Experimental study on penetration of dental implants into the maxillary sinus in different depths
Identifieur interne : 002F80 ( Pmc/Corpus ); précédent : 002F79; suivant : 002F81Experimental study on penetration of dental implants into the maxillary sinus in different depths
Auteurs : Weijian Zhong ; Binke Chen ; Xin Liang ; Guowu MaSource :
- Journal of Applied Oral Science [ 1678-7757 ] ; 2013.
Abstract
The exposing of dental implant into the maxillary sinus combined with membrane perforation might increase risks of implant failure and sinus complications.
The purpose of this study was to investigate the effects of the dental implant penetration into the maxillary sinus cavity in different depths on osseointegration and sinus health in a dog model.
Sixteen titanium implants were placed in the bilateral maxillary molar areas of eight adult mongrel dogs, which were randomly divided into four groups according to the different penetrating extents of implants into the sinus cavities (group A: 0 mm; group B: 1 mm; group C: 2 mm; group D: 3 mm). The block biopsies were harvested five months after surgery and evaluated by radiographic observation and histological analysis.
No signs of inflammatory reactions were observed in any maxillary sinus of the eight dogs. The tips of the implants with penetrating depth of 1 mm and 2 mm were found to be fully covered with newly formed membrane and partially with new bone. The tips of the implants with penetrating depth over 3 mm were exposed in the sinus cavity and showed no membrane or bone coverage. No significant differences were found among groups regarding implant stability, bone-to-implant contact (BIC) and bone area in the implant threads (BA).
Despite the protrusion extents, penetration of dental implant into the maxillary sinus with membrane perforation does not compromise the sinus health and the implant osseointegration in canine.
Url:
DOI: 10.1590/1679-775720130078
PubMed: 24473723
PubMed Central: 3891281
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PMC:3891281Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Experimental study on penetration of dental implants into the maxillary
sinus in different depths</title><author><name sortKey="Zhong, Weijian" sort="Zhong, Weijian" uniqKey="Zhong W" first="Weijian" last="Zhong">Weijian Zhong</name></author><author><name sortKey="Chen, Binke" sort="Chen, Binke" uniqKey="Chen B" first="Binke" last="Chen">Binke Chen</name></author><author><name sortKey="Liang, Xin" sort="Liang, Xin" uniqKey="Liang X" first="Xin" last="Liang">Xin Liang</name></author><author><name sortKey="Ma, Guowu" sort="Ma, Guowu" uniqKey="Ma G" first="Guowu" last="Ma">Guowu Ma</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24473723</idno><idno type="pmc">3891281</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3891281</idno><idno type="RBID">PMC:3891281</idno><idno type="doi">10.1590/1679-775720130078</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">002F80</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002F80</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Experimental study on penetration of dental implants into the maxillary
sinus in different depths</title><author><name sortKey="Zhong, Weijian" sort="Zhong, Weijian" uniqKey="Zhong W" first="Weijian" last="Zhong">Weijian Zhong</name></author><author><name sortKey="Chen, Binke" sort="Chen, Binke" uniqKey="Chen B" first="Binke" last="Chen">Binke Chen</name></author><author><name sortKey="Liang, Xin" sort="Liang, Xin" uniqKey="Liang X" first="Xin" last="Liang">Xin Liang</name></author><author><name sortKey="Ma, Guowu" sort="Ma, Guowu" uniqKey="Ma G" first="Guowu" last="Ma">Guowu Ma</name></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>The exposing of dental implant into the maxillary sinus combined with membrane
perforation might increase risks of implant failure and sinus complications.</p><sec><title>Objective</title><p>The purpose of this study was to investigate the effects of the dental implant
penetration into the maxillary sinus cavity in different depths on
osseointegration and sinus health in a dog model. </p></sec><sec><title>Material and Methods</title><p>Sixteen titanium implants were placed in the bilateral maxillary molar areas of
eight adult mongrel dogs, which were randomly divided into four groups according
to the different penetrating extents of implants into the sinus cavities (group A:
0 mm; group B: 1 mm; group C: 2 mm; group D: 3 mm). The block biopsies were
harvested five months after surgery and evaluated by radiographic observation and
histological analysis. </p></sec><sec><title>Results</title><p>No signs of inflammatory reactions were observed in any maxillary sinus of the
eight dogs. The tips of the implants with penetrating depth of 1 mm and 2 mm were
found to be fully covered with newly formed membrane and partially with new bone.
The tips of the implants with penetrating depth over 3 mm were exposed in the
sinus cavity and showed no membrane or bone coverage. No significant differences
were found among groups regarding implant stability, bone-to-implant contact (BIC)
and bone area in the implant threads (BA). </p></sec><sec><title>Conclusions</title><p>Despite the protrusion extents, penetration of dental implant into the maxillary
sinus with membrane perforation does not compromise the sinus health and the
implant osseointegration in canine.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Aimetti, M" uniqKey="Aimetti M">M Aimetti</name></author><author><name sortKey="Romagnoli, R" uniqKey="Romagnoli R">R Romagnoli</name></author><author><name sortKey="Ricci, G" uniqKey="Ricci G">G Ricci</name></author><author><name sortKey="Massei, G" uniqKey="Massei G">G Massei</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Berengo, M" uniqKey="Berengo M">M Berengo</name></author><author><name sortKey="Sivolella, S" uniqKey="Sivolella S">S Sivolella</name></author><author><name sortKey="Majzoub, Z" uniqKey="Majzoub Z">Z Majzoub</name></author><author><name sortKey="Cordioli, G" uniqKey="Cordioli G">G Cordioli</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Boyne, Pj" uniqKey="Boyne P">PJ Boyne</name></author><author><name sortKey="James, Ra" uniqKey="James R">RA 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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">24473723</article-id><article-id pub-id-type="pmc">3891281</article-id><article-id pub-id-type="doi">10.1590/1679-775720130078</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Articles</subject></subj-group></article-categories><title-group><article-title>Experimental study on penetration of dental implants into the maxillary
sinus in different depths</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>ZHONG</surname><given-names>Weijian</given-names></name></contrib><contrib contrib-type="author"><name><surname>CHEN</surname><given-names>Binke</given-names></name></contrib><contrib contrib-type="author"><name><surname>LIANG</surname><given-names>Xin</given-names></name></contrib><contrib contrib-type="author"><name><surname>MA</surname><given-names>Guowu</given-names></name><xref ref-type="corresp" rid="c01"></xref></contrib><aff> Department of Oral Maxillofacial Surgery, College of Stomatology, Dalian Medical University, Dalian, China.</aff></contrib-group><author-notes><corresp id="c01"><bold>Corresponding address:</bold> Guowu Ma - No. 9 West part of Lvshun Southern
Road - College of Stomatology, Dalian Medical University - Dalian 116044 - China -
Phone: 0411-86110398 - Fax: 0411-86110398 - e-mail:
<email>mgw640242000@yahoo.com.cn</email></corresp></author-notes><pub-date pub-type="ppub"><season>Nov-Dec</season><year>2013</year></pub-date><volume>21</volume><issue>6</issue><fpage>560</fpage><lpage>566</lpage><history><date date-type="received"><day>15</day><month>1</month><year>2013</year></date><date date-type="rev-recd"><day>19</day><month>6</month><year>2013</year></date><date date-type="accepted"><day>23</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>The exposing of dental implant into the maxillary sinus combined with membrane
perforation might increase risks of implant failure and sinus complications.</p><sec><title>Objective</title><p>The purpose of this study was to investigate the effects of the dental implant
penetration into the maxillary sinus cavity in different depths on
osseointegration and sinus health in a dog model. </p></sec><sec><title>Material and Methods</title><p>Sixteen titanium implants were placed in the bilateral maxillary molar areas of
eight adult mongrel dogs, which were randomly divided into four groups according
to the different penetrating extents of implants into the sinus cavities (group A:
0 mm; group B: 1 mm; group C: 2 mm; group D: 3 mm). The block biopsies were
harvested five months after surgery and evaluated by radiographic observation and
histological analysis. </p></sec><sec><title>Results</title><p>No signs of inflammatory reactions were observed in any maxillary sinus of the
eight dogs. The tips of the implants with penetrating depth of 1 mm and 2 mm were
found to be fully covered with newly formed membrane and partially with new bone.
The tips of the implants with penetrating depth over 3 mm were exposed in the
sinus cavity and showed no membrane or bone coverage. No significant differences
were found among groups regarding implant stability, bone-to-implant contact (BIC)
and bone area in the implant threads (BA). </p></sec><sec><title>Conclusions</title><p>Despite the protrusion extents, penetration of dental implant into the maxillary
sinus with membrane perforation does not compromise the sinus health and the
implant osseointegration in canine.</p></sec></abstract><kwd-group><kwd>Maxillary sinus</kwd><kwd>Dental implants</kwd><kwd>Complications</kwd></kwd-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>While a limited amount of bone is generally present at the edentulous posterior maxilla
due to atrophy of alveolar ridge and pneumatization of the maxillary sinus, several
techniques have been described in which dental implants are inserted marginally to the
bony sinus floor with a localized augmentation procedure<sup><xref ref-type="bibr" rid="r03">3</xref>,<xref ref-type="bibr" rid="r18">18</xref></sup>. Since these
approaches have become conventional treatments in Implant Dentistry, the risk of
exposing the implant to the maxillary sinus increased. The incidence of the sinus
membrane perforation was reported as 7% to 35%<sup><xref ref-type="bibr" rid="r05">5</xref>,<xref ref-type="bibr" rid="r16">16</xref>,<xref ref-type="bibr" rid="r17">17</xref></sup>, and the sinus lifting procedure was abandoned in some
studies because of the large perforation of the sinus membrane<sup><xref ref-type="bibr" rid="r10">10</xref>,<xref ref-type="bibr" rid="r21">21</xref></sup>.</p><p>In general, the sinus membrane perforation is considered as a potential risk factor for
implant failure and sinus infection. Some investigators claimed that the membrane
perforation was strongly associated with the occurrence of postoperative sinus
infection<sup><xref ref-type="bibr" rid="r06">6</xref>,<xref ref-type="bibr" rid="r22">22</xref></sup>, while others assumed that there was a correlation
between implant failure and sinus membrane perforation<sup><xref ref-type="bibr" rid="r08">8</xref>,<xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r13">13</xref></sup>. However, clinicians have generally reported that slight
membrane perforation after implant placement does not play a significant role in the
clinical outcome<sup><xref ref-type="bibr" rid="r04">4</xref>,<xref ref-type="bibr" rid="r15">15</xref>,<xref ref-type="bibr" rid="r19">19</xref></sup>. Nevertheless,
the available literature has not conclusively determined so far the significance of
implant exposure to the sinus cavity on implant survival and maxillary sinus
complication, particularly with respect to the histological evidences.</p><p>Because most reported results of the sinus membrane perforation are clinical
observations, they lack well-defined outcome criteria or control. In order to help
clinicians to make proper surgical decisions, data on a more controlled scientific level
is necessary to be provided.</p><p>The purpose of the present study was to evaluate the effects of dental implant exposure
to maxillary sinus cavity with penetrating depth of 1-3 mm on osseointegration and sinus
health in a dog model after a 5-months healing period.</p></sec><sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title><sec><title>Animals</title><p>Eight healthy adult male mongrel dogs (weight 14.8-19.5 kg, age 20-24 months old)
without any oral and systemic diseases were included in this study. The animals were
housed individually in indoor cages and the diet during the course of the experiment
was whole grain flour, cornmeal, soybean cake, fishbone meal, and eggs, according to
the general feeding program at Experimental Animal Center of Dalian Medical
University, China. The protocol for this animal study was approved by the Ethics
Committee of Dalian Medical University (protocol number: 2007-05A).</p></sec><sec><title>Experimental groups</title><p>A split-mouth randomized design, using four treatment protocols on the positions of
bilateral maxillary first molars, was employed. In total, 16 samples were used in
this study. Each implant recipient site was randomly assigned to one of the four
treatment protocols, and immediate implant placement was applied accordingly: (1)
group A (n=4), was control group without sinus floor penetration; (2) group B (n=4),
with penetrating depth of 1 mm; (3) group C (n=4), with penetrating depth of 2 mm;
(4) group D (n=4), with penetrating depth of 3 mm. The investigators ensured
unpredictability of the allocation sequence by coin toss before surgeries.</p></sec><sec><title>Surgical procedures</title><p>The dogs received 1 week of antibiotics prophylaxis (gentamicin sulfate, 16000000
U/day, Linggui Pharmaceutical Co.Ltd, Zhengzhou, China) to prevent infection. For all
the surgical procedures involved in this study, animals were anesthetized
intramuscularly with ketamine hydrochloride (10 mg/kg, Changchun Academy of Military
Medical Sciences, Changchun, China). The anesthesia was supplemented by local
administration of 2% lidocaine HCI with 1:100,000 epinephrine (2-4) ml, Shandong
Pharmaceutical Production Ltd, Shandong, China). The whole surgical procedure was
performed under sterile conditions by only one surgeon (W.Z.), with a decade of
clinical experience in Implant Dentistry.</p><p>After the maxillary first molars were extracted bilaterally with special care,
immediate implant placements were performed in the palatal sockets. Sixteen
custom-made threaded cylindrical implants of grade 5 pure titanium (Ø=3.75 mm, L=10
mm, CDIC, Sichuan University, China) were thoroughly examined and sterilized prior to
surgery. Each site was prepared with twist drills at low speed of 500 rpm while being
cooled with sterile saline at 4ºC. After the bone and mucous membrane of the sinus
floors were intentionally drilled through, the level of the sinus floor was detected
with a dental probe and the height of residual ridge was measured. Except for the
implants of control group placed within the alveolar bone without protruding into the
sinus cavity, the other twelve implants were placed bilaterally in the sinus in such
a way that they penetrated the bone and mucous membrane of the maxillary sinus floor
to the extent of 1 mm, 2 mm, or 3 mm, respectively. The buccal mucoperiosteal flaps
were released and sutured with 4-0 vicryl resorbable sutures.</p><p>To prevent postoperative infections, the animals received a daily penicillin
intramuscular injection (2 doses of 100,000 units/kg, Penicillin G sodium, Shandong
Pharmaceutical Production Ltd, Shandong, China) for one week, and plaque control was
ensured three times <italic>per</italic> week using a 0.2% chlorhexidine gel on
implant placement sites with soft toothbrush. A soft diet was given to the animals
during the healing period.</p></sec><sec><title>Resonance frequency analysis</title><p>The stability of the implants was assessed with RFA (Osstell<sup>TM</sup>,
Integration Diagnostics AB, Goteborg, Sweden) in implant stability quotient units at
the time of implant placement and 5 months later.</p></sec><sec><title>Sacrifice and samples preparation</title><p>Five months after surgery, the animals were sacrificed with overdose pentobarbital
sodium and vascular perfusion was undertaken with paraformaldehyde. The sample blocks
of maxilla with implants were harvested and the upper walls of the sinus were
eliminated to expose the sinus floor. The specimens were trimmed and immersed in 4%
paraformaldehyde in 0.1 M sodium phosphate buffer.</p></sec><sec><title>Observation and histological assessment</title><p>After a gross observation, radiographic examination was performed with periapical
radiograph using paralleling technique, and the X-ray beam was perpendicular to the
long axis of the implant and film. All samples were shot using the following exposure
conditions: 70 Kv tube voltage, 10 mA tube current and 0.32-second exposing time.
Thereafter, the membrane adjacent to the implant was processed into paraffin section
and stained with hematoxylin and eosin.</p><p>After dissection of the jawbones, each implant with a preserved 5-mm thickness of
peri-implant bone was removed as one piece of sample. Following dehydration in a
series of ascending grades of ethanol, the bone blocks were embedded in hard-grade
acrylic resin (LR WhiteTM, London Resin Company Ltd, Berkshire, England) and
polymerized in a dry heat oven at 60ºC. Blocks were cut longitudinally, sections were
ground to a thickness of 30 µm and stained with methylene blue and aniline red (Exact
Cutting and Grinding equipment, Exact Apparatebau, Norstedt, Germany). Three coronal
sections from central area of each implant were obtained for histological assessment.
Histomorphometric analysis of BIC and BA were performed using Scion Image software
(NIH, Bethesda, MD, USA).</p></sec><sec><title>Statistical analysis</title><p>The results of BIC and BA were recorded as mean value (standard deviation) from the
twelve sections of each group. Statistical analysis of differences between groups was
performed using one-way ANOVA with SPSS 11.0 software (SPSS Inc., Chicago, IL, USA).
Probability (P) values less than 0.05 were considered significant.</p></sec></sec><sec sec-type="results"><title>RESULTS</title><p>At the time of surgical procedure, the animals showed no clinical signs of any sinus
disorder. The postoperative healing was uneventful in all of the cases. All animals
recovered rapidly from surgeries and were healthy throughout the follow-up period. There
was not any sign of wound infection or other complications such as implant loosening or
falling. Two cover screws were exposed in the control group.</p><sec><title>Resonance frequency analysis</title><p>In all groups, primary stability was obtained and maintained to the time of
sacrifice. The values from implant stability quotient measurements were recorded at
the moment of implants placement and animal sacrifice (<xref ref-type="table" rid="t01">Table 1</xref>). No apparent differences were found among groups.</p><table-wrap id="t01" orientation="portrait" position="float"><label>Table 1</label><caption><p>Implant stability quotient values [Mean(SD)] measured by resonance frequency
analysis at the time of implant placement and animal sacrifice</p></caption><table frame="hsides" rules="groups"><thead><tr><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1"><bold>ISQ value</bold></td><td colspan="4" align="center" style="background-color:#CCCCCC" rowspan="1"><bold>Groups</bold></td></tr><tr><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><bold>A</bold></td><td align="center" rowspan="1" colspan="1"><bold>B</bold></td><td align="center" rowspan="1" colspan="1"><bold>C</bold></td><td align="center" rowspan="1" colspan="1"><bold>D</bold></td></tr></thead><tbody><tr><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">Placement</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">66.1(4.4)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">65.5(3.2)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">63.8(4.8)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">68(9.6)</td></tr><tr><td align="center" rowspan="1" colspan="1">Sacrifice</td><td align="center" rowspan="1" colspan="1">65(3.7)</td><td align="center" rowspan="1" colspan="1">64.2(4.5)</td><td align="center" rowspan="1" colspan="1">65.7(2.8)</td><td align="center" rowspan="1" colspan="1">63.6(11.2)</td></tr></tbody></table><table-wrap-foot><fn><p>ISQ: Implant stability quotient</p><p>SD: Standard Deviation</p></fn></table-wrap-foot></table-wrap></sec><sec><title>Gross examination</title><p>The bone and membrane of sinus floor remained intact in the control group (<xref ref-type="fig" rid="f01">Figure 1a</xref>). In group B and group C, the protruding
parts of implants that had been introduced into the sinus cavity for 1 mm and 2 mm
were fully covered with a thin layer of newly formed membrane with a healthy
appearance (<xref ref-type="fig" rid="f01">Figures 1b</xref>, <xref ref-type="fig" rid="f01">1c</xref>). In group D, the parts of implants that had been penetrated
into the sinus cavity for 3 mm were totally exposed in the sinus cavity with the
membrane surrounding the base of protruding parts (<xref ref-type="fig" rid="f01">Figure 1d</xref>). No signs of inflammation were observed in the sinus membranes
of all samples.</p><fig id="f01" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Gross observation of the apical portion of implant in sinus cavity. The bony
sinus floor in the control group (a) remained intact without implant exposure.
The tips with protruding depth of 1 mm (b) and 2 mm (c) were partially covered
with new bone and scars were left at the penetrating spots on the membrane
(arrows). The implant tip with protruding depth of 3 mm (d) was totally exposed
in the sinus cavity with no bone coverage and the penetrating hole was left on
the sinus membrane (arrow). SF: sinus floor; M: sinus membrane; B: bone of
lateral sinus wall</p></caption><graphic xlink:href="jaos-21-06-0560-g01"></graphic></fig></sec><sec><title>Radiographic examination</title><p>Radiographic examination of the sites of implantation demonstrated a close contact of
bone and implants without radiolucent areas. The tips of implants in the control
group were completely embedded in the alveolar bone (<xref ref-type="fig" rid="f02">Figure 2a</xref>). The tips of implants with the penetrating depth of 1 mm and 2
mm were surrounded by bone tissue (<xref ref-type="fig" rid="f02">Figures 2b</xref>,
<xref ref-type="fig" rid="f02">2c</xref>). The tips of implants with the
penetrating depth of 3 mm were found to protrude inside the sinus cavity without bone
coverage (<xref ref-type="fig" rid="f02">Figure 2d</xref>).</p><fig id="f02" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Radiographic examination of the sites of implantation. The tips of implants in
the control group (a) were completely embedded in the alveolar bone. The tips
of implants with penetrating depth of 1 mm (b) and 2 mm (c) were surrounded by
bone tissue. The tip of implant with the penetration depth of 3 mm was found to
protrude inside the sinus cavity with no bone coverage (d). Arrows indicate the
bony sinus floor</p></caption><graphic xlink:href="jaos-21-06-0560-g02"></graphic></fig></sec><sec><title>Histological examination</title><p>The sinus membrane presented no discernible inflammatory reactions in any of the
maxillary sinus cavities. The thickening epithelial lamina and increasing amount of
fibrous tissue in the lamina propria that was arranged in derangement were observed
in the membrane at the site of perforation. This indicated that the wound healing
process had occurred at this part of the membrane. In group D, the apical portion of
totally exposed implant was surrounded by respiratory epithelium without inflammatory
cells infiltration (<xref ref-type="fig" rid="f03">Figure 3</xref>).</p><fig id="f03" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Histological micrograph of the membrane surrounding the protruding portion of
implant in group D. Abundant blood vessels (arrows) were found in the lamina
propria with no inflammatory cells infiltration. E: epithelium. (Hematoxylin
and eosin)</p></caption><graphic xlink:href="jaos-21-06-0560-g03"></graphic></fig><p>Ground sections of bone blocks showed a successful osseointegration between all
implants and bony sinus floor, and the growing bone tissue was observed in the
retention hole of the implant which indicated an ongoing process of bone
regeneration. Although a perfect osseointegration had not been achieved at the
coronal parts in the control group, where a thin layer of fibrous tissue was present
at bone-implant interface, the apical portions of all implants in this group were
completely embraced by newly formed bone (<xref ref-type="fig" rid="f04">Figure
4a</xref>). In all the test groups, the apical parts of the implants became
integrated with the bony sinus floor that was mostly lamellar bone, whereas the
mid-portions were surrounded by trabecular bone and medullary spaces. Although the
coronal portions of the implants in group B were surrounded with fibrous connective
tissue, the apical parts were completely covered by new bone tissue (<xref ref-type="fig" rid="f04">Figure 4b</xref>). The uppermost parts of the implants in
group C were partially covered with regenerated bone tissue (<xref ref-type="fig" rid="f04">Figure 4c</xref>). However, the apical parts of implants in group D that
had protruded into the sinus cavity for 3 mm were not covered with bone tissue, but
perfect osseointegration was achieved without fibrous tissue formation in the
interface (<xref ref-type="fig" rid="f04">Figure 4d</xref>).</p><fig id="f04" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Typical histological micrographs of the coronal plane ground sections of the
control group (a), group B (b), group C (c), and group D (d). SC: sinus cavity;
B: buccal side; P: palatal side. (methylene blue and aniline red)</p></caption><graphic xlink:href="jaos-21-06-0560-g04"></graphic></fig></sec><sec><title>Histomorphometric analysis</title><p>The mean values of BIC and BA are displayed in <xref ref-type="table" rid="t02">Table
2</xref>. Statistical analysis revealed that no significant differences in the BIC
and BA were present among groups (P>0.05), although the relatively lower BIC and
BA values were observed in the control group.</p><table-wrap id="t02" orientation="portrait" position="float"><label>Table 2</label><caption><p>Comparison of the percentages of bone-implant contact and bone area in threads
[Mean(SD)] among groups</p></caption><table frame="hsides" rules="groups"><thead><tr><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1"><bold>Percentage</bold></td><td colspan="4" align="center" style="background-color:#CCCCCC" rowspan="1"><bold>Groups</bold></td></tr><tr><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><bold>A</bold></td><td align="center" rowspan="1" colspan="1"><bold>B</bold></td><td align="center" rowspan="1" colspan="1"><bold>C</bold></td><td align="center" rowspan="1" colspan="1"><bold>D</bold></td></tr></thead><tbody><tr><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">BIC</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">19.2(12.1)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">15.5(8.9)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">16.8(14.4)</td><td align="center" style="background-color:#CCCCCC" rowspan="1" colspan="1">10.3(11.6)</td></tr><tr><td align="center" rowspan="1" colspan="1">BA</td><td align="center" rowspan="1" colspan="1">34.7(21.3)</td><td align="center" rowspan="1" colspan="1">28.2(17.5)</td><td align="center" rowspan="1" colspan="1">32.2(24.5)</td><td align="center" rowspan="1" colspan="1">16.5(12.2)</td></tr></tbody></table><table-wrap-foot><fn><p>BIC: Bone-implant contact; BA: Bone area in threads</p><p>SD: Standard Deviation</p></fn></table-wrap-foot></table-wrap></sec></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>It is generally acknowledged that the implant displaced into the maxillary sinus can act
as a foreign body and thus can cause serious ongoing complications<sup><xref ref-type="bibr" rid="r07">7</xref>,<xref ref-type="bibr" rid="r09">9</xref></sup>.
It has also been reported that implant penetration into sinus cavity resulted in
recurrent rhino-sinusitis<sup><xref ref-type="bibr" rid="r14">14</xref></sup>. The most
likely explanation for this complication is that altered nasal airflow could induce
irritation of the nasal mucosa<sup><xref ref-type="bibr" rid="r12">12</xref></sup>. In
addition, nasal clearance could be disturbed by implant blockage of the mucociliary
pathway giving rise to inflammation<sup><xref ref-type="bibr" rid="r23">23</xref></sup>.
However, evidence is scarce concerning whether the length of implants penetration into
the sinus cavity might inhibit the spontaneous recovery of membrane perforation and
further result in development of rhino-sinusitis.</p><p>The present animal experiment was designed to evaluate whether there are differences
between minor and major penetrations of implants into maxillary sinus, with respect to
their effect on implant osseointegration and sinus complication. Despite the different
penetrating depths, the osseointegration in the interface between implant and bony sinus
floor was achieved, and no inflammatory reaction was observed in the surrounding sinus
membrane, suggesting that the exposed implants do not make the maxillary sinus membrane
vulnerable to complications.</p><p>Disruptive membrane around the apical portion of implant healed again and re-covered the
tips of implants provided the protruding depths were less than 2 mm. Regenerated bone
tissue was discovered on the uppermost part of some implants which indicated the
self-regenerating and new bone-inducing abilities of sinus membrane. Based on the
present result, it seems that under the circumstance of everyday practice, it is
relatively safe to control the implant protrusion depth to the extent of less than 2 mm
in case a healthy maxillary sinus was accidentally perforated.</p><p>Whereas, when the protruding depth was deeper than 3 mm, membrane coverage of the
exposed portion could not be achieved. Circular epithelium structure similar to gingival
cuff formed around the base of the protruding parts and did not show any sign of
inflammation. This observation may be explained by the direct attachment of the membrane
to the implants, forming a barrier to the sinus cavity. As for the parts that were not
covered with the sinus membrane, debris might accumulate on the surface of the exposed
apical part over time and become a potential predisposition to sinusitis.</p><p>It was reported that transient sinusitis was prone to develop in patients with a
predisposition for sinusitis<sup><xref ref-type="bibr" rid="r19">19</xref></sup>.
Unhealthy sinus with chronic inflammation or cyst combined with membrane perforation may
lead to severe acute sinus infection. It is prudent to evaluate all patients
preoperatively by intranasal examination to rule out those individuals with a history of
sinus pathology that could be aggravated by inflammation associated with the sinus lift
procedure. For implants that were accidentally penetrated through the sinus membrane and
exposed into the sinus cavity, provided that the sinus was healthy before operation and
necessary postoperative anti-infection management was given, these implants were
suggested to remain in place for follow-up observation<sup><xref ref-type="bibr" rid="r01">1</xref>,<xref ref-type="bibr" rid="r02">2</xref>,<xref ref-type="bibr" rid="r20">20</xref></sup>. But more clinical evidences were needed to confirm this
standpoint.</p><p>Because the immediate implant placement after extraction was performed in this study and
no bone grafting or any membrane technique was used, it was accessible that the poorly
embedded cervical portions of some implants in group A and B were encapsulated with
fibrous tissue resulting in relatively lower BIC and BA values. But the clinical
stability of these implants was achieved and the apical osseointegration was confirmed
by histological analysis.</p><p>Although the 5-months observational period was too short and an animal model cannot
exactly replicate the human environment, such studies may provide the best possible
answers to the problems relating implants exposed to the sinus cavity. However, further
investigations are necessary to evaluate long term effects of penetrating implant loaded
with prosthesis or combined with bone graft.</p></sec><sec sec-type="conclusions"><title>CONCLUSIONS</title><p>Within the limits of this study, we can conclude that, despite the different protrusion
extents, penetration of dental implants into the maxillary sinus with membrane
perforation does not compromise the implant osseointegration and the sinus health during
the 5-months observational period in canines. When the penetrating depth into the sinus
is less than 2 mm, the apical portion of implant could be re-covered by regenerating
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