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1995 JPR Desinfecci - N Total VS Parcial Quirynen
1995 JPR Desinfecci - N Total VS Parcial Quirynen
1459
1460 Quirynen et al. / Dent Res 74(8) 1995
Table 1. Descriptive statistics of examined population and dental status in 1st quadrant
Gender Age Smoker % of Sites with Probing Depth3 > 7 % of Sites with Angular % of Sites with Calculusa-C
mm Defectsa-b
Test group
#1 F 57 - 18.8 0 57.1
-
#2 F 46 26.3 33.3 16.7
-
#3 F 42 31.8 42.9 28.6
#4 M 56 +/- 45.5 42.9 14.3
#5 F 61 - 48.7 33.3 0
Control group
radiographs.
c
Supra- and/or subgingival estimated on intra-oral long-cone radiographs.
Taking all these aspects into consideration, one might hypothesize antiseptics. Just prior to the first session of scaling and root planing
that, in a normal periodontal treatment strategy (with consecutive root (baseline), and one and two months later, clinical parameters and
planings per quadrant or sextant at one- to two-week intervals), a re- plaque samples were taken from the right upper quadrant, chosen for
infection of a disinfected area might well occur before the completion of its accessibility. This study reports the short-term results; the patients
the treatment. This study aims to examine, both clinically and will be followed up to eight months after therapy.
microbiologically, the result of a full-mouth disinfection within a 24- Mechanical plaque and calculus removal
hour period combined with a prolonged supra-and subgingival
After gingival infiltration with a local anaesthetic, scalings and root
application of chlorhexidine.
planings were performed by one investigator (BV) with an assortment
Materials and methods of periodontal curettes (Hu-Friedy, Chicago, IL). The time spent per
quadrant was approximately one hour. The treated quadrants were
Patient selection
polished with 3 pastes with a decreasing order of abrasiveness: Zircate
Ten patients were included in this double-blind (for microbiological Prophy Paste® (Dentsply International Inc., Milford, DE), and Clean
data), randomized, parallel study on the basis of volunteership. The Polish® and Super Polish® (Hawe-Neos Dental, Bioggio, Switzerland).
patients were referred to the Department of Periodontology of the In the test group, the lower jaw was treated prior to the upper.
Catholic University of Leuven for treatment of advanced chronic
Local application of antiseptic (test group)
periodontitis. All subjects were medically healthy, and none of them
had used any antibiotics or antimicrobial product within the four Immediately after instrumentation of each jaw, an optimal disinfection
months before or during the study. The descriptive statistics of these was sought by (in chronologic order): (1) brushing the dorsum of the
patients together with their disease status are summarized in Table 1. tongue (by the patients) for 60 s with a chlorhexidine 1% gel (Hibigel®,
Each patient had at least 2 multi-rooted teeth and 3 single-rooted teeth SmithKline Beecham Consumer Brands SA, Genval, Belgium); (2)
in each quadrant, with, per quadrant, at least 4 sites having a probing rinsing twice with chlorhexidine 0.2% solution (Hibident®, SmithKline
depth of 7 mm or greater which also bled when probed. Radiographic Beecham Consumer Brands SA, Genval, Belgium) during one min (for
evidence of severe bone loss (> 1/2 the root length) was also present. the last 10 s the patients had to gargle, in an attempt for the Hibident®
After informed consent was obtained, the participants were randomly to reach the tonsils); (3) subgingival irrigation 3x within 10 min with
distributed between two treatment groups. The project protocol had chlorhexidine 1% gel (Hibigel®) of all the pockets by means of a syringe
previously received permission from the Ethical Committee of the with a needle on which marks had been put at 6 and 8 mm (a blunt
University Hospital. needle was introduced into the pocket until some resistance was met);
and (4) repeating the subgingival application at day 8. Additionally, the
Experimental design
subjects of the test group were instructed to rinse twice daily for one
The patients of the test group (five subjects) received a full-mouth min with a 0.2% solution of chlorhexidine (Hibident®) during 14 days.
scaling and root planing within 24 hours. In the control group (five
Oral hygiene
subjects), the scaling and root planing were performed quadrant by
Standard oral hygiene instructions were given in both groups,
quadrant with a time interval of 14 days (starting with the right upper
quadrant) and without the use of
J Dent Res 74(8) 1995 Full-mouth Disinfection for Periodontitis 1461
including interdental plaque control (toothpicks and/or interdental Ireland) and placed onto a microscope slide (Listgarten and Hellden,
brushes) and brushing of the dorsum of the tongue twice a day. Plaque 1978). The samples were then analyzed with a differential phase-
control and oral hygiene re-instruction were repeated at each visit (days contrast microscope (Laborlux S®, Wild Leitz, Heerbrugg, Switzerland)
2, 8, and 29 for the test group, days at a magnification of 480x, according to Listgarten and Hellden (1978).
1,15, and 29 for the control group). One hundred microorganisms, from fields selected at random, were
Questionnaire classified into four morphological categories (Mousques et ah, 1980):
coccoid cells, motile rods other than spirochetes, spirochetes, and the
The participants were asked to complete a questionnaire at each visit.
others (fusiforms, rods, and filaments). The samples were transferred
Besides mentioning any adverse effects, they were asked to estimate the
to the laboratory, where they were processed in less than 24 hours. All
degree of pain after treatment, on a numerical scale from 0 to 10, and to
microbiological procedures were performed by an investigator who
indicate the number of painkillers taken. They were also asked to
did not know the history of the sample.
measure their temperature. The use of antimicrobial products or
Culture techniques and identification
antibiotics was particularly questioned. From the initial 12 patients, two
had to be withdrawn because of the use of a wide-spectrum antibiotic Serial 10-fold dilutions were prepared in RTF. A volume of 0.1 mL of
for reasons not related to this study. the first three dilutions was plated on a selective TSBV plate
Clinical examination (Trypticase-soy-agar [BBL Microbiology Systems, Cockeysville, MD,
USA], supplemented with 75 pg/mL of bacitracin and 5 mg/mL
The clinical parameters were recorded by one investigator (BV) prior to
vancomycin) for the selection of A. actinomycetemcomitans (Slots,
scaling and root planing and at one and two months, in the right upper 1982). These plates were incubated in air with 5% C02 for three days. A.
quadrant only: (1) gingivitis index (Miihlemann and Son, 1971); (2)
actinomycetemcomitans was identified mainly on the basis of colonial
plaque index (Quigley and Hein, 1962); (3) probing depth measured to
morphology (small colonies with dark border and star-shaped inner
the nearest mm at each approximal site (buccally as well as palatally)
structure) and a positive catalase reaction. Representative isolates were
and in the middle of each root (buccally as well as palatally) by means
subjected to lactose and sucrose fermentation (Slots, 1981).
of a Merrit B® probe (Hu-Friedy, Chicago, IL); (4) gingival recession (in
For the identification and quantification of the other organisms, the
the middle of each root, only buccally and palatally), i.e., the distance
dilutions, 10'3 to 10'6, were plated in triplicate onto blood agar plates
from the cemento-enamel junction to the gingival margin measured to
(Blood Agar Base II, Oxoid, Basingstoke, UK) supplemented with
the nearest mm by the same probe; and (5) bleeding tendency up to 20 s
hemin (5 mg/mL), menadione (1 mg/mL), and 5% sterile horse blood.
after the pocket was probed until a slight resistance was felt. The mean Two series of the blood agar plates were incubated in 85% N2,10% COz,
plaque and gingivitis index and the mean percentage of pockets that and 5% H2 and another series in air for five days at 37°C. After this
bled after being probed were calculated for each tooth type (single- or
period, the total number of colony-forming units (CFU/mL) was
multi-rooted).
counted in both the aerobic and anaerobic cultures. For each colony
Plaque samples type (characterized by color, morphology, size, translucency, and
At baseline, and at one and two months, two pooled samples (from hemolysis) of the representative anaerobic plate, a typical colony was
three approximal sites) of the subgingival plaque were taken from both subcultured by streaking onto a blood agar plate (Columbia Agar,
single- and multi-rooted teeth (all located in the upper right quadrant). Oxoid, Basingstoke, UK) supplemented only with 5% sterile horse
For each tooth type (single- or multirooted), the three deepest pockets blood. After 24 to 48 hours of anaerobic incubation, the purified
were selected. All samples were taken from an undisturbed subgingival colonies were identified by means of Gram-staining, phase-contrast
flora and after removal of the supragingival plaque (Wikstrom et al., microscopy, and a series of biochemical tests. For the latter, the Rapid
1991). Prior to being sampled, the sites were isolated from saliva by the ID 32A® and the Strep 32® tests of the API System® (Biomerieux S.A.,
application of cotton rolls and were then gently dried with compressed Montalieu-Vercieu, France) were used for anaerobic organisms and
air to prevent contamination, since large differences in plaque streptococci species, respectively (Van Winkelhoff et al., 1988b). The
composition exist between different niches (Van der Velden et al., original plates were re-examined after 14 days of anaerobic incubation
1986). Four sterile medium paper points (Maillefer®, Ballaigues, to verify the number of CFU and the colony types.
Switzerland) were inserted into the selected pockets (two buccal and The major aim of this analysis was to identify the proportions of
two palatal) and kept in place for at least 10 s. Following removal, the predominant pathogenic organisms besides spirochetes (A.
paper points were transferred into a screw-capped vial containing 1 mL actinomycetemcomitans, B. forsythus, F. nucleatum, P. micros, P.
of transport medium RTF (Syed and Loesche, 1972). The two pooled gingivalis, P. intermedia, Eubacteria spp.) and benificial micro-
samples were homogenized by being vortexed for 30 s (Dahlen et al., organisms (Actinomyces spp., S. mitis and sanguis, Veillonella spp.),
1992). as suggested by Socransky and Haffajee (1992), and Wolff and co-
Differential phase-contrast microscopy workers (1994).
Statistical analysis
Phase-contrast microscopy was performed less than 15 min after
sampling to ensure the motility of the micro-organisms (Petit et al., Probing depth. Changes in probing depth over time were compared
1991). A small aliquot of fluid was aspirated into a sterile tuberculine between both treatment groups (only for pockets initially 7 or 8 mm)
syringe (Plastipak®, Becton Dickinson, Dublin, by means of a mixed procedure of the SAS statistical system (SAS
Institute Inc., 1992). A mixed model was
1462 Quirynen et al. / Dent Res 74(8) 1995
Table 2. Clinical parameters for sampled sites in the upper right quadrant per treatment modality and per tooth type at baseline and the one-and two-
month follow-up visits (means ± SD)
Tooth Treatment Plaque Gingivitis Baseline Probing Bleeding Plaque Gingivitis Probing Bleeding
Type Index Index Depth Index Index Index 1 Depth Index
GI/PI
Month
GI/PI
Single- Full 3.7 ± 0.9 2.6 ± 0.4 0.7 ± 0.2 6.7 ± 1.4 100 1.5 ±1.2 0.7 ± 0.4 0.7 ± 0.6 4.3 ± 1.7 80 ±10
rooted Partial 3.5 ± 0.9 2.3 ±1.0 0.6 ± 0.2 5.9 ±1.3 100 2.0 ±1.7 1.2 ±0.4 1.8 ±2.1 3.8 ± 1.3 90 ±10
Multi¬ Full 4.2 ± 0.6 2.8 ± 0.3 0.7 ±0.1 6.6 ±1.1 100 2.5 ±1.4 0.6 ± 0.5 0.3 ± 0.3 4.8 ± 0.6 70 ±30
rooted Partial 4.2 ± 0.5 2.2 ± 0.4 0.5 ± 0.1 6.7 ±1.4 100 3.4 ± 0.6 0.7 ±0.6 0.2 ± 0.2 5.0 ±1.2 90 ±10
(Continued on next page.)
fitted to the data, with treatment, time, and the interaction between transformed by an arcsin \/p transformation before statistical analysis.
treatment and time as a fixed effect, and patient as a random effect. A mixed model was fitted in which the treatment modality was a fixed
The different tooth types nested in a patient were modeled as a random effect, and the patient a random effect. The two measurements within a
factor. Within each tooth type, measurements of probing depth at patient (2 samples per patient) were modeled as repeated measures
baseline and one month, and at baseline and two months, were with a compound symmetry structure within a patient. Furthermore,
modeled as repeated measures with a compound symmetry structure. the measured variable at time 0 was used as a co-variable. The
The slopes of the two treatment modalities were compared, again treatment outcome after one and two months was tested against the
with the error stratum of the patient as background variability. error stratum of the patient, leading to an F-statistic with 8 df for the
denominator.
Microbiology. Differences between test and control group concerning
the microbiological data were also sought by means of a mixed- Results
procedure of the SAS statistical system (SAS Institute Inc., 1992). The
Clinical parameters
variables (proportion of spirochetes and motile rods together,
proportion of pathogenic organisms, and proportion of beneficial The mean plaque and gingivitis indices, probing depth, and bleeding
species), expressed in percentages, were tendency for the sampled sites are depicted per treatment modality and
per tooth type (single- vs. multirooted teeth) in Table 2. At baseline,
comparable recordings
SPIROCHETES (n-5) 8
0
40
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.
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4
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0 single¬ single-
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differences
0 result in clinically detectable changes (Listgarten et al.,
1978), more significant differences might be expected at further
follow-up visits.
The differences in treatment outcome can be explained by the
differences in the microbiological data. The change in the
gingivitis/plaque ratio after two months (Table 2) already indicates a
greater reduction in the pathogenicity of the plaque in the test group.
Moreover, the culture data showed, after the one-stage full-mouth
disinfection, a more significant decrease in the proportion of
pathogenic organisms (Fig. 5) paralleling a more important increase
in beneficial species (Fig. 6).
One can only speculate on the relative importance of each of the
five abovementioned steps in the test protocol, since all of them are
known to reduce the pathogenicity of the subgingival flora.
§ Test single-rooted ■ Test multi-rooted
However, some have only a short-(one week) to medium-term (two
HI Control single-rooted □ Control multi-rooted months) effect. Indeed, several reports have illustrated that, after a
single session of scaling and root planing, the subgingival flora
Figure 4. Changes over time in the relative proportion of potentially returns to baseline values, "qualitatively and quantitatively', within a
pathogenic organisms, by tooth type and treatment modality. These two- month period, at least when oral hygiene is not optimal, as was
changes were analyzed by means of a mixed-procedure test of the the case in this study (Mousques et al., 1980; Van Winkelhoff et al.
S.A.S. statistical package. Because spirochetes are considered
1988c; Sbordone et al., 1990). Moreover, several studies have
pathogenic (Socransky and Haffajee, 1992; Wolff et al., 1994) but
could not be cultured, they were included based on the phase- illustrated that an irrigation of the pockets with a chlorhexidine
contrast microscopic observations, and the proportion of the other solution (even if repeated weekly) failed to improve the effect of
micro-organisms was recalculated by the formula: new proportion = mechanical debridement at either a microscopic or clinical level over
old proportion x [(100 - % spirochetes) / 100]. (A. a six-month observation period (Braatz et al., 1985; MacAlpine et al.,
actinomycetemcomitans was observed only once in a very low
1985; Lander et al., 1986; Wennstrom et al., 1987). The supragingival
density, and B. forsythus and C. rectus were not detected at all.)
plaque growth inhibition by chlorhexidine mouthrinses (Hull, 1980)
might be responsible for the lower plaque and gingivitis scores for
The probing depth reduction noted in the control group falls the subjects in the test group at month 1. The effect of oral rinsing on
within the range of previous observations (Badersten et al., 1984), the subgingival flora, however, is negligible (Flotra et al., 1972).
while the test group achieved greater improvement. The differences The advantage of a one-stage full-mouth disinfection is the
between test and control groups (Fig. 1) were significant for pockets reduced probability of an intra-oral transmission of periodon-
with an initial depth of 7 and 8 mm. While the one-stage full-mouth topathogens from one of their niches to the
disinfection resulted in a mean pocket reduction from 7.3 to 4.0 mm
(SD ±1.2 mm), in the control group a reduction of only from 7.4 to 4.9
mm (SD ±1.4 mm) could be achieved. Since it takes several months
before microbiological
/ Dent Res 74(8) 1995 Full-mouth Disinfection for Periodontitis 1465
(Fig. 4). This is in contrast to the observations of Van Winkelhoff without further oral disinfection, a subgingival recolonization by P.
and co-workers (1988c), who reported, two months after a single course gingivalis in 58% of the examined pockets. The outcome of the present
of scaling and root planing therapy for A.
Table 3. Major complaints after full-mouth disinfection (test group) or after first-quadrant scaling and root planing (control group)
Pain Pain-killers (number of Fever (°C) Herpes Labialis
(numerical score3) tablets)
Test group
#1 0 0 37.8 -
- -
#2 6 6
#3 3 1 39.0 +
#4 7 2 38.5 +
#5 10 2 - -
Control group
- -
#1 8 1
- -
#2 0 0
- -
#3 5 1
- -
#4 7 2
#5 6 2 - -
a Scores from 0 to 10: 0 = no pain, 10 = extremely painful.
1466 Quirynen et al. ] Dent Res 74(8) 1995
actinomycetemcomitans-positive patients should be further assessed. periodontopathogens in "diseased" and "non-diseased" persons
The only patient (test group) with two sites positive for A. exhibiting poor oral hygiene. J Clin Periodontol 19:35-42.
actinomycetemcomitans showed an initial increase in concentration of Danser MM, Van Winkelhoff AJ, de Graaff J, Loos BG, Van der Velden
this organism, but at eight months, this organism disappeared. A U (1994). Short-term effect of full-mouth extraction on periodontal
possible explanation for this is the capacity for tissue invasion which pathogens colonizing the oral mucous membranes. J Clin
has been described for this organism (Christersson et al., 1987). Periodontol 21:484-489.
The increase in body temperature (Table 3), reported in the test Ellen RP (1978). The dental practitioner and systemic infections of oral
group (3/5), probably illustrates the important bacteremia during origin. Int Dent ] 28:295-308.
scaling and root planing (Ellen, 1978). Perhaps the increased amount of Flötra L, Gjermo P, Rölla G, Waerhaug J (1972). A 4-month study on the
micro-organisms introduced into the bloodstream and/or the effect of chlorhexidine mouthwashes on 50 soldiers. Scand J Dent
prolonged treatment time (four hours within a single day) Res 80:10-17.
overstimulated the host-defense mechanism. The occurrence of herpes Hull PS (1980). Chemical inhibition of plaque. J Clin Periodontol 7:431-
labialis in two of the five patients of the test group could be due to 442.
prolonged trauma or to the rise in body temperature. Lander PE, Newcomb GM, Seymour GJ, Powell RN (1986). The
In conclusion, the one-stage full-mouth disinfection showed antimicrobial and clinical effects of a single subgingival irrigation
significant clinical (pocket reduction) and microbiological (shift toward of chlorhexidine in advanced periodontal lesions. / Clin
a more beneficial flora) advantages on a short-term basis. Periodontol 13:74-80.
Listgarten MA, Hellden L (1978). Relative distribution of bacteria at
Acknowledgments
clinically healthy and periodontally diseased sites in humans. /
The authors wish to thank G. Depauw for his help with the Clin Periodontol 5:115-132.
microbiological procedures and L. Duchateau for the statistical analysis. Listgarten MA, Lindhe J, Hellden L (1978). Effect of tetracycline and/or
The financial support for this project was provided by the Faculty of scaling on human periodontal disease. Clinical, microbiological,
Medicine, Catholic University of Leuven. and histological observations. J Clin Periodontol 5:246-271.
References Loesche WJ, Svanberg ML, Pape HR (1979). Intraoral transmissions of
Streptococcus mutans by a dental explorer. ] Dent Res 58:1765-
Alaluusua S, Asikainen S, Lai CH (1991). Intrafamilial transmission of 1770.
Actinobacillus actinomycetemcomitans. ] Periodontol 62:207-210. Loos B, Claffey N, Egelberg J (1988). Clinical and microbiological effects
Asikainen S, Alaluusua S, Saxen L (1991). Recovery of A. of root debridement in periodontal furcation pockets. / Clin
actinomycetemcomitans from teeth, tongue and saliva. / Periodontol 15:453-463.
Periodontol 62:203-206. MacAlpine R, Magnusson I, Kiger R, Crigger M, Garret S, Egelberg J
Badersten A, Nilveus R, Egelberg J (1984). Effect of nonsurgical (1985). Antimicrobial irrigation of deep pockets to supplement oral
periodontal therapy. III. Single versus repeated instrumentation. / hygiene instruction and root debridement. I. Bi-weekly irrigation. J
Clin Periodontol 11:114-124. Clin Periodontol 12:568-577.
Barnett ML, Baker RL, Olson JW (1982). Material adherent to probes Magnusson I, Lindhe J, Yoneyama T, Liljenberg B (1984). Recolonization
during a periodontal examination. Light and electron microscopic of a subgingival microbiota following scaling in deep pockets. J
observations. / Periodontol 53:446-448. Braatz L, Garrett S, Clin Periodontol 11:193-207.
Claffey N, Egelberg J (1985). Antimicrobial irrigation of deep Mousques T, Listgarten MA, Phillips RW (1980). Effect of scaling and
pockets to supplement non-surgical periodontal therapy. II. Daily root planing on the composition of the human subgingival
irrigation. / Clin Periodontol 12:630-638. microbial flora. ] Periodont Res 15:144-151.
Caufield P, Gibbons R (1979). Suppression of Streptococcus mutans in Mühlemann HR, Son S (1971). Gingival sulcus bleeding—a leading
the mouths of humans by a dental prophylaxis and topically- symptom in initial gingivitis. Helv Odontol Acta 15:107-113.
applied iodine. J Dent Res 58:1317-1326. Christersson LA, Slots J, Müller H-P, Lange DE, Müller RF (1989). Actinobacillus
Zambon J J, Genco RJ (1985). Transmission and colonization of actinomycetemcomitans contamination of toothbrushes from
Actinobacillus actinomycetemcomitans in localized juvenile patients harboring the organism. / Clin Periodontol 16:388-390.
periodontitis patients. ] Periodontol 56:127-131. Oosterwaal PJM, Mikx FHM, van 't Hof MA, Renggli HH (1991). Short-
Christersson LA, Albini B, Zambon JJ, Wikesjo UME, Genco RJ (1987). term bactericidal activity of chlorhexidine gel, stannous fluoride
Tissue localization of Actinobacillus actinomycetemcomitans in gel and amine fluoride gel tested in periodontal pockets. ] Clin
human periodontitis. I. Light, immunofluorescence and electron Periodontol 18:97-100.
microscopic studies. / Periodontol 58:529-539. Papaioannou W (1994). The subgingival microflora around titanium
Dahlen G, Manji F, Baelum V, Fejerskov O (1992). Putative abutments under various clinical situations (Master's degree
thesis). Leuven, Belgium: Catholic Univ. of Leuven.
Pavicic MJAMP, Van Winkelhoff AJ, Douque NH, Steures RWR, de
Graaff J (1994). Microbiological and clinical effects of
metronidazole and amoxicillin in Actinobacillus
J Dent Res 74(8) 1995 Full-mouth Disinfection for Periodontitis 1467
actinomycetemcomitans-associated periodontitis. / Clin flora in various transport media. Applied Microbiol 24:638-644.
Periodontol 21:107-112. Van der Velden U, Van Winkelhoff AJ, Abbas F, De Graaff J (1986). The
Petit MDA, Van der Velden U, Van Winkelhoff AJ, De Graaff J (1991). habitat of periodontopathic micro-organisms. / Clin Microbiol
Preserving the motility of microorganisms. Oral Microbiol 13:243-248.
Immunol 6:107-110. Van Winkelhoff AJ (1994). Advances in antibiotic therapy and delivery
Petit MDA, Van Steenbergen, Timmerman MF, De Graaff J, Van der systems (abstract). / Parodontologie (Spec Iss Europerio 1994): 18.
Velden U (1994). Prevalence of periodontitis and suspected Van Winkelhoff AJ, Van der Velden U, Winkel EG, De Graaff J (1986).
periodontal pathogens in families of adult periodontitis patients. J Black-pigmented Bacteroides and motile organisms on oral
Clin Periodontol 21:76-85. mucosal surfaces in individuals with and without periodontal
Preus HR, Lassen J, Aass AM, Christersson LA (1993). Prevention of breakdown. / Periodont Res 21:434-439.
transmission of resistant bacteria between periodontal sites during Van Winkelhoff AJ, Van der Velden U, Clement M, De Graaff J (1988a).
subgingival application of antibiotics. / Clin Periodontol 20:299- Intra-oral distribution of black-pigmented Bacteroides species in
303. periodontitis patients. Oral Microbiol Immunol 3:83-85.
Quigley GA, Hein JW (1962). Comparative cleansing efficiency of Van Winkelhoff AJ, Clement M, Graaff J (1988b). Rapid
manual and power brushing. ] Am Dent Assoc 65:26-29. characterization of oral and nonoral pigmented Bacteroides
Quirynen M, Papaioannou W, van Steenberghe D (1995). Intraoral species with the ATB anaerobes ID system. / Clin Microbiol
transmission of micro-organisms. ] Dent Res (submitted). 26:1063-1065.
Rindom Schiott C, Briner WW, Loe H (1976). Two year oral use of Van Winkelhoff AJ, Van der Velden U, De Graaff J (1988c). Microbial
chlorhexidine in man. II. The effect on the salivary bacterial flora. J succession in recolonizing deep periodontal pockets after a single
Periodont Res 11:145-152. course of supra- and subgingival debridement. / Clin Periodontol
SAS Institute, Inc. (1992). The mixed procedure. In: SAS technical report 15:116-122.
P-229. SAS/STAT software: changes and enhancements. Release Van Winkelhoff AJ, de Groot P, Abbas F, de Graaff J (1994).
6.07. Cary, NC: pp. 287-368. Quantitative aspects of the subgingival distribution of
Sbordone L, Ramaglia L, Gulletta E, Iacono V (1990). Recolonization of Actinobacillus actinomycetemcomitans in a patient with localized
the subgingival microflora after scaling and root planing in human juvenile periodontits. J Clin Periodontol 21:199-202.
periodontitis. J Periodontol 61:579-584. Walsh MM, Buchanan SA, Hoover CI, Newbrun E, Taggart EJ,
Slots J (1981). Enzymatic characterisation of some oral and nonoral Armitage GC, et al. (1986). Clinical and microbiologic effects of
Gram-negative bacteria with the Api Zym system. J Clin single-dose metronidazole or scaling and root planing in
Microbiol 14:288-294. treatment of adult periodontitis. J Clin Periodontol 13:151-157.
Slots J (1982). Selective medium for the isolation of Actinobacillus Wennstròm JL, Dahlén G, Gròndahl K, Heijl L (1987). Periodic
actinomycetemcomitans. ] Clin Microbiol 15:606-609. subgingival antimicrobial irrigation of periodontal pockets.
Slots J (1986). Bacterial specificity in adult periodontitis. A summary of II. Microbiological and radiographical observations. J Clin
recent work. / Clin Periodontol 13:912-917. Periodontol 14:573-580.
Slots J, Rams TE (1990). Antibiotics in periodontal therapy: advantages Wikstròm M, Renvert S, Dahlén G, Johnsson T (1991). Variance in
and disadvantages. J Clin Periodontol 17:479-493. recovery of periodontitis-associated bacteria caused by sampling
Slots J, Rams TE (1991). New views on periodontal microbiota in special technique and laboratory processing. Oral Microbiol Immunol
patient categories. J Clin Periodontol 18:411-420. 6:102-106.
Socransky SS, Haffajee AD (1992). The bacterial etiology of destructive Wolff L, Dahlén G, Aeppli D (1994). Bacteria as risk markers for
periodontal disease: current concepts. / Periodontol 63:322-331. periodontitis. / Periodontol 64:498-510.
Syed SA, Loesche WJ (1972). Survival of human dental plaque