogenous dentin
- osteoblast surface area/bone surface area (percent),             grafting, the following parameters were examined:
- bone volume/total volume (percent).                              - BV/TV, expressing the percentage of newly formed
The nomenclature, symbols, and measure units of the                     bone,
histomorphometric indices were expressed as recom-                 - OC.N/micron, expressing the number of osteoclasts
mended by the Histomorphometry Nomenclature Com-                        per micron,
mittee of the American Society for Bone and Mineral                - OCS/BS, expressing the number of total osteoclasts
Research.                                                               observed on bone volume.
Cells were fixed in 3% paraformaldehyde in cacodylate              The results obtained were as follows:
buffer
0.1 M for 15 min, then washed with the same buffer.
                                                                   • BV/TV (Bone volume/Tissue Volume) %.
TRAcP activity was detected histochemically using Sig-
ma- Aldrich kit #386, following the manufacturer’s sug-
gested instructions.                                                Site   Section 1       Section 2   Section 3   Average ±
                                                                                                                   SEM
Results                                                             1       27%            30%         28%         28.3 ± 0.88
From the results obtained, it can be seen that autolo-              2      55%             61%         58%         58.0 ± 1.73
gous dentin matrix and bovine-derived xenografts (Bio-              3      21%             17%         23%         20.4 ± 1.76
Oss) achieved better bone regeneration with a greater
amount of newly formed bone (expressed by the BV/TV                 4      80%             83%         88%         83.7 ± 1.30

Annali di Stomatologia 2020; XI (1-4): 2-9                                                                                       6
    Clinical and histomorphometric comparison of autologous dentin graft versus a deproteinized bovine bone graft for Socket

    • OC.N/micron                                                   surrounded by newly formed, mature, and compact bone
                                                                    tissue, with no bone gaps along with the interface.
     Site   Section 1    Section 2    Section      Average ±        The bone was always found to be in close contact with
                                      3            SEM              the particles themselves. In addition, no inflammatory in-
     1       8μm         11μm         5μm          8μm              filtrate was evident. Histomorphometry showed that the
                                                                    newly formed bone was 38%± 1.6%, the intertrabecular
     2      21μm         22μm         20μm         21μm             spaces 33%±1.6%, and the residual material was 30%±
     3      5μm          8μm          6μm          6μm              1.4%.
     4      1μm          0μm          2μm          1μm              Regarding the sites without any graft, where there was
                                                                    natural healing, there was evidence of neoformation of
                                                                    bone tissue with wide gaps.
    • OCS/BS                                                        No inflammatory infiltrate was found.
                                                                    The neoformed bone was 37%± 3.2%, the intertrabecular
     Site   Section 1    Section 2     Section 3    Average ±       spaces 44% ±1.3%, and the residual material was 0%.
                                                    SEM
     1      15%          20%           18%          17.6%           Discussion
     2      35%          32%           42%          36.3%           The presence of neoformed bone was observed in all
     3      13%          16%           21%          16.6%           samples examined.
                                                                    Therefore, it can be stated that the biomaterials consid-
     4      3%           0%            2%           1.6%
                                                                    ered in this study resulted in bone neoformation.
                                                                    However, the phenomena of bone neoformation are not
    Regarding on group 2, which included xenograft with             sufficient to clarify the greater usefulness of one bioma-
    deproteinized bovine bone (Bio-Oss), and group 3, in-           terial over another. Therefore, the amount of mineralized
    cluding sites left to heal naturally, the following were ex-    bone, the amount of intertrabecular spaces, and the
    amined:                                                         amount of residual biomaterial were also considered in
    - BV/TV, expressing the amount of newly formed bone,            our study.
    - The percentage of intertrabecular spaces,                     Based on the parameters analyzed, there are differenc-
    - The percentage of residual material.                          es between the various biomaterials, particularly in the
    The results obtained were as follows:                           amount of residual biomaterial.
                                No fillers      Bio-Oss             Autologous dentin matrix turns out to be the most stable
                                                                    “biomaterial” in comparison with Bio-Oss and traditional
     New bone                   37%±3.2%        38%±1.6%            healing whose residual percentage is higher, given the
     Inter-trabecular spa-      44%±1.3%        32%±1.6%            same elapsed time (in agreement with the international
     ces                                                            literature and concerning Bio-Oss identified as the “gold
     Residual material          0%              30%±1.4%            standard” among grafting biomaterials).
                                                                    Regarding the type of material replacement, in bone tis-
    As for Bio-Oss, sections of some samples showed os-             sue or fibrous tissue, we can argue that traditional heal-
    teoblastic activities with affixation of bone directly on the   ing was the process that gave the highest percentage of
    surface of the particles, most of which appeared to be          fibrous tissue formation.




    Figure 6. Transverse section of patient’s jaw bone.
    TRAcP histochemical staining highlighting cells expressing the enzyme tartrate-resistant acid phosphatase enzyme.
    40X magnification.
    Red arrows = osteoclasts \ o = bone tissue.

7                                                                                        Annali di Stomatologia 2020; XI (1-4): 2-9
G. Gallusi et al.




Figure 7. Longitudinal section of patient’s maxillary bone.
2.5X magnification. Methylene blue II staining.
Images are representative of at least 3 sections analyzed at different depths.
O = bone tissue \ red arrows = osteoblasts \ black arrows = osteocytes



Nevertheless, differences, even considerable ones,                 Further randomized clinical trials are needed to establish
were still found among the various retrievals, even with           its regenerative potential in various periodontal weak-
the same material used, in the type of tissue regener-             nesses.
ated. These disparities are related to individual patient
factors that play an equally important role such as:
- general health conditions of the same,                           References
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                                                                       A systematic review. J. Clin. Periodontol. 2009;36:1048–
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morphological condition of the post-extraction alveolus.               view of post- extractional alveolar hard and soft tissue
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