Journal of the International Academy of Periodontology

Transcription

Journal of the International
Academy of Periodontology
The official journal of the International Academy of Periodontology
Volume 13Number 1 January 2011
Published by
Stephen Hancocks Ltd
JIAP
JIAP Jan
Oct 11
10 OFC.indd
OFC.indd 11
22/12/2010
23/09/2010 10:21:43
13:01:19
INFORMATION FOR AUTHORS
Manuscripts
Manuscripts for publication and all correspondence should be sent to Dr. Mark R.
Patters, Editor, Journal of the International Academy of Periodontology, University
of Tennessee College of Dentistry, Office of Academic Affairs, 875 Union Avenue,
Memphis, TN USA, 38163, e-mail: [email protected]. Printed submissions sent
to the above address must be prepared as described below and accompanied by a
standard floppy disk containing an electronic copy of the manuscript. The floppy
disk should be labelled with the manuscript title, author(s) and specific version
of the word processing program used. In lieu of printed manuscripts, electronic
submissions done entirely in Microsoft Word (PC or Mac) will be accepted at the
above e-mail address. Effective 1 January 2006, the corresponding author of a
manuscript submitted for publication in the Journal of the International Academy
of Periodontology must be a member of the International Academy of Periodontology or, in lieu of membership, pay a submission fee of US$100. An application for
membership can be found at http://www.perioiap.org/join_iap.htm. Those authors
choosing to pay the submission fee should contact the Editor at [email protected]
before submitting the manuscript.. All submissions must be written in English and
will be subject to peer and editorial review.
Articles for publication will be considered under the following headings:
original research, clinical case reports and review articles relevant to all aspects of
periodontology and implantology. Articles must be original and may not have been
submitted or accepted for publication elsewhere, with the exception of presentation
at a scientific meeting and publication as an abstract. A signed statement to this effect
should be included with the submission of the manuscript. Research that involves
studies on humans must conform to the Declaration of Helsinki and the authors
must indicate that appropriate informed consent was obtained.
Research reports
State the problem and objectives clearly, describe the methods and materials in
detail, report the results clearly using the minimum number of figures and tables;
and, bearing in mind previously published work, discuss the results, the conclusions,
and the clinical implications.
Clinical case reports
Discuss a clinical challenge; describe the treatment method and discuss the results in
light of previously published methods of treatment of individual patients.
Literature reviews
Record the sequence of development of a particular aspect of periodontology in
detail, as briefly and succinctly as possible. The review should cover the topic completely and be thoroughly referenced. At least one contributing author of a review
must have personal experience with relevant research.
Letters to the Editor
Letters may address relevant matters of concern to the membership of the International Academy of Periodontology or offer constructive criticism of articles published
by JIAP. Letters must be concise and signed. If the letter comments on a published
article, it should contain appropriate references. The letter will be referred to the
author(s) of the original work so that they will have an opportunity to respond.
Editorials
Editorials may be solicited from authorities to provide a unique perspective on published articles, or to comment on other items of interest to the membership.
Copyright statement
A copyright transfer statement will accompany the galley proofs of accepted, typeset
manuscripts. The form must be signed by at least one of the authors and returned
with the corrected proofs.
Manuscript preparation
Manuscripts must be submitted in quadruplicate (one original and three copies) and
should be typewritten, double-spaced on one side only of A4 or 8.5 x 11 inch paper,
with at least 25 millimetre (1 inch) margins on all four sides. Articles generally should
not exceed 10–12 pages (excluding references, tables, figure legends and figures)
and should be limited to no more than six authors. Additional contributing authors
will be listed as an addendum to the manuscript. Abbreviations should be placed in
parenthesis after the first complete use of the term(s) to be abbreviated. Use generic
names for drugs and for dental materials. Give trade names and manufacturers’ names
and addresses in parentheses.
Title page
Should include for each author the full name and title, academic degrees, and institutional affiliations. The corresponding author should also include a street address,
telephone and fax numbers, and e-mail address. Only individuals who have made a
substantial contribution to the work and who agree to take public responsibility for
the content of the work should be included. If the work was supported by a grant,
the name of the supporting organization and the grant number should appear on
the title page. The address for reprint requests will be assumed to that of the corresponding author unless otherwise specified.
Abstract and Key Words
Abstracts are required for all articles, and should be limited to 250 words typed
double-spaced on a separate page. The abstract should serve as a concise
summary of the manuscript, including objective, methods, results and conclusions.
Abbreviations should not be used in the abstract. Please provide three to six key
words (Dental Descriptors, Index to Dental Literature and/or Index Medicus) to
be used for indexing purposes.
Text
The body of the manuscript should contain an Introduction, a detailed review of the
Materials and Methods, a description in logical sequence of Results, and a Discussion
section with Conclusions.
Acknowledgements and Conflict of Interest
Include acknowledgement of those individuals who contributed to the publication,
source of financial support, and any financial relationships of any of the authors
which may pose a perceived conflict of interest.
References
In the text the author’s (authors’) name(s) and date of publication should be used as
either: “in a similar study (Anderson and Morgan, 1992)”, or “Conversely, Blinkhorn
(1994) found that.” If there are more than two authors, the first author and year are
cited in the text; for example, “(Spencer et al., 1995)”. Citation of authors of more
than one paper in a single year are shown as 1995a; 1995b; etc. Multiple references
in the text should appear in chronological order separated by semicolons. Authors
of unreferenced work should appear in the text only.
The list of references at the end of the text should be double-spaced and
arranged alphabetically by name of first author. All authors should be listed unless
there are more than six, when only the first three should be given followed by et al.
This should be followed by the title of the article, the full name of the journal (in
italics); the year of publication; the volume number (in bold); and the first and last
page numbers in full. Please follow the punctuation used in the examples below.
Papers submitted with an incoreectly formatted reference list will be held without
review until a corrected reference list is provided.
Examples:
Reference to an article: Shiloah, J. and Patters, M.R. Repopulation of Periodontal
Pockets by Microbial Pathogens in the Absence of Supportive Therapy. Journal
of Periodontology 1996; 67:130–139.
Reference to a book: Schuster, G.S. Oral Microbiology and Infectious Diseases, 3rd ed.
Philadelphia: B. C. Decker, 1990; 516–522.
Reference to a chapter in a book: Chesney, J., Patters, M.R. and Budreau-Patters, A.
Oral Infections. In Long, S., Prober, C. and Pickering, L. (Eds): Principles and
Practice of Pediatric Infectious Disease. New York. John Wiley and Sons, 1996.
Reference to a dissertation or thesis: James, A. On the Immune Response to GTR
Membranes in Periodontics. PhD, Liverpool, UK. 1994; 15–25.
Reference to a report: Committee on Mercury Hazards in Dentistry. Code of
Practice for Dental Mercury Hygiene. London: Department of Health and
Social Security, 1979; Publication No. DHSS 79-F372.
Reference to an abstract: Patters, M.R., Shiloah, J., Dean, J.W., Bland, P. and
Toledo, G. The Consequence of Infection of Treated Periodontal Pockets
by Microbial Pathogens. Journal of Dental Research 1997; 76 (special issue),
111 (Abst).
Tables
Each table must be submitted on a separate sheet of paper, double spaced throughout,
including column heads, footnotes, and data. They should be numbered with arabic
numerals according to their order of mention in the text. Tables should be self-explanatory and supplement, not duplicate, the text. All footnotes should immediately
follow the table, and all abbreviations should be defined in the footnote.
Illustrations
Illustrations should be numbered with arabic numerals in order of their mention in
the text. They may be submitted in colour or black and white, but colour will be used
at the Editor’s discretion where it enhances the text. In general, the Editor will require
that clinical photographs and stained histologic specimens be submitted and published
in colour. In such cases, the authors’ must agree in advance to pay the increased
printing costs for publishing the colour figures. If submitting electronically, figures
should be submitted in jpeg format. Glossy photographic prints, transparencies, or
good quality laser prints are also acceptable if submitting via post. Lettering must be
clear and large enough to remain legible in the event of reduction of the figure in reproduction. One set of original illustrations must accompany the original manuscript.
Copies of the illustrations, if legible, can be submitted with the additional copies of
the manuscript. They should be labeled with the author’s name, figure number and
an arrow to indicate the top edge using adhesive labels in the margin or on the back
of the illustration. Typed labels are preferred as ink and pen or pencil pressure may
damage the emulsion of carefully prepared photographic prints.
Legends
All illustrations should be listed by legend on a separate sheet of paper, type-written,
double-spaced, and numbered to correspond with the numbering in the text.
Permissions
Direct quotations, tables, and illustrations that have appeared in copyright material
must be accompanied by written permission for their use from the copyright owner
and the original author, along with complete information as to the source. Photographs of identifiable persons must be accompanied by signed releases showing
informed consent. If an illustration is taken from previously published material, the
legend must give full credit to the original source.
Statements and opinions expressed in the articles and communications herein
are those of the author(s) and not necessarily those of the Editor(s) or publisher, and
the Editor(s) and publisher disclaim any responsibility or liability for such material.
Authors must disclose to the Editor any financial interest they may have in products
mentioned in their article.
The Journal will endeavour to provide a decision to the authors within 16 weeks
of arrival of the paper at the editorial office, provided that the corresponding author
has a functioning e-mail address. Reliance on overseas mail may delay the decision
from reaching the author within the above time frame. Manuscripts submitted
for review that do not follow these instructions may be delayed until corrected or
returned unreviewed.
Volume 13
Number 1
January 2011
ISSN 1466–2094
EDITORIAL BOARD
Mark R Patters
Editor
Memphis, TN, USA
Andrea B Patters
Associate Editor
Sultan Al Mubarak
Riyadh, Saudi Arabia
P Mark Bartold
Adelaide, SA, Australia
Michael Bral
New York, NY, USA
Nadine Brodala
Chapel Hill, NC, USA
Cai-Fang Cao
Beijing, People’s Republic of China
Chong-Pyoung Chung
Seoul, Korea
Daniel Etienne
Paris, France
Journal
of the
International Academy of
Periodontology
The Effect of Different Interdental Cleaning Devices on Gingival Bleeding
Nanning A. M. Rosema, Nienke L. Hennequin-Hoenderdos, Claire E. Berchier,
Dagmar E. Slot, Deborah M. Lyle and Godefridus A. van der Weijden
2
Additive or Synergistic Antimicrobial Effects of Amoxicillin and
Metronidazole on Whole Plaque Samples: A Preliminary Report
Clemens Walter, Eva M. Kulik, Roland Weiger, Nicola U. Zitzmann and
Tuomas Waltimo
11
Clinical and Microbiological Comparison of Three Non-surgical
Protocols for the Initial Treatment of Chronic Periodontitis
Carlos Serrano, Nidia Torres, Angela Bejarano, Marcela Caviedes and
María Eugenia Castellanos
17
13th International Biennial Congress - Registration Form
27
Erhan Firatli
Istanbul, Turkey
Kohji Hasegawa
Tokyo, Japan
Vincent J Iacono
Stony Brook, NY, USA
Isao Ishikawa
Tokyo, Japan
Georges Krygier
Paris, France
Yoji Murayama
Okayama, Japan
Hamdy Nassar
Cairo, Egypt
Angela R C Pack
Dunedin, New Zealand
David Paquette
Chapel Hill, NC, USA
Stephen Polins
Boston, MA, USA
Rok Schara
Ljubljana, Slovenia
Lior Shapira
Jerusalem, Israel
Uros Skaleric
Ljubljana, Slovenia
Aubrey Soskolne
Jerusalem, Israel
Thomas E Van Dyke
Boston, MA, USA
JIAP Jan 11 Contents pp1.indd 97
The Journal of the International Academy of Periodontology is the official journal of the International Academy of
Periodontology and is published quarterly (January, April, July and October) by Stephen Hancocks Ltd in association with Dennis
Barber Ltd.
Manuscripts, prepared in accordance with the Information for Authors should be submitted to the Editor, Dr. Mark R. Patters, University
of Tennessee, Department of Periodontology, 875 Union Avenue, Memphis, TN 38163, USA. Electronic submissions will be accepted and
should be sent to [email protected]. Instructions to Authors are available at: http://www.perioiap.org/publications.htm#JOURNAL
All enquiries concerning advertising, subscriptions, inspection copies and back issues should be addressed to Mrs. Kelly Ogilvie
McLean, Goldman School of Graduate Dentistry, Boston University, 100 E. Newton Street, Boston, MA, USA 02118. Tel: +1 617
638-4758; Fax: +1 617 638-4799. Email: [email protected]. Whilst every effort is made by the publishers and Editorial Board to see
that no inaccurate or misleading opinion or statement appears in this Journal they wish to make clear that the opinions expressed in
the articles, correspondence, advertisements etc., herein are the responsibility of the contributor or advertiser concerned. Accordingly, the publishers and the Editorial Board and their respective employees, offices and agents accept no liability whatsoever for the
consequences of any such inaccurate or misleading opinion or statement.
© 2011 International Academy of Periodontology.
All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any
means, electronic, mechanical, photocopying, or otherwise, without permission of the Academy.
Produced in Great Britain by Dennis Barber Limited, Lowestoft, Suffolk
23/12/2010 10:18:46
Journal of the International Academy of Periodontology 2011 13/1: 2–10
The Effect of Different Interdental Cleaning
Devices on Gingival Bleeding
Nanning A. M. Rosema1, Nienke L. Hennequin-Hoenderdos1,
Claire E. Berchier1, Dagmar E. Slot1, Deborah M. Lyle2 and
Godefridus A. van der Weijden1
Department of Periodontology, Academic Centre for Dentistry
Amsterdam ACTA, University of Amsterdam and VU University
Amsterdam,The Netherlands, and 2Water Pik Inc, Fort Collins, CO, USA
1
Abstract
Objective: To compare the effectiveness of an oral irrigator (OI) with a prototype jet
tip or a standard jet tip to floss as adjunct to daily toothbrushing on gingival bleeding.
Methods: In this single masked, 3-group parallel, 4-week home use experiment, 108
subjects were randomly assigned to one of three groups: 1) OI with a prototype jet tip;
2) OI with a standard jet tip; 3) waxed dental floss. All groups used their assigned product once a day as adjunct to twice daily toothbrushing for two minutes with a standard
ADA reference toothbrush. Professional instructions were given by a dental hygienist in
OI use or floss use according to written instructions. All subjects also received a toothbrush instruction leaflet (Bass technique). Subjects were assessed for both bleeding and
plaque at baseline and after two weeks and four weeks and were instructed to brush
their teeth approximately 2 to 3 hours prior to their assessment. Results: With respect to
mean bleeding scores the ANCOVA analysis with baseline as covariate and week 4 as
dependent variable showed a significant difference between groups in favor of both the
oral irrigator groups. For plaque, however, no significant difference among groups was
observed. Conclusion: When combined with manual toothbrushing the daily use of an
oral irrigator, either with prototype or standard jet tip, is significantly more effective in
reducing gingival bleeding scores than is the use of dental floss, as determined within
the limits of this 4-week study design.
Key words: Floss, dental water jet, oral irrigator, water flosser, gingivitis, bleeding,
plaque, toothbrush
Introduction
Biofilms are 3-dimensional arrangements of bacteria
that are loosely or more firmly adherent to teeth and
tissue (Costerton et al., 1994). Biofilms consist of microcolonies of bacteria embedded in slimy matrices and are
self-sufficient, dynamic communities that can survive in
hostile environments (Marsh and Bradshaw, 1995) The
regular removal of dental plaque biofilm, which contains
the bacteria responsible for caries formation and for
the etiology of gingivitis and periodontitis, is the wellaccepted conditio sine qua non of dental health (Gorur et al.,
2009). Mechanical removal is considered the most effective method to control the growth of the oral biofilm. The
most common device used for mechanical plaque control
Correspondence to: N.A.M. Rosema. Department of Periodontology, Academic Centre for Dentistry Amsterdam (ACTA),
University of Amsterdam and VU University Amsterdam, Gustav Mahlerlaan 3004 1081 LA Amsterdam, The Netherlands.
E-mail: [email protected]
is either a manual or power toothbrush. As toothbrush
efficacy is limited to the surfaces of the teeth it can access
(facial, lingual, and occlusal), another device is needed to
clean the interdental area and the proximal surfaces of
the teeth and surrounding gingivae. Other factors that
affect the efficacy of mechanical plaque biofilm removal
include brushing frequency, brushing time, toothbrush
design, and brushing technique (Jepsen et al., 1998; Van
der Weijden et al., 1993).
For most people, however, total plaque biofilm
removal is not a realistic goal. It is difficult for patients
to effectively remove or disrupt the biofilm from all
surfaces of the teeth on a daily basis (Douglass et al.,
1993; Brown et al., 1993). On average, people reduce
their plaque scores by approximately 50% by brushing
(Jepsen et al., 1998). Therefore, compliance with instructions is a major consideration when recommending any
self-care device. To be truly patient-centered, practitioners must shift to recommending available tools that,
besides having demonstrated efficacy in reducing inflammation based on scientific evidence, are also preferred
by patients (Slot et al., 2008).
© International Academy of Periodontology
JIAP 10-005 Rosema.indd 2
04/01/2011 11:37:43
A dental water jet or water flosser or oral irrigator
(OI) is an electric device that delivers a pulsating fluid
via controlled pressure which is aimed at the removal
of interdental and subgingival plaque biofilm on tooth
surfaces to reduce inflammation as a supplement to
toothbrushing (Lobene, 1969; Drisko et al., 1987; Cobb et
al., 1988; Flemmig et al., 1990; Chaves et al., 1994; Flemmig et al.,1995; Barnes et al., 2005; Gorur et al., 2009).
The OI was introduced to the dental profession in 1962
and has been studied extensively for the past decades.
Clinical studies demonstrate that an OI is safe and can
significantly reduce bleeding and gingivitis in a variety
of cohorts (Lobene et al., 1969; Flemmig et al., 1990;
Brownstein et al., 1990; Burch et al., 1994; Newman et
al., 1994; Flemmig et al., 1995; Felo et al., 1997; Barnes
et al., 2005; Sharma et al., 2008). However, erythrosinebased plaque indices have yielded equivocal data. Some
studies have shown a reduction in plaque indices with
the use of the OI compared to toothbrushing alone
(Burch et al., 1994; Felo et al., 1997; Cutler et al., 2000;
Al Mubarak et al., 2002; Sharma et al., 2008), while other
studies showed no significant differences (Ciancio et al,
1989; Brownstein et al., 1990; Walsh et al., 1992; Chaves
et al., 1994; Fine et al., 1994).
The OI is likely to provide a particular benefit in
terms of gingival health to a large part of the general
public that does not clean the interproximal spaces
on a regular basis (Research, Science and Therapy
Committee, 2005). In 2001 the American Academy of
Periodontology stated, “Among individuals who do not
perform excellent oral hygiene, supragingival irrigation
with or without medicaments is capable of reducing
gingival inflammation beyond that normally achieved
by toothbrushing alone. This effect is likely due to the
flushing out of subgingival bacteria (Research, Science
and Therapy Committee, 2001).” In a 2005 position
paper, the American Academy of Periodontology stated
that “supragingival lavage can assist individuals with
gingivitis or poor oral hygiene. The greatest benefit is
seen in patients who perform inadequate interproximal
cleansing. Patients report that the OI facilitates the
removal of food debris in posterior areas, especially
in cases of fixed bridges or orthodontic appliances,
when the proper use of interdental cleaning devices is
difficult” (Research, Science and Therapy Committee,
2005). However, anecdotal discussions and commentary
continue concerning the appropriate use and efficacy
of this instrument. OI devices can be used with water
but also with antimicrobial agents (Flemmig et al., 1990,
Brownstein et al., 1990, Jolkovsky et al., 1990; Newman
et al., 1994, Fine et al., 1994; Chaves et al., 1994; Flemmig
et al., 1995; Felo et al., 1997).
The objective of the present study was to test the
adjunctive effect to toothbrushing of an OI with either
a prototype jet tip or a standard tip in the potential to
3
improve gingival health over a 4-week period. This prototype tip, which is configured with filaments, may help
the user guide the tip along the gingival margin and the
interproximal area. Both OI tips were compared to the
use of dental floss. These treatments were combined
with the use of a regular flat trimmed manual toothbrush
together with a standard dentifrice.
Materials and methods
Study population
One hundred seventy-two subjects (non-dental students)
from different universities and colleges in and around
Amsterdam responded to an e-mail advertisement and
reported for a screening appointment. The volunteers
were informed about the study, first in a recruitment
letter and secondly at the screening. Participation was
not limited by race or gender. Subjects received a written
explanation of the background of the study, its objectives and their involvement. Before screening for their
suitability they were all requested to give their written
informed consent. Subjects were required to fulfill the
following criteria: ≥18 years of age, a minimum of
five evaluable teeth in each quadrant (with no partial
dentures, orthodontic banding or wires); moderate
gingivitis (50% bleeding on marginal probing, Galgut et
al., 1998), an absence of oral lesions and/or periodontal
pockets > 5 mm and/or generalized recession, and the
absence of pregnancy and systemic diseases such as
AIDS, cirrhosis, diabetes, any adverse medical history
or long-term medication, or any physical condition that
limits manual dexterity. All subjects received oral and
written information about the products and purpose
of the study. One hundred eight subjects met the inclusion criteria and were enrolled into the study, which
was conducted in accordance to the ethical principles
that have their origin in the Declaration of Helsinki and
was consistent with Good Clinical Practice guidelines.
Medical Ethics Committee approval was obtained prior
to the start of the study (MEC 09/198 #09.17.1322).
All assessments took place at the Department of Periodontology at ACTA, Amsterdam, The Netherlands in
September and October, 2009.
Study products
Three different interdental products were tested in this
study, one product per group, with 36 subjects enrolled
in each group. All subjects received a standard toothbrush (Oral-B Indicator 35, Procter & Gamble, Cincinnati, OH, USA, Figure 1) and standard fluoride dentifrice
(Everclean, HEMA, Amsterdam, The Netherlands).
In addition, subjects were randomized (see below for
details) into one of three groups for assignment of an
interdental cleaning device:
04/01/2011 11:37:43
4
Journal of the International Academy of Periodontology (2011) 13/1
Group 1 (OIP): OI (DWJ-Waterpik® Ultra Water
Flosser, Fort Collins, CO, USA) with a prototype jet tip
(Figure 2, test group).
Group 2 (OIS): OI (DWJ-Waterpik® Ultra Water
Flosser, Fort Collins, CO, USA) with a standard jet tip
(Figure 3, benchmark control group, Husseini et al., 2008).
Group 3 (DF): standard waxed floss (Johnson &
Johnson, New Brunswick, NJ, USA) (Figure 4, control
group).
Clinical assessment
Clinical parameters were assessed at baseline (S1), week
2 (S2), and week 4 (S3). First gingivitis and then plaque
was scored. All gingivitis assessments were carried out
by the same trained examiner (NLH). All plaque assessments were carried out by a second trained examiner
(CEB). All examinations were carried out under the
same conditions. All teeth were examined for both
indices at six sites per tooth (disto-buccal, mid-buccal,
mesio-buccal, disto-lingual, mid-lingual, mesio-lingual)
except for 3rd molars.
Criteria
Gingivitis was assessed as the primary outcome using
the bleeding on marginal probing index (BOMP) as
described by Van der Weijden et al. (1994a, 1994b) and
Lie et al. (1998). In short, the gingival margin is probed
at an angle of approximately 60° to the longitudinal axis
of the tooth and the absence or presence of bleeding
is scored within 30 seconds of probing on a scale 0 - 2
(0 = no bleeding, 1 = pinprick bleeding, 2 = excessive
bleeding).
Plaque was assessed as a secondary outcome using
the Turesky (1970) modification of the Quigley & Hein
(1962) plaque index (TQHPI) as described in detail by
Figure 2. OIP - oral irrigator with prototype tip Figure 1. Toothbrush - Oral-B indicator 35
Figure 3. OIS - oral irrigator with standard tip
Figure 4. DF - standard waxed dental floss
04/01/2011 11:37:47
5
Flowchart
Screening
Screening
172 subjects
Excluded
64 subjects
Baseline (S1)
Total: 108 subjects
Group 1: 36 subjects
BOMP & TQHPI
Professional instruction
2 Weeks (S2)
Drop-out
2 subjects
Total: 106 subjects
BOMP & TQHPI
Drop-out
2 subjects
4 Weeks (S3)
Total: 104 subjects
BOMP & TQHPI
Statistical
Analyses
(ITT)
Total: 104 subjects
Figure 5. Flowchart
Paraskevas et al. (2007). Briefly, the teeth were dyed using a new cotton swab with fresh disclosing solution
(Mira-2-Ton®; Hager & Werken GmbH & Co. KG.
Duisburg, Germany) for each quadrant in order to disclose the plaque. Subsequently, the absence or presence
of plaque was recorded on a 6-point scale (0-5, 0 = no
plaque, 5 = plaque covering more than two-thirds of
the tooth surface).
Study design
This study was designed as single masked, 3-group parallel, 4-week home use experiment. After meeting the inclu-
sion criteria, completion of a medical questionnaire and
informed consent, subjects returned to the clinic for their
first (baseline) assessment (S1) for both clinical parameters (bleeding on marginal probing and plaque). At the
start of the experiment all subjects received a unique trial
number. Subjects were randomly assigned to one of three
groups according to a randomization list (www.random.
org). The allocation of products was carried out by the
study coordinator, who was responsible for allocation
concealment. All products were distributed in such a way
that blindness of the examiners was assured. At the last
visit (S3) the study coordinator assured blindness of the
04/01/2011 11:37:48
6
examiners by collecting the study products in a separate
room from where the clinical examinations took place.
Subjects were also instructed not to mention anything
to the examiners that could lead to allocation disclosure.
During the 4-week experimental phase OIS and
OIP subjects used the OI once a day in the evening
with lukewarm tap water and were instructed to finish
one container of 500 ml at each occasion. Subjects in
the control group (DF) used standard waxed dental
floss once a day in the evening. At the baseline visit
(S1), immediately following the baseline assessment,
subjects used their allocated product for the first time.
The study coordinator (NAMR) was present to provide
detailed verbal instruction, a demonstration to ensure
correct use, and aid with further personal instruction
when necessary. Subjects in both OI groups were
instructed to use the OI according to the instruction
leaflet provided by the manufacturer. Subjects in the DF
group were instructed to use their product according
to the description of Van der Weijden et al. (2008). All
subjects in each group were instructed to brush twice a
day in their normal manner, once in the morning after
breakfast and once in the evening. In the evening they
subsequently used their assigned product (OI or DF).
All participants were instructed to refrain from using
any other oral hygiene product or device such as toothpicks, interdental brushes, mouthrinses, etc., during the
study period. To check for compliance, subjects were
asked to register the time of use of the products onto
a calendar record chart.
After two weeks (S2), subjects returned to the clinic
for the second clinical assessment for both gingivitis
and plaque. After four weeks (S3), subjects visited the
clinic for their final assessment for both parameters.
Subjects were asked to return all products provided for
this study as well as the calendar record chart. On each
occasion subjects were instructed to brush between 2
and 3 hours prior to their appointments to avoid the
risk of increased bleeding on probing as a result of
toothbrushing (Abbas et al., 1990). The day prior to each
appointment all subjects received an SMS-message as a
reminder with the following text: “Remember that you have
an appointment at ACTA! Note that you need to brush your
teeth 2-3 hours prior to your visit. See you tomorrow! ACTA.”
After the final assessment habitual oral hygiene procedures were resumed.
Data analyses
The unit of analysis was the subject and collected data
were analyzed as intention to treat. The bleeding scores
were used as the main response variable (Galgut et al.,
1998) and plaque scores as secondary response variable.
A priori calculations with an alpha of 0.05, a difference
of 0.0883 (between groups) of the bleeding index with
80% power, based on a pooled SD of 0.13 as derived
from previous studies supported a sample size of 105.
An analysis of covariance (ANCOVA) with S1 as covariate and S3 as dependent variable was performed to
compare groups over time (Heynderickx et al., 2005).
Analyses comparing differences between the test and
control groups at each time point were performed
using non-parametric tests. Explorative analyses were
performed to investigate the origin of the overall differences. P values of < 0.05 were accepted as statistically
significant.
Results
Of 108 subjects who started the trial, four subjects did
not complete the protocol. One chose not to continue
the trial for personal reasons. Another left the country
and moved abroad. Two did not attend the second visit
because of scheduling conflicts. This resulted in a study
population of 104 subjects providing evaluable data
(Figure 5). The study population data on demographics
and pre-study floss habits are presented in Table 1. No
adverse events were reported by any of the subjects who
participated in this study.
Results for bleeding on probing are presented in Table
2. The overall ANCOVA analysis showed a statistically
significant difference between the three groups (p =
0.007). Mean overall reductions after four weeks of use
(S1 to S3) were 0.15 for the OIP group, 0.17 for the OIS
group, and 0.02 for the DF group. The mean bleeding
scores of the three groups did not differ significantly at
baseline. At session 2 the scores decreased for all three
groups. Post testing showed that both the OI groups
provided significantly lower bleeding scores as compared
to the DF group. At session 3 a statistically significant
difference could be detected among the three groups.
Post testing showed that again both the OI groups had
significantly lower bleeding scores as compared to the
DF group. The 95% confidence interval of the difference compared to the DF group at S3 was -0.27 ± -0.04
for the OIP group and -0.28 ± -0.05 for the OIS group.
Results for plaque index are presented in Table 3.
With regard to the plaque scores the overall ANCOVA
analysis showed no statistically significant differences
among the three groups (p = 0.126). Mean overall reductions after four weeks of use (S1 to S3) were -0.09
for the OIP group, 0.06 for the OIS group, and 0.01
for the DF group.
Discussion
Effective brushing remains the most obvious way of
maintaining low levels of plaque and good gingival
health. Gingivitis is known to be associated with the
onset of periodontitis, and although the relationship between these two conditions may not be fully understood,
the importance of maintaining good gingival health and
04/01/2011 11:37:48
7
Table 1. Demographic data and pre-study flossing habits of the study population.
N
Female
Male
Age [range] (SD)
Daily floss users
Weekly floss users
Monthly floss users
Seldom/never floss users
Total
OIP
OIS
DF
104
74
30
21.8 [18-36]
6
16
20
62
34
24
10
21.9 (3.2)
2
7
9
16
34
27
7
21.1 (2.3)
1
4
7
22
36
23
13
22.4 (3.1)
3
5
4
24
OIP, oral irrigation device with prototype jet tip; OIS, oral irrigation device with standard jet
tip; DF, dental floss
Table 2. Mean bleeding index (BOMP) and mean % bleeding scores for all groups at all sessions.
N
Session 1
Session 2
Session 3
OIP - index
%
34
0.82 (0.25)
46 %
0.65 (0.24)
37 %
0.67 (0.26)†
39 %
OIS index
%
34
0.83 (0.23)
46 %
0.61 (0.27)*
34 %
DF - index
%
36
0.86 (0.26)
47 %
0.579
p - value
(Kruskal Wallis)
Relative Reduction
Relative Reduction
S1 – S2
S1 – S3
20 %
15 %
0.66 (0.26)*
38 %
26 %
17 %
0.74 (0.26)
41 %
0.84 (0.30)
47 %
13 %
0%
0.084
0.016
Standard deviation in parentheses. Univariate analyses of covariance with session 1 as covariate and session 3 as dependent variable. (p = 0.007). *Statistically significant difference compared to DF group, p < 0.05 (Mann-Whitney). †Statistically significant difference compared to DF group, p = 0.020 (Mann-Whitney). OIP, oral irrigation device with prototype
jet tip; OIS, oral irrigation device with standard jet tip; DF, dental floss
Table 3. Mean Quigley & Hein plaque scores ± standard
deviation for all groups at all sessions. OIP
OIS
DF
N
Session 1
Session 2
Session 3
34
34
36
1.64 ± 0.43
1.79 ± 0.34
1.60 ± 0.26
1.61 ± 0.34
1.74 ± 0.29
1.51 ± 0.27
1.73 ± 0.37
1.73 ± 0.28
1.59 ± 0.27
Univariate analyses of covariance with session 1 as covariate
and session 3 as dependent variable. (p = 0.126). OIP, oral
irrigation device with prototype jet tip; OIS, oral irrigation
device with standard jet tip; DF, dental floss
preventing periodontitis is well recognised (Van Dyke et
al., 1999). As the interproximal area is known as where
the onset of gingival inflammation is likely to occur,
the reason for interproximal plaque control seems clear.
Although it is universally recognized that interproximal
cleansing is essential for controlling periodontal disease
(Löe, 1979), many people have difficulty accomplishing
this with traditional dental floss (Asadoorian, 2006).
Thus, compliance with floss is low (Warren and Chater,
1996), and various adjuncts for interdental cleaning have
been studied. Dental floss, toothpicks, woodsticks and
interdental brushes have all been recommended for
this purpose.
The present study focussed on the ability to reduce
gingival inflammation in a population of young individuals with moderate gingivitis using an OI. The OI works
through the direct application of a pulsed stream of
water or other solution. A study duration of four weeks
was chosen to monitor the changes in the bleeding index,
which meets the ADA guidelines on OI’s for studies assessing the effects of adjunctive therapies on reduction
of gingivitis (ADA, 2008). Studies of longer duration
will more clearly demonstrate the clinical benefit that
subjects will obtain from this product.
The efficacy of use of floss on the bleeding index
was considered inconclusive in a systematic review by
Berchier et al. (2008). The results of the present study are
04/01/2011 11:37:48
8
in support of this statement. In contrast, in the present
study both OI groups did show statistically significant
improvements after four weeks. At the end of the study
both OI groups show a significant 15 - 17% reduction
of the bleeding index as compared to baseline. For the
DF group this difference was not observed. Comparisons among groups showed a significant difference at
four weeks between the DF group and both OI groups.
The absolute difference of 8% and 9% at four weeks
for both OI groups as compared to the floss group reveals a relative effect of 17% (OIP) and 19% (OIS). In
consideration of the ADA guidelines for oral irrigators,
the results of the present study do not reach the lower
limit of superiority of 20% as estimated proportionate
reduction related to clinical relevance as compared to
standard oral hygiene procedures (ADA, 2008). However, the ADA also has guidelines on adjunctive dental
therapies (ADA, 1997). In those guidelines a lower limit
of 15% is applied. The study outcomes of the present
study do comply with this guideline, indicating a potential beneficial effect for the OI.
With respect to plaque, the DF group started with a
markedly lower score as compared to both OI groups.
All subjects were instructed to brush 2-3 hours prior
to examination, to reduce the risk of greater bleeding
tendency (Abbas et al., 1990). As the difference in PI
scores was consistent throughout the study and was not
reflected in bleeding index scores, it seems that subjects
who were randomly allocated to the floss group coincidently performed better instant plaque removal by
brushing at visit days. In a study carried out by Galgut
et al. (2000) the effect of unevenly distributed baseline
data is discussed and it was concluded that this might
not influence the results and the conclusions drawn.
Historically, plaque reductions are considered a prerequisite for an oral hygiene device to be considered
effective (Löe et al., 1965). A recent systematic review
(Husseini et al., 2008) reported no statistically significant
reduction in plaque when the OI was used as an adjunct
to toothbrushing when compared to toothbrushing only.
Despite a lack of effect on plaque index, the studies that
were included in this review did find a significant effect
on bleeding and gingival indices. The mechanisms of
actions underlying these clinical changes for the bleeding
index in the absence of a clear effect on plaque are not
understood, although different hypotheses have been
put forward (Husseini et al., 2008). One of the hypotheses is that supragingival irrigation alters the population of key pathogens, reducing gingival inflammation
(Flemming et al., 1995). Another hypothesis is that the
water-pulsation may alter the specific host-microbial
interaction in the subgingival environment (Chaves et
al., 1994). There is also the possibility that the beneficial
action of an OI is at least partly because of the removal
of loosely adherent soft deposits interfering with plaque
maturation and stimulation of the immune response
(Frascella et al., 2000). Other explanations could be a
mechanical stimulation of the gingiva or a combination of the above-mentioned factors (Frascella et al.,
2000; Flemmig et al., 1990). Furthermore, irrigation may
reduce the thickness of the plaque, which may not be
easily detectable using 2-dimensional scoring systems
(Jolkovsky et al., 1990).
The absence of an effect for DF at four weeks may
also seem surprising. A transient effect of 6% BI reduction was observed at two weeks. However, a recent
systematic review supports this finding that dental floss
has no significant effect on plaque or bleeding indices
(Berchier et al., 2008). The small effect observed at two
weeks is most likely the result of a novelty or Hawthorne
effect. The Hawthorne effect is a reaction of subjects to
the realization they are in a study and are being observed
(Adair et al., 1984). The novelty effect and Hawthorne
effect can be considered as certain placebo effects. The
impact of a placebo effect should not be underestimated
(Finniss et al., 2010). In a study by Feil et al. (2002), the
Hawthorne effect was intentionally used and shown to
improve oral health. The novelty effect is something
that could have influenced all groups within this model.
Subjects were pre-selected on having “no experience”
with an OI, whereas only six out of the 104 were regular
flossers (Table 1). The rebound that is observed from
the 2-week to the 4-week follow-up is, however, most
evident in the floss users. With respect to the Hawthorne
effect, this is probably not only present in the DF group
but also in both OI groups, as subjects were selected on
having a bleeding index of > 50%. However at session
1 the bleeding index was already reduced to 46-47%
for all three groups. This indicates that subjects already
acted as if they were entered into the protocol before
the first assessment of the primary response variable.
The results of the present study add to the existing
data and clearly show a reduction in inflammation from
using an OI. Interestingly, the reduction in bleeding
could not be linked to plaque removal. This is similar
to data presented by Flemmig et al. (1990) showing no
change in plaque scores for either the brushing group
or the brushing and irrigation group from baseline to 6
months, but a significant difference in bleeding on probing and gingival index scores in favor of the irrigation
group. Likewise, Flemmig et al. (1995) reported that the
water irrigation group was significantly better at reducing
bleeding on probing and gingival index scores compared
to the regular oral hygiene group at six months. Also
in this study there were no statistically significant differences detected in plaque scores among the groups.
Chaves et al. (1994) found similar reductions in plaque
scores for water irrigation compared to toothbrushing alone, and a significant difference for bleeding on
probing in favor of the irrigation group at six months.
04/01/2011 11:37:48
These studies support the present data in finding no
correlation between reduction of plaque biofilm and
inflammation in 3-6 months.
Conclusion
There is a long-standing, well-documented body of
evidence supporting the use of an oral irrigator. An oral
irrigator is at least as effective as dental floss for reducing
gingival bleeding and gingivitis. When combined with
manual toothbrushing the use of an oral irrigator, either
with a prototype or standard jet tip, is significantly more
effective in reducing gingival bleeding scores as compared to the use of dental floss, as determined within
the limits of this 4-week study design.
Acknowledgment
The study was performed in commission of ACTA
Research BV.
Waterpik Inc, Fort Collins, CO, USA initiated the
study project and provided study products. ACTA
Research BV received financial support for their commitment to appoint this project to the Department of
Periodontology of ACTA.
D.M. Lyle is the director of professional and clinical affairs for Water Pik, Inc. The authors employed by
ACTA declare that they have no conflict of interest.
References
ADA. Acceptance program guidelines: Adjunctive dental therapies
for the reduction of plaque and gingivitis. American Dental Association Council on Scientific Affairs, September 1997.
ADA. Acceptance program guidelines: Oral irrigating devices.
American Dental Association Council on Scientific Affairs, 2008.
Adair J.G. The Hawthorne effect: a reconsideration of the methodological artifact. Journal of Applied Psychology 1984; 69:334-345.
Al-Mubarak, S., Ciancio, S., Aljada, A. et al. Comparative evaluation of adjunctive oral irrigation in diabetes. Journal of Clinical
Periodontology 2002; 29:295-300.
Asadoorian, J. Flossing. Canadian dental hygienists association position statement. Canadian Journal of Dental Hygiene 2006; 40:1-10.
Abbas, F., Voss, S., Nijboer, A., Hart, A.A. and Van der Velden, U.
The effect of mechanical oral hygiene procedures on bleeding
on probing. Journal of Clinical Periodontology 1990; 17:199-203.
Barnes, C.M., Russell, C.M., Reinhardt, R.A., Payne, J.B. and Lyle,
D.M. Comparison of irrigation to floss as an adjunct to tooth
brushing: effect on bleeding, gingivitis, and supragingival plaque.
Journal of Clinical Dentistry 2005; 16:71-77.
Berchier, C.E., Slot, D.E., Haps, S. and Van der Weijden, G.A. The
efficacy of dental floss in addition to a toothbrush on plaque
and parameters of gingival inflammation: a systematic review.
International Journal of Dental Hygiene 2008; 6:265-279.
Brown, L.J. and Löe, H. Prevalence, extent, severity and progression
of periodontal disease. Periodontology 2000 1993; 2:57-71.
Brownstein, C.N., Briggs, S.D., Schweitzer, K.L., Briner, W.W., and Kornman, K.S. Irrigation with chlorhexidine to resolve naturally occurring gingivitis. Journal of Clinical Periodontology 1990; 17:588-593.
Burch, J.B., Lanese, R. and Ngam, P. A two-month study of the
effects of oral irrigation and automatic toothbrush use in an
adult orthodontic population with fixed appliances. American
Journal of Orthodontics and Dentofacial Orthopedics 1994; 106:121-126.
9
Chaves, E.S., Kornman, K.S, Manwell, M.A., Jones, A.A., Newbold,
D.A. and Wood, R.C. Mechanism of irrigation effects on gingivitis. Journal of Periodontology 1994; 65:1016-1021.
Ciancio, S.G., Mather, M.L., Zambon, J.J. and Reynolds, H.S. Effect
of chemotherapeutic agent delivered by an oral irrigation device
on plaque, gingivitis, and subgingival microflora. Journal of Periodontology 1989; 60:310-315.
Cobb, C.M., Rodgers, R.L. and Killoy, W.J. Ultrastructural examination of human periodontal pockets following the use of an oral
irrigation device in vivo. Journal of Periodontology 1988; 59:155-163.
Costerton J.W., Lewandowski Z., DeBeer D., Caldwell, D., Korber,
D. and James, G. Biofilms, the customized microniche. Journal
of Bacteriology 1994; 176:2137-2142.
Cutler, C.W., Stanford, T.W., Abraham, C., Cederberg, R.A., Boardman, T.J. and Ross, C. Clinical benefits of oral irrigation for
periodontitis are related to reduction of pro-inflammatory
cytokine levels and plaque. Journal of Clinical Periodontology 2000;
27:134-143.
Douglass, C.W. and Fox, C.H. (1993) Cross-sectional studies in
periodontal disease: current status and implications for dental
practice. Advances in Dental Research 1993; 7:25-31.
Drisko, C.L., White, C.L., Killoy, W.J. and Mayberry, W.E. Comparison of dark-field microscopy and a flagella stain for monitoring
the effect of a Water Pik on bacterial motility. Journal of Periodontology 1987; 58:381-386.
Feil, P.H., Grauer, J.S., Gadbury-Amyot, C.C., Kula, K. and McCunniff, M.D. Intentional use of the Hawthorne effect to improve
oral hygiene compliance in orthodontic patients. Journal of Dental
Education 2002; 66:1129-1135.
Felo, A., Shibly, O., Ciancio, S.G., Lauciello, F.R. and Ho, A. Effects
of subgingival chlorhexidine irrigation on peri-implant maintenance. American Journal of Dentistry 1997; 10:107-110.
Fine, J.B., Harper, D.S., Gordon, J.M., Hovliaras, C.A. and Charles,
C.H. Journal of Periodontology 1994; 65:30-36.
Finniss, D.G., Kaptchuk, T.J., Miller, F. and Benedetti, F. Biological,
clinical, and ethical advances of placebo effects. Lancet 2010;
375:686-695.
Flemmig, T.F., Newman, M.G., Doherty, F.M., Grossman, E.,
Meckel, A.H. and Bakdash, M.B. Supragingival irrigation with
0.06% chlorhexidine in naturally occurring gingivitis. I. 6 month
clinical observations. Journal of Periodontology 1990; 61:112-117.
Flemmig, T.F., Epp, B., Funkenhauser, Z., et al. Adjunctive supragingival irrigation with acetylsalicylic acid in periodontal supportive
therapy. Journal of Clinical Periodontology 1995; 22:427-433.
Frascella J.A., Fernández P., Gilbert R.D. and Cugini M. A randomized, clinical evaluation of the safety and efficacy of a novel
oral irrigator. Am J Dent 2000; 13:55–58.
Galgut, P.N. and O’Mullane, D. Statistical analysis of data derived
from clinical variables of plaque and gingivitis. Journal of Clinical
Galgut, P.N. Management of data used in clinical trials which is
unevenly distributed at baseline. Current Medical Research Opinion
2000: 16:46-55.
Gorur, A., Lyle, D.M., Schaudinn, C. and Costerton, J.W. Biofilm
removal with a dental water jet. Compendium of Continuing Education in Dentistry 2009; 30:1-6.
Heynderickx, I. and Engel, J. Statistical methods for testing plaque
removal efficacy in clinical trials. Journal of Clinical Periodontology
2005; 32:677-683.
Husseini, A., Slot, D.E. and Van der Weijden, G.A. The efficacy of
oral irrigation in addition to a toothbrush on plaque and the
clinical parameters of periodontal inflammation: a systematic
review. International Journal of Dental Hygiene 2008; 6:304-314.
Jepsen, S. The role of manual toothbrushes in effective plaque control: Advantages and limitations. In: Lang, N.P., Attström, R. and
Löe, H. (Eds): Proceedings of the European Workshop on Mechanical
Plaque Control. Berlin: Quintessenz Verlag 1998, 121-137.
04/01/2011 11:37:48
10
Jolkovsky, D.L., Waki, M.Y., Newman, M.G., et al. Clinical and
microbiological effects of subgingival and gingival marginal
irrigation with chlorhexidine gluconate. Journal of Periodontology
1990; 61:663-669.
Lie, M.A., Timmerman, M.F., Van der Velden, U. and Van der Weijden, G.A. Evaluation of 2 methods to assess gingival bleeding in
smokers and non-smokers in natural and experimental gingivitis.
Journal of Clinical Periodontology 1998; 25:695-700.
Löe, H., Theilade, E. and Jensen, S.B. Experimental gingivitis in man.
Journal of Periodontology 1965; 36:177-187.
Löe, H. Mechanical and chemical control of dental plaque. Journal
of Clinical Periodontology 1979; 6:32-36.
Lobene, R.R. The effect of a pulsed water pressure cleansing device
on oral health. Journal of Periodontology 1969; 40:667-670.
Marsh, P.D. and Bradshaw, D.J. Dental plaque as a biofilm. Journal
of Industrial Microbiology 1995; 15:169-175.
Newman, M.G., Cattabriga, M., Etienne, D., et al. Effectiveness of
adjunctive irrigation in early periodontitis: multi-center evaluation. Journal of Periodontology 1994; 65:224-229.
Quigley, G.A. and Hein, J.W. Comparative cleansing efficiency of
manual and power brushing. Journal of the American Dental Association 1962; 65:26-29.
Paraskevas, S, Rosema, N.A., Versteeg, P., Timmerman, M.F., van der
Velden, U. and Van der Weijden G.A. The additional effect of a
dentifrice on the instant efficacy of toothbrushing: a crossover
study. Journal of Periodontology 2007; 78:1011-1016.
Research, Science and Therapy Committee, American Academy of
Periodontology Position Paper. The role of supra- and subgingival irrigation in the treatment of periodontal diseases. Journal
of Periodontology 2005; 76:2015-2027.
Research, Science and Therapy Committee, American Academy of
Periodontology Position Paper. Treatment of plaque-induced
gingivitis, chronic periodontitis, and other clinical conditions.
Sharma, N.C., Lyle, D.M., Qaqish, J.G., Galustians, J. and Schuller, R. Effect of a dental water jet with orthodontic tip on plaque and bleeding
in adolescent patients with fixed orthodontic appliances. American
Journal of Orthodontics and Dentofacial Orthopedics 2008; 133:565-571.
Slot, D.E., Dörfer, C.E. and Van der Weijden GA. The efficacy of
dental floss in addition to a toothbrush on plaque and parameters
of gingival inflammation: a systematic review. International Journal
of Dental Hygiene 2008; 6:265-279.
Turesky, S., Gilmore, N.D. and Glickman, L. Reduced formation
by chloromethyl analogue of vitamin C. Journal of Periodontology
1970; 41:41-43.
Van Dyke, T.E., Offenbacher, S., Pihlstrom, B., Putt, M.S. and
Trummel, C. What is gingivitis? Current understanding of prevention, treatment, measurement, pathogenesis and relation to
periodontitis. Journal of the International Academy of Periodontology
1999; 1:3-15.
Van der Weijden, G.A., Timmerman, M.F., Nijboer, A., Lie, M.A.
and Van der Velden, U. A comparative study of electric toothbrushes for the effectiveness of plaque removal in relation to
toothbrushing duration. Timer study. Journal of Clinical Periodontology 1993; 20:476-481.
Van der Weijden, G.A., Timmerman, M.F., Saxton, C.A., Russell, J.I.,
Huntington, E. and Van der Velden, U. Intra-/inter-examiner
reproducibility study of gingival bleeding. Journal of Periodontal
Research 1994a; 29:236-241.
Van der Weijden, G.A., Timmerman, M.F., Reijerse, E., Nijboer, A.
and Van der Velden, U. Comparison of different approaches to
assess bleeding on probing as indicators of gingivitis. Journal of
Clinical Periodontology 1994b; 21:589-594.
Van der Weijden, G.A., Echevaria, J.J., Sanz, M. and Lindhe J. Mechanical supragingival plaque control. In: Lindhe, J., Lang, N.P.
and Karring, T. (Eds): Clinical Periodontology and Implant Dentistry,
5th edition. Munskgaard. Wiley-Blackwell, 2008.
Walsh, T.F., Glenwright, H.D. and Hull, P.S. Clinical effects of
pulsed oral irrigation with 0.02% chlorhexidine digluconate in
patients with adult periodontitis. Journal of Clinical Periodontology
1992; 19:245-248.
Warren, P.R. and Chater, B.V. An overview of established interdental
cleaning methods. Journal of Clinical Dentistry 1996; 7:65-69.
04/01/2011 11:37:48
Additive or Synergistic Antimicrobial Effects
of Amoxicillin and Metronidazole on Whole
Plaque Samples: A Preliminary Report
Clemens Walter1,2, Eva M. Kulik3, Roland Weiger1, Nicola U.
Zitzmann1 and Tuomas Waltimo3
Department of Periodontology, Endodontology and Cariology,
School of Dentistry, University Basel, Switzerland; 2Department of
Oral Surgery, School of Dentistry, University of Birmingham, United
Kingdom; 3Institute for Preventive Dentistry and Oral Microbiology,
School of Dentistry, University Basel, Switzerland
1
Abstract
Objective: In vitro data on the susceptibility of oral bacteria to the combination of metronidazole and amoxicillin is limited. The aim of this preliminary study was to determine
the susceptibility of whole subgingival plaque samples to amoxicillin and metronidazole
and to their combination. Methods: Prior to any treatment procedures subgingival
plaque samples from patients with severe generalized periodontitis were taken. Appropriate dilutions were plated on Columbia blood agar supplemented with the following
agents: 3 µg/mL amoxicillin, 8 µg/mL amoxicillin, 8 µg/mL metronidazole, 16 µg/mL
metronidazole, 3 µg/mL amoxicillin plus 8 µg/mL metronidazole or 8 µg/mL amoxicillin plus 16 µg/mL metronidazole. All plates were incubated anaerobically at 36°C for
14 days and the colony forming units (CFU) were determined. Results: Both applied
metronidazole concentrations were able to decrease the CFU counts by approximately
one order of magnitude in a log10 scale. Amoxicillin 3 µg/mL revealed a reduction of
2.4 log10 CFU, whereas 50% of the samples did not grow on the plates supplemented
with 8 µg/mL of amoxicillin. There was no anaerobic bacterial growth on agar plates
supplemented with the combination of amoxicillin and metronidazole even at the lower
antibiotic concentrations. Conclusion: Susceptibility screening of subgingival samples to
metronidazole and amoxicillin and to their combination seems to offer a rational basis
for the selection of adjunctive antibiotic therapy
Key words: Antibiotics, synergistic effect, aggressive periodontitis, metronidazole,
amoxicillin
Introduction
Periodontal diseases are multifactorial biofilm-associated
infections. A distinct differentiation between aggressive
and chronic forms is difficult (Meyer et al., 2004), even
on the basis of microbiological findings (Mombelli et al.,
2002; Ximenez-Fyvie et al., 2006; Schacher et al., 2007).
Hence, the diagnosis of “aggressive periodontitis” is
primarily based on clinical and radiological characteristics, on patient’s age, and on findings derived during
clinical follow-up. Due to the infection-induced nature
of periodontal diseases, antimicrobial therapies based
on microbiological examinations may improve the treat-
Correspondence to: Prof. Dr. Nicola U. Zitzmann, Department of Periodontology, Endodontology and Cariology,
School of Dentistry, University Basel, Hebelstrasse 3, CH4056 Basel, Switzerland. Email: [email protected]
ment outcome of advanced and/or aggressive forms
of periodontitis.
First attempts to control periodontal diseases with
the adjunctive use of antibiotics included systemic administration of tetracyclines, amoxicillin with or without
clavulanic acid, clindamycin and metronidazole (Listgarten et al., 1978; Lekovic et al., 1983; Gordon et al., 1985;
Magnusson et al., 1989). Another adjunctive treatment
approach was topical administration of various antibiotics or antiseptics (Lindhe et al., 1979; Needleman and
Watts, 1989; Stabholz et al., 2000). Two decades ago,
the combination of metronidazole and amoxicillin - so
called “van Winkelhoff-Cocktail” - was introduced as
an adjunctive systemic therapy for periodontitis treatment (Van Winkelhoff et al., 1989). This regimen was
specifically designed for treatment of diseases associated
with Aggregatibacter (Actinobaccillus) actinomycetemcomitans,
for which a synergistic in vitro effect between the two
substances or their metabolites has been reported
JIAP 10-004 Zitzmann.indd 11
04/01/2011 11:39:02
12
(Pavicic et al., 1994a; Pavicic et al., 1994b). Clinical studies on aggressive forms of periodontitis have revealed
improved outcomes within observation periods up to
five years, provided that the adjunctive treatment with
the combination of amoxicillin and metronidazole was
strictly combined with mechanical biofilm removal
(Buchmann et al., 2002; Guerrero et al., 2005; Kaner et al.,
2007a; Kaner et al., 2007b). Moreover, improved clinical
advantages of this regimen were found in a placebocontrolled study comparing the antibiotic combination
to the agents alone, again as adjunctive to mechanical,
non-surgical periodontal treatment (Rooney et al., 2002).
In this report, the treatment outcomes of subjects with
advanced chronic periodontal disease were independent
from the initial microbiological findings. Recently, this
strategy of combining amoxicillin and metronidazole
was used for the treatment of generalized “aggressive
periodontitis” without targeting against specific microorganisms (Guerrero et al., 2005).
Whenever antibiotics are administrated as an adjunctive periodontal treatment, existing or possibly developing resistance of the associated microflora should be
carefully considered. In vitro findings have suggested that
there are remarkable differences in resistance profiles of
certain oral bacterial species (Van Winkelhoff et al., 2005;
Lakhssassi et al., 2005). Recent findings in microbiological susceptibility testing have indicated the rationale of
the examination of mixed microbial cultures instead of,
or in addition to, the individual disease-associated strains
(Karbach et al., 2007). Such in vitro data about bacterial
susceptibility to the combination of amoxicillin and
metronidazole is hitherto scarce.
The aim of the present preliminary study was to
determine the susceptibility of whole subgingival plaque
samples to amoxicillin and metronidazole and to their
combination.
Materials and methods
Patients and sampling
Four generally healthy patients with severe generalized
chronic or aggressive periodontitis were recruited from
the pool of patients from the Department of Periodontology, Endodontology and Cariology at the School
of Dental Medicine, University of Basel, Switzerland.
Diagnosis was based on clinical and radiographic findings, related to age and the severity of destruction (Table
1, Figure 1a-b, Armitage, 1999). Clinical measurements
of probing pocket depth and attachment level were
performed with the probe PCPUNC-15 (Hu-Friedy,
Chicago, IL, USA). All recruited patients (one female
and three males with a mean age of 40.8 years) were current or former heavy smokers and had neither received
any earlier periodontal treatment nor systemic or topical
antibiotics one year prior to the sampling. The female
patient was not pregnant.
Subgingival plaque samples were taken for antibiotic
resistance analysis. At least the two deepest periodontal
pockets with bleeding on probing were selected for
microbiological sampling. Supragingival plaque was
removed, the sampling site was isolated using cotton
rolls and gently dried with air. A sterile paper point was
inserted to the bottom of the pocket, left in place for
20 s and placed in 0.5 ml of thioglycolate broth (bioMérieux, Genf, Switzerland; Casas et al., 2007).
Microbiological procedures
Immediately after sampling, pooled paper points were
vortexed for one minute and serially diluted in thioglycolate broth. For the determination of the total anaerobic
bacterial count, 100 mL of the dilutions were plated on
Columbia blood agar plates (Columbia Agar Base [BBL
Becton Dickinson, Allschwil, Switzerland] enriched
with 4 mg/L hemin, 1 mg/L menadione, and 50 ml/L
human blood).
For quantification of the proportion of microorganisms resistant to either amoxicillin and/or metronidazole, Columbia blood agar plates supplemented with the
following concentrations of the respective antimicrobial
agent were used: 3 mg/mL amoxicillin (Fluka, Buchs,
Switzerland), 8 mg/mL amoxicillin, 8 mg/mL metronidazole (Fluka), 16 mg/mL metronidazole, 3 mg/mL
amoxicillin plus 8 mg/mL metronidazole or 8 mg/mL
amoxicillin plus 16 mg/mL metronidazole. The concentrations of the antibiotics were adopted from van
Winkelhoff et al. (2000) and/or the Clinical Laboratory
and Standards Institute (2007). All plates were incubated
anaerobically (10% CO2, 10% H2, 80% N2) at 36°C
for 14 days and the colony forming units (CFUs) were
determined.
Results
Microbial findings
Microbiological data are presented in Table 2. The
total anaerobic plaque count (CFU) ranged from 3.1
x 106 to 7.2 x 107 among the plaque samples, and the
percentage of black-pigmented bacteria ranged from
40 to 80%. All samples showed a decrease of bacterial growth on agar by approximately 1 log with both
concentrations of the antibiotic agent (8 mg/mL and
16 mg/mL). All agar plates supplemented with 3 mg/
mL amoxicillin showed a reduced bacterial growth by
log 2.4, whereas two out of four samples revealed no
growth on the plates supplemented with 8 mg/mL of
amoxicillin (Table 2). On agar plates supplemented with
the combination of amoxicillin and metronidazole, no
anaerobic bacterial growth was detected even at lower
antibiotic concentrations.
04/01/2011 11:39:02
Additive and/or synergistic in vitro effect of antibiotics
13
Table 1. Profile of study patients and clinical characteristics.
Patient
Age Periodontal
diagnosis
Smoking status
Number of
teeth
Number of sites with PPD
Number of
≥ 6 mm
sites with BOP+
1
45
GAgP
Former smoker
30 pack years
29
165
174
2
32
GAgP
Current smoker
15 pack years
29
92
133
3
38
GAgP
Current smoker
17 pack years
25
69
96
4
48
GChP
Current smoker
30 pack years
27
25
46
BOP, bleeding on probing; GAgP, generalized aggressive periodontitis; GChP, generalized chronic periodontitis
Figure 1a.
Figure 1b.
Figure 1. Patient N° 2 was diagnosed with generalized aggressive periodontitis due to extensive bone loss at the
age of 32 years. a) Clinical intraoral photographs; b) Full-mouth periapical radiographs
Table 2. Microbiological characteristics and results of the antibiotic susceptibility analyses.
Bacterial growth on Bacterial growth on agar plates supplemented with different concentrations of metronidazole
or amoxicillin
agar plates
(control)
Patient
1
2
3
4
CFU
% BPB
4.0 x 107
1.0 x 107
3.1 x 106
7.2 x 107
40
50
40
80
CFU
CFU
CFU
CFU
CFU
CFU
amoxicillin amoxicillin metronida- metronida- amoxicillin 3 mg/mL amoxicillin 8 mg/mL
+ metronidazole
+metronidazole
zole
zole
8 mg/mL
3 mg/mL
16 mg/mL
8 mg/mL
16 mg/mL
8 mg/mL
9.0 x 104
8.0 x 103
8.4 x 104
4.0 x 105
1.0 x 104
3.0 x 105
6.0 x 106
6.0 x 105
6.0 x 105
1.3 x 106
1.5 x 107
6.0 x 105
1.3 x 106
1.5 x 106
-
-
BPB, black-pigmented bacteria; CFU, colony forming units
04/01/2011 11:39:04
14
Discussion
The present preliminary study using subgingival plaque
samples demonstrated reduced bacterial growth in the
presence of low concentrations of metronidazole or
amoxicillin, while higher amoxicillin concentrations
inhibited bacterial growth in two out of four samples.
Interestingly, the combination of metronidazole and
amoxicillin was effective against microorganisms in all
subgingival plaque samples at lower antibiotic concentrations. This in vitro observation suggests an additive
or synergistic mode of action for these agents, which
is likely to be beneficial for infection control, as demonstrated by recent clinical studies (van Winkelhoff et
al., 1989; Buchmann et al., 2002; Rooney et al., 2002;
Guerrero et al., 2005; Kaner et al., 2007a; Kaner et al.,
2007b). It may be hypothesized that the targeted use of
this additive/synergistic effect, which is either based on
growth inhibition or on bacteriocidal effects, may offer
a strategy against the development and/or the control
of resistant strains.
The introduced method testing microbial susceptibility to a frequently administrated combination of
antibiotics is a novel approach, which enlightens the
capacity of additive and/or synergistic effects between
the two substances. A synergistic effect of two antibiotics needs to be evaluated on a species level, and
was documented for Aggregatibacter actinomycetemcomitans
(Pavicic et al., 1994a; Pavicic et al., 1994b). The authors
suggested a higher rate of metronidazole uptake by
bacterial cells simultaneously incubated with amoxicillin. Resistance of anaerobic bacteria to metronidazole
hardly ever occurred (Seifert and Dalhoff, 2010). In
the current material, bacterial growth was detected in
all four subgingival plaque samples, which is indicative
of metronidazole-resistant strains and emphasizes the
need for susceptibility testing in selected patients with
infections involving anaerobic bacteria. The results of
the current study should be, however, interpreted with
caution due to the limited number of subjects included,
and the lack of specific bacterial strain characterisation.
However, the mixed subgingival plaque samples used
here represented the expected general characteristics
in terms of relative proportions of back-pigmented
anaerobes in the total culturable flora.
This preliminary study was restricted to current
or former heavy smokers, who have an increased risk
for the onset and progression of periodontal diseases
(Warnakulasuriya et al., 2010). Cigarette smoking is likely
to affect the composition of the oral microflora due to
a decrease in oxygen tension in periodontal pockets,
and may promotes a selection of anaerobic bacteria
(Hanioka et al., 2000). However, the literature has been
indecisive as to whether a specific smoking-associated
microbial profile exists (van Winkelhoff et al., 2001; van
der Velden et al., 2003). Interestingly, recent evidence
from a randomized controlled trial suggests a benefit
of adjunctive antimicrobial therapy with metronidazole
and amoxicillin in the non-surgical periodontal treatment of smokers with chronic periodontitis (Matarazzo
et al., 2008).
The culture technique used in the current investigation may have some shortcomings: (i) restricted
to growth of viable bacteria, (ii) strict sampling and
transport conditions essential, (iii) specific laboratory
equipment and experienced personnel required for
bacterial culturing, (iv) time needed for bacterial growth
on appropriate media, (v) specific pathogens in the
subgingival plaque may not be detected. However, the
main advantage of the technique used is the probability
of an analysis of bacterial resistance against the combination of antibiotics, in particular against amoxicillin
and metronidazole. The diversity of the oral microflora,
reaching up to 700 different bacterial species (Kazor et
al., 2003), makes it impossible to analyze every single
bacterial strain regarding a genetic profile encoding for
antibiotic resistance. In addition, the molecular mechanisms of bacterial resistance to antibiotics are quite far
from being completely understood. Therefore, the antibiotic susceptibility of a subgingival plaque sample or
of putative periodontal pathogens needs to be analyzed
by conventional culture techniques (Armitage, 2003).
A major concern of the presented approach is the
natural biofilm association of the subgingival bacterial
samples analysed. A biofilm is a difficult therapeutic
target because of its three-dimensional structure, which
protects the bacteria from the host response as well as
from antimicrobial agents (Socransky and Haffajee,
2002; Eick and Pfister, 2004). The methodology of
the present report allowed the interactions between
culturable microorganisms, but no attempt was made
to mimic other characteristics of the subgingival plaque.
Different results may be expected when a biofilm of
mixed microbial samples is formed on an appropriate
substrate prior to their susceptibility testing. However,
such an approach is currently not available. The chosen
methodology aims to provide an approach for clinically
relevant susceptibility testing.
According to the contemporary understanding of
the pathogenesis, periodontal diseases are caused by
an opportunistic infection with a conglomerate of
potentially periopathogenic microorganisms organized
in the subgingival biofilm. A number of different test
methods and procedures are available for qualitative
and quantitative microbiological diagnostics of putative
periopathogens. However, the pathogenic potential of
a certain putative periodontal pathogen against the host
can hitherto not be determined. Moreover, major individual differences in the immune response are caused
by a number of acquired or genetic factors. Although
specific bacteria have a periopathogenic potential or
04/01/2011 11:39:05
Additive and/or synergistic in vitro effect of antibiotics
may initiate periodontal inflammation, it is still difficult
to determine the microbiota responsible for the onset
and progression of disease in the individual subject.
Thus, in the diagnosis and therapy of periodontal diseases, microbiological identification and susceptibility
testing of single disease-associated strains may be of
limited value (Mombelli et al., 2002; Sanz et al., 2004).
Instead or in addition to the conventional approach of
microbiological diagnostics, susceptibility testing of the
entire subgingival plaque sample may offer additional
valuable information for the choice of the antibiotic to
be administered adjunctively.
Improved therapy outcomes indicate that patients
with periodontal diseases - particularly those with highly
destructive forms (aggressive and/or advanced) - may
profit from an adjunctive antibiotic therapy using amoxicillin and metronidazole (Guerrero et al., 2005; Kaner et
al., 2007a). However, due to the increased use of antibiotics and the alarming development of resistant strains,
antibiotics should be administered with care, and testing the susceptibility of a given individual’s microflora
may have an increasing importance (Walker, 1996; Van
Winkelhoff et al. 2005; Lakhssassi et al., 2005; Walter
and Weiger, 2006). Therefore, microbial testing can not
be recommended for routine dental practise. However,
some patients, in particular those in need of adjunctive
antimicrobial therapy, may profit from the information
about potential therapeutic targets (Armitage, 2003).
Susceptibility testing of whole subgingival samples to
metronidazole and amoxicillin and to their combination
seems to offer a rational diagnostic tool to the selection
of adjunctive antibiotic therapy. In the event of an unfavorable response, i.e. bacterial growth on agar plates
supplemented with amoxicillin and metronidazole,
another antibiotic has to be tested and subsequently
applied for adjunctive antimicrobial therapy.
The current report about susceptibility analyses of
subgingival plaque samples was initiated as a proof-ofprinciple study. The microbial results derived from the
audit of four cases may indicate a potential benefit for
further analysis in a larger clinical microbiological trial.
Acknowledgements
We gratefully acknowledge the technical assistance of
Mrs. Krystyna Lenkeit (Dental School, University Basel,
Switzerland) and the constructive criticism of Prof. em.
Jürg Meyer (Dental School, University Basel, Switzerland). There is no conflict of interest.
References
Armitage, G. C. Development of a classification system for periodontal diseases and conditions. Annuals of Periodontology 1999; 4:1-6.
Armitage, G. C. Diagnosis of periodontal diseases. Journal of Periodontology 2003; 74:1237-1247.
Buchmann, R., Nunn, M. E., Van Dyke, T. E. and Lange, D. E. Aggressive periodontitis: 5-year follow-up of treatment. Journal of
15
Casas, A., Herrera, D., Martin-Carnes, J., Gonzalez, I., O’Connor,
A. and Sanz, M. Influence of sampling strategy on microbiologic results before and after periodontal treatment. Journal of
Clinical and Laboratory Standards Institute Methods for antimicrobial susceptibility testing of anaerobic bacteria; approved
standard M11-A7. CLSI, Payne, WA, USA. 2007.
Eick, S. and Pfister, W. Efficacy of antibiotics against periodontopathogenic bacteria within epithelial cells: an in vitro study.
Gordon, J., Walker, C., Lamster, I. et al. Efficacy of clindamycin
hydrochloride in refractory periodontitis. 12-month results.
Guerrero, A., Griffiths, G. S., Nibali, L. et al. Adjunctive benefits of
systemic amoxicillin and metronidazole in non-surgical treatment of generalized aggressive periodontitis: a randomized
placebo-controlled clinical trial. Journal of Clinical Periodontology
2005; 32:1096-1107.
Hanioka, T., Tanaka, M., Takaya, K., Matsumori, Y. and Shizukuishi,
S. Pocket oxygen tension in smokers and non-smokers with
periodontal disease. Journal of Periodontology 2000; 71:550-554.
Kaner, D., Christan, C., Dietrich, T., Bernimoulin, J. P., Kleber, B.
M. and Friedmann, A. Timing affects the clinical outcome of
adjunctive systemic antibiotic therapy for generalized aggressive periodontitis. Journal of Periodontology 2007a; 78:1201-1208.
Kaner, D., Bernimoulin, J. P., Hopfenmüller, W., Kleber, B. M. and
Friedmann, A. Controlled-delivery chlorhexidine chip versus
amoxicillin/metronidazole as adjunctive antimicrobial therapy
for generalized aggressive periodontitis: a randomized controlled
clinical trial. Journal of Clinical Periodontology 2007b; 34:880-891.
Karbach, J., Callaway, A., Willershausen, B., Wagner, W., Geibel, M.
A. and Al-Nawas, B. Antibiotic resistance testing of the total
implant-associated micro-flora and its pure isolates. European
Journal of Medical Research 2007; 12:120-128.
Kazor, C. E., Mitchell, P. M., Lee, A. M., Stokes, L. N., Loesche,
W. J., Dewhirst, F. E. and Paster, B. J. Diversity of bacterial
populations on the tongue dorsa of patients with halitosis and
healthy patients. Journal of Clinical Microbiology 2003; 41:558-563.
Lakhssassi, N., Elhajoui, N., Lodter, J. P., Pineill, J. L. and Sixou, M.
Antimicrobial susceptibility variation of 50 anaerobic periopathogens in aggressive periodontitis: an interindividual variability study. Oral Microbiology and Immunology 2005; 20:244-252.
Lekovic, V., Kenney, E. B., Carranza, F.A. Jr. and Endres, B. The
effect of metronidazole on human periodontal disease. A
clinical and bacteriological study. Journal of Periodontology 1983;
54:476-480.
Lindhe, J., Heijl, L., Goodson, J. M. and Socransky, S. S. Local tetracycline delivery using hollow fiber devices in periodontal therapy.
Listgarten, M. A., Lindhe, J. and Hellden, L. Effect of tetracycline
and/or scaling on human periodontal disease. Clinical, microbiological, and histological observations. Journal of Clinical Periodontology 1978; 5:246-271.
Magnusson, I., Clark, W. B., Low, S. B., Maruniak, J., Marks, R. G.
and Walker, C.B. Effect of non-surgical periodontal therapy
combined with adjunctive antibiotics in subjects with “refractory” periodontal disease. (I). Clinical results. Journal of Clinical
Matarazzo, F., Figueiredo, L. C., Cruz, S. E. B. , Faveri, M. and Feres,
M. Clinical and microbiological benefits of systemic metronidazole and amoxicillin in the treatment of smokers with chronic
periodontitis: a randomized placebo-controlled study. Journal of
Clinical Periodontology 2008; 35:885–896.
Meyer, J., Lallam-Laroye, C. and Dridi, M. Aggressive periodontitis what exactly is it? Journal Clinical Periodontology 2004; 31:586-587.
Mombelli, A., Casagni, F. and Madianos, P. N. Can presence or
absence of periodontal pathogens distinguish between subjects
with chronic and aggressive periodontitis? A systematic review.
Journal of Clinical Periodontology 2002; 29 Suppl 3:10-21.
04/01/2011 11:39:05
16
Needleman, I. G. and Watts, T.L. The effect of 1% metronidazole
gel in routine maintenance of persistent furcation involvement
in human beings. Journal of Periodontology 1989; 60:699-703.
Pavicic, M. J., van Winkelhoff, A. J., Pavicic-Temming, Y. A. and de
Graaff, J. Amoxycillin causes an enhanced uptake of metronidazole in Actinobacillus actinomycetemcomitans: a mechanism of synergy. Journal of Antimicrobial Chemotherapy 1994a; 34:1047-1050.
Pavicic, M. J., van Winkelhoff, A. J., Douque, N. H., Steures, R. W. and
de Graaff, J. Microbiological and clinical effects of metronidazole
and amoxicillin in Actinobacillus actinomycetemcomitans-associated
periodontitis. A 2-year evaluation. Journal of Clinical Periodontology
1994b; 21:107-112.
Rooney, J., Wade, W. G., Sprague, S. V., Newcombe, R. G. and Addy,
M. Adjunctive effects to non-surgical periodontal therapy of
systemic metronidazole and amoxycillin alone and combined.
A placebo-controlled study. Journal of Clinical Periodontology 2002;
29:342-350.
Sanz, M., Lau, L., Herrera, D., Morillo, J. M. and Silva, A. Methods
of detection of Actinobacillus actinomycetemcomitans, Porphyromonas
gingivalis and Tannerella forsythensis in periodontal microbiology,
with special emphasis on advanced molecular techniques: a
review. Journal of Clinical Periodontology 2004; 31:1034-1047.
Schacher, B., Baron, F., Rossberg, M., Wohlfeil, M., Arndt, R. and
Eickholz, P. Aggregatibacter actinomycetemcomitans as indicator for
aggressive periodontitis by two analysing strategies. Journal of
Clinical Periodontology 2007; 34:566-573.
Seifert, H. and Dalhoff, A. German multicentre survey of the
antibiotic susceptibility of Bacteroides fragilis group and Prevotella
species isolated from intra-abdominal infections: results from
the PRISMA study. Journal of Antimicrobial Chemotherapy 2010;
65:2405-2410
Socransky, S. S. and Haffajee, A. D. Dental biofilms: difficult therapeutic targets. Periodontology 2000 2002; 28:12-55.
Stabholz, A., Shapira, L., Mahler, D. et al. Using the PerioChip in
treating adult periodontitis: an interim report. Compendium of
Continuing Education in Dentistry 2000; 21:325-8, 330-332.
van Winkelhoff, A. J., Rodenburg, J. P., Goene, R. J., Abbas, F.,
Winkel, E. G. and de Graaff, J. Metronidazole plus amoxycillin
in the treatment of Actinobacillus actinomycetemcomitans-associated
periodontitis. Journal of Clinical Periodontology 1989; 16:128-131.
van Winkelhoff, A. J., Gonzales, D. H., Winkel, E. G., DellemijnKippuw, N., Vandenbroucke-Grauls, C. M. and Sanz, M. Antimicrobial resistance in the subgingival microflora in patients with
adult periodontitis. A comparison between The Netherlands and
Spain. Journal of Clinical Periodontology 2000; 27:79-86.
van Winkelhoff, A. J., Bosch-Tijhof, C. J., Winkel, E. G. and van der
Reijden, W. A. Smoking affects the subgingival microflora in
periodontitis. Journal of Periodontology 2001; 72:666-671.
van Winkelhoff, A. J., Herrera, D., Oteo, A. and Sanz, M. Antimicrobial profiles of periodontal pathogens isolated from periodontitis
patients in The Netherlands and Spain. Journal of Clinical Periodontology 2005; 32:893-898.
van der Velden, U., Varoufaki, A., Hutter, J. W., et al. Effect of smoking and periodontal treatment on the subgingival microflora.
Walker, C. B. The acquisition of antibiotic resistance in the periodontal microflora. Periodontology 2000 1996; 10:79-88.
Walter, C. and Weiger, R. Antibiotics as the only therapy of untreated
chronic periodontitis: a critical commentary. Journal of Clinical
Warnakulasuriya, S., Dietrich, T., Bornstein, M. M., et al. Oral health
risks of tobacco use and effects of cessation. International Dental
Journal 2010; 60:7-30
Ximenez-Fyvie, L. A., Maguer-Flores, A., Jacobo-Soto, V., LaraCordoba, M., Moreno-Borjas, J. Y. and Cantara-Maruri, E.
Subgingival microbiota of periodontally untreated Mexican
subjects with generalized aggressive periodontitis. Journal of
04/01/2011 11:39:05
Clinical and Microbiological Comparison of
Three Non-surgical Protocols for the Initial
Treatment of Chronic Periodontitis
Carlos Serrano, Nidia Torres, Angela Bejarano, Marcela Caviedes and María Eugenia Castellanos
School of Dentistry, Pontificia Universidad Javeriana, Bogotá, Colombia
Abstract
Objective: To compare the clinical and microbiological effects of three protocols for nonsurgical periodontal therapy, including full-mouth scaling and root planing plus systemic
antibiotics, on the treatment of chronic periodontitis patients. Methods: Twenty-nine
patients diagnosed with moderate to severe chronic periodontitis, selected according
to specific criteria, were randomly assigned to one of three treatment groups: quadrant
scaling, full-mouth scaling, and full-mouth scaling supplemented by systemic antibiotics. Antibiotic selection was based on the results of individual susceptibility testing.
Oral hygiene instructions and reinforcement were given during the study. All patients
received a clinical periodontal and microbiological examination at baseline and at reexamination, 4-6 weeks after therapy. Means and standard deviations were calculated
and differences between groups were analyzed via the Kruskal-Wallis test, p < 0.05.
Results: The mean age of the study sample was 49.1 ± 11.6 years old, and there were
17 men and 12 women. Patients treated with antibiotics showed antimicrobial susceptibility for amoxicillin and doxycycline. All study groups showed a similar significant
improvement in periodontal parameters. Plaque scores were reduced in a range of
29.0% to 42.6%. Bleeding on probing was reduced by 34.8% to 55.0%; the reduction
for the full-mouth scaling group was larger. Mean reduction in pocket depth was 1.2
to 1.3 mm in all groups. Mean bacterial counts were reduced in the groups receiving
full-mouth treatment, but not in the quadrant treatment group. Conclusion: The three
protocols for non-surgical periodontal treatment demonstrated a similar positive effect
on clinical parameters; however, only full-mouth treatment groups showed a reduction
in anaerobic microbial counts at re-examination.
Key words: Chronic periodontitis, scaling and root planing, antibiotics, full-mouth scaling
Introduction
The main goal of periodontal therapy is to control the
infection associated with chronically inflamed tissues
through a series of activities aimed at reducing the
bacterial destructive effect, such as oral hygiene instruction, subgingival debridement and surgical pocket
reduction. These protective measures, when reinforced
by meticulous self-performed oral hygiene and regular
professional maintenance, lead to the re-establishment
of periodontal health (Tunkel et al., 2002; van der Wejden
and Timmerman, 2002). Initial therapy for disease includes root surface instrumentation procedures, scaling
and root planing, usually performed on jaw quadrants
Correspondence to: Carlos Serrano, MSc., Specialist in Periodontology, Department of Periodontal System, School of
Dentistry, Pontificia Universidad Javeriana, Carrera 7 # 40-62,
Edificio de Odontología, Bogotá, Colombia. E-mail: serrano-c@
javeriana.edu.co
during a series of appointments. Systematic reviews on
non-surgical periodontal therapy have considered scaling and root planing an effective treatment, measured
by clinical parameters such as reduction of bleeding
upon probing, reduction of probing pocket depth and
gain in probing attachment level (van der Wejden and
Timmerman, 2002; Hung and Douglass, 2002; Hallmon
and Rees, 2003). Studies on the microbiological effect
of scaling and root planing have shown that it produces
a marked disruption of the subgingival biofilm, leading
to decreased levels and proportion of sites colonized by
periodontal pathogens (Teles et al., 2006).
Considering that periodontal pathogens can be
found in different intra-oral niches besides periodontal
pockets, such as the tongue, the tonsils, the saliva and
other mucous membranes (van Winkelhoff et al., 1986;
Asikainen et al., 1991), and that translocation of pathogens from the above niches or untreated periodontal
pockets to recently treated pockets is possible (Quyrinen
et al., 1996), the Leuven University research group de-
JIAP 10-003 Serrano.indd 17
22/12/2010 09:41:22
18
veloped the full-mouth disinfection concept (Quyrinen
et al., 1995). This treatment protocol includes scaling
and root planing in two sessions within 24 hours, and
usage of different therapeutic forms of clorhexidine
for brushing the tongue, rinsing the mouth, spraying
the tonsils and irrigating pockets. Reports from the
original research group have concluded that full-mouth
disinfection has a beneficial effect in the treatment of
moderate and severe periodontitis, evidenced by 15%
greater reduction in bleeding on probing, 1.3-1.8 mm
greater reduction in probing pocket depth, and ≥ 1.5
mm additional gain in probing attachment level over
quadrant scaling (Mongardini et al., 1999; Quyrinen et
al., 2006). A modification of the full-mouth disinfection
protocol is one stage full-dentition scaling and root planing only, since it was identified as the key component
responsible for the additional clinical and microbiological improvements over traditional treatment (Quyrinen
et al., 2000). During recent years, several clinical reports
on the effect of full-mouth treatment concepts have
yielded contradictory findings (Apatzidou and Kinane,
2004; Koshy et al., 2005; Wennstrom et al., 2005; JervoeStorm et al., 2006; Zanatta et al., 2006). Two recent
systematic reviews concluded that differences between
full-mouth disinfection, full-mouth scaling and root
planing and traditional treatment were modest, so that
any of the three treatment modalities may be used for
initial therapy for chronic periodontitis (Lang et al., 2008;
Eberhard et al., 2008).
Considering the lack of significant differences between full-mouth treatment concepts and traditional
therapy referred to in systematic reviews (Lang et al.,
2008; Eberhard et al., 2008), and the additional clinical
benefit over scaling and root planing described for the
adjunctive use of systemic antibiotics (Herrera et al.,
2002; Haffajee et al., 2003), Cionca et al. (2009) studied
the effects of combining metronidazole and amoxicillin,
proper oral hygiene, and scaling and root planing over 24
hours in chronic periodontitis patients. The authors conducted a placebo-controlled clinical trial of six months
duration, reporting significant clinical improvements for
both patient groups, but greater reduction in the number
of pockets > 4 mm and percentage of sites with bleeding on probing for subjects receiving amoxicillin and
metronidazole. In conclusion, the authors stated that
systemic antibiotics significantly improved the clinical
outcome of full-mouth non-surgical periodontal therapy
and reduced the need for additional therapy.
The purpose of this study was to compare the clinical and microbiological effects of three protocols for
non-surgical periodontal therapy, including full-mouth
scaling and root planing plus systemic antibiotics, on the
treatment of chronic periodontitis patients.
Materials and Methods
Study design
This was a parallel design, randomized clinical trial
performed at the Specialist Periodontal Clinic, School
of Dentistry, Javeriana University in Bogotá, Colombia.
Approval for the protocol was obtained from the Ethics
Committee, Javeriana University; all patients signed an
informed consent form before the start of the study.
Patients
Twenty-nine patients were recruited from new referrals
to the Javeriana University, Specialist Clinic, according
to the following criteria: age ranging from 25-75 years;
possession of a minimum of 16 teeth; diagnosis of
chronic periodontitis (according to the criteria of the
International Classification System for Periodontal
Diseases [Armitage, 1999]) with severity ranging from
moderate to severe and multiple sites showing clinical
attachment loss ≥ 3 mm in all jaw quadrants; available
for participation in a follow-up examination after two
months. Patients were excluded if they had uncontrolled
systemic conditions, such as diabetes or cardio-vascular
disease, or required antibiotic coverage for treatment;
were pregnant or breast-feeding; were taking medication that could affect the periodontal condition or had
received antibiotic therapy during the previous three
months; had suspected or confirmed allergy to antibiotic agents, including β-lactam or tetracycline group
antibiotics; or were current smokers, defined as having
a consumption rate of ≥ 10 cigarettes per day.
Experimental design
Enrolled subjects were randomly assigned by a computer-generated table to one of three non-surgical
treatment modalities (Research Randomizer, Social
Psychology Network, 1997-2009):
Control group (Q): scaling and root planing quadrant
by quadrant at weekly intervals.
Full-mouth scaling and root planing (FM): fullmouth scaling and root planing performed over two
consecutive days.
Full-mouth scaling and root planing plus antibiotics
(FMa): full-mouth scaling and root planing performed
over two consecutive days combined with the administration of systemic antibiotics determined by susceptibility testing for each subject.
All patients had a clinical examination and microbiological sampling before any treatment procedure
was performed (baseline), and at a period 4-6 weeks
after the last appointment for scaling and root planing
(re-examination).
22/12/2010 09:41:22
Clinical and Microbiological Comparison of Three Non-surgical Protocols for the Initial Treatment of Chronic Periodontitis
Clinical examination
Clinical measurements of bleeding on probing, probing pocket depth and clinical attachment level were
performed on all present teeth at six tooth surfaces.
Four surfaces were examined for the O´Leary plaque
score [percentage of presence/absence of plaque using
a disclosing solution: mesial, buccal, distal and lingual
(O´Leary, 1972)]. Probing pocket depth (PPD) was
measured with a manual periodontal probe to the closest
millimeter. Bleeding on probing (BoP) was recorded as
the percentage of sites bleeding after probing pocket
depth measurements. Specific analysis was performed
for moderate pockets (5 - 6 mm), and for deep pockets
(≥ 7 mm). The gingival margin (GM) level was measured
from the gingival margin to a reference point, either the
cemento-enamel junction or the margin of a restoration. In case of gingival recession, the gingival margin
level has a negative value. The probing attachment level
(PAL) was measured as ± GM – PD. Reduction in the
percentage of sites with PPD ≥ 4 mm from baseline to
re-examination was recorded.
Microbiological examination
After cotton roll isolation and removal of supragingival
plaque, pooled microbial samples were taken with paper
cones from the deepest periodontal pocket in each quadrant for 15 seconds (Mombelli et al., 1991). Samples were
placed in vials containing anaerobic VMGA III transport
medium (Möller, 1966) and transferred for processing.
At the microbiological laboratory, samples were
vortex-mixed for 30 seconds and serially diluted 10-fold
five times. One hundred μL of 10-1 dilution was plated
on blood agar and incubated for three days under aerobic
conditions. One hundred μL of 10-4 dilution was plated
on anaerobic Wilkins-Chalgren agar (Oxoid, United
Kingdom); plates were incubated for seven days at 37 ºC
in 80% N2, 10% CO2 and 10% H2. Colony forming units
(CFU) were enumerated on blood and Wilkins-Chalgren
agar plates after the period of incubation. Presumptive
identification of periodontal pathogens was performed
based on colony morphology, Gram staining, aerotolerance test and a commercial identification micromethod
system (RapID ANA II, Oxoid, United Kingdom).
Patients randomly assigned to the FMa group had
an antimicrobial susceptibility testing on identified periodontal pathogen colonies, mainly Porphyromona gingivalis,
Prevotella intermedia, Fusobacterium nucleatum and Wollinela
spp. Five different commercially available antibiotic strips
were used: amoxicillin, metronidazole, azithromycin,
tetracycline and doxycycline (E-test, AB Biodisk, Solna,
Sweden). Viable pure colonies were homogenized in
0.85% saline solution and adjusted to the MacFarland
turbidity standard 1.0. Using a sterile glass rod, 0.1 mL
of the inoculum was spread over Wilkins-Chalgren agar
plates and allowed to dry for 15 minutes. E-test strips
19
were gently placed over the agar surface and incubated
under anaerobic conditions for three days. The intersection between the zone of bacterial inhibition and the
E-test strip represented the minimal inhibitory concentration (MIC). The antibiotic with the lowest MIC
was selected to be used; if several tests were made for
the same patient the antibiotic with the lowest average
MIC was chosen.
Treatment procedures
Scaling and root planing were performed by three
periodontal graduate students (AB, MC and MEC).
The FM and FMa received scaling and root planing on
two consecutive days; in addition, for the FMa group
the antibiotic showing the lowest minimal inhibitory
concentration was prescribed for a one-week period.
The control group (Q) received scaling and root planing in four sessions, quadrant by quadrant, at one-week
intervals. All scaling was performed using manual curettes (Hu-Friedy, Chicago, IL, U.S.A.) and ultrasonic
magnetostrictive instruments (Cavitron, Dentsply, York,
PA, U.S.A.) without any time restriction.
At the baseline examination, all patients were given
detailed oral hygiene instructions, including toothbrush
and dental floss or inter-dental brush use. No mouth
rinses were used during the study. Patients received oral
hygiene reinforcement at weeks 2 and 4. Teeth judged
ready to be extracted due to poor periodontal condition
were extracted and not included for analysis; restorations
with overhangs were replaced during treatment.
Statistical analysis
Mean and standard deviation values for the O´Leary
plaque score, percentage of BoP, PPD, PAL and percentage of pockets were calculated for each subject. Mean
and standard deviation of logarithmically transformed
CFU counts were calculated. The changes within groups
from baseline to re-examination were analyzed using the
paired Wilcoxon test. The differences between groups
were analyzed using the Kruskal-Wallis test. The level
of significance was set at p < 0.05.
Results
A total of twenty-nine patients completed the clinical
study: 10 patients in the control Q group, nine patients
in the FM group, and 10 patients in the FMa group.
The mean age of the patient sample was 49.1 ± 11.6
years old; there were 17 men and 12 women. Twenty-six
patients were non-smokers, two patients were smoking
2 - 5 cigarettes per day, and a third patient smoked 2 - 3
cigarettes per week. Demographic characteristics of the
patient sample are described in Table 1.
Antimicrobial susceptibility testing results for the
10 subjects included in the FMa group revealed that in
four subjects, the lowest MIC value was for amoxicil-
22/12/2010 09:41:22
20
Table 1. Demographic characteristics of the patient sample
Number of patients
Mean age
Gender male/female
Q
FM
FMa
10
46.6 (10.9)
6/4
9
52.8 (10.6)
6/3
10
48.2 (13.3)
4/6
0
0
20
20
40
40
%
60
60
80
80
100
100
Q, control; FM, full mouth scaling and root planing; FMa, full mouth scaling and root planing plus systemic antibiotics
Q
FM
BL
Q
FMa
FM
BL
Final
Figure 2. Percentage of sites with bleeding on probing
0
20
40
60
80
Figure 1. Change in O`Leary plaque score FMa
Final
Q
FM
BL
FMa
Final
Figure 3. Percentage of sites with probing pocket depth
(PPD) ≥ 4 mm
22/12/2010 09:41:23
lin; for the other six subjects the lowest value was for
doxycycline. As a consequence, four subjects received
amoxicillin 875 mg twice a day for seven days; and six
subjects received doxycycline 100 mg once a day for
seven days.
Plaque scores
All study groups showed a high level of plaque accumulation at baseline before oral hygiene instructions were given, Q 56.7% ± 22.8, FM 77.8% ± 38.7
and FMa 47.3% ± 18.2. Nevertheless, with a random
group assignment the O`Leary plaque score was higher
for the FM group than for the other two groups. At
re-examination, all three groups showed a statistically
significant improvement in the O`Leary plaque score,
with mean reduction values ranging from 29.0% for
the FMa group to 42.6% for the FM; no statistically
significant differences were detected among the three
groups at re-examination (Figure 1).
Bleeding on probing
Percentage of sites bleeding on probing was equally
high for all three groups at baseline: at re-examination,
a statistically significant reduction in percentage of sites
bleeding on probing was present in all groups. For the
Q, the BoP percentage decreased from 78.7 ± 26.3% to
44.0 ± 29.0%, for the FM from 88.6 ± 17.8% to 33.6 ±
24.0%, and for the FMa from 80.0 ± 14.5% to 46.3 ±
27.9%. There were no statistically significant differences
when the three groups were compared; however, the FM
group obtained a 20% greater BoP percentage reduction
when compared with the other two groups (Figure 2).
Reduction in the percentage of pockets
At baseline, the percentage of sites with increased
PPD varied from 36.3% ± 20.9 for the FMa group, to
45.0% ± 28.1 for the Q group. A statistically significant
reduction in the percentage of sites showing PPD ≥ 4
mm was observed at re-examination compared with
baseline in all three groups. The reduction in percentage had a range from 12 to 17%; the greatest reduction
was obtained in the Q group, and the least in the FM
group. However, no statistically significant differences
were obtained between groups (Figure 3).
21
Probing pocket depth
The mean baseline PPD was similar in all three groups:
it varied from 5.0 ± 0.6 mm for the Q group to 5.5 ± 0.7
mm for the FM group. At re-examination, all three groups
showed a 1.2 - 1.3 mm significant reduction of PPD; no
significant differences were present among the groups.
When a separate analysis for pockets initially 5 - 6 mm
and ≥ 7 mm was performed, no significant differences
were found for mean change values among the three
groups, but greater variability in the healing response of
deep pockets was found for the Q group (Table 2, Figures
4, 5). Not all patients exhibited ≥ 7 mm deep pockets at
baseline: three patients in the Q group and one patient
each in the FM and FMa groups did not have pockets in
that depth category.
Probing attachment level
A significant gain in PAL of about 1.0 mm was measured
at re-examination for the three groups. No significant
differences were found among the groups.
Microbiological anaerobic CFU counts
Great variability in log-transformed anaerobic CFU
counts characterized the subjects in the three groups,
which was reflected in high standard deviation values.
As a partial consequence, no significant differences were
observed in CFU counts at re-examination compared
with baseline. A decrease in log-transformed CFU
counts was measured for the FM and FMa groups,
0.34 and 1.33 respectively. In contrast, a slight increase
was measured for the Q group, -0.41 log-transformed
CFU count. Nevertheless, no significant differences
were obtained among the three study groups (Figure 6).
Of interest, only in the FMa group were there patients
whose oral flora was below microbiological culture detection levels for anaerobes at re-examination (Figure 6).
Discussion
The results of the present study showed that periodontal
therapy in all three study groups resulted in a significant
improvement of periodontal clinical parameters. The
percentage of BoP sites was reduced in the range of
34 - 55%, PPD was reduced by 1.2 - 1.3 mm, and the
PAL gain was approximately 1 mm. These changes in
Table 2. Mean probing pocket depth (SD) values according to 5 - 6 and ≥ 7 mm depth categories
Q
Baseline
Re-examination
Change
FM
FMa
5-6
≥7
5-6
≥7
5-6
≥7
5.2 (0.1)
4.0 (0.6)
1.2 (0.5)
7.4 (0.3)
5.3 (1.6)
2.1 (1.3)
5.5 (0.2)
4.2 (0.9)
1.3 (0.6)
8.0 (0.8)
6.2 (0.8)
1.8 (0.9)
5.4 (0.2)
4.0 (0.7)
1.4 (0.5)
7.5 (0.4)
5.8 (1.1)
1.7 (0.9)
Q, control; FM, full mouth scaling and root planing; FMa, full mouth scaling and root planing plus systemic antibiotics
22/12/2010 09:41:23
3
4
Milímetros
5
6
22
Q
FM
BL
FMa
Final
2
4
Milímetros
6
8
10
Figure 4. Probing pocket depth reduction from baseline: 5 - 6
mm depth category Q
FM
BL
FMa
Final
0
2
4
6
Figure 5. Probing pocket depth reduction from baseline: ≥ 7
mm depth category
Q
FM
BL
FMa
Final
Figure 6. Log-transformed anaerobic bacterial colony counts
22/12/2010 09:41:23
clinical parameters are in the same range as results of
systematic literature reviews on the effects of nonsurgical periodontal therapy (van der Wejden and Timmerman, 2002; Hung and Douglass, 2002). The majority
of subjects in the present study showed great severity
of periodontal disease, as over 40% of the surfaces
were affected by periodontal pockets with a mean PPD
range of 5.0 - 5.5 mm, and a large number of pockets
≥ 7 mm deep were present.
No significant differences were found between
the control group receiving quadrant scaling and root
planing, and the other two groups receiving full-mouth
scaling and root planing. This is in agreement with two
recently published systematic reviews on the effects of
full-mouth treatment concepts: they concluded that only
modest differences were present between quadrant and
full-mouth treatment (Eberhard et al., 2008; Lang et al.,
2008). Noteworthy, in the present study the FM group
had a 20% greater reduction in BoP percentage compared with the other two groups; however, due to a large
standard deviation, this difference was not statistically
significant. The systematic review by Lang et al. (2008)
reported an opposite finding, as the weighted mean difference for BoP percentage reduction was 8.45% larger
in the quadrant scaling groups.
Of interest, no additional clinical benefit was obtained from systemic antibiotic administration even if
the antibiotic showing the lowest microbial inhibitory
concentration was selected. This is contradictory to
the conclusion of systematic reviews on the effects of
systemic antimicrobials as adjuncts to non-surgical periodontal treatment. The review of Herrera et al. (2002)
reported a small additional gain in PAL of 0.3 mm and
additional reduction of PPD ranging from 0.05 to 0.6
mm for patients receiving systemic antibiotics. Specific
significant additional effects were found for the use
of spiramycin regarding PPD change, and amoxicillin
plus metronidazole regarding PAL change. The review
of Haffajee et al. (2003) found that adjunctive systemic
antibiotics led to an additional gain in PAL of 0.29 mm
for pockets initially 4 - 6 mm deep, and of 0.45 mm for
pockets initially ≥ 7 mm deep. Separate analysis by antibiotic type showed that tetracycline and metronidazole
had a significant adjunctive benefit, followed by borderline results for the combination of amoxicillin plus
metronidazole. In the present study, no greater reduction
of PPD or gain of PAL was found in patients receiving
systemic antibiotics, even when considering specific
categories of initial PPD. As a possible explanation for
the lack of any additional effect for systemic antibiotic
administration, patient selection or antibiotic regime
could be analyzed. The current sample age range was
wide (25 - 75 years old), which could lead to the inclusion
of subjects with different rates of disease progression
and tissue destruction, even if all patients exhibited
23
clinical characteristics of chronic periodontitis. The 10
patients included in the FMa group were distributed
to receive amoxicillin (four cases) or doxycycline (six
cases); this reduced number of subjects does not allow
analyzing the effect of each antibiotic in addition to
non-surgical treatment. The combination of different
antibiotics was not tested in the present study, even if
the combination of amoxicillin and metronidazole in
addition to scaling and root planing has been found to
improve the clinical outcome of periodontal therapy
on different populations (Pavicic et al., 1994; Winkel et
al., 2001; Guerrero et al., 2005). The combination was
not used for the present population due to the large
levels of antimicrobial resistance to metronidazole. It
may be that antibiotic regimens could have different
adjunctive clinical benefits based on population variation for microbial antibiotic susceptibility. Nevertheless,
healing in pockets initially ≥ 7 mm deep demonstrated
a smaller range of variability in the FMa than in the Q
group, where box plots for baseline and re-examination
nearly overlap. The less variable healing response in the
antibiotic group could lead to clinical differences during
a longer healing time.
Several methods of describing the effect of periodontal therapy on microbiological parameters have
been used in the literature: for example, change in bacterial counts, proportion of colonized sites, or level of
specific periodontal pathogens, including presence or
absence at different threshold values (Teles, 2006). The
systematic review by Lang et al. (2008) stated an equally
positive improvement in microbiological parameters
for quadrant and full-mouth scaling and root planing.
However, in the present study no improvement in bacterial counts was seen in the Q group, whereas both
full-mouth treatment groups showed decreased bacterial counts, the change being larger in the group that
received antibiotics. Using similar methods, Quyrinen et
al. (2000) found a small decrease in microbial counts for
quadrant scaling, compared to a larger 1 logarithmic unit
decrease in full-mouth treatment protocols, a comparable finding to the present study. On the contrary, studies
that have used polymerase chain reaction techniques to
detect specific periodontal pathogens before and after
periodontal treatment have not found significant differences between quadrant and full-mouth treatment
groups (Jervoe-Storm et al., 2007; Koshy et al., 2005). An
exception occurred for Treponema denticola, which had a
larger reduction in the full-mouth treatment group in
the report by Apatzidou et al. (2004).
The articles by Cionca et al. (2009, 2010) performed
a clinical and microbiological comparison between fullmouth scaling and full-mouth scaling supplemented by
systemic amoxicillin and metronidazole. The clinical
results showed a significant clinical improvement for
both treatment groups: bleeding on probing was re-
22/12/2010 09:41:23
24
duced by 37 to 45%, PPD was reduced by 1.2 - 1.3 mm,
and gain in PAL was 0.7 to 0.9 mm., showing a similar
clinical improvement to the present study. The main
outcome of therapy in the Cionca et al. (2009) report
was the number of sites with PPD ≥ 4 mm and bleeding on probing. This figure was significantly reduced
in both treatment groups, with a statistically greater
reduction for the group receiving antibiotics: 4.4 versus
1.3 remaining bleeding pockets. The present study used
a different method, as the percentage of sites ≥ 4 mm
deep, independent of bleeding on probing, was calculated. The microbiological study by Cionca et al. (2010)
reported lower bacterial counts for both study groups,
without any significant difference between them, similar
to the present study. The addition of systemic antibiotics
produced a greater reduction in the detection frequency
of Aggregatibacter actinomycetemcomitans and P. gingivalis.
Significant levels of antibiotic resistance to periodontal pathogens in samples taken from Colombian
patients has led to the suggestion of performing antibiotic susceptibility testing before adjunctive antibiotic
therapy (Ardila et al., 2010; Serrano et al., 2009). In
the present study, amoxicillin or doxycycline was used
for the treatment of the 10 patients included in the
FMa group. Few studies have analyzed the effect of
amoxicillin administration alone as an adjunct to nonsurgical periodontal therapy, while the combination of
amoxicillin and metronidazole is more common (van
Winkelhoff et al., 1992). It has been reported that the
combination regimen produced a larger improvement
in clinical parameters compared to placebo therapy,
especially for patients who were initially positive for A.
actinomycetemcomitans and P. gingivalis, and who became
negative at re-examination (Pavicic et al., 1994; Winkel
et al., 2001). However, a combination regimen was not
used in the present study, as bacterial isolates showed
significant resistance against metronidazole, a finding
that has been described by other research groups in
the same geographic area (Jaramillo et al., 2005; Ardila
et al., 2010). The use of systemic doxycycline, 100 mg a
day, as an adjunct of periodontal therapy, has produced
additional benefits in the periodontal treatment of diabetic patients (Grossi et al., 1997; Martorelli de Lima et
al., 2004; Llambés et al., 2005). Lately, those prescribing
doxycycline have looked not only for its antimicrobial
effect but also for inhibition of matrix metalloproteinases (Salvi and Lang 2005).
An inclusion criterion in systematic reviews about the
effects of full-mouth non-surgical periodontal therapy
has been study duration of 3 or 6 months (Eberhardt et
al., 2008; Lang et al., 2008). Nevertheless, in the present
study re-examination was performed after 4 to 6 weeks
in order to assess the need for surgical periodontal therapy in patients affected primarily by severe chronic periodontitis. A consensus report by the American Academy
of Periodontology stated that a 4- to 6-week interval
seems appropriate to assess the initial response to nonsurgical periodontal therapy (Ciancio, 1989). The review
article by Segelnick and Weinberg (2006) proposed to
perform re-evaluation of basic periodontal therapy 4 to
8 weeks after scaling and root planing, based on evidence
from clinical studies and the histology of periodontal
wound healing. However, Badersten et al. (1981, 1984)
reported that clinical improvement after therapy leveled
off after 3 - 4 months for moderate periodontal cases,
but the periodontal condition could continue to improve
even for 6 to 9 months in advanced periodontal cases.
The present study showed a trend toward larger PPD
reduction for deep pockets and greater microbial count
reduction in the group receiving full-mouth therapy
supplemented by antibiotics; probably this trend would
become significant in a longer healing time.
In the present study, scaling and root planing was
performed by periodontal graduate students. Different
literature reports showed that experienced operators
have better results regarding calculus removal during
non-surgical instrumentation than graduate students
(Brayer et al., 1989; Fleischer et al., 1989). Nevertheless,
results of the present study are similar to the outcome
of non-surgical therapy reported in systematic reviews
in the literature.
Conclusion
The three protocols for non-surgical periodontal treatment demonstrated a similar positive effect on clinical
parameters; however, only full-mouth treatment groups
showed a reduction in anaerobic microbial counts at
re-examination.
Acknowledgement and conflict of interest
The authors declare there are no conflicts of interest.
This study was supported by a research grant from the
Research Promotion Office, Javeriana University.
References
Apatzidou, D.A. and Kinane, D.F. Quadrant root planing versus
same-day full-mouth root planing I. Clinical findings. Journal of
Apatzidou, D.A., Riggio, M.P. and Kinane, D.F. Quadrant root planing versus same-day full-mouth root planing II: Microbiological
findings. Journal of Clinical Periodontology 2004; 31:141-148.
Ardila, C.M., Granada, M.I. and Guzman, I.C. Antibiotic resistance
of subgingival species in chronic periodontitis patients. Journal
of Periodontal Research 2010; 45:557-563.
Armitage G.C. Development of a classification system for periodontal diseases and conditions. Annals of Periodontology 1999; 4:1-6.
Asikainen, S., Alaluusua, S. and Saxén, L. Recovery of A. actinomycetemcomitans from teeth, tongue and saliva. Journal of Periodontology
1991; 62:203-206.
Badersten, A., Nilveus, R. and Egelverg, J. Effect of non-surgical
periodontal therapy. I. Moderately advanced periodontitis. Journal
22/12/2010 09:41:23
Badersten, A., Nilveus, R. and Egelberg, J. Effect of non-surgical
periodontal therapy. II. Severely advanced periodontitis. Journal
Brayer, W.K., Mellonig, J.T., Dunlap, R.L., Marinak, K.W. and Carson,
R.E. Scaling and root planing effectiveness: the effect of root
surface access and operator experience. Journal of Periodontology
1989; 60:67-72.
Ciancio, S.G. Non-surgical periodontal treatment. In: Proceeding of
the World Workshop in Clinical Periodontics. American Academy of
Periodontology; 1989: 11-14
Cionca, N., Giannopoulou, C., Ugolotti, G. and Mombelli, A. Amoxicillin and metronidazole as an adjunct to full-mouth scaling and
root planing of chronic periodontitis. Journal of Periodontology
2009; 80:364-371.
Cionca, N., Giannopoulou, C., Ugolotti, G. and Mombelli, A. Microbiologic testing and outcomes of full-mouth scaling and root
planing with or without amoxicillin/metronidazole in chronic
periodontitis. Journal of Periodontology 2010:81:15-23.
Eberhardt, J., Jervoe-Storm, P.M., Needleman, I., Worthington,
H. and Jepsen, S. Full-mouth treatment concepts for chronic
periodontitis: a systematic review. Journal of Clinical Periodontology
2008; 35:591-604.
Fleischer, H.C., Mellonig, J.T., Brayer, W.K., Gray, J.L. and Barnett,
J.D. Scaling and root planing efficacy in multirooted teeth. Journal
Grossi, S.G., Skrepcinski, F.B., deCaro, T., et al. Treatment of periodontal disease in diabetes reduces glycated hemoglobin. Journal
Guerrero, A., Griffiths, G.S., Nibali, L., et al. Adjunctive benefit of
systemic amoxicillin and metronidazole in non-surgical treatment of generalized aggressive periodontitis: a randomized
placebo-controlled clinical trial. Journal of Clinical Periodontology
2005; 32:1096-1107.
Haffajee, A.D., Socransky, S.S. and Gunsolley, J.C. Systemic antiinfective periodontal therapy. A systematic review. Annals of
Hallmon, W.W. and Rees, TD. Local anti-infective therapy: mechanical and physical approaches. A systematic review. Annals of Periodontology 2003; 8:99-114.
Herrera, D., Sanz, M., Jepsen, S., Needleman, I. and Roldán, S. A
systematic review on the effect of systemic antimicrobials as
an adjunct to scaling and root planing in periodontitis patients.
Journal of Clinical Periodontology 2002; 29(Suppl. 3):136-159.
Jaramillo, A., Arce, R.M., Herrera, D., Betancourth, M., Botero J.E.
and Contreras, A. Clinical and microbiological characterization
of periodontal abscesses. Journal of Clinical Periodontology 2005;
32:1213-1218.
Jervoe-Storm, P.M., Semaan, E., AlAhdab, H., Engel, S., Fimmers,
R. and Jepsen, S. Clinical outcomes of quadrant root planing
versus full-mouth root planing. Journal of Clinical Periodontology
2006; 33:209-215.
Jervoe-Storm, P.M., AlAhdab, H., Semaan, E., Fimmers, R. and
Jepsen, S. Microbiological outcome of quadrant versus fullmouth root planing as monitored by real-time PCR. Journal of
Koshy, G., Kawashima, Y., Kiji, M., et al. Effects of single-visit fullmouth ultrasonic debridement versus quadrant-wise ultrasonic
debridement. Journal of Clinical Periodontology 2005; 32:734-743.
Lang, N.P., Tan, W.C., Krähenmann, M.A. and Zwahlen, M. A systematic review of the effects of full-mouth debridement with
and without antiseptics in patients with chronic periodontitis.
Journal of Clinical Periodontology 2008; 35(Suppl. 8):8-21.
Llambés, F., Silvestre, F.J., Hernández-Mijares, A., Guiha, R. and
Caffesse, R. Effect of non-surgical periodontal treatment with
or without doxycycline on the periodontium of type 1 diabetic
patients. Journal of Clinical Periodontology 2005; 32:915-920.
Martorelli de Lima, A.F., Cury, C.C., Palioto, D.B., Duro, A.M., Da
25
Silva, R.C. and Wolff, L.F. Therapy with adjunctive doxycycline
local delivery in patients with type 1 diabetes mellitus and periodontitis. Journal of Clinical Periodontology 2004; 31:648-653.
Möller, AJ. Microbiological examination of root canals and periapical tissues of human teeth. Methodological studies. Odontologisk
Tidskrift 1966; 74(Suppl. 1):1-380.
Mombelli, A., McNabb, H. and Lang, NP. Black-pigmenting Gramnegative bacteria in periodontal disease. II. Screening strategies
for detection of P. gingivalis. Journal of Periodontal Research 1991;
26:308-313.
Mongardini, C., van Steenberghe, D., Dekeyser, C. and Quirynen, M.
One stage full-mouth versus partial-mouth disinfection in the
treatment of chronic adult or generalized early-onset periodontitis. I. Long-term clinical observations. Journal of Periodontology
1999; 70:632-645.
O’Leary, T.J., Drake, R.B. and Naylor, J.E. The plaque control record.
Journal of Periodontology 1972; 43:38.
Pavicic, M.J., van Winkelhoff, A.J., Douqué, N.H., Steures, R.W. and
de Graaf, J. Microbiological and clinical effect of metronidazole
and amoxicillin in Actinobacillus actinomycetemcomitans-associated
periodontitis. A 2-year evaluation. Journal of Clinical Periodontology
1994; 21:107-112.
Quirynen, M., Bollen, C.M., Vandekerckhove, B.N., Dekeyser, C.,
Papaioannou, W. and Eyssen, H. Full- versus partial-mouth
disinfection in the treatment of periodontal infections: shortterm clinical and microbiological observations. Journal of Dental
Research 1995; 74:1459-1467.
Quirynen, M., Papaioannou, W. and van Steenberghe, D. Intraoral
transmission and the colonization of oral hard surfaces. Journal
Quirynen, M., Mongardini, C., Pauwels, M., Bollén, C., van Eldere,
L and van Steenberghe, D. One stage full- vs. partial-mouth
disinfection in the treatment of patients with chronic adult or
early-onset periodontitis. Part II: Long-term impact on microbial
load. Journal of Periodontology 1999; 70:646-656.
Quirynen, M., Mongardini, C., de Soete, M., et al. The role of chlorhexidine in the one-stage full-mouth disinfection treatment
of patients with advanced adult periodontitis. Journal of Clinical
Quirynen, M., De Soete, M., Boschmans, G., et al. “Benefit of onestage full-mouth disinfection” is explained by disinfection and
root planing within 24 hours: a randomized controlled trial.
Salvi, G.E. and Lang, N.P. Host response modulation in the management of periodontal diseases. Journal of Clinical Periodontology
2005; 32(Suppl. 6):108-129.
Segelnick, S.L. and Weinberg, M.A. Reevaluation of initial therapy:
When is the appropriate time? Journal of Periodontology 2006;
77:1598-1601.
Serrano, C., Torres, N., Valdivieso, C., Castaño, C., Barrera, M. and
Cabrales, M.A. Antibiotic resistance of periodontal pathogens
obtained from frequent antibiotic users. Acta Odontologica Latinoamericana 2009; 22:99-104.
Teles, R.P., Haffajee, A.D. and Socransky, S.S. Microbiological goals
of periodontal therapy. Periodontology 2000, 2006; 42:180-208.
Tunkel, J., Heinecke, A. and Flemming, T.F. A systematic review of
efficacy of machine-driven and manual subgingival debridement
in the treatment of chronic periodontitis. Journal of Clinical Periodontology 2002; 29(Suppl. 3):72-81.
Van der Wejden, G.A. and Timmerman, M.F. A systematic review
on the clinical efficacy of subgingival debridement in the treatment of chronic periodontitis. Journal of Clinical Periodontology
2002; 29(Suppl. 3):55-71.
Van Winkelhoof, A.J., Van der Velden, U., Winkel, E.G. and de Graaf,
J. Black-pigmented bacteroides and motile organisms on oral
mucosal surfaces in individuals with and without periodontal
breakdown. Journal of Periodontal Research 1986; 21:434-439.
22/12/2010 09:41:24
26
Van Winkelhoff, A.J., Tojhof, C.J. and de Graaf, J. Microbiological
and clinical results of metronidazole plus amoxicillin therapy in
Actinobacillus actinomycetemcomitans–associated periodontitis. Journal
Wennstrom, J.L., Tomasi, C., Bertele, A. and Dellasega, E. Full-mouth
ultrasonic debridement versus quadrant scaling and root planing
as an initial approach in the treatment of chronic periodontitis.
Winkel, E.G., Van Winkelhoff, A.J., Timmerman, T.F., Van der
Velden, U. and Van der Wejden, G.A. Amoxicillin plus metronidazole in the treatment of adult periodontitis patients. A
double-blind placebo-controlled study. Journal of Clinical Periodontology 2001; 28:296-305.
Zanatta, G.M., Bittencourt, S., Nociti Jr., F.H., Sallum, E.A., Sallum,
A.W. and Casati, MZ. Periodontal debridement with povidoneiodine in periodontal treatment: Short-term clinical and biochemical observations. Journal of Periodontology 2006; 77:498-505.
22/12/2010 09:41:24
International Academy of Periodontology
Lviv, Ukraine
June 16-18, 2011
13th International Biennial Meeting
Please complete form and return to: Congress Secretariat, 36 Pasichna Str, 79038 Lviv, Ukraine,
Ms. Olena Uhryn phone: +38 (32) 2512039, fax: +38 (32) 2512151, e-mail: [email protected]
Name: __________________________________________
Institution: __________________________________________
Mailing Address: __________________________________________
City: ___________________ Zip: _______________
Country: _____________
Telephone: ______________ Fax: ________________
e-mail:_______________
Participation in Gala-dinner YES NO
Accompanying guest (Gala-dinner only) YES NO
CONGRESS FEE-US dollars
Dentists
Dentists members of Ukrainian Oral Implantology
Association and International Academy of
Periodontology
Dental technicians
Dental technicians members of Ukrainian Oral
Implantology association and International Academy of
Periodontology
Dental hygienists and dentists’ assistants
Students
BEFORE
02/15/2011
270.00
BEFORE
03/15/2011
300.00
AFTER
03/15/2011
350.00
250.00
280.00
300.00
170.00
200.00
250.00
150.00
180.00
230.00
120.00
50.00
150.00
75.00
170.00
100.00
DO YOU NEED OUR HELP IN HOTEL RESERVATION, PLEASE MARK YOUR CHOICE
1. Opera
Double Junior Suite Luxury Apartment Single 2. Dnister
Single Double Junior Suite Luxury Apartment 3. Vintage
Single Double Junior Suite Luxury Apartment 4. George
Single Double Junior Suite Luxury Apartment 5. Eurohotel
Single Double Junior Suite Luxury Apartment 6. Cytadel
Double Junior Suite Luxury Apartment Single 7. Swiss hotel
Single Double Junior Suite Luxury Apartment 8. Viden
Single Double Junior Suite Luxury Apartment Please indicate date of arrival and departure:
Check-in:______________ Check-out:______________
JIAP Liv reg.indd 27
23/12/2010 12:08:16
28
International Academy of Periodontology
Lviv, Ukraine
June 16-18, 2011
13th International Biennial Meeting
HOTEL RATES*** (grivna)
Hotel
Single
Opera
800 / 950
Dnister
500 /
600/850
Vintage
750
George
600/650
Eurohotel
500
Cytadel
990/1390
Swiss hotel
500 / 650
Viden
450 / 520 /
640
double
1050 / 1250
500 / 600 /
850
950
600/650
600 / 700
1200 / 1600
600 / 750
500 / 570 /
690
junior suite
1450
luxury apartments
2250
950
1500
750
900
1100 / 1250
1550
850
1300 / 1700
2900
1500 / 2520
520 / 550
650 / 700
NOTE: please make hotel reservation before 1 February 2011
*** Do not forget to leave for yourself the copy of completed registration form
*** Please note that usually check-in and check-out time is 12 a.m.
*** Above hotel rates are valid for the moment of printing this announcement and could be
changed by hotel administration.
For more up to-date information please refer to organizing committee or look for second
announcement
1US$ = 8 grivna
Ukrainian National Bank exchange rate on 1/09/2010
JIAP Liv reg.indd 28
23/12/2010 12:08:16
IAP Membership Application Form
Membership entitles the individual to receive
the quarterly Journal of International Academy
of Periodontology, and attend IAP Congresses
at a discounted rate. The IAP has recently been
recognized as the official “Periodontal arm” of
the Federation Dentaire Internationale (FDI) and
collaborates with the FDI to provide speakers
for Continuing Education courses, particularly in
developing regions of the world.
I wish to apply to become a member of the
International Academy of Periodontology in one of
the following membership categories:
Name: ......................................................................................................................
.........................................................................................................................................
Postal Address: ..............................................................................................
.........................................................................................................................................
.........................................................................................................................................
.........................................................................................................................................
City: ............................................................................................................................
Active ($60.00 USD)- for any dentist who is
registered with a specialist postgraduate qualification
in Periodontology
State: ........................................................................................................................
Associate ($60.00 USD)- for any dentist who is not
qualified for Active membership, and any person
who is certified to practice dental hygiene, or perform
duties relevant to the practice of periodontics
Country: .................................................................................................................
Student ($30.00 USD)- for dental school graduates
who are presently in postgraduate training in
periodontology
Zip/Post Code: ................................................................................................
Email: .......................................................................................................................
Telephone: ..........................................................................................................
FAX: ..........................................................................................................................
Institutional ($150.00 USD)- for National Societies
and Educational organizations
Please mark the category of membership for which you are applying.
 Active
$60.00
 Associate
$60.00
 Student
$30.00
 Institutional
$150.00
 Corporate
$1,500.00
**Please note: Student membership must be accompanied by an official letter with an official stamp from the
Dean or Director of Studies at their Institute**
METHODS OF PAYMENT:
Payment by credit card-Membership applications can be sent by fax 617-638-4799 or by mail.
Payment by check-must by a US Dollar Check-Drawn on a US Bank and made payable to
“The International Academy of Periodontology”
 Visa
or
 MasterCard
Name on Card: ...............................................................................................................................................................................................................................................
Card number: .............................................................................................................................................. Expiry Date: ............................................................
Signature: ..........................................................................................................................................................
IAP Membership to:
Boston University Goldman School of Dental Medicine, 100 East Newton Street G107, Boston, MA 02118
Phone: 617-638-4758
Fax: 617-638-4799.
E-mail: [email protected].
Web: www.perioiap.org
Waterpik_Evolution_JIAP_January_f.pdf
1
12/8/10
1:44 PM
The Evolution of Floss
Easier and More Effective Than String Floss!
The Waterpik® Water Flosser continues to outperform traditional
floss in study after study. New clinical research confirms that the
Water Flosser is significantly more effective than
string floss at reducing gingival bleeding. It's
easy to use, and your patients who don't
like to floss will love that it only takes
a minute a day.
So make an evolutionary step in your
practice. For better patient compliance
and superior results, recommend the
Waterpik® Water Flosser.
REMOVES
99.9%
OF PLAQUE
Effective Plaque Removal
Proven in laboratory
tests to remove
99.9% of plaque
biofilm from treated
areas in 3 seconds.
Untreated Treated
Independent study. Go to www.waterpik.com for details.
UP TO
2X
AS EFFECTIVE
AS STRING
FLOSS
Improved Gingival Health
Clinically proven up to twice
as effective as string
floss in reducing
gingival bleeding
Brushing
& String
after 14 days.
Flossing
Brushing &
Waterpik®
Water Flosser
Independent clinical study. Data on file.
NEW
Plaque Seeker™ Tip
Innovative new tip design
to help remove even more
stubborn plaque
biofilm from hard
to reach areas.
For an abstract of the latest clinical research, please
visit our website.
www.waterpik.com
Join the conversation at community.waterpik.com,
and
TM

Journal of the International Academy of Periodontology

Transcription

Similar documents

education

Periodontal Treatment - University of Adelaide

Dec 2005 - the EFP

The Roots of Periodontology - New Mexico Dental Hygienists

Viajet

Sep 2012 - the EFP

basic periodontal treatment in dogs and cats

Influence of trauma from occlusion on progression

Fall 2012 Newswire - Washington State Society of Orthodontists

Frictional keratosis of the vestibule

Moonlight Deuces Heidt`s Hot Rod Shop Plaque