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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Peri-Implant Tissue Findings in Bone Grafted Oral Cancer Patients Compared to non Bone Grafted Patients without Oral Cancer</title>
<author><name sortKey="Wolff, Jan" sort="Wolff, Jan" uniqKey="Wolff J" first="Jan" last="Wolff">Jan Wolff</name>
<affiliation><nlm:aff id="aff1"><institution>Oral and Maxillofacial Unit, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Agata, Hideki" sort="Agata, Hideki" uniqKey="Agata H" first="Hideki" last="Agata">Hideki Agata</name>
<affiliation><nlm:aff id="aff2"><institution>Division of Molecular Therapy, Advanced Clinical Research Center, The Institute of Medical Science, The University of Tokyo</institution>
<addr-line>Tokyo</addr-line>
<country>Japan.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Sandor, George K" sort="Sandor, George K" uniqKey="Sandor G" first="George K." last="Sándor">George K. Sándor</name>
<affiliation><nlm:aff id="aff3"><institution>Department of Oral and Maxillofacial Surgery, University of Oulu</institution>
<addr-line>Oulu</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Regea–Institute for Regenerative Medicine, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Haimi, Suvi" sort="Haimi, Suvi" uniqKey="Haimi S" first="Suvi" last="Haimi">Suvi Haimi</name>
<affiliation><nlm:aff id="aff4"><institution>Regea–Institute for Regenerative Medicine, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">24421999</idno>
<idno type="pmc">3886081</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3886081</idno>
<idno type="RBID">PMC:3886081</idno>
<idno type="doi">10.5037/jomr.2011.2402</idno>
<date when="2012">2012</date>
<idno type="wicri:Area/Pmc/Corpus">000693</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000693</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Peri-Implant Tissue Findings in Bone Grafted Oral Cancer Patients Compared to non Bone Grafted Patients without Oral Cancer</title>
<author><name sortKey="Wolff, Jan" sort="Wolff, Jan" uniqKey="Wolff J" first="Jan" last="Wolff">Jan Wolff</name>
<affiliation><nlm:aff id="aff1"><institution>Oral and Maxillofacial Unit, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Agata, Hideki" sort="Agata, Hideki" uniqKey="Agata H" first="Hideki" last="Agata">Hideki Agata</name>
<affiliation><nlm:aff id="aff2"><institution>Division of Molecular Therapy, Advanced Clinical Research Center, The Institute of Medical Science, The University of Tokyo</institution>
<addr-line>Tokyo</addr-line>
<country>Japan.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Sandor, George K" sort="Sandor, George K" uniqKey="Sandor G" first="George K." last="Sándor">George K. Sándor</name>
<affiliation><nlm:aff id="aff3"><institution>Department of Oral and Maxillofacial Surgery, University of Oulu</institution>
<addr-line>Oulu</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Regea–Institute for Regenerative Medicine, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Haimi, Suvi" sort="Haimi, Suvi" uniqKey="Haimi S" first="Suvi" last="Haimi">Suvi Haimi</name>
<affiliation><nlm:aff id="aff4"><institution>Regea–Institute for Regenerative Medicine, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Oral & Maxillofacial Research</title>
<idno type="eISSN">2029-283X</idno>
<imprint><date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<sec sec-type="objectives"><title>Objectives</title>
<p>The aim of this study was to compare microbiological, histological, and
mechanical findings from tissues around osseointergrated dental implants in
patients who had undergone tumour resection and subsequent bone grafting
with non bone grafted patients without a history of oral cancer and to
develop an effective tool for the monitoring of the peri-implant tissues. A
third aim was to assess and compare the masticatory function of the two
patient groups after reconstruction with dental implants.</p>
</sec>
<sec sec-type="material and methods"><title>Material and Methods</title>
<p>A total of 20 patients were divided into 2 groups. The first group was
edentulous and treated with dental implants without the need for bone
grafting. The second edentulous group, with a history of oral cancer
involving the mandible, received onlay bone grafts with concurrent placement
of dental implants. Microbiological, histological, mechanical and
biochemical assessment methods, crevicular fluid flow rate, hygiene-index,
implant mobility, and the masticatory function were analysed and compared in
both patient groups.</p>
</sec>
<sec sec-type="results"><title>Results</title>
<p>The microbiological examinations showed no evidence of the three most common
pathogenic bacteria: <italic>Porphyromonas gingivalis</italic>
, <italic>Prevotella intermedius</italic>
,
<italic>Actinobacillus actinomycetencomitans</italic>
. A causal relationship between specific
microbes and peri-implant inflammation could not be found. All biopsies in
both patient groups revealed early signs of soft tissue peri-implant
inflammation.</p>
</sec>
<sec sec-type="conclusions"><title>Conclusions</title>
<p>The crevicular fluid volume and grade of gingival inflammation around the
dental implants were related. Peri-implant tissue findings were similar in
the two patient groups despite the history of oral cancer and the need for
bone grafting at the time of dental implant placement.</p>
</sec>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Oral Maxillofac Res</journal-id>
<journal-id journal-id-type="iso-abbrev">J Oral Maxillofac Res</journal-id>
<journal-id journal-id-type="publisher-id">JORM</journal-id>
<journal-title-group><journal-title>Journal of Oral & Maxillofacial Research</journal-title>
</journal-title-group>
<issn pub-type="epub">2029-283X</issn>
<publisher><publisher-name>Stilus Optimus</publisher-name>
<publisher-loc>Kaunas, Lithuania</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24421999</article-id>
<article-id pub-id-type="pmc">3886081</article-id>
<article-id pub-id-type="publisher-id">v2n4e2ht</article-id>
<article-id pub-id-type="doi">10.5037/jomr.2011.2402</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Paper</subject>
</subj-group>
</article-categories>
<title-group><article-title>Peri-Implant Tissue Findings in Bone Grafted Oral Cancer Patients Compared to non Bone Grafted Patients without Oral Cancer</article-title>
</title-group>
<contrib-group><contrib id="contrib1" contrib-type="author" corresp="yes"><name><surname>Wolff</surname>
<given-names>Jan</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib id="contrib2" contrib-type="author"><name><surname>Agata</surname>
<given-names>Hideki</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib id="contrib3" contrib-type="author"><name><surname>Sándor</surname>
<given-names>George K.</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib id="contrib4" contrib-type="author"><name><surname>Haimi</surname>
<given-names>Suvi</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
</contrib-group>
<aff id="aff1" rid="aff1"><sup>1</sup>
<institution>Oral and Maxillofacial Unit, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</aff>
<aff id="aff2" rid="aff2"><sup>2</sup>
<institution>Division of Molecular Therapy, Advanced Clinical Research Center, The Institute of Medical Science, The University of Tokyo</institution>
<addr-line>Tokyo</addr-line>
<country>Japan.</country>
</aff>
<aff id="aff3" rid="aff3"><sup>3</sup>
<institution>Department of Oral and Maxillofacial Surgery, University of Oulu</institution>
<addr-line>Oulu</addr-line>
<country>Finland.</country>
</aff>
<aff id="aff4" rid="aff4"><sup>4</sup>
<institution>Regea–Institute for Regenerative Medicine, University of Tampere</institution>
<addr-line>Tampere</addr-line>
<country>Finland.</country>
</aff>
<author-notes><corresp>Jan Wolff,
<institution>Oral and Maxillofacial Unit, University of Tampere</institution>
<addr-line>P.O. Box 2000, FI-33521 Tampere</addr-line>
<country>Finland</country>
<phone>+358405571199</phone>
Fax: +358335518498<email>jan.wolff@regea.fi</email>
</corresp>
</author-notes>
<pub-date pub-type="collection"><season>Oct-Dec</season>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>1</day>
<month>1</month>
<year>2012</year>
</pub-date>
<volume>2</volume>
<issue>4</issue>
<elocation-id>e2</elocation-id>
<history><date date-type="received"><day>1</day>
<month>6</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>23</day>
<month>8</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement> Copyright © Wolff J, Agata H, Sándor GK, Haimi S.
Published in the JOURNAL OF ORAL &
MAXILLOFACIAL RESEARCH (http://www.ejomr.org), 1 January 2012.</copyright-statement>
<copyright-year>2011</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><license-p>This is an open-access article, first published in the JOURNAL OF
ORAL & MAXILLOFACIAL RESEARCH, distributed under the terms of the
Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 Unported
License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/">http://creativecommons.org/licenses/by-nc-nd/3.0/</ext-link>
), which permits unrestricted non-commercial use, distribution, and
reproduction in any medium, provided the original work and is properly
cited. The copyright, license information and link to the original
publication on <ext-link ext-link-type="uri" xlink:href="http://www.ejomr.org">http://www.ejomr.org</ext-link>
must be included.</license-p>
</license>
</permissions>
<self-uri xlink:type="simple" xlink:href="http://www.ejomr.org/JOMR/archives/2011/4/e2/v2n4e2ht.htm"></self-uri>
<abstract><title>ABSTRACT</title>
<sec sec-type="objectives"><title>Objectives</title>
<p>The aim of this study was to compare microbiological, histological, and
mechanical findings from tissues around osseointergrated dental implants in
patients who had undergone tumour resection and subsequent bone grafting
with non bone grafted patients without a history of oral cancer and to
develop an effective tool for the monitoring of the peri-implant tissues. A
third aim was to assess and compare the masticatory function of the two
patient groups after reconstruction with dental implants.</p>
</sec>
<sec sec-type="material and methods"><title>Material and Methods</title>
<p>A total of 20 patients were divided into 2 groups. The first group was
edentulous and treated with dental implants without the need for bone
grafting. The second edentulous group, with a history of oral cancer
involving the mandible, received onlay bone grafts with concurrent placement
of dental implants. Microbiological, histological, mechanical and
biochemical assessment methods, crevicular fluid flow rate, hygiene-index,
implant mobility, and the masticatory function were analysed and compared in
both patient groups.</p>
</sec>
<sec sec-type="results"><title>Results</title>
<p>The microbiological examinations showed no evidence of the three most common
pathogenic bacteria: <italic>Porphyromonas gingivalis</italic>
, <italic>Prevotella intermedius</italic>
,
<italic>Actinobacillus actinomycetencomitans</italic>
. A causal relationship between specific
microbes and peri-implant inflammation could not be found. All biopsies in
both patient groups revealed early signs of soft tissue peri-implant
inflammation.</p>
</sec>
<sec sec-type="conclusions"><title>Conclusions</title>
<p>The crevicular fluid volume and grade of gingival inflammation around the
dental implants were related. Peri-implant tissue findings were similar in
the two patient groups despite the history of oral cancer and the need for
bone grafting at the time of dental implant placement.</p>
</sec>
</abstract>
<kwd-group><kwd>caugment bone graft</kwd>
<kwd>cancer of the jaw</kwd>
<kwd>osseointegrated dental implantation</kwd>
<kwd>mastication</kwd>
<kwd>continuity of patient care</kwd>
<kwd>patient monitoring.</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec><title>INTRODUCTION</title>
<p>Maxillofacial procedures which restore form and function may result in a host of
problems that can affect the quality of life of patients. The focus on patient care
has shifted towards preservation of form and function with the careful selection of
appropriate reconstruction techniques [<xref ref-type="bibr" rid="B1">1</xref>
].
Oral implant treatment aims to restore the masticatory and speech function in
patients suffering from atrophic jaws or who have undergone tumour resection and
subsequent bone grafting with the intention of providing a better quality of
life.</p>
<p>The monitoring of dental implant health following tumour surgery may be valuable for
such patients. Although oral implants have enjoyed high clinical success rates over
the years, complications and failures due to peri-implant diseases remain a
challenge [<xref ref-type="bibr" rid="B2">2</xref>
]. It is, therefore, important to
identify patients who are at increased risk of developing peri-implantitis at an
early stage. Anatomical alterations following tumour resection may make it more
difficult for some cancer patients to keep their implant hardware clean [<xref ref-type="bibr" rid="B3">3</xref>
]. In many cases, initial plaque development
around dental implants starts in inaccessible spaces that cannot be properly cleaned
by patients. Preventive regimens are simple methods to stop the transition from
healthy to diseased implants. At the present time, the monitoring of dental implants
is based on an individual recall-system [<xref ref-type="bibr" rid="B4">4</xref>
].
To date, no general guidelines exist for oral implant care following oral cancer
treatment. Cross-sectional and longitudinal studies report the prevalence of
peri-implantitis in healthy patients as varying between 28% and 56% [<xref ref-type="bibr" rid="B5">5</xref>
]. Since clinical signs of peri-implantitis may
not always be obvious, it is of importantance to develop an efficient method of
monitoring dental implants especially in tumour patients who have undergone
reconstructive surgery.</p>
<p>The main objective of this study was to compare the soft tissue findings and
treatment outcomes regarding masticatory function in two groups of edentulous
patients: those patients with a history of oral cancer treated with dental implants
and concurrent bone grafting versus patients with no history of oral cancer and who
did not require bone grafting at the time of implant placement. A further objective
of this study was to compare different microbiological, histological, mechanical and
biochemical assessment methods for implant monitoring in order to develop oral care
monitoring tools for patients who have undergone reconstructive surgery and
treatment with dental implants.</p>
</sec>
<sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title>
<p><bold>Study design</bold>
</p>
<p>This study was conducted in accordance with the Ethical Committee of Hanover
University, Hanover, Germany in compliance with the Helsinki Declaration. Ten
edentulous adult patients (6 males and 4 females), treated with osseointergrated
implants, were enrolled in the study. The second group of patients consisted of 10
patients (7 males and 3 females) that had undergone ablative surgery due to
early-stage oral squamous cell cancer followed by reconstruction of the left
mandible in a two stage operative procedure. The second procedure included the use
of autogenous bone blocks and particulate bone from the anterior or posterior iliac
crest and the simultaneous placement of Brånemark dental implants. The average age
was 54.3 years with a range of 42 and 67 years. Brånemark implants of 10 to 13 mm in
length with a diameter of 3.75 mm were used. All implants had been in situ for at
least 13 and up to 69 months for an average of 27.8 months and had been loaded with
a full-arch metal-resin framework. No patients with a history of radiation therapy
were included in this study. None of the patients in either group had any major
systemic or metabolic illnesses. All patients in both groups had stopped smoking for
at least 6 months before inclusion into this study. Prior to the study a total of 3
patients had been smokers, patient EJ (without a bone graft) and patients WT, DH
with a bone graft.</p>
<p><bold>Microbiological evaluation</bold>
</p>
<p>A total of forty probes were taken from the twenty patients. With each patient, two
different areas of the mouth flora (gingival area) were randomly analysed. Using a
sterile polyester fibre-tipped applicator (Falcon, manufactured for Becton Dickonson
Vacutainer systems, Franklin Lakes, New Jersey, USA), the first probe on the
vestibular aspect was taken 1 cm caudal to the implant shoulder. The swab was then
immediately immersed in a transport medium (Port-A-Cul<sup>®</sup>
Universal-System, Becton Dickonson GmbH, Heidelberg, Germany) to maintain the viability of the aerobic and
anaerobic microorganisms during transit.</p>
<p>The second probe was taken using a sterile 0.50 x 40 mm diameter blunt needle
(Sterican<sup>®</sup>
, Luer Lock, B. Braun, Melsungen, Germany) connected to a sterile 2 ml
syringe (Injekt, B. Braun, Melsungen, Germany). The needle was placed vestibularly
into the implant gingival junction with light pressure applied in order to reach the
base of the sulcus pocket. Using the syringe, crevicular fluid was aspirated. The
needle surface was then immediately wiped using a sterile swab. Then, the needle was
immediately placed into the transport medium.</p>
<p>The anaerobic and aerobic microorganisms were cultivated on selective and
non-selective agar plates for 48 hours in aerobic, microaerophilic, and anaerobic
environments. The cultured specimens were identified using the following
characteristics: micro-organism morphology, colony appearance, carbohydrate
fermentation, amino acid hydrolysis, pattern of fermentation products, and enzyme
profiles. The cultivation of microorganisms was evaluated separately based on the
guidelines laid down by the American society of Microbiology [<xref ref-type="bibr" rid="B6">6</xref>
], the Centre of disease control [<xref ref-type="bibr" rid="B7">7</xref>
], and Bergey's Manual of Systematic Bacteriology [<xref ref-type="bibr" rid="B8">8</xref>
].</p>
<p><bold>Histopathological evaluation</bold>
</p>
<p>A total of 20 (4 mm) V shaped gingival biopsies of the peri-implant tissue that was
connected to the implant were randomly obtained from both patient groups using a
sterile size eleven scalpel. All biopsies were taken from the buccal periodontal
tissue at the area 33 (16 biopsies), area 34 (3 biopsies) and area 35 (1 biopsy) so
as to minimise differences in tissue structure. The biopsies were obtained under
local anaesthesia. The local anaesthetic agent (Xylocain<sup>®</sup>
2% with 1:100.000
adrenaline, Astra Chemicals, Sweden) was injected into the vestibular mandibulary
sulcus at least 1 cm from the proposed biopsy site in order to minimize local
anaesthetic infiltration into the biopsy. The tissue was orientated in exactly the
same way for all patients and immediately immersed into a 10% formalin solution. One
or two sutures were used to achieve primary closure and all biopsy sites healed
without complications.</p>
<p>The biopsies were cut into 5 micrometre thick sections and stained with
Hematoxylin-Eosin. The sections were examined under a Leitz Laborlux 12 microscope
(Ernst Leitz GmbH, Wetzlar, Germany). The presence of inflammatory cell infiltrates
was then scored by using a modified scoring system, originally described by Tagge et
al. [<xref ref-type="bibr" rid="B9">9</xref>
] and later modified by Adell et al.
[<xref ref-type="bibr" rid="B10">10</xref>
] and Lekholm et al. [<xref ref-type="bibr" rid="B11">11</xref>
].</p>
<p>To score the material microscopically, criteria for no, normal, low, mild, moderate,
and severe degrees of gingival inflammation were established according to the
density of the inflammatory cells. The following modified system of scoring was
used:</p>
<list list-type="bullet"><list-item><p>0→ No inflammation.</p>
</list-item>
<list-item><p>1→ Normal gingiva: scattered areas of chronic inflammatory cells were
accepted as normal, if the cells occurred singly or in small bands.</p>
</list-item>
<list-item><p>2→ Low inflamed gingiva: an accumulation of chronic inflammatory cells
of small bands that were not continuous.</p>
</list-item>
<list-item><p>3→ Mildly inflamed gingiva: an accumulation of chronic inflammatory
cells that formed a thin, continuous band.</p>
</list-item>
<list-item><p>4→ Moderately inflamed gingiva: a dense infiltrate of chronic
inflammatory cells that replaced the gingival fibres.</p>
</list-item>
<list-item><p>5→ Severely inflamed gingiva: a generalized, dense accumulation of
chronic inflammatory cells that replaced most of the gingival fibres.</p>
</list-item>
</list>
<p><bold>Biochemical and mechanical evaluation</bold>
</p>
<p>The volume of crevicular fluid in the implant sulcus was measured using a
Periotron<sup>®</sup>
(Harco Electronics, Dental Products Division, Winnipeg, Canada).
Periopaper<sup>®</sup>
(Harco Electronics) was inserted into the implant sulcus for 10
seconds, and was then placed between the upper and lower counterparts of the
Periotron<sup>®</sup>
. The volume of crevicular fluid was measured as
Periotron<sup>®</sup>
units. The principle of the Periotron<sup>®</sup>
is to measure
the frequency circuit containing the condensor made from the two Periotron<sup>®</sup>
counterparts and the Periopaper<sup>®</sup>
.</p>
<p>The hygiene-index (HI) was determined by staining the bacterial deposits on the
implant with a colouring solution (MIRA 2-Tone<sup>®</sup>
, Disclosing Solution,
Lorvic Corporation, St. Louis, MO, U.S.A.). The blue stain aided the detection of
plaque. The presence of plaque was divided into four implant surfaces. The presence
or absence (yes/no-decision) on all four implant surfaces divided by the total
number of surfaces determined the index [<xref ref-type="bibr" rid="B15">15</xref>
].
A HI-value of 100 indicated an implant free of plaque; a HI-value of 0 indicated
plaque accumulation on all four surfaces of an implant.</p>
<p>Implant mobility was determined by using the Periotest<sup>®</sup>
M (Medizintechnik
Gulden, Germany) that detects the damping characteristics of the implant and the
peri-implant tissues as a whole. The range in Periotest<sup>®</sup>
M values shown by
clinically immobile oral implants depends on the damping characteristics of their
surrounding tissues with bone in successful implants and fibrous tissue
marsupialization in failed implants.</p>
<p><bold>Masticatory function</bold>
</p>
<p>Masticatory function was evaluated using a chewing gum test. This method is used as
an indicator of implant masticatory function [<xref ref-type="bibr" rid="B12">12</xref>
]. The chewing gum (Meiji Chewing-Gum Co., Aichi, Japan) contains two
bases (base A and B). Base A includes a lactone form (Phloxine), a food additive,
and Base B includes sodium bicarbonate. The phloxine additive develops a red colour
in alkaline conditions. To evaluate the masticatory function, both chewing gum
components were given to the patient. Patients were instructed to make fifty chewing
strokes at random (both the left and right sides of their oral cavity). Both chewing
gum bases were mixed together by the process of mastication and a change in the
colour of the chewing gum occurred.</p>
<p>The evaluation of the colour of the chewing gum was carried out immediately using the
Chroma-Meter<sup>®</sup>
CR 200 (Minolta Camera Co., Ltd., Osaka, Japan) that uses a
xenon lamp for colour analysis. This system evaluates the degree of colour of the
chewing gum. The chewing gum developed a different colour as a result of mixing
during mastication and, therefore, its light reflection value changed. The new
colours were evaluated by using the L*, a*, b* colour system. The L*, a*, b* system
is based on the recommendations of the Commission International de L` Eclairage
(C.I.E., 1976). The degree of colour change from grey (4.33 a*) to red (> 4.33
a*) gave an approximate analysis of the masticatory function. Grey indicated a low
and red a high masticatory function.</p>
<p><bold>Statistical analysis</bold>
</p>
<p>Statistical analysis was performed by using SPSS (SPSS Software, Chicago, Illinois,
USA). Nonparametric methods were used to evaluate statistical significances. The
groups were compared statistically using the Mann-Whitney U - Wilcoxon Rank Sum W
Test for the evaluation of significances and the T-Test for equality of means.
Spearman correlation coefficient was used for correlation analyses.</p>
</sec>
<sec sec-type="results"><title>RESULTS</title>
<p><bold>Microbiological evaluation</bold>
</p>
<p>Microbiological examination of the crevicular fluid in both patient groups showed no
evidence of <italic>Porphyromonas gingivalis</italic>
, <italic>Prevotella intermedius</italic>
,
<italic>Actinobacillus
actinomycetencomitans</italic>
that are all known to be associated with peri-implant disease
(<xref ref-type="fig" rid="fig3">Figure 3</xref>
). The assessment of the oral
mucosa flora proved to be normal, as only aerobic, micro-aerophillic, and anaerobic
species of the normal mouth flora could be isolated (<xref ref-type="fig" rid="fig1">Figure 1</xref>
).<italic> Staphylococcos aureus</italic>
, which is considered a normal resident
of the oral cavity, was present in the mouth flora of two patients.</p>
<fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Microbiological examination of the crevicular fluid showed no evidence of the
three most important pathogenic bacteria: <italic>Porphyromonas gingivalis</italic>
,
<italic>Prevotella intermedius</italic>
, <italic>Actinobacillus actinomycetencomitans</italic>
.</p>
</caption>
<graphic xlink:href="jomr-02-e2-g001"></graphic>
</fig>
<p>The following two micro-organisms were isolated from both patient groups:
<italic>Candida albicans</italic>
and <italic>Enterococcus</italic>
. Neither of these is usually associated with the
subgingival micro flora in healthy adults with periodontitis [<xref ref-type="bibr" rid="B13">13</xref>
]. </p>
<p>Histopathological evaluation</p>
<p>Histopathological findings showed that all patients had histologically evident
inflammation in the gingival area adjacent to the implant (Figures <xref ref-type="fig" rid="fig2A">2A</xref>
and <xref ref-type="fig" rid="fig2B">2B</xref>
). There was a clear pattern of proliferation and increased density of
mononuclear and polymorphonuclear cells in the sulcular epithelium around the
implants. Based on microscopic findings, six non-specific categories of inflammation
were identified using a modified inflammation score originally described by Tagge et
al. [<xref ref-type="bibr" rid="B9">9</xref>
]. The mean degree of the peri-implant
inflammation was 2.9 ranging from 1 to 5 with a standard deviation of 1.37.</p>
<fig id="fig2A" orientation="portrait" position="float"><label>Figure 2A</label>
<caption><p>Box-plot representing peri-implant inflammation: no significant difference
was found between the two patient groups (P > 0.05).</p>
</caption>
<graphic xlink:href="jomr-02-e2-g002A"></graphic>
</fig>
<fig id="fig2B" orientation="portrait" position="float"><label>Figure 2B</label>
<caption><p>The relationship between CFFR and inflammation score with 95% confidence
intervals. The amount of crevicular fluid flow is compared to the grade of
peri-implant inflammation.</p>
</caption>
<graphic xlink:href="jomr-02-e2-g002B"></graphic>
</fig>
<fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Graph showing masticatory function evaluation. The chewing-gum developed a
different colour during mastication and, therefore, a different light
reflection value. The degree of colour change from grey (4.33 a*) to red (>
4.33 a*) gave an approximate analysis of the masticatory function. Grey is
indicating a low and red a high masticatory function.</p>
</caption>
<graphic xlink:href="jomr-02-e2-g003"></graphic>
</fig>
<p><bold>Biochemical and mechanical evaluation</bold>
</p>
<p>The mean crevicular fluid flow rate (CFFR) for all patients was 26.0 (SD 12.26)
ranging from 4 to 45 (patients with a bone graft 24.1 [SD 15.06] and without a bone
graft 27.9 [SD 9.09]) (Table 1). According to Dietrich et al. [<xref ref-type="bibr" rid="B14">14</xref>
], CFFR mean values of 10 to 40 is a sign of slight gingival
inflammation and values less than 10 show no signs of gingival inflammation. Values
over 40 are considered as a sign of peri-implant tissue inflammation. In <xref ref-type="fig" rid="fig2B">Figure 2B</xref>
, the amount of crevicular fluid flow
is compared to the grade of peri-implant inflammation. <xref ref-type="fig" rid="fig2B">Figure 2B</xref>
demonstrates that a high peri-implant inflammation
is followed by an increase in the amount of crevicular fluid produced around the
peri-implant tissue. The correlation between crevicular fluid flow and peri-implant
inflammation was 0.68 (P = 0.029) in patients with a bone graft and 0.36 (P = 0.31)
in patients without a bone graft.</p>
<table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label>
<caption><p>Differences between pre- and postsurgical parameters for class II and III
patients</p>
</caption>
<table frame="hsides" rules="groups" width="850"><thead><tr><td rowspan="1" colspan="1"></td>
<td colspan="10" align="center" rowspan="1"><bold>Patients with a bone graft</bold>
</td>
<td align="center" rowspan="1" colspan="1"></td>
<td colspan="10" align="center" rowspan="1"><bold>Patients without a bone graft</bold>
</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1"><bold>Recall-values</bold>
</td>
<td align="center" rowspan="1" colspan="1"> L.G. </td>
<td align="center" rowspan="1" colspan="1"> D.H. </td>
<td align="center" rowspan="1" colspan="1"> K.K. </td>
<td align="center" rowspan="1" colspan="1"> I.G. </td>
<td align="center" rowspan="1" colspan="1"> I.F. </td>
<td align="center" rowspan="1" colspan="1"> I.H. </td>
<td align="center" rowspan="1" colspan="1"> G.H. </td>
<td align="center" rowspan="1" colspan="1"> C.A. </td>
<td align="center" rowspan="1" colspan="1"> H.M. </td>
<td align="center" rowspan="1" colspan="1"> H.N. </td>
<td align="center" rowspan="1" colspan="1"></td>
<td align="center" rowspan="1" colspan="1"> L.M. </td>
<td align="center" rowspan="1" colspan="1"> I.W. </td>
<td align="center" rowspan="1" colspan="1"> H.W. </td>
<td align="center" rowspan="1" colspan="1"> R.I. </td>
<td align="center" rowspan="1" colspan="1"> M.R. </td>
<td align="center" rowspan="1" colspan="1"> I.H. </td>
<td align="center" rowspan="1" colspan="1"> D.E. </td>
<td align="center" rowspan="1" colspan="1"> P.K. </td>
<td align="center" rowspan="1" colspan="1"> H.H. </td>
<td align="center" rowspan="1" colspan="1"> E.L. </td>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1"><bold>Hygiene-Index</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 50 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 75 </td>
<td align="center" rowspan="1" colspan="1"> 0 </td>
<td align="center" rowspan="1" colspan="1"> 0 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 75 </td>
<td align="center" rowspan="1" colspan="1"></td>
<td align="center" rowspan="1" colspan="1"> 50 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 100 </td>
<td align="center" rowspan="1" colspan="1"> 75 </td>
<td align="center" rowspan="1" colspan="1"> 75 </td>
<td align="center" rowspan="1" colspan="1"> 0 </td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Periotest<sup>®</sup>
</bold>
</td>
<td align="center" rowspan="1" colspan="1"> -1 </td>
<td align="center" rowspan="1" colspan="1"> -5 </td>
<td align="center" rowspan="1" colspan="1"> +3 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -5 </td>
<td align="center" rowspan="1" colspan="1"></td>
<td align="center" rowspan="1" colspan="1"> -1 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -4 </td>
<td align="center" rowspan="1" colspan="1"> -3 </td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Crevicular-Fluid-Flow</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 4 </td>
<td align="center" rowspan="1" colspan="1"> 27 </td>
<td align="center" rowspan="1" colspan="1"> 35 </td>
<td align="center" rowspan="1" colspan="1"> 7 </td>
<td align="center" rowspan="1" colspan="1"> 10 </td>
<td align="center" rowspan="1" colspan="1"> 10 </td>
<td align="center" rowspan="1" colspan="1"> 32 </td>
<td align="center" rowspan="1" colspan="1"> 41 </td>
<td align="center" rowspan="1" colspan="1"> 30 </td>
<td align="center" rowspan="1" colspan="1"> 45 </td>
<td align="center" rowspan="1" colspan="1"></td>
<td align="center" rowspan="1" colspan="1"> 20 </td>
<td align="center" rowspan="1" colspan="1"> 15 </td>
<td align="center" rowspan="1" colspan="1"> 35 </td>
<td align="center" rowspan="1" colspan="1"> 25 </td>
<td align="center" rowspan="1" colspan="1"> 45 </td>
<td align="center" rowspan="1" colspan="1"> 30 </td>
<td align="center" rowspan="1" colspan="1"> 33 </td>
<td align="center" rowspan="1" colspan="1"> 25 </td>
<td align="center" rowspan="1" colspan="1"> 18 </td>
<td align="center" rowspan="1" colspan="1"> 33 </td>
</tr>
</tbody>
</table>
</table-wrap>
<p>The mean HI was similar in both groups 80 (SD 32.91) ranging from 0 to 100 (<xref ref-type="table" rid="T1">Table 1</xref>
). The mean Periotest<sup>®</sup>
was
-3.05 (SD 1.76) with a range from -5 to 3 and separately for patients with a bone
graft -2.80 (SD 2.35) and for patients without a bone graft -3.30 (SD 0.30) (Table
1). According to Teerlink et al. [<xref ref-type="bibr" rid="B14">14</xref>
] and
Chavez et al. [<xref ref-type="bibr" rid="B15">15</xref>
], these values suggest that
all implants were clinically firm.</p>
<p><bold>Masticatory function</bold>
</p>
<p>The masticatory function test provided a functional analysis of the implants and
their superstructures (<xref ref-type="fig" rid="fig2A">Figure 2</xref>
). The mean
chewing-gum value for all patients was 21.76 (SD 10.64) a* ranging from 6.07 a* to
37.79 (patients with a bone graft 21.47 [SD 9.82] and for patients without a bone
graft 21.96 [SD 10.64]) (<xref ref-type="fig" rid="fig2A">Figure 2</xref>
).</p>
<p>In a pilot study performed by Matsui et al. [<xref ref-type="bibr" rid="B12">12</xref>
] on German patients, the following mean-values were described: 28.76
a* (SD 1.76) for fully dentate patients and 10.05 a* (SD 2.58) for patients with a
full denture. </p>
<p>The masticatory function was compared to the grade of peri-implant inflammation, and
no significant correlation was observed. For patients with or without a bone graft
the correlation values (rs) were respectively -0.53 (P = 0.28) and 0.11 (P = 0.78).
One patient had a lower chewing-function value than the mean value for patients with
full dentures. In contrast, three patients achieved chewing-values of fully dentate
patients. All other patients in the study had a satisfactory chewing function. </p>
<p>Similarly the masticatory function was compared to the Periotest values and no
significant correlation was observed. For patients with or without a bone graft the
correlation values (rs) were respectively 0.70 (P = 0.13) and 0.11 (P = 0.78).</p>
</sec>
<sec sec-type="discussion"><title>DISCUSSION</title>
<p>Both patient groups showed similar microbiological and histological findings that
indicated an early form of peri-implantitis. Microbiota associated with peri-implant
disease have often been reported to be similar to the microbiota associated with
periodontitis such as <italic>P. gingivalis</italic>
, <italic>P. intermedia</italic>
and
<italic>A. actinomycetencomitans</italic>
[<xref ref-type="bibr" rid="B17">17</xref>
,<xref ref-type="bibr" rid="B18">18</xref>
,<xref ref-type="bibr" rid="B19">19</xref>
]. </p>
<p>Surprisingly, none of the above-mentioned bacteria could be isolated. One explanation
why the microflora around the implants of our patients could be different is due to
the fact that they were all edentulous. The bacteria colonizing our patients
originated primarily from the surfaces of adjacent soft tissues in comparison to
partially edentulous patients, whose dental microflora could have originated from
the adjacent dentition. This consequently leads to new questions regarding possible
differences in the microbial environment of edentulous and non edentulous patients.
One interesting finding was the high presence of <italic>Staphylocaccus aureus</italic>
in 60% of the
non-grafted and 50% of the grafted patients this has also been reported by Renvert
et al. [<xref ref-type="bibr" rid="B17">17</xref>
]. The cause affect relationship in
our patients with higher peri-implant inflammation could be due to hygienic neglect.
However, a causal relationship between specific microbes and peri-implant
inflammation could not be found. All biopsies displayed different amounts of
lymphocytes, plasma cells, and granulocytes subjacent to the peri-implant
epithelium. The peri-implant inflammation could be due to plaque-associated
micro-organisms that had accumulated around the peri-implant sulcus. When the
peri-implant inflammatory exudates were collected by using Periopaper<sup>®</sup>
, it was not
surprising to detect different levels of CFFR values. This could be due to the
different number of protein fragments in the inflammatory exudates, depending on the
degree of peri-implant inflammation. This corresponds to the results in the
literature that show a direct relationship between CFFR values and the degree of
peri-implant inflammation. </p>
<p>The comparison between the inflammation score and the masticatory function (see
results) show, that there is a slight tendency in patients with a bone graft to
develop lower masticatory functions when the peri-implant inflammation score is
high. This result cannot be seen in patients without a bone graft. Furthermore a
comparison between the masticatory function and the Periotest<sup>®</sup>
values in
both patient groups demonstrate that low Periotest<sup>®</sup>
values (-5→high;
0→low) affect the masticatory function negatively. </p>
<p>The differences in the masticatory functions of the cancer patient group could be the
result of change in the bone configuration hence bony structure after tumour
surgery. Differences in the cancellous bone structure muscle strength and the
elasticity of the jaw subsequently cause a different mechanical environment. Other
factors, e.g., mechanical trauma from sharp exposed marginal fixtures threads
against the mucosa may have also contributed to the development of lower masticatory
values.</p>
</sec>
<sec sec-type="conclusions"><title>CONCLUSIONS</title>
<p>The microbiological species profile was almost identical in both
patient groups. The microbiological examinations showed no evidence of the three
most common pathogenic bacteria: <italic>Porphyromonas gingivalis</italic>
,
<italic>Prevotella intermedius</italic>
,
<italic>Actinobacillus actinomycetencomitans</italic>
. It was not possible from the results of this
study to claim proof for a direct cause and effect relationship between specific
microorganisms and the tissue inflammation around the implants.All biopsies in both
patient groups revealed early signs of soft tissue peri-implant inflammation. The
crevicular fluid volume and grade of gingival inflammation around the dental
implants were related.The only difference between the two patient groups was the
slightly worse masticatory function in the oral cancer patients that had undergone
reconstructive surgery, however this study shows that patients that have undergone
reconstructive surgery can be successfully rehabilitated by means of bone grafts and
dental implants resulting in improvements in eating ability and quality of life.
Implant monitoring and oral care is of the utmost importance for patients who have
undergone reconstructive surgery.</p>
</sec>
</body>
<back><ack><sec sec-type="acknowledgments and disclosure statements"><title>ACKNOWLEDGMENTS AND DISCLOSURE STATEMENTS</title>
<p>This work was carried out in the Department of Oral and Maxillofacial Surgery,
Hanover University (M.H.H.), Germany. During these studies, many colleagues
collaborated and we hold them in high regard. We wish to extend our warmest
thanks to all those in the Department of Oral and Maxillofacial Surgery and the
other Departments with whom we worked closely.</p>
<p>Special thanks to Mika Helminen for his statistical advice.</p>
<p>The authors declare that they have no conflict of interest.</p>
</sec>
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