{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T03:12:54Z","timestamp":1789096374456,"version":"build-2803163510"},"reference-count":49,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2012,11,23]],"date-time":"2012-11-23T00:00:00Z","timestamp":1353628800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"name":"Temple University School of Dentistry"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J of Periodontal Research"],"published-print":{"date-parts":[[2013,8]]},"abstract":"<jats:sec><jats:title>Background and Objective<\/jats:title><jats:p>Beta\u2010lactam antibiotics prescribed in periodontal therapy are vulnerable to degradation by bacterial \u03b2\u2010lactamases. This study evaluated the occurrence of \u03b2\u2010lactamase\u2010positive subgingival bacteria in chronic periodontitis subjects of USA origin, and assessed their <jats:italic>in vitro<\/jats:italic> resistance to metronidazole at a breakpoint concentration of 4\u00a0\u03bcg\/mL.<\/jats:p><\/jats:sec><jats:sec><jats:title>Material and Methods<\/jats:title><jats:p>Subgingival plaque specimens from deep periodontal pockets with bleeding on probing were removed from 564 adults with severe chronic periodontitis before treatment. The samples were transported in <jats:styled-content style=\"fixed-case\">VMGA III<\/jats:styled-content> and then plated onto: (i) nonselective enriched Brucella blood agar (<jats:styled-content style=\"fixed-case\">EBBA<\/jats:styled-content>) and incubated anaerobically for 7\u00a0d; and (ii) selective trypticase soy\u2010bacitracin\u2010vancomycin (<jats:styled-content style=\"fixed-case\">TSBV<\/jats:styled-content>) and incubated for 3 d in air + 5% <jats:styled-content style=\"fixed-case\">CO<\/jats:styled-content><jats:sub>2<\/jats:sub>. At the end of the incubation periods, the bacterial test species were identified and quantified. Specimen dilutions were also plated onto <jats:styled-content style=\"fixed-case\">EBBA<\/jats:styled-content> plates supplemented with 2\u00a0\u03bcg\/mL of amoxicillin, a combination of 2\u00a0\u03bcg\/mL of amoxicillin plus 2\u00a0\u03bcg\/mL of the \u03b2\u2010lactamase inhibitor clavulanic acid, or 4\u00a0\u03bcg\/mL of metronidazole, followed by anaerobic incubation for 7\u00a0d. Bacterial test species presumptively positive for \u03b2\u2010lactamase production were identified by growth on <jats:styled-content style=\"fixed-case\">EBBA<\/jats:styled-content> primary isolation plates supplemented with amoxicillin alone and no growth on <jats:styled-content style=\"fixed-case\">EBBA<\/jats:styled-content> primary isolation plates containing both amoxicillin plus clavulanic acid. A subset of such isolates was subjected to nitrocefin\u2010based chromogenic disk testing to confirm the presence of \u03b2\u2010lactamase activity. <jats:italic>In vitro<\/jats:italic> resistance to 4\u00a0\u03bcg\/mL of metronidazole was noted when growth of test species occurred on metronidazole\u2010supplemented <jats:styled-content style=\"fixed-case\">EBBA<\/jats:styled-content> culture plates.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Two\u2010hundred and ninety\u2010four (52.1%) of the study subjects yielded \u03b2\u2010lactamase\u2010producing subgingival bacterial test species, with <jats:italic>Prevotella intermedia\/nigrescens<\/jats:italic>,<jats:italic> Fusobacterium nucleatum<\/jats:italic> and other <jats:italic>Prevotella<\/jats:italic> species most frequently identified as \u03b2\u2010lactamase\u2010producing organisms. Of the \u03b2\u2010lactamase\u2010producing bacterial test species strains recovered, 98.9% were susceptible <jats:italic>in vitro<\/jats:italic> to metronidazole at 4\u00a0\u03bcg\/mL.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>The occurrence of \u03b2\u2010lactamase\u2010positive subgingival bacterial species in more than half of the subjects with severe chronic periodontitis raises questions about the therapeutic potential of single\u2010drug regimens with \u03b2\u2010lactam antibiotics in periodontal therapy. The <jats:italic>in vitro<\/jats:italic> effectiveness of metronidazole against nearly all recovered \u03b2\u2010lactamase\u2010producing subgingival bacterial species further supports clinical periodontitis treatment strategies involving the combination of systemic amoxicillin plus metronidazole.<\/jats:p><\/jats:sec>","DOI":"10.1111\/jre.12031","type":"journal-article","created":{"date-parts":[[2012,11,23]],"date-time":"2012-11-23T09:22:25Z","timestamp":1353662545000},"page":"493-499","source":"Crossref","is-referenced-by-count":56,"title":["Prevalence of \u03b2\u2010lactamase\u2010producing bacteria in human periodontitis"],"prefix":"10.1111","volume":"48","author":[{"given":"T. E.","family":"Rams","sequence":"first","affiliation":[{"name":"Department of Periodontology and Oral Implantology and Oral Microbiology Testing Service Laboratory Temple University School of Dentistry Philadelphia PA USA"},{"name":"Department of Microbiology and Immunology Temple University School of Medicine Philadelphia PA USA"},{"name":"Department of Oral Microbiology Center for Dentistry and Oral Hygiene University Medical Center Groningen University of Groningen Groningen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J. E.","family":"Degener","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology University Medical Center Groningen University of Groningen Groningen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. J.","family":"van Winkelhoff","sequence":"additional","affiliation":[{"name":"Department of Oral Microbiology Center for Dentistry and Oral Hygiene University Medical Center Groningen University of Groningen Groningen The Netherlands"},{"name":"Department of Medical Microbiology University Medical Center Groningen University of Groningen Groningen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2012,11,23]]},"reference":[{"key":"e_1_2_6_2_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-0722.2000.108003163.x"},{"key":"e_1_2_6_3_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-302X.1987.tb00276.x"},{"key":"e_1_2_6_4_1","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.23.6.1127-1133.1986"},{"key":"e_1_2_6_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.femsle.2004.11.023"},{"key":"e_1_2_6_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-302x.2004.00159.x"},{"key":"e_1_2_6_7_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.1997.tb00226.x"},{"key":"e_1_2_6_8_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-051x.2000.027007520.x"},{"key":"e_1_2_6_9_1","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.47.4.1443-1446.2003"},{"key":"e_1_2_6_10_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1399-302X.1999.140604.x"},{"key":"e_1_2_6_11_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.0902-0055.2001.00096.x"},{"key":"e_1_2_6_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/0266-4356(90)90085-Y"},{"key":"e_1_2_6_13_1","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1046\/j.0906-6713.2002.003421.x","article-title":"Periodontal diagnoses and classification of periodontal diseases","volume":"34","author":"Armitage GC","year":"2005","journal-title":"Periodontol 2000"},{"key":"e_1_2_6_14_1","first-page":"1","article-title":"Microbiological examination of root canals and periapical tissues of human teeth","volume":"74","author":"M\u00f6ller \u00c5JR","year":"1966","journal-title":"Odontol Tidskr"},{"key":"e_1_2_6_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-302X.1993.tb00614.x"},{"key":"e_1_2_6_16_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cll.2007.07.012"},{"key":"e_1_2_6_17_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-302X.1988.tb00080.x"},{"key":"e_1_2_6_18_1","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.15.4.606-609.1982"},{"key":"e_1_2_6_19_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-302X.1986.tb00318.x"},{"key":"e_1_2_6_20_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.1996.tb00556.x"},{"key":"e_1_2_6_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.anaerobe.2011.03.017"},{"key":"e_1_2_6_22_1","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-33-3-628"},{"key":"e_1_2_6_23_1","first-page":"1","article-title":"Susceptibility testing of bacteria and fungi. Report from \u201cthe Norwegian Working Group on Antibiotics\u201d","volume":"103","author":"Bergan T","year":"1997","journal-title":"Scand J Infect Dis Suppl"},{"key":"e_1_2_6_24_1","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.00037-09"},{"key":"e_1_2_6_25_1","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1128\/jcm.34.5.1321-1322.1996","article-title":"Stability of amoxicillin\u2010clavulanate in BACTEC medium determined by high\u2010performance liquid chromatography and bioassay","volume":"34","author":"Moore TD","year":"1996","journal-title":"J Clin Microbiol"},{"key":"e_1_2_6_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.1999.tb02521.x"},{"key":"e_1_2_6_27_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-051x.2000.027002079.x"},{"key":"e_1_2_6_28_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2004.75.11.1553"},{"key":"e_1_2_6_29_1","doi-asserted-by":"publisher","DOI":"10.1086\/512810"},{"key":"e_1_2_6_30_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-695X.1993.tb00334.x"},{"key":"e_1_2_6_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0924-8579(99)00056-4"},{"key":"e_1_2_6_32_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0765.2010.01274.x"},{"key":"e_1_2_6_33_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.2009.01425.x"},{"key":"e_1_2_6_34_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12275-011-0519-1"},{"key":"e_1_2_6_35_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.1993.tb00334.x"},{"key":"e_1_2_6_36_1","doi-asserted-by":"publisher","DOI":"10.1093\/jac\/dkl287"},{"key":"e_1_2_6_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/0003-9969(80)90102-8"},{"key":"e_1_2_6_38_1","first-page":"50","article-title":"\u03b2\u2010lactamase producing anaerobic bacteria in the oropharynx and their clinical relevance","volume":"57","author":"Nord CE","year":"1988","journal-title":"Scand J Infect Dis Suppl"},{"key":"e_1_2_6_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/0030-4220(91)90358-J"},{"key":"e_1_2_6_40_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.1989.60.8.467"},{"key":"e_1_2_6_41_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-051X.1990.tb00024.x"},{"key":"e_1_2_6_42_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2710.1992.tb01220.x"},{"key":"e_1_2_6_43_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.1986.57.10.613"},{"key":"e_1_2_6_44_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-051x.2001.028007597.x"},{"key":"e_1_2_6_45_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.1985.56.6.352"},{"key":"e_1_2_6_46_1","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-051X.2002.290809.x"},{"key":"e_1_2_6_47_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2009.090276"},{"key":"e_1_2_6_48_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0757.2010.00356.x"},{"key":"e_1_2_6_49_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2011.110432"},{"key":"e_1_2_6_50_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2012.110625"}],"container-title":["Journal of Periodontal Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fjre.12031","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fjre.12031","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/jre.12031","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,30]],"date-time":"2023-10-30T08:28:06Z","timestamp":1698654486000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/jre.12031"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,11,23]]},"references-count":49,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2013,8]]}},"alternative-id":["10.1111\/jre.12031"],"URL":"https:\/\/doi.org\/10.1111\/jre.12031","archive":["Portico"],"relation":{},"ISSN":["0022-3484","1600-0765"],"issn-type":[{"value":"0022-3484","type":"print"},{"value":"1600-0765","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,11,23]]}}}