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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Bone remodeling at microscrew interface near extraction site in the
beagle dog mandible-histologic and immunohistochemical analyses</title>
<author><name sortKey="Wei, Guangxi" sort="Wei, Guangxi" uniqKey="Wei G" first="Guangxi" last="Wei">Guangxi Wei</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hu, Yun" sort="Hu, Yun" uniqKey="Hu Y" first="Yun" last="Hu">Yun Hu</name>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff04">Department of Pediatric Dentistry, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zheng, Leilei" sort="Zheng, Leilei" uniqKey="Zheng L" first="Leilei" last="Zheng">Leilei Zheng</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Huo, Jinfeng" sort="Huo, Jinfeng" uniqKey="Huo J" first="Jinfeng" last="Huo">Jinfeng Huo</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tang, Tian" sort="Tang, Tian" uniqKey="Tang T" first="Tian" last="Tang">Tian Tang</name>
<affiliation><nlm:aff id="aff05">Department of Orthodontics, West China College of Stomatology, Sichuan University, Chengdu, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Feng" sort="Deng, Feng" uniqKey="Deng F" first="Feng" last="Deng">Feng Deng</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">24212991</idno>
<idno type="pmc">3881839</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3881839</idno>
<idno type="RBID">PMC:3881839</idno>
<idno type="doi">10.1590/1679-775720130160</idno>
<date when="2013">2013</date>
<idno type="wicri:Area/Pmc/Corpus">002F78</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002F78</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Bone remodeling at microscrew interface near extraction site in the
beagle dog mandible-histologic and immunohistochemical analyses</title>
<author><name sortKey="Wei, Guangxi" sort="Wei, Guangxi" uniqKey="Wei G" first="Guangxi" last="Wei">Guangxi Wei</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hu, Yun" sort="Hu, Yun" uniqKey="Hu Y" first="Yun" last="Hu">Yun Hu</name>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff04">Department of Pediatric Dentistry, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zheng, Leilei" sort="Zheng, Leilei" uniqKey="Zheng L" first="Leilei" last="Zheng">Leilei Zheng</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Huo, Jinfeng" sort="Huo, Jinfeng" uniqKey="Huo J" first="Jinfeng" last="Huo">Jinfeng Huo</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tang, Tian" sort="Tang, Tian" uniqKey="Tang T" first="Tian" last="Tang">Tian Tang</name>
<affiliation><nlm:aff id="aff05">Department of Orthodontics, West China College of Stomatology, Sichuan University, Chengdu, P. R. China.</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Feng" sort="Deng, Feng" uniqKey="Deng F" first="Feng" last="Deng">Feng Deng</name>
<affiliation><nlm:aff id="aff01">Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff02">Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff03">College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Applied Oral Science</title>
<idno type="ISSN">1678-7757</idno>
<idno type="eISSN">1678-7765</idno>
<imprint><date when="2013">2013</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Extraction is often used as part of orthodontic therapy, and good control of
anchorage is a key step after extraction. Although microscrews can be implanted close
to the extraction site in order to achieve orthodontic support, the efficiency of
bone remodeling at the implant-bone interface near the extraction region is
dubious.</p>
<sec><title>Objective</title>
<p>The purpose of this study was to investigate bone remodeling of the
bone-microscrew interface near the tooth extraction site, in the absence of
loading.</p>
</sec>
<sec><title>Material and Methods</title>
<p>Third and fourth premolars were extracted from the mandibles of beagle dogs,
followed by placement of test microscrews near the extraction sites. Control
microscrews were placed further away from the extraction site. All samples were
collected after 1, 3, 8, or 12 weeks of healing following extraction. The bone
remodeling process at the interface was evaluated using histologic and
immunohistochemical analyses.</p>
</sec>
<sec><title>Results</title>
<p>Initially, a large number of inflammatory cells were aggregated at the interface.
The expression levels of core binding factor (Cbfa1), osteocalcin (OC) and
transforming growth factor beta (TGF-β) were inconspicuous in both groups, whereas
tumor necrosis factor alpha (TNF-α) was strongly expressed, especially in the test
groups (P<0.05). Subsequently, the expression levels of Cbfa1, OC and TGF-β
were found to increase significantly, and active osteogenesis was observed.</p>
</sec>
<sec><title>Conclusions</title>
<p>During week 1, inflammatory reaction is a major concern at the bone-microscrew
interface near the extraction site. However, with healing, the influence of
extraction on the remodeling of bone surrounding the microscrews decreases, thus
facilitating successful treatment.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Appl Oral Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">J Appl Oral Sci</journal-id>
<journal-id journal-id-type="publisher-id">J. Appl. Oral. Sci.</journal-id>
<journal-title-group><journal-title>Journal of Applied Oral Science</journal-title>
</journal-title-group>
<issn pub-type="ppub">1678-7757</issn>
<issn pub-type="epub">1678-7765</issn>
<publisher><publisher-name>Faculdade de Odontologia de Bauru da Universidade de São
Paulo</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24212991</article-id>
<article-id pub-id-type="pmc">3881839</article-id>
<article-id pub-id-type="doi">10.1590/1679-775720130160</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Bone remodeling at microscrew interface near extraction site in the
beagle dog mandible-histologic and immunohistochemical analyses</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>WEI</surname>
<given-names>Guangxi</given-names>
</name>
<xref ref-type="aff" rid="aff01">1</xref>
<xref ref-type="aff" rid="aff02">2</xref>
<xref ref-type="aff" rid="aff03">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>HU</surname>
<given-names>Yun</given-names>
</name>
<xref ref-type="aff" rid="aff02">2</xref>
<xref ref-type="aff" rid="aff03">3</xref>
<xref ref-type="aff" rid="aff04">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>ZHENG</surname>
<given-names>Leilei</given-names>
</name>
<xref ref-type="aff" rid="aff01">1</xref>
<xref ref-type="aff" rid="aff02">2</xref>
<xref ref-type="corresp" rid="c01"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>HUO</surname>
<given-names>Jinfeng</given-names>
</name>
<xref ref-type="aff" rid="aff01">1</xref>
<xref ref-type="aff" rid="aff02">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>TANG</surname>
<given-names>Tian</given-names>
</name>
<xref ref-type="aff" rid="aff05">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>DENG</surname>
<given-names>Feng</given-names>
</name>
<xref ref-type="aff" rid="aff01">1</xref>
<xref ref-type="aff" rid="aff02">2</xref>
<xref ref-type="aff" rid="aff03">3</xref>
</contrib>
</contrib-group>
<aff id="aff01"><label>1</label>
Department of Orthodontics, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</aff>
<aff id="aff02"><label>2</label>
Chongqing Research Center for Oral Diseases and Biomedical Science, College of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</aff>
<aff id="aff03"><label>3</label>
College of Biomedical Engineering, Chongqing Medical University, Chongqing, P. R. China.</aff>
<aff id="aff04"><label>4</label>
Department of Pediatric Dentistry, the Affiliated Hospital of Stomatology, Chongqing Medical University, Chongqing, P. R. China.</aff>
<aff id="aff05"><label>5</label>
Department of Orthodontics, West China College of Stomatology, Sichuan University, Chengdu, P. R. China.</aff>
<author-notes><corresp id="c01"><bold>Corresponding address:</bold>
LeiLei Zheng - Chongqing Research Center for Oral
Diseases and Biomedical Science - College of Stomatology - Chongqing Medical
University - 426#, Songshibei Road - Yubei District - Chongqing - 401147- P. R. China
- Phone: 86-23-88860107 - Fax: +86 23 8886 0222 - e-mail:
<email>zheng_lei_lei@163.com</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><season>Sep-Oct</season>
<year>2013</year>
</pub-date>
<volume>21</volume>
<issue>5</issue>
<fpage>443</fpage>
<lpage>451</lpage>
<history><date date-type="received"><day>08</day>
<month>2</month>
<year>2013</year>
</date>
<date date-type="rev-recd"><day>26</day>
<month>7</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>06</day>
<month>8</month>
<year>2013</year>
</date>
</history>
<permissions><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>This is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial License which permits unrestricted
non-commercial use, distribution, and reproduction in any medium, provided the
original work is properly cited. </license-p>
</license>
</permissions>
<abstract><p>Extraction is often used as part of orthodontic therapy, and good control of
anchorage is a key step after extraction. Although microscrews can be implanted close
to the extraction site in order to achieve orthodontic support, the efficiency of
bone remodeling at the implant-bone interface near the extraction region is
dubious.</p>
<sec><title>Objective</title>
<p>The purpose of this study was to investigate bone remodeling of the
bone-microscrew interface near the tooth extraction site, in the absence of
loading.</p>
</sec>
<sec><title>Material and Methods</title>
<p>Third and fourth premolars were extracted from the mandibles of beagle dogs,
followed by placement of test microscrews near the extraction sites. Control
microscrews were placed further away from the extraction site. All samples were
collected after 1, 3, 8, or 12 weeks of healing following extraction. The bone
remodeling process at the interface was evaluated using histologic and
immunohistochemical analyses.</p>
</sec>
<sec><title>Results</title>
<p>Initially, a large number of inflammatory cells were aggregated at the interface.
The expression levels of core binding factor (Cbfa1), osteocalcin (OC) and
transforming growth factor beta (TGF-β) were inconspicuous in both groups, whereas
tumor necrosis factor alpha (TNF-α) was strongly expressed, especially in the test
groups (P<0.05). Subsequently, the expression levels of Cbfa1, OC and TGF-β
were found to increase significantly, and active osteogenesis was observed.</p>
</sec>
<sec><title>Conclusions</title>
<p>During week 1, inflammatory reaction is a major concern at the bone-microscrew
interface near the extraction site. However, with healing, the influence of
extraction on the remodeling of bone surrounding the microscrews decreases, thus
facilitating successful treatment.</p>
</sec>
</abstract>
<kwd-group><kwd>Bone remodeling</kwd>
<kwd>Core binding factor</kwd>
<kwd>Osteocalcin</kwd>
<kwd>Transforming growth factor alpha</kwd>
<kwd>Transforming growth factor beta</kwd>
</kwd-group>
<funding-group><award-group><funding-source>General Program of National Natural Science Foundation for Young
Scholars of China</funding-source>
<award-id>81000463</award-id>
<award-id>10902075</award-id>
</award-group>
<award-group><funding-source>Foundation of the General Program of Chongqing Natural
Science</funding-source>
<award-id>cstc2012jja10053</award-id>
</award-group>
<award-group><funding-source>Foundation of the Chongqing Municipal Health Bureau</funding-source>
<award-id>2012-2-126</award-id>
</award-group>
<award-group><funding-source>Foundation of the Chongqing Municipal Commission of
Education</funding-source>
<award-id>kj120329</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
<body><sec><title>INTRODUCTION</title>
<p>Anchorage control is a challenge to nearly every orthodontist. Since the first
successful attempt to move teeth against a fixed screw by Linkow<sup><xref ref-type="bibr" rid="r12">12</xref>
</sup>
(1969), the application of microscrews
in orthodontic treatment has become a mainstay in contemporary orthodontics<sup><xref ref-type="bibr" rid="r07">7</xref>
,<xref ref-type="bibr" rid="r14">14</xref>
</sup>
. Owing to its miniature size, the interradicular site is the most
common choice for microscrews in orthodontic clinical treatment<sup><xref ref-type="bibr" rid="r09">9</xref>
</sup>
. Moreover, palatal implants, the implant
system for orthodontic anchorage, have shown promising results in recent years by
achieving maximal intraoral orthodontic anchorage purposes<sup><xref ref-type="bibr" rid="r01">1</xref>
</sup>
. However, orthodontists are often faced with complicated
challenges, such as: 1) the low-order maxillary sinus that hinders implantation in the
molar area, 2) the maxillary tubercle and external oblique line where implanting
microscrews is a greater challenge compared to the flat areas in the jaw bone, 3) the
complicated surgical placement for palatal implants<sup><xref ref-type="bibr" rid="r18">18</xref>
</sup>
, and 4) too many missing teeth or rampant caries/periodontitis
within the same quadrant. These factors make it very difficult to identify the ideal
location for implants. Although microscrews can be implanted close to the extraction
site in order to achieve orthodontic support, the stability of the microscrews and the
efficiency of bone remodeling at the implant-bone interface near the extraction region
is dubious. To our knowledge, this issue has not been resolved.</p>
<p>Literature reports<sup><xref ref-type="bibr" rid="r11">11</xref>
,<xref ref-type="bibr" rid="r17">17</xref>
</sup>
show that extraction undoubtedly leads to a decrease of
bone density in the extraction vicinity. Miyawaki and his colleagues<sup><xref ref-type="bibr" rid="r14">14</xref>
</sup>
(2003) proved that the decrease in bone
density increases the risk of non-integration at the implant-bone interface. Zheng's
examination indicated that the risk of loosening of microscrews near extraction site was
the most severe in the first week following implant placement<sup><xref ref-type="bibr" rid="r21">21</xref>
</sup>
. In addition, there are several factors associated with
the stability of microscrews, such as the diameter of the miniscrew, proximity with
dental roots and inflammation within peri-implant tissue. To understand and overcome
these challenges, numerous studies have been conducted, with the aim of promoting bone
tissue remodeling at the implant-bone interface to increase stability of microscrews
under diverse conditions<sup><xref ref-type="bibr" rid="r13">13</xref>
,<xref ref-type="bibr" rid="r19">19</xref>
,<xref ref-type="bibr" rid="r21">21</xref>
</sup>
. However, the various animal and clinical studies have focused on
the stability of microscrews under loading in order to mimic the actual clinical process
as closely as possible. This leads to the evaluation of microscrew stability under the
influence of iatrogenic factors such as intention, direction and occasion of
loading.</p>
<p>In order to determine the ideal implantation strategy for loading, clinical
orthodontists certainly need to understand the state of the bone-device interface during
the healing process. In accordance with the change rule of bone healing<sup><xref ref-type="bibr" rid="r15">15</xref>
</sup>
, the bone remodeling process at the
interface was evaluated at 1, 3, 8 or 12 weeks following implantation. In this study, we
hypothesized that tooth extraction will influence bone tissue remodeling near the
microscrews, and we evaluated this effect <italic>via</italic>
histologic and
immunohistochemical analyses.</p>
</sec>
<sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title>
<sec><title>Animals and surgical procedures</title>
<p>Twelve male beagles meeting the following criteria were selected: 18 months of age,
10 kg in weight, presence of fourth premolars on mandible, and healthy with no
malocclusion and periodontal diseases. They were handled according to the
experimental protocol approved by the Bioethics Committee of Sichuan University,
China (Number of permit: SYXIC111 2009-045, China).</p>
<p>The animal model was described as our previous study<sup><xref ref-type="bibr" rid="r21">21</xref>
</sup>
. All the third and the forth premolars were
surgically extracted from the mandibles. Ninety-six microscrews (diameter 1.6 mm,
length 6 mm) (Medicon Company, Tuttlingen, Germany), were placed between the mesial
and distal roots of P2, P3, P4, and M1, on the buccal side of the mandible, 6 mm
beneath the top of the alveolar crest (<xref ref-type="fig" rid="f01">Figures
1a</xref>
and <xref ref-type="fig" rid="f01">1b</xref>
). The test implants (48
microscrews) were placed near the extraction sites (between the mesial and distal
roots of P3 and P4), and the control implants (48 microscrews) were placed at the
normal sites (between the mesial and distal roots of P2 and M1) (<xref ref-type="fig" rid="f02">Figures 2a</xref>
and <xref ref-type="fig" rid="f02">2b</xref>
).
Microscrews in both the test and control groups experienced no loading. The beagles
were fed liquid diet in order to avoid the impact of hard food on the microscrews,
and were finally executed at 1, 3, 8 or 12 weeks following implantation.</p>
<fig id="f01" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Images illustrating placement sites of microscrews in the mandible of beagle
dogs. (a) Clinical picture of microscrews in mandible. (b) Transverse section
of mandible with black dots indicating the precise site of microscrews</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g01"></graphic>
</fig>
<fig id="f02" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Radiographs illustrating implanted microscrews. (a) Radiograph of microscrew
implanted between the roots of first molar. (b) Radiograph of a microscrew
implanted near an extraction site</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g02"></graphic>
</fig>
</sec>
<sec><title>Histologic analysis</title>
<p>The mandibles were removed from the executed animals and carefully sectioned into
small tissue blocks (10x10x6 mm). Each tissue block contained one microscrew
surrounded by at least 4 mm-thick bone tissue. The blocks were fixed in cold buffered
formalin, pH 7.0, for 3-6 days and then demineralized in 20% tetrasodium
ethylenediaminetetraacetic acid (EDTA, pH 7.0) for about 4 to 6 months until the
microscrews could be easily removed without breaking the implant-bone interface. All
paraffin-embedded blocks were cut into 4 µm-thick slices. Some tissue sections were
stained with Masson's Trichrome for descriptive analysis and determination of
neutrophil and osteoblast densities. For the determination of cell density, 5
histological fields of the implant-bone interface were randomly selected and the
number of neutrophils and osteoblast was counted by manual method using 200×
magnification coupled to Nikon E600 microscope (Nikon Instruments Inc, Melville,
USA). The cell-density was calculated by the mean of cell number <italic>per</italic>
field.</p>
</sec>
<sec><title>Immunohistochemistry analysis</title>
<p>Following paraffin removal from the tissue sections, they were hydrated by incubation
in 95%, 90%, 80%, and 70% ethanol for 5 minutes. After antigen retrieval with TRIS
EDTA (pH 9.0) solution for 30 min, sections were immersed in PBS-H202 (0.01 ml, pH
7.0, PBS 99 ml + 30% H202 1 ml) for 20-30 minutes, at room temperature (23ºC) to
eliminate the endogenous peroxidase. The sections were first washed in distilled
water for 5 min, and then washed in phosphate-buffered saline (PBS) for another 5
minutes. Before incubation in primary antibody, sections were immersed in non-immune
serum (5% bovine serum albumin, BSA) and diluted 1:5-1:20 for 30 minutes without
wash. Following the above step, the sections were incubated with mouse anti-dog OC
antibodies (1:75, R&D Systems, Minneapolis, MN), rabbit anti-dog TGF-β antibodies
(1:100, Santa Cruz Biotechnologies, Inc, Santa Cruz, CA, USA) and caprine anti-dog
TNF-α antibodies (1:200, R&D Systems, Minneapolis, MN, USA) at 4ºC overnight.
Next, the sections were sequentially incubated with secondary biotinylated goat
anti-mouse antibodies (Santa Cruz Biotechnologies, Inc, Santa Cruz, CA, USA), mouse
anti-rabbit antibodies (1:200, R&D Systems, Minneapolis, MN, USA) and pig
anti-caprine antibodies (1:100, R&D Systems, Minneapolis, MN, USA) for 30 minutes
at 23ºC. The sections were washed and the specific antibody binding reaction was
amplified using streptavidin peroxidase. Diaminobenzidine (DAB 0.5 mg/ml) staining
and counterstaining with hematoxylin were performed to provide enhanced orientation
of the tissue topography. Finally, the sections were dehydrated in an ethanol
gradient and mounted for microscopic observation. As negative controls, slides were
incubated with PBS 1% instead of primary specific antibodies. The images were
acquired at 200× magnification using a Nikon E600 microscope (Nikon Instruments Inc,
Melville, USA). All files were saved in tagged-image file format (TIFF). The integral
optical density (IOD) of the target protein was measured with Image-Pro Plus 5.0
(Media Cybernetics, Rockville, MD, USA). In the process of measurement, the value was
defined firstly by determining the positive staining of control sections, and was
used to automatically analyze images of all samples that were stained under identical
conditions.</p>
</sec>
<sec><title>In situ hybridization</title>
<p><italic>In situ</italic>
hybridization for Cbfa1 was performed using
digoxigenin-labeled riboprobes. Before unsealing, the Cbfa1 probes were briefly
centrifuged and immersed in ddH<sub>2</sub>
O. These probes were then stored at -20ºC
until needed. Deparaffinage, hydration and deactivation of endogenous enzymes in the
paraffin sections were performed as mentioned in the previous section. Tissue
sections were dropped in pepsin diluted 3% citric acid for 30 min at 37ºC, fixed for
10 min (1% paraformaldehyde (0.1 M PBS, PH 7.0-7.6)), and washed in distilled water 3
times. The sections were pre-hybridized for 2 hours at 37-42ºC using 20 µL
pre-hybridization solution <italic>per</italic>
sections, and then they were
hybridized with the probe (2 µg/ml) diluted in hybridization buffer and in 2×SSC
(standard saline citrate) for 16-18 h at 38-42ºC. The sections were washed
sequentially in 0.2×SSC, blocked with blocking solution and then incubated with
anti-mouse antibody for 1 h at 37ºC, washed in PBS. These sections were then exposed
to SABC (Strept Avidin-Biotin Complex) and Biotin peroxidase for 30 min at 37ºC, and
washed again in PBS. Finally, sections were stained, counterstained, dehydrated and
mounted. The expression of cbfa1 was quantified using the same methodology for
immunohistochemical analysis.</p>
</sec>
<sec><title>Statistical analysis</title>
<p>All statistical analyses were performed with SPSS software (SPSS, Chicago, Ill).
Student's t-test was used to determine statistical differences in the values between
the test groups and the control groups. Data were presented as means with standard
deviations. A difference of P<0.05 was accepted statistically significant.</p>
</sec>
</sec>
<sec sec-type="results"><title>RESULTS</title>
<p>Histologic and immunohistochemical sections from the samples are shown in <xref ref-type="fig" rid="f04">Figures 4</xref>
-<xref ref-type="fig" rid="f09">9</xref>
.
Twelve male beagles received 93 samples. Three samples were omitted due to the loss of
microscrews in the test group at week 1.</p>
<fig id="f04" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Graphs showing the changes in the density of neutrophil and osteoblast in both
groups at 1, 3, 8 and 12-weeks healing time. <sup>*</sup>
indicates statistically
significant differences</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g04"></graphic>
</fig>
<fig id="f05" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>Graphs showing the changes in expression of Cbfa1, osteocalcin (OC), TGF-β and
TNF-α, in both groups at 1, 3, 8 and 12-week healing time. <sup>*</sup>
indicates
statistically significant differences. (a) At week 8, the expression in the test
group was significantly higher than in the control group (p<0.01). (b) The
expression of OC reached peak values at week 8 and subsequently decreased.
Significant differences were observed at week 3 and values of OC in the control
group were significantly higher than in the test group (p<0.01). (c). The peak
of TGF-β in the control group appeared at week 8, and subsequently went down to
the level as in week 3. At week 3, significant differences were observed between
both groups, but the expression of TGF-β in test groups was stronger than in
control groups (p<0.01). (d) Significant differences in expression between two
groups were observed at week 1 and week 3, and the values in the test group were
higher than those in the control group (p< 0.01)</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g05"></graphic>
</fig>
<fig id="f06" orientation="portrait" position="float"><label>Figure 6</label>
<caption><p>Immunohistochemical staining of Cbfa1 in sections from beagle mandible from test
(a and c) and control groups (b and d), during weeks 3 and 8. The expression of
Cbfa1 in both groups reached peak values at week 3, but there were no
statistically significant differences between test group (a) and control group
(b). At week 8, significant differences were observed between both groups, and the
expression of Cbfa1 in test group (c) was stronger than in control group (d).
Magnification: 200x</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g06"></graphic>
</fig>
<fig id="f07" orientation="portrait" position="float"><label>Figure 7</label>
<caption><p>Immunohistochemical staining of osteocalcin (OC) in beagle mandible sections from
test (a and c) and control groups (b and d), during weeks 3 and 8. The expression
of OC in control group (b) was stronger than in test group (a) at week 3. The
expression levels of OC in both groups reached peak values at week 8 (c, d). No
statistically significant differences were observed between the two groups at week
8. Magnification: a and b; 40x, c and d; 100x</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g07"></graphic>
</fig>
<fig id="f08" orientation="portrait" position="float"><label>Figure 8</label>
<caption><p>Immunohistochemical staining of TGF-β in sections from beagle mandible from test
(a and b) and control group (c and d), during weeks 3 and 8. The expression of
TGF-β in test group reached the peak values at week 3 (a). The expression in
control groups was low at week 1 (d) and reached the peak values at week 8 (c).
There were statistically significant differences between two groups at week 3. The
values in test group were higher than in control group (b). Magnification: 40x</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g08"></graphic>
</fig>
<fig id="f09" orientation="portrait" position="float"><label>Figure 9</label>
<caption><p>Immunohistochemical staining of TNF-α in beagle mandible sections from test (a and
c) and control group (b and d), during weeks 3 and 8. Statistically significant
differences were observed between the two groups at week 3. The TNF-α values in
test group (a) were higher than in control group (b). The expression in test group
(c) and control group (d) presented a downward trend at week 8. Magnification:
40x</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g09"></graphic>
</fig>
<sec><title>Histologic findings</title>
<p>At week 1, a large number of neutrophil were aggregated at the bone-screw interface
(<xref ref-type="fig" rid="f03">Figure 3a</xref>
). In the test group, the
neutrophil density was higher (p<0.01) while the osteoblast density was lower
(p<0.01) in relation to control group (<xref ref-type="fig" rid="f04">Figure
4</xref>
). There were new bone layers in the test group at week 3 (<xref ref-type="fig" rid="f03">Figure 3b</xref>
). By week 8, many active osteoblasts
gathered along the interface and excreted a large-scale bone matrix around the
microscrew (<xref ref-type="fig" rid="f03">Figure 3c</xref>
). By week 12, there was a
mass of mature lamellar bone in the implant-bone interface, calcified to a degree
close to that of normal bone tissue (<xref ref-type="fig" rid="f03">Figure
3d</xref>
). However, the amount of dematrix bone in the control group was greater
than in the test group at week 3 and week 8.</p>
<fig id="f03" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Histologic analysis at the implant-bone interface in the test group (lower
panel) and control group (upper panel) using Masson staining. (a) In the test
group, a large number of neutrophils were aggregated at the interface at week 1
while a large amount of fibrous tissue was aggregated in the control group. (b)
the new bone layer in the test group at week 3. (c) A large-scale dematrix bone
(DB) excreted by osteoblasts around the microscrew was observed in both groups
at week 8. (d) A mass of mature lamellar bone in the implant-bone interface in
both groups at week 12 (Masson stain). Magnification: a, b, c, d; 200x</p>
</caption>
<graphic xlink:href="jaos-21-05-0443-g03"></graphic>
</fig>
</sec>
<sec><title>Immunohistochemistry analysis</title>
<p>The expression of Cbfa1 in both groups reached a peak at week 3 (<xref ref-type="fig" rid="f05">Figure 5</xref>
). At week 8, the expression in the test group was higher
significantly than in the control group (<xref ref-type="fig" rid="f06">Figure
6</xref>
) (p<0.01). The expression of OC reached peak values at week 8 and
subsequently decreased (<xref ref-type="fig" rid="f05">Figure 5</xref>
). Significant
differences were observed at week 3 and values of OC in the control group were
significantly higher than in the test group (<xref ref-type="fig" rid="f07">Figure
7</xref>
) (p<0.01). The TGF-β values in test groups reached a peak at week 3.
At week 3, significant differences were observed between both groups, but the
expression of TGF-β in test groups was stronger than in control groups (<xref ref-type="fig" rid="f08">Figure 8</xref>
) (p<0.01). The mean levels of TNF-α in
both groups were high in the first three weeks after implantation. Significant
differences in expression between two groups were observed at week 1 and week 3, and
the values in the test group were higher than those in the control group (<xref ref-type="fig" rid="f09">Figure 9</xref>
) (p<0.01).</p>
</sec>
</sec>
<sec sec-type="discussion"><title>DISCUSSION</title>
<p>Owing to its miniature size and simple surgical placement, miniscrews are easy to place
in the maxillae and mandibles, with the aim of providing skeletal anchorage for
orthodontic patients. However, in face of the variety of oral conditions seen
clinically, orthodontists often need to choose the most suitable miniscrew site, and at
present, interradicular sites are the most common choice. In this study, all miniscrews
were placed between the mesial and distal roots of P2, P3, P4 and M1 at the buccal side
of the mandible of beagles. In order to avoid damaging the roots of neighboring teeth,
as reported in a study by Asscherickx, et al.<sup><xref ref-type="bibr" rid="r02">2</xref>
</sup>
(2005), radiographs of the beagle mandibles were taken to confirm
that the furcation angles of the roots of P2, P3, P4, and M1 of all beagles were above
50 degrees. Moreover, the radiographs, at a later stage, had revealed that implantation
between the mesial and distal roots of P2, P3, P4 and M1 were accurate, and these sites
had not interfered with the roots of neighboring teeth or other important structures of
the mandible.</p>
<p>In this study, histologic findings from the test group revealed that, at week 1, the
original bone was destroyed, with aggregation of a large number of inflammatory cells at
the screw-bone interface. Active osteoblasts were gathered around the new bone by week
3. Moreover, by week 8, osteoblasts had secreted a large-scale bone matrix around the
microscrew. Literature had reported that, during the first week, pull-out strength of
the miniscrews was significantly lower near the extraction site than it was at a
distance away from it, followed by an increase in strength during weeks 3 and 8. This
indicates that inflammatory reaction and bone resorption at the implant-bone interface
were 2 major initial events following implantation. This likely explains why 3
microscrews in the test group failed at this stage. However, subsequent to longer
healing time and formation of new bone, the risks surroundings the stability of
microscrews decreased significantly, as can be confirmed by the ensuing molecular
regulation of osteogenesis around the miniscrews.</p>
<p>At week 1, the expression of Cbfa1, OC and TGF-β was inconspicuous in control and test
groups. In contrast, TNF-α expression in both groups was most robust following
implantation. This suggests that there emerged a mass of macrophages and osteoclast
mediated by TNF-α<sup><xref ref-type="bibr" rid="r03">3</xref>
,<xref ref-type="bibr" rid="r10">10</xref>
</sup>
, which aggravated directly the damage of interface bone,
especially in the test group, which likely caused 3 microscrews to fail in this group.
However, due to the low-expression of Cbfa1, OC and TGF-β, bone formation and bone
mineralization triggered by osteoblasts were still inconspicuous during this
stage<sup><xref ref-type="bibr" rid="r04">4</xref>
,<xref ref-type="bibr" rid="r05">5</xref>
,<xref ref-type="bibr" rid="r08">8</xref>
</sup>
. In addition, literature
reports have suggested that extraction leads to a decrease in bone density in the
surrounding vicinity, which increases the risk of non-integration at the implant-bone
interface<sup><xref ref-type="bibr" rid="r11">11</xref>
,<xref ref-type="bibr" rid="r14">14</xref>
,<xref ref-type="bibr" rid="r17">17</xref>
</sup>
. Thus, it is
safe to assume that infiltration of numerous inflammatory cells had reduced the
stability of the microscrews at week 1, and that the area near the extraction site was
not suitable for implantation, even without loading.</p>
<p>Tu, et al.<sup><xref ref-type="bibr" rid="r16">16</xref>
</sup>
(2007) discovered that
alveolar bone defects were largely filled with fibrous connective tissues 3 weeks after
surgery in normal mice. In contrast, wound healing was dramatically delayed in
Cbfa1-deficient mice. Therefore, with the increasing level of Cbfa1, the most active
period of bone remodeling possibly occurred at week 3 post-implantation. Although the
high-intensity expression of Cbfa1 was not significantly different at week 3 between the
two groups in our study, it maintained its intensity until week 8 in the test groups,
and decreased significantly in the control groups. Esposito, et al.<sup><xref ref-type="bibr" rid="r06">6</xref>
</sup>
(2010) showed that the most active period
of bone remodeling following extraction was week 8, which may explain why the level of
Cbfa1 was higher in test groups at week 8. Likewise, the expression of TGF-β and OC was
high from week 3 to week 8. Thus, active osteoblasts and large-scale new bone were
formed at this stage. Osteogenesis was observed at the implant-bone interface during
this stage, and the expression of TNF-α, as well as the inflammation mediated by it,
began to decline significantly. On the other hand, the expression of OC in the control
group was higher than in the test group at week 3. TNF-α can likely inhibit the
expression of matrix protein genes at week 310. However, by week 8, the expression level
of TGF-β and OC was the same in both the test and control groups. Literature<sup><xref ref-type="bibr" rid="r21">21</xref>
</sup>
reported that values of microscrew
pull-out strength were similar between the test and the control groups at week 8. Thus,
these findings suggest that, with a longer period of healing, the risk of microscrew
instability decreased significantly, and that, by week 8, the remodeling of the
interface bone, both in test and control groups, tended to be similar.</p>
<p>As for week 12, there was a large amount of mature lamellar bone at the implant-bone
interface, calcified to a degree that was similar to that of normal bone tissue. The
expression of TGF-β, OC and Cbfa1 began to decline, which illustrated a decline in bone
tissue remodeling. TNF-α expression had begun to rebound, which suggests that lack of
corresponding bone stimulation aggravates bone resorption<sup><xref ref-type="bibr" rid="r20">20</xref>
</sup>
.</p>
</sec>
<sec sec-type="conclusions"><title>CONCLUSIONS</title>
<p>After investigating the remodeling of the bone-microscrew interface near extraction
sites via histologic and immunohistochemical analysis, we conclude that:</p>
<p>In the early days, the bone remodeling of extraction will affect stability of microscrew
near extraction;</p>
<p>Subsequent to a longer healing period, the influence of extraction on the remodeling of
interface bone surrounding microscrews decreases;</p>
<p>Irrespective of the location of the interface, near or away from an extraction site,
microscrews are suitable for implantation.</p>
</sec>
</body>
<back><ack><sec><title>ACKNOWLEDGMENTS</title>
<p>Supported by the General Program of National Natural Science Foundation for Young
Scholars of China (81000463, 10902075); Foundation of the General Program of
Chongqing Natural Science (cstc2012jja10053); Foundation of the Chongqing Municipal
Health Bureau (2012-2-126); Foundation of the Chongqing Municipal Commission of
Education (kj120329).</p>
</sec>
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