Antimicrobial resistance of aerobes and facultative anaerobes isolated from the oral cavity
Identifieur interne : 000601 ( Pmc/Corpus ); précédent : 000600; suivant : 000602Antimicrobial resistance of aerobes and facultative anaerobes isolated from the oral cavity
Auteurs : Ellen Cristina Gaetti-Jardim ; Antônio Carlos Marqueti ; Leonardo Perez Faverani ; Elerson Gaetti-Jardim JúniorSource :
- Journal of Applied Oral Science [ 1678-7757 ] ; 2010.
Abstract
This study evaluated the resistance to antimicrobials of aerobes and facultative anaerobes isolated from patients wearing complete dentures, patients with gingivitis and periodontitis, and periodontally health subjects.
Three hundred and four isolates were tested. The minimal inhibitory concentrations of the drugs were evaluated through the agar dilution method using Mueller-Hinton agar.
The most active antimicrobial drugs were the carbapenems (meropenem and imipenem),
and resistance to these drugs was restrict to 1.6-2.3% of the isolates, as well as
ciprofloxacin and rifampin. Microbial resistance to ampicillin,
amoxicillin/clavulanic acid, cefoxitin, cephalothin, amikacin, chloramphenicol and
nalidixic acid was particularly high. In most cases, the resistance to β-lactams
was mediated by the production of hydrolytic enzymes, especially in gram-negative
enteric rods, while
The results of this investigation confirmed that the oral cavity of patients with periodontitis and gingivitis, and particularly edentulous patients wearing complete dentures, could harbor microorganisms with several antimicrobial resistance markers, and these microorganisms are frequently implicated in multiresistant, systemic, oral or nosocomial infections.
Url:
DOI: 10.1590/S1678-77572010000600004
PubMed: 21308284
PubMed Central: 3881752
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PMC:3881752Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Antimicrobial resistance of aerobes and facultative anaerobes isolated
from the oral cavity</title><author><name sortKey="Gaetti Jardim, Ellen Cristina" sort="Gaetti Jardim, Ellen Cristina" uniqKey="Gaetti Jardim E" first="Ellen Cristina" last="Gaetti-Jardim">Ellen Cristina Gaetti-Jardim</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Marqueti, Antonio Carlos" sort="Marqueti, Antonio Carlos" uniqKey="Marqueti A" first="Antônio Carlos" last="Marqueti">Antônio Carlos Marqueti</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Faverani, Leonardo Perez" sort="Faverani, Leonardo Perez" uniqKey="Faverani L" first="Leonardo Perez" last="Faverani">Leonardo Perez Faverani</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Gaetti Jardim Junior, Elerson" sort="Gaetti Jardim Junior, Elerson" uniqKey="Gaetti Jardim Junior E" first="Elerson" last="Gaetti-Jardim Júnior">Elerson Gaetti-Jardim Júnior</name><affiliation><nlm:aff id="aff02"> DDS, MSc, PhD, Associate Professor of Microbiology, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">21308284</idno><idno type="pmc">3881752</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3881752</idno><idno type="RBID">PMC:3881752</idno><idno type="doi">10.1590/S1678-77572010000600004</idno><date when="2010">2010</date><idno type="wicri:Area/Pmc/Corpus">000601</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000601</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Antimicrobial resistance of aerobes and facultative anaerobes isolated
from the oral cavity</title><author><name sortKey="Gaetti Jardim, Ellen Cristina" sort="Gaetti Jardim, Ellen Cristina" uniqKey="Gaetti Jardim E" first="Ellen Cristina" last="Gaetti-Jardim">Ellen Cristina Gaetti-Jardim</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Marqueti, Antonio Carlos" sort="Marqueti, Antonio Carlos" uniqKey="Marqueti A" first="Antônio Carlos" last="Marqueti">Antônio Carlos Marqueti</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Faverani, Leonardo Perez" sort="Faverani, Leonardo Perez" uniqKey="Faverani L" first="Leonardo Perez" last="Faverani">Leonardo Perez Faverani</name><affiliation><nlm:aff id="aff01"> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</nlm:aff></affiliation></author><author><name sortKey="Gaetti Jardim Junior, Elerson" sort="Gaetti Jardim Junior, Elerson" uniqKey="Gaetti Jardim Junior E" first="Elerson" last="Gaetti-Jardim Júnior">Elerson Gaetti-Jardim Júnior</name><affiliation><nlm:aff id="aff02"> DDS, MSc, PhD, Associate Professor of Microbiology, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</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="2010">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Objectives</title><p>This study evaluated the resistance to antimicrobials of aerobes and facultative
anaerobes isolated from patients wearing complete dentures, patients with
gingivitis and periodontitis, and periodontally health subjects. </p></sec><sec><title>Material and methods</title><p>Three hundred and four isolates were tested. The minimal inhibitory concentrations
of the drugs were evaluated through the agar dilution method using Mueller-Hinton
agar. </p></sec><sec><title>Results</title><p>The most active antimicrobial drugs were the carbapenems (meropenem and imipenem),
and resistance to these drugs was restrict to 1.6-2.3% of the isolates, as well as
ciprofloxacin and rifampin. Microbial resistance to ampicillin,
amoxicillin/clavulanic acid, cefoxitin, cephalothin, amikacin, chloramphenicol and
nalidixic acid was particularly high. In most cases, the resistance to β-lactams
was mediated by the production of hydrolytic enzymes, especially in gram-negative
enteric rods, while <italic>enterococci</italic> did not evidence production of
these enzymes. The association amoxicillin/clavulanic acid was not effective in
28.3% of the tested isolates. </p></sec><sec><title>Conclusions</title><p>The results of this investigation confirmed that the oral cavity of patients with
periodontitis and gingivitis, and particularly edentulous patients wearing
complete dentures, could harbor microorganisms with several antimicrobial
resistance markers, and these microorganisms are frequently implicated in
multiresistant, systemic, oral or nosocomial infections.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Barbosa, Fcb" uniqKey="Barbosa F">FCB Barbosa</name></author><author><name sortKey="Mayer, Mpa" uniqKey="Mayer M">MPA Mayer</name></author><author><name sortKey="Saba Chujfi, E" uniqKey="Saba Chujfi E">E Saba-Chujfi</name></author><author><name sortKey="Cai, S" uniqKey="Cai S">S Cai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baudry, Pj" uniqKey="Baudry P">PJ Baudry</name></author><author><name sortKey="Nichol, K" uniqKey="Nichol K">K Nichol</name></author><author><name sortKey="Decorby, M" uniqKey="Decorby M">M DeCorby</name></author><author><name sortKey="Mataseje, L" uniqKey="Mataseje L">L Mataseje</name></author><author><name sortKey="Mulvey, Mr" uniqKey="Mulvey M">MR Mulvey</name></author><author><name sortKey="Hoban, Dj" uniqKey="Hoban D">DJ 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<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">21308284</article-id><article-id pub-id-type="pmc">3881752</article-id><article-id pub-id-type="doi">10.1590/S1678-77572010000600004</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Articles</subject></subj-group></article-categories><title-group><article-title>Antimicrobial resistance of aerobes and facultative anaerobes isolated
from the oral cavity</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>GAETTI-JARDIM</surname><given-names>Ellen Cristina</given-names></name><xref ref-type="aff" rid="aff01">1</xref></contrib><contrib contrib-type="author"><name><surname>MARQUETI</surname><given-names>Antônio Carlos</given-names></name><xref ref-type="aff" rid="aff01">1</xref></contrib><contrib contrib-type="author"><name><surname>FAVERANI</surname><given-names>Leonardo Perez</given-names></name><xref ref-type="aff" rid="aff01">1</xref></contrib><contrib contrib-type="author"><name><surname>GAETTI-JARDIM JÚNIOR</surname><given-names>Elerson</given-names></name><xref ref-type="aff" rid="aff02">2</xref><xref ref-type="corresp" rid="c01"></xref></contrib></contrib-group><aff id="aff01"><label>1</label> MSc, Graduate student, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</aff><aff id="aff02"><label>2</label> DDS, MSc, PhD, Associate Professor of Microbiology, Department of Pathology and Propedeutics, Araçatuba Dental School, UNESP, Araçatuba, SP, Brazil.</aff><author-notes><corresp id="c01"><bold>Corresponding address:</bold> Dr. Elerson Gaetti Jardim Júnior - Faculdade de
Odontologia de Araçatuba-UNESP - Rua José Bonifácio, 1193 - 16015-050 -Araçatuba, SP
- Brasil - Phone/Fax: +55-18-3636-2797/3636-3200 - e-mail:
<email>egaettij@foa.unesp.br</email></corresp></author-notes><pub-date pub-type="ppub"><season>Nov-Dec</season><year>2010</year></pub-date><volume>18</volume><issue>6</issue><fpage>551</fpage><lpage>559</lpage><history><date date-type="received"><day>13</day><month>3</month><year>2009</year></date><date date-type="rev-recd"><day>25</day><month>3</month><year>2010</year></date><date date-type="accepted"><day>30</day><month>5</month><year>2010</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 License, which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly
cited.</license-p></license></permissions><abstract><sec><title>Objectives</title><p>This study evaluated the resistance to antimicrobials of aerobes and facultative
anaerobes isolated from patients wearing complete dentures, patients with
gingivitis and periodontitis, and periodontally health subjects. </p></sec><sec><title>Material and methods</title><p>Three hundred and four isolates were tested. The minimal inhibitory concentrations
of the drugs were evaluated through the agar dilution method using Mueller-Hinton
agar. </p></sec><sec><title>Results</title><p>The most active antimicrobial drugs were the carbapenems (meropenem and imipenem),
and resistance to these drugs was restrict to 1.6-2.3% of the isolates, as well as
ciprofloxacin and rifampin. Microbial resistance to ampicillin,
amoxicillin/clavulanic acid, cefoxitin, cephalothin, amikacin, chloramphenicol and
nalidixic acid was particularly high. In most cases, the resistance to β-lactams
was mediated by the production of hydrolytic enzymes, especially in gram-negative
enteric rods, while <italic>enterococci</italic> did not evidence production of
these enzymes. The association amoxicillin/clavulanic acid was not effective in
28.3% of the tested isolates. </p></sec><sec><title>Conclusions</title><p>The results of this investigation confirmed that the oral cavity of patients with
periodontitis and gingivitis, and particularly edentulous patients wearing
complete dentures, could harbor microorganisms with several antimicrobial
resistance markers, and these microorganisms are frequently implicated in
multiresistant, systemic, oral or nosocomial infections.</p></sec></abstract><kwd-group><kwd>Periodontitis</kwd><kwd>Gingivitis</kwd><kwd>Bacteria</kwd><kwd>Anti-bacterial agents</kwd></kwd-group><funding-group><award-group><funding-source>The State of São Paulo Research Foundation</funding-source><award-id>#1998/6555-2</award-id><award-id>2007/54851-0</award-id></award-group></funding-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>Oral cavity may act as a reservoir for superinfecting microorganisms commonly associated
to systemic and opportunistic infections<sup><xref ref-type="bibr" rid="r12">12</xref></sup> especially in elderly wearing complete dentures<sup><xref ref-type="bibr" rid="r05">5</xref></sup>. In addition, either use or misuse of
antimicrobial drugs associated with poor oral hygiene would facilitate the colonization
of the oral cavity by these microorganisms, as well as the dissemination of their
resistance genes amongst the members of oral microbiota<sup><xref ref-type="bibr" rid="r10">10</xref>,<xref ref-type="bibr" rid="r12">12</xref></sup>.</p><p>The use of complete dentures<sup><xref ref-type="bibr" rid="r05">5</xref></sup> or the
development of periodontitis<sup><xref ref-type="bibr" rid="r01">1</xref>,<xref ref-type="bibr" rid="r10">10</xref></sup> may create suitable nutritional
conditions for superinfecting pathogens, such as Gram-negative enteric rods,
pseudomonads, and enterococci, which may be commonly associated with refractory oral and
nosocomial infections. Moreover, the loss of the balance between the host's immune
response and the microbiota's virulence has resulted in several oral infections, such as
denture stomatitis and Endodontic, periodontal or periapical infections.</p><p>However, in case of history of previous use of antimicrobials or immune suppression, the
clinician may suspect of the participation of facultative anaerobes and aerobes in the
infectious process. These microorganisms have presented a very diverse antimicrobial
susceptibility profile in comparison to strict anaerobes4. In addition, in spite of the
role that facultative anaerobes and aerobes would play in head and neck infections, most
of dentists have been instructed to prescribe antimicrobial drugs only directed against
strict anaerobes<sup><xref ref-type="bibr" rid="r04">4</xref></sup>.</p><p>Although local and surgical procedures have remained the basis of odontogenic infections
treatment, antimicrobial drugs may act as adjuvants in this therapeutic, especially in
anatomical sites where surgical procedures could not be performed. However, the
determination of resistance patterns to antimicrobial drugs of oral microorganisms has
not constituted a routine procedure<sup><xref ref-type="bibr" rid="r09">9</xref></sup>.</p><p>This study evaluated the frequency of antimicrobial resistance among isolates of aerobic
and facultative anaerobic bacteria harvested from the oral cavity of patients wearing
complete dentures, patients with gingivitis and chronic periodontitis, and periodontally
healthy subjects.</p></sec><sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title><sec><title>Study Population</title><p>A total of 250 patients (84 males and 166 females; mean age 43.03 years), followed up
within an 8-year period at the Araçatuba Dental School, UNESP, Brazil, from February,
1998 to March, 2008 were enrolled in this study. Forty-one patients wore complete
dentures, 89 exhibited gingivitis, 70 chronic periodontitis and 50 were periodontally
healthy, following the criteria described in the literature<sup><xref ref-type="bibr" rid="r23">23</xref></sup>. Demographic and additional characteristics of the
patients are presented in <xref ref-type="table" rid="t01">Table 1</xref>.</p><table-wrap id="t01" orientation="portrait" position="float"><label>Table 1</label><caption><p>Demographic and additional characteristics of the patients</p></caption><table frame="hsides" rules="groups"><thead><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>Characteristic</bold></td><td align="center" rowspan="1" colspan="1"><bold>Dentate</bold></td><td align="center" rowspan="1" colspan="1"><bold>Edentulous</bold></td></tr><tr><td rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"><bold>patients N (%)</bold></td><td align="center" rowspan="1" colspan="1"><bold>patients N (%)</bold></td></tr></thead><tbody><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Gender </bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Male (N=84)</td><td align="center" rowspan="1" colspan="1"> 65 (31.1)</td><td align="center" rowspan="1" colspan="1">19 (46.3)</td></tr><tr><td rowspan="1" colspan="1">Female (N=166)</td><td align="center" rowspan="1" colspan="1">144 (68.9)</td><td align="center" rowspan="1" colspan="1">22 (53.7)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>Education</bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Illiterate (N=27)</td><td align="center" rowspan="1" colspan="1">16 (7.7)</td><td align="center" rowspan="1" colspan="1">11 (26.8)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Elementary school (N=179)</td><td align="center" rowspan="1" colspan="1">149 (71.3)</td><td align="center" rowspan="1" colspan="1">30 (73.2)</td></tr><tr><td rowspan="1" colspan="1">High school (N=44)</td><td align="center" rowspan="1" colspan="1"> 44 (21.0)</td><td align="center" rowspan="1" colspan="1">0 (0.0)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>History of tobacco consumption</bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Yes<sup><xref ref-type="table-fn" rid="t01-fn01">1</xref></sup> (N=45)</td><td align="center" rowspan="1" colspan="1"> 82 (39.2)</td><td align="center" rowspan="1" colspan="1">15 (36.6)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">No (N=5)</td><td align="center" rowspan="1" colspan="1">127 (60.8)</td><td align="center" rowspan="1" colspan="1">26 (63.4)</td></tr><tr><td rowspan="1" colspan="1"><bold>History of alcohol consumption</bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Yes<sup><xref ref-type="table-fn" rid="t01-fn02">2</xref></sup> (N=75)</td><td align="center" rowspan="1" colspan="1"> 61 (29.2)</td><td align="center" rowspan="1" colspan="1">14 (34.1)</td></tr><tr><td rowspan="1" colspan="1">No (N=175)</td><td align="center" rowspan="1" colspan="1">148 (70.8)</td><td align="center" rowspan="1" colspan="1">27 (65.9)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>History of antimicrobial drugs use</bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Yes (N=15)</td><td align="center" rowspan="1" colspan="1">13 (6.2)</td><td align="center" rowspan="1" colspan="1">2 (4.9)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">No (N=235)</td><td align="center" rowspan="1" colspan="1">196 (93.7)</td><td align="center" rowspan="1" colspan="1">39 (95.1)</td></tr><tr><td rowspan="1" colspan="1"><bold>History of oral surgeries in the previous 5 years</bold></td><td align="center" rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"></td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Yes (N=29)</td><td align="center" rowspan="1" colspan="1"> 22 (10.5)</td><td align="center" rowspan="1" colspan="1"> 7 (17.1)</td></tr><tr><td rowspan="1" colspan="1">No (N=221)</td><td align="center" rowspan="1" colspan="1">187 (89.5)</td><td align="center" rowspan="1" colspan="1">34 (82.9)</td></tr></tbody></table><table-wrap-foot><fn id="t01-fn01"><label>1</label><p>At least 10 cigarettes per day over the last 5 years.</p></fn><fn id="t01-fn02"><label>2</label><p>At least two daily doses of cachaça, a distilled alcoholic beverage product of
distillation of fermented sugarcane juice with alcoholic contents of 38-48%
v/v.</p></fn></table-wrap-foot></table-wrap><p>Thirteen patients had received amoxicillin or ampicillin due to medical prescription
three months before sample collection, while two patients received azithromycin. Two
patients had used trimethoprim/ sulfamethoxazole for treatment of oral minor infections,
respiratory or urinary infections. Exclusion criteria included: diabetes, systemic
diseases and other chronic infections (except for periodontitis or gingivitis),
prosthetic heart valves, previous endocarditis, transplants, pregnant or lactating
women, and history of antimicrobial drug use within the period of three months before
sample collection. Since it is not possible to determine with accuracy of antimicrobial
drug use in individuals with history of self-medication, it was established that these
patients should be excluded from the study.</p><p>A written informed consent form approved by the Institutional Review Board of Araçatuba
Dental School, UNESP (Proc.27/2000 and 34/2006) was signed by all participants. After
sample collection, the dentate patients were referred to restorative and periodontal
treatment, while edentulous patients were directed to prosthetic dentistry.</p></sec><sec><title>Microorganisms</title><p>Clinical samples of resting saliva, oral mucosa, tongue, and both supragingival and
subgingival biofilm were collected from periodontally healthy subjects and patients with
gingivitis and periodontitis. Supragingival samples were obtained by scaling;
subgingival samples were obtained by using 3 sterile paper points (Dentsply Ind. Co.
Ltd., Petrópolis, RJ, Brazil), which were inserted into the apical region of periodontal
pockets or gingival crevices for 60 s. Oral mucosa samples were collected by a sterile
swab, while saliva was collected by using Salivette devices (Cortisol-Salivette,
Sarstedt AG & Co., Nümbrecht, Nordrhein-Westfalen, Germany). In the edentulous
patients wearing complete dentures, clinical samples from palate, dorsum of tongue, and
fornix were collected by using swabs<sup><xref ref-type="bibr" rid="r05">5</xref></sup>.
Clinical samples were transferred to a VMGA III medium<sup><xref ref-type="bibr" rid="r18">18</xref></sup>. The clinical samples of subgingival biofilm were pooled
before transportation.</p><p>Clinical specimens were inoculated in peptone water and ethyl violet azide broth (Difco
Laboratories, Detroit, MI, USA), and incubated both at room temperature and 37ºC, for
3-7 days. After that, from the bacterial growth observed in peptone water, aliquots of
0.1 ml were transferred to Eosin Methylene Blue agar, SS agar, MacConkey agar (Difco
Laboratories) and Brilliant Green agar. From the tubes containing EVA broth, 0.1 mL was
transferred to Bile Esculin agar (Difco Laboratories). Agar plates were incubated in
aerobiosis, at 37ºC, for 48 h<sup><xref ref-type="bibr" rid="r10">10</xref></sup>.</p><p>Clinical specimens were also diluted in VMG I<sup><xref ref-type="bibr" rid="r18">18</xref></sup> and plated on tryptic soy agar (TSA), supplemented with both 0.5%
yeast extract and 5% horse blood, and incubated in aerobiosis, at 37ºC, for 48 h, for
isolation of non-enteric aerobes and facultative anaerobes. The isolates were identified
by Gram staining, colony morphology on agar plates, respiratory test, catalase assay,
and biochemical identification kits (API Test System, BioMérieux, Marcelle l'Etoile,
Provence-Alpes-Côte d'Azur, France).</p><p>A total of 304 isolates were subjected to susceptibility tests, as follows:
<italic>Bukholderia cepacia</italic> complex (5 isolates), <italic>Citrobacter
freundii</italic> (7 isolates), <italic>Enterobacter cloacae</italic> (18 isolates),
<italic>E. intermedius</italic> (6 isolates), <italic>E. sakazakii</italic> (9
isolates), <italic>Enterococcus</italic> sp. (18 isolates), <italic>E. faecalis</italic>(31 isolates), <italic>E. faecium</italic> (8 isolates), <italic>Escherichia
coli</italic> (6 isolates), <italic>Klebsiella oxytoca</italic> (11 isolates),
<italic>K. pneumoniae</italic> (3 isolates), <italic>Morganella morganii</italic> (17
isolates), <italic>Pantoea agglomerans</italic> (7 isolates), <italic>Proteus
mirabilis</italic> (5 isolates), <italic>P. vulgaris</italic> (7 isolates),
<italic>Providencia alcalifaciens</italic> (6 isolates), <italic>Pseudomonas
aeruginosa</italic> (15 isolates), <italic>P. fluorescens</italic> (4 isolates),
<italic>Serratia</italic> sp. (9 isolates), <italic>S. liquefaciens</italic> (9
isolates), <italic>Staphylococcus</italic> sp. (9 isolates), <italic>S. aureus</italic>(10 isolates), <italic>S. epidermidis</italic> (17 isolates), <italic>S.
hominis</italic> (8 isolates), <italic>Streptococcus</italic> sp. (9 isolates),
<italic>S. oralis</italic> (7 isolates), <italic>S. sanguinis</italic> (9 isolates),
<italic>S. mitior</italic> (4 isolates), <italic>S. salivarius</italic> (11
isolates), <italic>S. mutans</italic> (7 isolates), <italic>S. pneumoniae</italic> (6
isolates), and <italic>S. pyogenes</italic> (6 isolates).</p></sec><sec><title>Antimicrobial Susceptibility Tests</title><p>All isolates were examined for susceptibility to antimicrobial agents by agar dilution
method<sup><xref ref-type="bibr" rid="r19">19</xref></sup>. When CLSI
antimicrobial breakpoints were not established, the breakpoints adopted by the British
Society for Antimicrobial Chemotherapy<sup><xref ref-type="bibr" rid="r03">3</xref></sup> were followed. Mueller-Hinton agar (MHA) was used for all isolates.
In tests involving oral <italic>streptococci</italic>, 5% horse blood was added to MHA
plates in order to support microbial growth.</p><p>Thus, five pure colonies of each bacterial strain were inoculated into 2 mL of sterile
Mueller Hinton broth or brain heart infusion broth supplemented with yeast extract (oral
<italic>streptococci</italic>) and incubated at 37ºC for 12-24 h. The turbidity was
adjusted to match a 0.5 McFarland turbidity standard. The bacterial inocula were
standardized in 10<sup><xref ref-type="bibr" rid="r05">5</xref></sup> cells<sup><xref ref-type="bibr" rid="r09">9</xref></sup> and transferred to Mueller-Hinton agar
plates containing the antimicrobial agent and control plates (without drugs), using a
Steer's replicator (Cefar Diagnostica Ltda, São Paulo, SP, Brazil). The test and control
agar plates were incubated aerobically or under CO<sub>2</sub> (10% CO<sub>2 </sub>+
conventional atmosphere, for oral <italic>streptococci</italic>) at 37ºC, for 48 h.</p><p>A total of 14 antibiotics or associations were tested. The antibiotics tested consisted
of the following drugs: amikacin, ampicillin, amoxicillin/clavulanic acid, cefoxitin,
cephalothin, chloramphenicol, ciprofloxacin, doxycycline, gentamicin, imepenem,
meropenem, nalidixic acid, rifampin, and tetracycline. Antimicrobials were tested in
twofold dilution series ranging from 0.06 to 256 µg/mL. After incubation, the organisms
were classified as sensitive or resistant, according to CLSI<sup><xref ref-type="bibr" rid="r19">19</xref></sup> and BSAC<sup><xref ref-type="bibr" rid="r03">3</xref></sup> guidelines. <italic>E. coli</italic> ATCC 25922, <italic>S.
aureus</italic> ATCC 29213, <italic>P. aeruginosa</italic> ATCC 27853, and <italic>E.
faecalis</italic> ATCC 29212 were used in the assays involving facultative
anaerobes.</p></sec><sec><title>Detection of β-lactamases</title><p>The isolates resistant to β-lactams were also tested for β-lactamase activity by both
chromogenic cephalosporin and biological method<sup><xref ref-type="bibr" rid="r09">9</xref></sup>. These two methods were performed because nitrocefinbased
β-lactamase assays have not proven useful in detecting β-lactamase production by some
microorganisms. In all tests, <italic>S. aureus</italic> ATCC 29213 was used as the
positive control of β-lactamase production.</p><p>The chromogenic cephalosporin β-lactamase assay using cefinase disks was performed
according to the manufacturer's instructions (Calbiochem, San Diego, California,
USA).This description was briefly the following: 6-mm-diameter filter paper disks
impregnated with nitrocefin were moistened with 0.85% NaCl, and several fragments of the
tested microorganisms' colonies were transferred to the disk. After 10-60 min, the disks
were examined regarding the appearance of a pink-red coloration, which has been
characteristic of the degradation of nitrocefin.</p><p>In the biological method, 20 µL of the resistant isolate cultures were plated on the
surface of Mueller-Hinton agar containing 0.5 µg/mL of the tested β-lactam to which the
tested microorganism showed to be resistant. These plates were then incubated in
aerobiosis at 37ºC, for 48 h. After this incubation period, the cultures were exposed to
chloroform fumes for 20 min. and then covered with 5 mL of semi-solid brain heart
infusion (BHI) agar (0.7% agar) previously inoculated with 10<sup><xref ref-type="bibr" rid="r06">6</xref></sup> cells of <italic>S. pyogenes</italic> FOA-94F14 sensitive
to all tested β-lactams in a concentration of ≤0.06 µg/mL. The Petri dishes were then
incubated under aerobiosis for 24 h at, 37ºC. After incubation, presence or absence of
streptococcal growth was checked. The presence of this growth halo was indicative of the
β-lactam degradation.</p></sec><sec><title>Statistical analysis</title><p>Differences between clinical parameters and the frequency of pathogen detection or
presence of microbial resistance for each subject were analyzed by the Chi-square,
Mann-Whitney or Fisher's exact test. Inter-relationships among different microorganisms
were evaluated using the Spearman's correlation coefficient test.</p></sec></sec><sec sec-type="results"><title>RESULTS</title><p>Significant levels of resistance were observed for all β-lactams, excepting for imepenem
and meropenem, which respectively presented 2.3% and 1.6% of resistance. The most
prominent resistance was observed for ampicillin, amoxicillin and cephalothin, which
respectively reached 44.4%, 43.1% and 33.2% (<xref ref-type="table" rid="t02">Table
2</xref>). Enteric gram-negative rods and pseudomonads were the most resistant
isolates. Out of 304 tested isolates, 178 were resistant to at least one β-lactam,
representing 58.6% of all tested microorganisms, and 112 resistant isolates were
β-lactamases producers, which represented 36.8% of all tested isolates and 62.9% of all
β-lactam resistant bacteria. These hydrolyzing enzymes seemed to be the major mechanism
of resistance to this class of antimicrobials, excepting for
<italic>enterococci</italic>, which did not produce such compounds.</p><table-wrap id="t02" orientation="portrait" position="float"><label>Table 2</label><caption><p>Resistance to β-lactams of aerobes and facultative anaerobes isolated from oral
cavity of patients wearing complete denture as well as gingivitis and
periodontitis patients</p></caption><table frame="hsides" rules="groups"><thead><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>Microorganisms (number of isolates)</bold></td><td colspan="7" align="center" rowspan="1"><bold> Resistance Prevalence (%) </bold></td><td align="center" rowspan="1" colspan="1"><bold>Production of β-lactamases (%)</bold></td></tr><tr><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><bold>AM</bold></td><td align="center" rowspan="1" colspan="1"><bold>AMX</bold></td><td align="center" rowspan="1" colspan="1"><bold>AMC</bold></td><td align="center" rowspan="1" colspan="1"><bold>CF</bold></td><td align="center" rowspan="1" colspan="1"><bold>CP</bold></td><td align="center" rowspan="1" colspan="1"><bold>IM</bold></td><td align="center" rowspan="1" colspan="1"><bold>ME</bold></td><td align="center" rowspan="1" colspan="1"></td></tr></thead><tbody><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"> </td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>B. cepacia</italic><sup><xref ref-type="table-fn" rid="t02-fn01">1</xref></sup> (5)</td><td align="center" rowspan="1" colspan="1">100.0</td><td align="center" rowspan="1" colspan="1">100.0</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">40.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>C. freundii</italic> (7)</td><td align="center" rowspan="1" colspan="1">57.1</td><td align="center" rowspan="1" colspan="1">57.1</td><td align="center" rowspan="1" colspan="1">28.5</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">42.9</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">57.1</td></tr><tr><td rowspan="1" colspan="1"><italic>E. cloacae</italic> (18)</td><td align="center" rowspan="1" colspan="1">77.8</td><td align="center" rowspan="1" colspan="1">77.8</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">61.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">72.2</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>E. intermedius</italic> (6)</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td></tr><tr><td rowspan="1" colspan="1"><italic>E. sakazakii</italic> (9)</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">100.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">44.4</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>Enterococcus sp.</italic> (18)</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">38.9</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr><td rowspan="1" colspan="1"><italic>E. faecalis</italic> (31)</td><td align="center" rowspan="1" colspan="1">19.4</td><td align="center" rowspan="1" colspan="1">19.4</td><td align="center" rowspan="1" colspan="1">19.4</td><td align="center" rowspan="1" colspan="1">19.4</td><td align="center" rowspan="1" colspan="1">38.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>E. faecium</italic> (8)</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">62.5</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">25.0</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr><td rowspan="1" colspan="1"><italic>E. coli</italic> (6)</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">66.7</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>K. oxytoca</italic> (11)</td><td align="center" rowspan="1" colspan="1">63.6</td><td align="center" rowspan="1" colspan="1">45.5</td><td align="center" rowspan="1" colspan="1">45.5</td><td align="center" rowspan="1" colspan="1">9.1</td><td align="center" rowspan="1" colspan="1">27.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">63.6</td></tr><tr><td rowspan="1" colspan="1"><italic>K. pneumoniae</italic> (3)</td><td align="center" rowspan="1" colspan="1">100.0</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">100.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>M. morganii</italic> (17)</td><td align="center" rowspan="1" colspan="1">70.6</td><td align="center" rowspan="1" colspan="1">70.6</td><td align="center" rowspan="1" colspan="1">29.4</td><td align="center" rowspan="1" colspan="1">23.5</td><td align="center" rowspan="1" colspan="1">52.9</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">70.6</td></tr><tr><td rowspan="1" colspan="1"><italic>P. agglomerans</italic> (7)</td><td align="center" rowspan="1" colspan="1">85.7</td><td align="center" rowspan="1" colspan="1">85.7</td><td align="center" rowspan="1" colspan="1">85.7</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">42.9</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">85.7</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. mirabilis</italic> (5)</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">80.0</td></tr><tr><td rowspan="1" colspan="1"><italic>P. vulgaris</italic> (7)</td><td align="center" rowspan="1" colspan="1">71.4</td><td align="center" rowspan="1" colspan="1">71.4</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">71.4</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. alcalifaciens</italic> (6)</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">66.7</td></tr><tr><td rowspan="1" colspan="1"><italic>P. aeruginosa</italic> (15)</td><td align="center" rowspan="1" colspan="1">86.7</td><td align="center" rowspan="1" colspan="1">86.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">13.3</td><td align="center" rowspan="1" colspan="1">13.3</td><td align="center" rowspan="1" colspan="1">40.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. fluorescens</italic> (4)</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">25.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">50.0</td></tr><tr><td rowspan="1" colspan="1"><italic>Serratia sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">77.8</td><td align="center" rowspan="1" colspan="1">77.8</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">55.6</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">77.8</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. liquefaciens</italic> (9)</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">66.7</td></tr><tr><td rowspan="1" colspan="1"><italic>Staphylococcus sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">66.7</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. aureus</italic> (10)</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">60.0</td></tr><tr><td rowspan="1" colspan="1"><italic>S. epidermidis</italic> (17)</td><td align="center" rowspan="1" colspan="1">23.5</td><td align="center" rowspan="1" colspan="1">23.5</td><td align="center" rowspan="1" colspan="1">11.8</td><td align="center" rowspan="1" colspan="1">23.5</td><td align="center" rowspan="1" colspan="1">29.4</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">35.3</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. hominis</italic> (8)</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">50.0</td><td align="center" rowspan="1" colspan="1">25.0</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">50.0</td></tr><tr><td rowspan="1" colspan="1"><italic>Streptococcus sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>Streptococcus<sup><xref ref-type="table-fn" rid="t02-fn02">2</xref></sup> spp.</italic> (50)</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr><td rowspan="1" colspan="1">Total (304)</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">43.1</td><td align="center" rowspan="1" colspan="1">28.3</td><td align="center" rowspan="1" colspan="1">22.7</td><td align="center" rowspan="1" colspan="1">33.2</td><td align="center" rowspan="1" colspan="1">2.3</td><td align="center" rowspan="1" colspan="1">1.6</td><td align="center" rowspan="1" colspan="1">36.8</td></tr></tbody></table><table-wrap-foot><fn><p>AM, ampicillin; AMX, amoxicillin; AMC, amoxicillin/clavulanic acid; CF,
cefoxitin; CP, cephalothin; IM, imepenem; ME, meropenem.</p></fn><fn id="t02-fn01"><label>1</label><p><italic>Burkholderia cepacia</italic> complex</p></fn><fn id="t02-fn02"><label>2</label><p><italic>Streptococcus</italic> species (N): <italic>S. oralis</italic> (7),
<italic>S. sanguinis</italic> (9), <italic>S. mitior</italic> (4),
<italic>S. salivarius</italic> (11), <italic>S. mutans</italic> (7),
<italic>S. pneumoniae</italic> (6), <italic>S. pyogenes</italic> (6).</p></fn></table-wrap-foot></table-wrap><p>The association amoxicillin/clavulanic acid was active on less than half of ampicillin
or amoxicillin resistant isolates. Resistance to this association was detected in 28.3%
of the targeted microorganisms and it was particularly frequent in <italic>E.
cloacae</italic>, genera <italic>Klebsiella, Serratia</italic> and<italic>Pseudomonas,</italic> as well as in <italic>B. cepacia</italic> complex, <italic>E.
faecium, P. agglomerans, P. alcalifaciens</italic> and <italic>S.
aureus</italic>.</p><p>In relation to cephalosporins, the resistance to both cefoxitin and cephalothin was
disseminated in all tested microbial genera, particularly in pseudomonads, <italic>E.
cloacae, staphylococci</italic>, and <italic>enterococci</italic>. Some isolates of
<italic>E. cloacae, K. oxytoca, P. agglomerans, P. alcalifaciens</italic> and
<italic>Serratia</italic> sp. presented a broad spectrum resistance to β-lactam
antibiotics, and produced β-lactamases that were active on penicillins and
cephalosporins. This would suggest that the oral cavity of dentate patients and,
particularly, edentulous patients wearing complete dentures could harbor bacterial
strains able to produce broad spectrum β-lactamases.</p><p>The results presented in <xref ref-type="table" rid="t02">Table 2</xref> show that
carbapenems were the only β-lactams that had a significant antimicrobial activity on
<italic>enterococci, staphylococci</italic>, pseudomonads and
<italic>Enterobacteriaceae</italic>. The resistance to imepenem was similar to that
observed to meropenem and restricted to a few isolates of <italic>staphylococci, P.
aeruginosa, E. faecium</italic> and <italic>M. morganii</italic>.</p><p>Variable levels of resistance to aminoglycosides were also observed. Resistance to
amikacin was more prevalent among gram-positive cocci of genera
<italic>Enterococcus,</italic> and <italic>Staphylococcus</italic>, while gentamicin
resistance was common in <italic>P. aeruginosa, P. alcalifaciens, C. freundii,</italic>and <italic>E. cloacae</italic> (<xref ref-type="table" rid="t02">Table 2</xref>).
Resistance to chloramphenicol, doxycycline, nalidixic acid and, specially, tetracycline
was frequent in most of the targeted microorganisms, while rifampin was effective
against most of these isolates, excepting for some gram-negative enteric rods,
<italic>staphylococci</italic>, and pseudomonads. The resistance to ciprofloxacin was
almost restricted to <italic>staphylococci</italic> and <italic>streptococci</italic>,
besides an isolate of <italic>E. intermedius</italic> and other isolate of <italic>P.
aeruginosa</italic> (<xref ref-type="table" rid="t03">Table 3</xref>).</p><table-wrap id="t03" orientation="portrait" position="float"><label>Table 3</label><caption><p>Susceptibility of the isolates to amikacin, chloramphenicol, ciprofloxacin,
doxycycline, gentamicin, nalidixic acid, rifampin, and tetracycline</p></caption><table frame="hsides" rules="groups"><thead><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>Microorganism (number of isolates)</bold></td><td colspan="8" align="center" rowspan="1"><bold>Resistance Prevalence (%) </bold></td></tr><tr><td rowspan="1" colspan="1"> </td><td align="center" rowspan="1" colspan="1"><bold>AK</bold></td><td align="center" rowspan="1" colspan="1"><bold>CHR</bold></td><td align="center" rowspan="1" colspan="1"><bold>CPR</bold></td><td align="center" rowspan="1" colspan="1"><bold>DC</bold></td><td align="center" rowspan="1" colspan="1"><bold>GE</bold></td><td align="center" rowspan="1" colspan="1"><bold>NA</bold></td><td align="center" rowspan="1" colspan="1"><bold>RF</bold></td><td align="center" rowspan="1" colspan="1"><bold>TE</bold></td></tr></thead><tbody><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"> </td><td colspan="8" align="center" rowspan="1"> </td></tr><tr><td rowspan="1" colspan="1"><italic>B. cepacia</italic><sup><xref ref-type="table-fn" rid="t03-fn01">1</xref></sup> (5)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">40.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>C. freundii</italic> (7)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">28.6</td></tr><tr><td rowspan="1" colspan="1"><italic>E. cloacae</italic> (18)</td><td align="center" rowspan="1" colspan="1">5.6</td><td align="center" rowspan="1" colspan="1">38.9</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">38.9</td><td align="center" rowspan="1" colspan="1">5.6</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">5.6</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>E. intermedius</italic> (6)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">16.7</td></tr><tr><td rowspan="1" colspan="1"><italic>E. sakazakii</italic> (9)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">11.1</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>Enterococcus sp.</italic> (18)</td><td align="center" rowspan="1" colspan="1">66.7</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">38.9</td></tr><tr><td rowspan="1" colspan="1"><italic>E. faecalis</italic> (31)</td><td align="center" rowspan="1" colspan="1"> 83.9</td><td align="center" rowspan="1" colspan="1">35.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">12.9</td><td align="center" rowspan="1" colspan="1">9.7</td><td align="center" rowspan="1" colspan="1">71.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">61.3</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>E. faecium</italic> (8)</td><td align="center" rowspan="1" colspan="1">87.5</td><td align="center" rowspan="1" colspan="1">62.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">25.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">37.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">37.5</td></tr><tr><td rowspan="1" colspan="1"><italic>E. coli</italic> (6)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">16.7</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">16.7</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>K. oxytoca</italic> (11)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">9.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">18.2</td><td align="center" rowspan="1" colspan="1">9.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr><td rowspan="1" colspan="1"><italic>K. pneumoniae</italic> (3)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>M. morganii</italic> (17)</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">29.4</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">11.8</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">41.2</td></tr><tr><td rowspan="1" colspan="1"><italic>P. agglomerans</italic> (7)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">28.5</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. mirabilis</italic> (5)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">60.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">40.0</td></tr><tr><td rowspan="1" colspan="1"><italic>P. vulgaris</italic> (7)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">28.6</td><td align="center" rowspan="1" colspan="1">14.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">14.3</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. alcalifaciens</italic> (6)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">83.3</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1"> 50.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">66.7</td></tr><tr><td rowspan="1" colspan="1"><italic>P. aeruginosa</italic> (15)</td><td align="center" rowspan="1" colspan="1">13.3</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">6.7</td><td align="center" rowspan="1" colspan="1">46.7</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">86.7</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">73.3</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>P. fluorescens</italic> (4)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">25.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">25.0</td></tr><tr><td rowspan="1" colspan="1"><italic>Serratia sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">55.6</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. liquefaciens</italic> (9)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">33.3</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">44.4</td><td align="center" rowspan="1" colspan="1">55.6</td></tr><tr><td rowspan="1" colspan="1"><italic>Staphylococcus sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">22.2</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. aureus</italic> (10)</td><td align="center" rowspan="1" colspan="1">30.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">40.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">10.0</td><td align="center" rowspan="1" colspan="1">20.0</td><td align="center" rowspan="1" colspan="1">10.0</td><td align="center" rowspan="1" colspan="1">60.0</td></tr><tr><td rowspan="1" colspan="1"><italic>S. epidermidis</italic> (17)</td><td align="center" rowspan="1" colspan="1">17.7</td><td align="center" rowspan="1" colspan="1">29.4</td><td align="center" rowspan="1" colspan="1">35.3</td><td align="center" rowspan="1" colspan="1">29.4</td><td align="center" rowspan="1" colspan="1">11.8</td><td align="center" rowspan="1" colspan="1">17.7</td><td align="center" rowspan="1" colspan="1">17.7</td><td align="center" rowspan="1" colspan="1">58.8</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>S. hominis</italic> (8)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">37.5</td><td align="center" rowspan="1" colspan="1">12.5</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">50.0</td></tr><tr><td rowspan="1" colspan="1"><italic>Streptococcus sp.</italic> (9)</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">0.0</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><italic>Streptococcus<sup><xref ref-type="table-fn" rid="t03-fn02">2</xref></sup> spp.</italic> (50)</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">8.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">4.0</td><td align="center" rowspan="1" colspan="1">0.0</td><td align="center" rowspan="1" colspan="1">12.0</td></tr><tr><td rowspan="1" colspan="1">Total (304)</td><td align="center" rowspan="1" colspan="1">19.4</td><td align="center" rowspan="1" colspan="1">24.0</td><td align="center" rowspan="1" colspan="1">6.6</td><td align="center" rowspan="1" colspan="1">15.5</td><td align="center" rowspan="1" colspan="1">8.6</td><td align="center" rowspan="1" colspan="1">21.1</td><td align="center" rowspan="1" colspan="1">5.6</td><td align="center" rowspan="1" colspan="1">33.2</td></tr></tbody></table><table-wrap-foot><fn><p>AK, amikacin; CHR, chloramphenicol; CPR, ciprofloxacin; DC, doxycycline; GE,
gentamicin; NA, nalidixic acid; RF, rifampin; TE, tetracycline.</p></fn><fn id="t03-fn01"><label>1</label><p><italic>Burkholderia cepacia</italic> complex</p></fn><fn id="t03-fn02"><label>2</label><p><italic>Streptococcus</italic> species (N): <italic>S. oralis</italic> (7),
<italic>S. sanguinis</italic> (9), <italic>S. mitior</italic> (4),
<italic>S. salivarius</italic> (11), <italic>S. mutans</italic> (7),
<italic>S. pneumoniae</italic> (6), <italic>S. pyogenes</italic> (6).</p></fn></table-wrap-foot></table-wrap><p>The main relationship between periodontal conditions and the presence of resistant
microorganisms was linked to higher prevalence of enteric Gram-negative in patients with
periodontitis or gingivitis, and these bacteria were less susceptible to antimicrobial
agents. Antimicrobial use in the period prior to sample collection, and consumption of
tobacco and alcohol did not significantly affect the occurrence of resistant
microorganisms. The results suggest that factors that increase the presence of enteric
bacteria in the oral cavity eventually collaborate with the increase in the prevalence
of resistant microorganisms. <xref ref-type="table" rid="t04">Table 4</xref> presents
the prevalence of resistant microorganisms in edentulous patients wearing complete
dentures, periodontally healthy subjects, patients with gingivitis and patients with
periodontitis.</p><table-wrap id="t04" orientation="portrait" position="float"><label>Table 4</label><caption><p>Presence of antimicrobial resistant aerobes and facultative anaerobes in dentate
patients with different periodontal health conditions and edentulous patients
wearing complete dentures</p></caption><table frame="hsides" rules="groups"><thead><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"><bold>Patients (N)</bold></td><td colspan="6" align="center" rowspan="1"><bold>Presence of resistant isolates - number
(%)</bold></td></tr><tr><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><bold>β-lactams</bold></td><td align="center" rowspan="1" colspan="1"><bold>AMN</bold></td><td align="center" rowspan="1" colspan="1"><bold>CHR</bold></td><td align="center" rowspan="1" colspan="1"><bold>QNL</bold></td><td align="center" rowspan="1" colspan="1"><bold>RF</bold></td><td align="center" rowspan="1" colspan="1"><bold>TE</bold></td></tr></thead><tbody><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1"> </td><td colspan="6" align="center" rowspan="1"> </td></tr><tr><td rowspan="1" colspan="1">Periodontally healthy subjects (N=50)</td><td align="center" rowspan="1" colspan="1"> 5 (10.0)</td><td align="center" rowspan="1" colspan="1">0 (0.0)</td><td align="center" rowspan="1" colspan="1">2 (4.0)</td><td align="center" rowspan="1" colspan="1">3 (6.0)</td><td align="center" rowspan="1" colspan="1">0 (0.0)</td><td align="center" rowspan="1" colspan="1">11 (22.0)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Patients with gingivitis (N= 89)</td><td align="center" rowspan="1" colspan="1">29 (32.6)</td><td align="center" rowspan="1" colspan="1">21 (23.6)</td><td align="center" rowspan="1" colspan="1">10 (11.2)</td><td align="center" rowspan="1" colspan="1"> 9 (10.1)</td><td align="center" rowspan="1" colspan="1">2 (2.2)</td><td align="center" rowspan="1" colspan="1">20 (22.5)</td></tr><tr><td rowspan="1" colspan="1">Patients with periodontitis (N= 70)</td><td align="center" rowspan="1" colspan="1">55 (78.6)</td><td align="center" rowspan="1" colspan="1">31 (44.3)</td><td align="center" rowspan="1" colspan="1"> 9 (12.9)</td><td align="center" rowspan="1" colspan="1">12 (17.1)</td><td align="center" rowspan="1" colspan="1">1 (1.4)</td><td align="center" rowspan="1" colspan="1">28 (40.0)</td></tr><tr style="background-color:#CCCCCC"><td rowspan="1" colspan="1">Edentulous patients (N=41)</td><td align="center" rowspan="1" colspan="1">34 (82.9)</td><td align="center" rowspan="1" colspan="1">23 (56.1)</td><td align="center" rowspan="1" colspan="1">28 (68.3)</td><td align="center" rowspan="1" colspan="1">23 (56.1)</td><td align="center" rowspan="1" colspan="1"> 6 (14.6)</td><td align="center" rowspan="1" colspan="1">27 (65.9)</td></tr></tbody></table><table-wrap-foot><fn><p>AMN, aminoglycosides; CHR, chloramphenicol; QNL, quinolones; RF, rifampin; TE,
tetracycline.</p></fn></table-wrap-foot></table-wrap><p>The results presented in <xref ref-type="table" rid="t04">Table 4</xref> showed a close
correlation between the presence of microorganisms resistant to β-lactams and the use of
complete dentures (Chi-square test, p<0.01) and to a lesser extent, patients with
periodontitis (Chi-square test, p=0.012) or gingivitis (Chi-square test, p=0.02). The
same phenomenon was also detected in relation to resistance to aminoglycosides and
chloramphenicol. However, the occurrence of tetracycline-, quinolone- and/or
rifampin-resistant microorganisms was similar in periodontally healthy subjects and
patients with gingivitis. The levels of resistance to rifampin were reduced and a low
prevalence of such isolates was observed from all dentate patients.</p></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>The patterns of susceptibility to antimicrobial drugs amongst aerobes and facultative
anaerobes have evidenced the presence of a multiresistance phenotype, both in isolates
from human resident microbiota and from exogenous environment<sup><xref ref-type="bibr" rid="r08">8</xref>,<xref ref-type="bibr" rid="r16">16</xref></sup>. Accordingly,
antibiotic resistance raised among commensal bacteria has been supposed to represent a
major feature in the development of resistance within bacterial pathogens. In addition,
the detection of resistant bacteria in commensal microbiota has pointed to the oral
cavity as a possible source for transmission of genes associated to antimicrobial
resistance in pathogenic bacteria<sup><xref ref-type="bibr" rid="r12">12</xref></sup>.</p><p>β-Lactam agents, such as penicillins, cephalosporins and carbapenems, have been among
the most frequently prescribed antibiotics worldwide. In this investigation, most of the
tested microorganisms showed to be resistant to ampicillin. The levels of resistance to
ampicillin in isolates of <italic>Enterobacteriaceae</italic> was similar to those
described by literature<sup><xref ref-type="bibr" rid="r01">1</xref>,<xref ref-type="bibr" rid="r06">6</xref>,<xref ref-type="bibr" rid="r11">11</xref></sup>, however, they were lower than those reported by Gonçalves, et
al.<sup><xref ref-type="bibr" rid="r12">12</xref></sup> (2007).</p><p>The association between β-lactams and β-lactamase inhibitors has been frequently used in
the treatment of odontogenic infections, particularly those infections where the patient
had presented a history of previous use of β-lactams. However, in refractory mixed
infections where aerobes and facultative anaerobes had been involved, this association
has seemed to lead to a poor treatment outcome, since the expression of combined
resistance to ampicillin and to amoxicillin/clavulanic acid has been frequent in
gram-negative enteric rods and <italic>staphylococci</italic>, as shown in <xref ref-type="table" rid="t01">Table 1</xref> and also described in literature<sup><xref ref-type="bibr" rid="r06">6</xref>,<xref ref-type="bibr" rid="r12">12</xref></sup>.</p><p><italic>Enterococci</italic> have been often associated to refractory odontogenic
infections, such as dental abscesses and both Endodontic and periapical infections. The
results presented here have evidenced that these <italic>cocci</italic> were just
susceptible to carbapenems, ciprofloxacin, gentamicin and rifampin. On the other hand,
<italic>enterococci</italic> resistant to ampicillin were also resistant to
amoxicillin/ clavulanic acid association, which was not in agreement with the findings
of Ferrari, Cai and Bombana<sup><xref ref-type="bibr" rid="r07">7</xref></sup> (2005).
These authors reported a high susceptibility to ampicillin and a variable susceptibility
to ciprofloxacin for <italic>enterococci</italic> from Endodontic infections, while Das,
et al.<sup><xref ref-type="bibr" rid="r06">6</xref></sup> (2006) verified a high
resistance of <italic>E. faecalis</italic> strains to gentamicin and ciprofloxacin.</p><p>The cephalosporins have greatly varied in susceptibility to β-lactamases. Cephalothin
has been more resistant to hydrolysis by β-lactamases of <italic>staphylococci</italic>,
whereas cefoxitin has been more resistant to β-lactamases produced by aerobic
gram-negative rods<sup><xref ref-type="bibr" rid="r03">3</xref></sup>. <xref ref-type="table" rid="t01">Table 1</xref> not only confirms these data, but also
shows a disseminated resistance to both cefoxitin and cephalothin among aerobic
gram-positive <italic>cocci</italic> and gram-negative <italic>bacilli</italic>, as also
reported in literature<sup><xref ref-type="bibr" rid="r06">6</xref>,<xref ref-type="bibr" rid="r16">16</xref></sup>.</p><p>It has been verified that carbapenems are the only β-lactams active against most of
enteric microorganisms and other facultative anaerobes and aerobes<sup><xref ref-type="bibr" rid="r02">2</xref></sup>, particularly
<italic>staphylococci</italic><sup><xref ref-type="bibr" rid="r20">20</xref></sup>and enteric gram-negative <italic>bacilli</italic><sup><xref ref-type="bibr" rid="r20">20</xref></sup>. However, some resistance to carbapenems in aerobes and
facultative anaerobes has been described, especially in gram-negative enteric rods,
coagulase-positive <italic>staphylococci</italic> and several species of genera
<italic>Streptococcus</italic> and <italic>Enterococcus</italic><sup><xref ref-type="bibr" rid="r13">13</xref>,<xref ref-type="bibr" rid="r15">15</xref></sup>. The resistance to imepenem was similar to that observed to
meropenem and restrict to a few isolates of <italic>staphylococci, P. aeruginosa, E.
faecium</italic>, and <italic>M. morganii</italic>. This was also observed by Pillar,
et al.<sup><xref ref-type="bibr" rid="r20">20</xref></sup> (2008).</p><p>In this present investigation, most of isolates resistant to β-lactam were β-lactamase
producers. However, 37.1% of the β-lactam resistant microorganisms were not β-lactamase
producers. Some of these "non-producers" could be producers of non-exportable
β-lactamases, as it has been previously reported for some gram-negative
bacteria<sup><xref ref-type="bibr" rid="r14">14</xref></sup>. Another explanations
for this fact would be that these "non-producers" could harbor other mechanisms of
resistance (e.g.: alteration of structure of penicillin-binding proteins), or that the
method's sensitivity did not allow the detection of these enzymes<sup><xref ref-type="bibr" rid="r08">8</xref></sup>.</p><p>Both the production of low affinity penicillin binding proteins<sup><xref ref-type="bibr" rid="r21">21</xref></sup> and the impermeability of the outer
membrane to these drugs could also be involved in the resistance to β-lactams, even in
β-lactamase producers. In this sense, <italic>enterococci</italic> in general and
<italic>E. faecium</italic> in particular would be intrinsically more resistant to
penicillin and ampicillin than the other <italic>streptococci</italic>. Ampicillin and
amoxicillin resistance in <italic>E. faecium</italic> have occurred due to the
expression of the low-affinity class B penicillin-binding protein 5 (PBP5). However,
higher levels of resistance in clinical isolates have been only rarely associated with
increased levels of PBP 5 expression<sup><xref ref-type="bibr" rid="r22">22</xref></sup>. More commonly, mutations that have been presumed to lower the affinity
for β-lactam antibiotics have been identified within PBP5 genes of highly resistant
clinical isolates<sup><xref ref-type="bibr" rid="r21">21</xref></sup>.</p><p>Aminoglycoside antibiotics have not been usually recommended in the treatment of
odontogenic infections. However, its use in association with other drugs, especially
β-lactams, has been frequent in oral surgery. The susceptibility to gentamicin and
amikacin was high among most of the tested microorganisms, but some
<italic>enterococci</italic> were highly resistant to amikacin. On the other hand,
resistance to gentamicin was more concentrated on <italic>C. freundii, E. cloacae, P.
aeruginosa</italic>, and some <italic>staphylococci</italic>.</p><p>The activity of gentamicin and amikacin against most aerobes and facultative anaerobes
has been well described in literature<sup><xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r12">12</xref>,<xref ref-type="bibr" rid="r16">16</xref></sup>, and these drugs have been the most frequently used in
nosocomial and opportunistic infections involving these microorganisms. However,
resistance has been observed in <italic>Enterobacteriaceae</italic> and
<italic>Pseudomonadaceae</italic>, ranging from 1.0% to 17.9% in gram-negative
enteric rods for amikacin and from 2.8% to 38.5% for gentamicin<sup><xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r24">24</xref></sup>. An expressive resistance to these drugs has also been detected for
<italic>staphylococci</italic> and <italic>enterococci</italic>, as well as genus
<italic>Klebsiella</italic><sup><xref ref-type="bibr" rid="r06">6</xref>,<xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r17">17</xref></sup>.</p><p>Chloramphenicol has been a broad spectrum antimicrobial largely used in the treatment of
nosocomial infections, particularly when <italic>Enterobacteriaceae</italic> species
were involved and its use has been rare in dentistry. <xref ref-type="table" rid="t03">Table 3</xref> shows that <italic>enterococci</italic> were the most resistant to
chloramphenicol amongst the tested microorganisms. Moreover, some resistance was
disseminated in most target microorganisms. On the other hand, this phenomenon has been
described mainly in <italic>enterococci</italic> and <italic>streptococci
viridans</italic>, although some enteric gram-negative rods resistant to this drug
have been detected<sup><xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r12">12</xref></sup>. The results presented here, however, would not justify
the use of this antimicrobial agent in the treatment of serious infections involving
these superinfecting bacteria.</p><p>The resistance to ciprofloxacin was manly restricted to some isolates of genera
<italic>Staphylococcus</italic> and <italic>Streptococcus</italic>, while just two
isolates of gram-negative rods (<italic>E. intermedius</italic> and <italic>P.
aeruginosa</italic>) were resistants amongst the tested microorganisms. This was in
accordance with most of available data in literature<sup><xref ref-type="bibr" rid="r01">1</xref>,<xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r12">12</xref></sup>. However, it contrasted with Huang, et al.<sup><xref ref-type="bibr" rid="r15">15</xref></sup> (2007), who showed high levels of
resistance to ciprofloxacin in oxacillin-resistant <italic>S. aureus</italic> (100%),
extended spectrum β-lactamase (ESBLs) producers <italic>K. pneumoniae</italic> (82%),
<italic>S. marcescens</italic> (40%), <italic>streptococci</italic> (33%), and
<italic>P. aeruginosa</italic> (9%). Since this drug has not been either frequently
used by Brazilian dentists or as part of self-medication, it would be possible that the
antimicrobial resistance profiles of isolates from hospitals would have been
significantly different from those observed in commensal microbiota, as described by
Pillar, et al.<sup><xref ref-type="bibr" rid="r20">20</xref></sup> (2008).</p><p>Resistance to tetracycline also has been often registered in facultative anaerobes and
aerobes, which have seemed to be disseminated in the human and animal
microbiota<sup><xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r12">12</xref></sup>. This phenomenon could be related to its extensive use
in medicine, veterinary and dentistry. The distribution of the resistance to
tetracycline, as observed in <xref ref-type="table" rid="t02">Table 2</xref>, was
similar to that previously reported<sup><xref ref-type="bibr" rid="r11">11</xref>,<xref ref-type="bibr" rid="r16">16</xref></sup>, and slightly higher than the results of
Gonçalves, et al.<sup><xref ref-type="bibr" rid="r12">12</xref></sup> (2007). The
resistance to tetracycline was similar between gram-positive <italic>cocci</italic> and
gram-negative bacilli, as previously observed<sup><xref ref-type="bibr" rid="r16">16</xref></sup>, while resistance to doxycycline was more prevalent among
gram-negative enteric rods and pseudomonades, which represented 76.9% of all resistant
isolates. The most commonly detected doxycycline resistant species were <italic>C.
freundii, E. cloacae, P. aeruginosa</italic>, and <italic>P. alcalifaciens.</italic>The high resistance of pseudomonades from oral cavity to doxycycline was previously
reported by Barbosa, Mayer and SabaChujfi<sup><xref ref-type="bibr" rid="r01">1</xref></sup> (2001). These results did not support the use of doxycycline or
tetracycline in life threatening infections.</p><p>Rifampin has been widely used in the treatment of several life threatening infections as
well as minor oral infections for many years<sup><xref ref-type="bibr" rid="r04">4</xref></sup>. In the clinical samples, the low frequency of rifampin resistance
was relevant and confined to <italic>staphylococci</italic> and the genera
<italic>Providencia</italic> and <italic>Serratia</italic>, as well as to
pseudomonades. However, these authors showed that the rifampin resistance ranged from
17.2% to 30.0% among <italic>enterococci</italic>, while Ferrari, Cai and
Bombana<sup><xref ref-type="bibr" rid="r07">7</xref></sup> (2005) detected this
resistance in 58.3% of <italic>enterococci</italic>. On the other hand, the present
investigation found that all <italic>enterococci</italic> were susceptible to rifampin,
and these results seem to endorse rifampin as an important therapeutic alternative in
mixed and nosocomial infections, particularly where clinical signs evidenced the
participation of multi-drug resistant microorganisms.</p><p>Although patients with periodontitis and edentulous patients are considerably older than
patients with gingivitis and periodontally healthy patients, the influence of age on the
distribution of resistant microorganisms is reduced when data from patients with the
same age and with different periodontal status are compared, showing that this factor
alone does not seem relevant. Moreover, a great proportion of bacterial strains
presented resistance to ampicillin, amoxicillin and amoxicillin/ clavulanic acid and
some isolates of <italic>E. cloacae, K. oxytoca, P. agglomerans, P.
alcalifaciens</italic>, and <italic>Serratia</italic> sp. presented a broad spectrum
resistance to β-lactam antibiotics, producing β-lactamases active on penicillins and
cephalosporins.</p><p>The presence of the enterobacteria and pseudomonads and other superinfecting
microorganisms may be relevant in gingivitis and periodontitis etiology, especially in
immunosuppressed patients<sup><xref ref-type="bibr" rid="r01">1</xref>,<xref ref-type="bibr" rid="r10">10</xref></sup>. However, the role of enteric bacteria
in the periodontal diseases etiology remains unclear, and it must be an alert to
clinicians who use systemic antibiotics, such as ciprofloxacin, as an adjunct in the
periodontitis treatment in these patients<sup><xref ref-type="bibr" rid="r09">9</xref></sup>.</p></sec><sec sec-type="conclusions"><title>CONCLUSIONS</title><p>The results of this investigation confirmed that the oral cavity of patients with
periodontitis and gingivitis, and particularly edentulous patients wearing complete
dentures could harbor microorganisms with several antimicrobial resistance markers, and
these microorganisms are frequently implicated in multiresistant, systemic, oral or
nosocomial infections.</p></sec></body><back><ack><sec><title>ACKNOWLEDGEMENTS</title><p>This study was partially supported by grants from The State of São Paulo Research
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